Open access peer-reviewed chapter

Adaptation to Water Stress in Soybean: Morphology to Genetics

Written By

Tuanjie Zhao, Muqadas Aleem and Ripa Akter Sharmin

Submitted: October 9th, 2017 Reviewed: November 6th, 2017 Published: December 20th, 2017

DOI: 10.5772/intechopen.72229

Chapter metrics overview

1,961 Chapter Downloads

View Full Metrics


Soybean (Glycine max L.) is the most important legume and oilseed crop. As a leguminous crop, it plays an irreplaceable role towards the sustainable agricultural system with biological nitrogen fixation. However, its production can be dramatically decreased by the occurrence of water stress. Water stress including drought and flooding induces the morpho-physiological and biochemical changes at different growth stages, which negatively affects the adaptability and yield of soybean. Genetic diversity that ensures productivity in challenging environment exists within germplasm, their wild relatives and species that are adapted to the water stress. The discovery of gene mapping, QTLs associated with root traits, slow canopy wilting, nitrogen fixation and flooding tolerance have accomplished significant progress in breeding programs. Identification of drought-responsive genes and transcription factors such as WRKY, DREBs, ERFs, ZIP, ZFP, MYB and NAC are valuable to ameliorate the water stress in soybean. Understanding the genetic mechanism using transcriptomic and proteomic approaches would be the ultimate choice for mitigating the water stress. Integration of well-designed soybean breeding program coupled with omic techniques would pave the way for developing drought and flooding resilient soybean cultivars.


  • soybean
  • drought
  • flooding
  • stress tolerance
  • quantitative trait locus
  • genomics
  • genetic diversity

1. Introduction

Soybean is an important leguminous crop in the world, providing an essential source of protein to human diet, feed for live-stock and as bio-diesel for industry [1, 2]. Soybean seeds consist of 40% protein, 20% oil, 35% carbohydrate and ~5% ash [3]. As compared to other oilseed crops, soybean collectively occupies around 6% of the world’s land under cultivation [4]. Due to the rapid rise in the commercial value of soybean in an international market, the total area under soybean cultivation has been increasing from last three decades. Soybean is an important cash crop with a total production of over 313.05 million metric tons in 2015–2016 (USDA data). During this year, the USA has been the world’s leading producer of soybean representing 35% of the world production, followed by Brazil with 31%, Argentina with 17%, China with 4%, India with 3%, Paraguay with 3% and Canada with 2% (USDA data).

Water stress including drought and flooding is considered as a major threat, limiting growth and yield of plants [5, 6]. Drought is caused by insufficient rainfall or irrigation which results in soil drying, whereas, in flooding, water exists in soil solution causing water logging and submergence. In response to drought and flooding stress, 40–60% yield losses have been reported in soybean [7, 8]. High temperature, low humidity in atmosphere and water deficiency are the main causes of drought [9, 10]. Drought stress affects germination rate and early seedling growth of the plant [11, 12]. Under water deficit conditions, a significant reduction in germination, hypocotyl length, root and shoot fresh and dry weight were observed whereas the root length is increased [13]. It also affects the carbon assimilation and phenology of the plant [10]. Prolonged drought stress at different growth stages has profound effect on soybean growth and yield [14].

To counteract the adverse effects of drought, the soybean plant adopts three mechanisms i.e. escape, tolerance, and avoidance [15]. In the escape mechanism, the plant completes its life cycle before the onset of drought. Normally, the plants complete their life cycle very quickly and produce few seeds. For instance, early planting of soybean helps to avoid drought, and is largely practiced in the USA—planting in March to April affords escape from water stress [16, 17]. Drought avoidance is performed by maintaining high water potential, grow deeper in soil, stomatal control of transpiration rate, and by reduction of water loss from tissues. The tolerance mechanism includes low tissue water potential, maintenance of turgor through osmotic adjustments [18, 19].

Flooding ranks second after drought, causing yield reduction in soybean [20, 21]. Flooding stress can be categorized as waterlogging or submergence. In waterlogging stress, root goes under water while shoots remains above ground, whereas, during submergence, plant is completely immersed in water saturated soil. As plants are aerobic, hypoxia (insufficient oxygen) or anoxia (complete absence of oxygen) causes losses in crop production. Soybean is more sensitive to flooding stress resulting in yield decline by reducing photosynthesis nitrogen fixation and biomass accumulation. Flooding stress can happen during any growing stage, especially in the seed germination and vegetative stages leads to substantial decrease of soybean grain yield [22] (Table 1). In addition, flooding stress hampers yield production during vegetative (17–43%) and reproductive stage (50–56%) [41].

Growth stage Experimental material Indicator Ref.
Under drought stress
Germination 4 Bulgarian lines & one USA variety Germination, shoot and root length, fresh and dry weight [23]
Germination L17, M9, Clark, M7, Hobbit and Williams Root and shoot length, germination rate and percentage of germination [24]
Second trifoliate leaves Jindou 21 (C12), Mengjin 1 (W05) and Union (C08) Gas exchange, water relation parameters, total chlorophyll, proline contents of leaves, root xylem pH, plant growth and root traits [25]
Third trifoliate leaf (V3) A5409RG, Jackson and Prima 2000 Root architecture, shoot parameters [26]
Flowering and pod-filling stage Habit, L17 and M17 Leaf relative water content, chemical osmolytes and chlorophyll content [27]
V4, R1 and R3 growth stages. Eight soybean cultivars Highest number of node/plant, number of pod/main stem, pod/sub stem and pod/plant [28]
Reproductive stage (R6–R7) 41 soybean accessions increases in metaxylem number [29, 30]
Adult PI578477A,PI088444,PI458020 Yield, root architecture [31]
Adult BARI Soybean 5, BARI Soybean 6, Shohag and BD2331 relative performance (RP), tolerance (TOL), drought susceptibility index (DSI) [32]
Under flooding stress
Seedlings stage Soybean Secondary aerenchyma formation [33]
Seedling stage 11 soybean genotypes Primary/adventitious roots and root nodules, stem and leaf biomass [34] [35]
Vegetative and flowering stage Taekwang and Asoaogari Root morphological traits, adventitious roots and Photosynthesis [36]
Cotyledon-stage seedlings 92 Soybean Lines Root architecture [37]
Flowering stage Cultivars Fundacep 53 RR and BRS Macota Fermentative metabolism and carbohydrate contents in roots and nodules [38]
Flowering stage Five soybean cultivars Nodule number, nodule dry weight, chlorophyll content, carbon exchange rate, dry matter accumulation and nitrogen content [39]
Seedling stage 162 soybean accessions Root development [40]

Table 1.

A list of drought- and flooding-related parameters at different growth stages of soybean.

For mitigating the negative impact of flooding stress, plants use a number of strategies for their survival, mainly escape and quiescence strategies [42, 43]. In escape strategy, morphological (aerenchyma development, shoot elongation and adventitious root formation) and anatomical alterations allow the plant to exchange gas between cells and atmosphere. The Quiescence strategy suppresses morphological changes to save energy and resources and retard plant growth. This strategy depends on anaerobic energy production [42, 44].

Understanding the genetic base for water stress tolerance in diverse soybean is a fundamental issue that contributes for the genetic improvement. This chapter will present the research progress about the situation of soybean tolerance to water stress at germination, seedling and adult plant stages. It also includes the current knowledge about QTL mapping, gene discovery and ‘omic’ technologies relevant to drought and flooding tolerance that will be helpful to understand drought and flooding-tolerance mechanisms in soybean.


2. Genetic diversity of water stress tolerance in soybean

2.1. Different response of soybean to water stress

2.1.1. Morphological performance

Drought induces morphological changes in plants, enabling them to sense and rapidly adapt to the stress. Root-related traits are crucial in maintaining crop yield in soybean [45]. Drought alters the root system architecture (root depth, root angle and root branching density) [27]. For instance, root architecture was characterized in field under normal and water deficit conditions using three soybean cultivars (Jackson, Prima 2000 and A5409RG). As a result, Prima 2000 (drought-tolerant cultivar) has an intermediate root phenotype with a root angle of 40–60°, while a shallow root phenotype along with root angle of <40° has been observed in drought-sensitive cultivar A5409RG [27].

Depth of rooting system influenced by the elongation of taproot also plays an important role for plant survival under water deficit [27, 46]. An increase in number of root tips, root length, root surface area and root volume was observed under water limited conditions. Several studies have proposed that roots having large xylem number, diameters, lateral root systems with more root hairs are indicators of drought tolerance [31, 47, 48]. Jackson is considered as drought escaping cultivar with long and deep roots into the soil permitting better water uptake compared with drought-sensitive cultivars [27, 49]. Under water-limited conditions, Plant Introduction (PI) 578477A and 088444 exhibited higher yield due to higher lateral root number in clay soil [50]. It was reported that deeper region of soil has high root density under seasonal drought as compared to dry surface of soil [51]. In addition, total root length/ plant weight, dry root weight/plant weight and root volume/plant weight were positively correlated with drought tolerance [52]. Therefore, studying the relationship between root traits and drought is helpful to develop drought-resistant cultivar.

Root-to-shoot ratio is also a good indicator to allocate the resources between different plant components. The water-limited environment increases the root-to-shoot ratio. For example, in soybean, root-to-shoot ratio increased by 13% indicates the flow of biomass towards roots [53]. The drought-tolerant soybean genotype (C12) showed a higher root-to-shoot ratio than the susceptible genotype (C08) under restricted soil water with application of exogenous ABA. To cope with drought stress, leaf morphology also plays an important role. Under water-limited conditions, plants reduce their leaf area by closing stomata. Due to water scarcity, reduction in soybean plant leaf area has been reported [54]. In contrast, drought-tolerant soybean cultivar exhibited a greater leaf area rather than less-tolerant cultivar under hydric stress condition [55].

Aerenchyma formation is a major indicator that facilitates gas exchange between aerial and submerged plant parts (shoots and/or roots) to avoid flooding stress [56, 57]. Flooding stress induces two kinds of aerenchyma i.e. primary (cortical) [58] and secondary (white and spongy tissues) [33]. A number of aquatic plants develop cortical aerenchymatous tissue by cell disintegration (lysigenous aerenchyma) and cell separation (schizogenous aerenchyma) [59]. In rice, barley, maize and wheat, lysigenous aerenchyma is induced by flooding [60, 61]. In some species, especially in soybean, secondary aerenchyma having a spongy parenchyma cell layer develops through cell division of phellogen [44, 62]. Secondary aerenchyma is morphologically and anatomically different from cortical aerenchyma (lysigenous and schizogenous aerenchyma) [33]. Waterlogging stimulated the formation of aerenchyma and adventitious roots in soybean plants facilitating transport of oxygen from shoot to root [62, 63, 64]. Under waterlogging condition, adventitious roots are formed in several flooded plants including soybean [61, 62, 65]. However, adventitious roots are absent in soybean seedlings under complete submergence [66]. Under flooding conditions, secondary aerenchyma consisting of white and spongy tissues develops within a few weeks in stems, roots and root nodules of soybean [33]. Aerenchyma formations initiated by ethylene, Ca2+, and ROS signalling through a programmed cell death process are involved in aerenchyma development [60, 67].

Rapid shoot elongation is another escape mechanism for adaptation in waterlogging stress [68]. It has been reported that lower stem of soybean having hypertrophic lenticels helps oxygen entry into the aerenchyma [64]. Flooding also causes a significant reduction in leaf number, leaf area, canopy height and dry weight at maturity in soybean crops.

2.1.2. Physiological and biochemical response under drought stress

Stress-responsive mechanisms have been studied at the physiological and biochemical level in soybean under drought and flooding stress. To optimize the use of water under water deficit conditions, stomatal control is considered as major physiological indicator. For instance, in soybean, stomatal conductance decreased by 42% in drought-stressed leaves rather than normal leaves [69]. Owing to dehydration, MG/BR46 (drought tolerant soybean variety) showed faster decline in stomatal conductance as compared to BR16 (drought-susceptible variety) (65 versus 50% reduction) [55]. In same study, prolonged drought stress (45 days) exhibited no profound impact on stomatal conductance of BR16 while it had reached 79% in the MG/BR46. Several studies have provided strong evidence that drought-tolerant soybean genotypes (C12 and W05) exhibited a higher reduction in stomatal conductance rather than the susceptible one (C08) [25]. In soybean, ABA is involved in the reduction of stomatal conductance and photosynthesis. For instance, after imposition of exogenous application of ABA under soil drying, leaf stomatal conductance of soybean tolerant genotype C12 declined than the susceptible one (C08).

Maintenance of cell turgidity and water-use efficiency are important indicators to cope with drought stress [26]. Soybean introduction line PI 416937 is an excellent example of drought tolerance by limiting transpiration rate and maintaining a lower osmotic potential. An increase in WUE was observed in drought-tolerant genotype (C12) by regulating stomatal closure during the entire period of water deficiency [25, 52].The maintenance of cell turgidity under water-limited conditions may be achieved by adjusting the osmotic potential in response to the accumulation of proline, sucrose, soluble carbohydrates, glycine betaine and other solutes [70].The accumulation of solutes under water deficit condition is known as osmotic adjustment. Some authors have reported higher proline content in drought-tolerant crop species such as bean [71]. In soybean, water stress exhibited significant increase in proline contents in drought tolerance as well as susceptible genotype, but tolerant genotypes recovered to pre-stress levels more quickly after rehydration [25].

The production of ROS, such as superoxide radical (O2), hydroxyl radical (OH˙) and hydrogen peroxide (H2O2), is one of the biochemical responses causing damage to DNA, proteins and lipids [72] under drought stress. The toxicity of ROS may be limited by antioxidant enzymatic (superoxide dismutase, catalase, and glutathione peroxidase) and non-enzymatic scavengers [73, 74]. For instance, drought stress increased activities of some antioxidant enzymes (catalase, glutathione reductase and superoxide dismutase) in soybean varieties which were positively correlated to seed yield [75].

Under flooding stress, plant undergoes different physiological and biochemical adaptations. For instance, in soybean, a significant reduction in photosynthetic activity and stomatal conductance was observed in Essex and Forrest within 48 h of flooding at vegetative and reproductive growth stages. Waterlogging also decreases biological nitrogen fixation, as nodules need adequate oxygen to maintain nitrogenase activity for aerobic respiration and contributing adenosine triphosphate [41]. As a consequence of flooding stress, a reduction in root hydraulic conductivity has also been reported [76]. Several studies have provided the correlation between stomatal conductance and carbon fixation. In flooded plants, photosynthetic activities were reduced by restricting CO2 due to stomatal closure [77, 78]. Furthermore, due to the higher concentration of CO2 assimilation in flooded soil, biomass and soybean root elongation eventually repressed [79].

Tamang et al. [66] reported that submergence stimulates starch degradation, soluble carbohydrates and ATP in cotyledons and hypocotyls of soybean seedlings. Extensive submergence degrades the chlorophyll contents in aerial parts of several terrestrial plants [80, 81]. However, under submergence, abundance of chlorophyll a and b remained nearly constant in soybean [66]. The decrease in photosynthetic activity with long-term flooding may be triggered by the reduction in chlorophyll, transpiration and ribulose-1,5-biphosphate (RuBP) carboxylase activity. These combined effects against flooding declined the crop growth, net assimilation and leaf expansion of plants. Blocking of hypertrophic lenticels at the base of stem restricted O2 transport into the roots resulting in reduction of plant growth under hypoxic conditions [82]. Flooding stress causes higher production of ROS resulting in oxidative damage to proteins related to photosynthetic apparatus [83]. As a result, the scavenging activity is overpassed under flooding stress.

2.2. Parameters for measuring the tolerance degree of water stress

2.2.1. Parameters related to seed tolerance

Seeds need a suitable condition to have a good germination. The germination rate and percentage of different cultivars were affected by levels of drought stress. In soybean, drought stress simulated by polyethylene glycol PEG-6000 significantly reduced seed germination percentage (Table 1). An increase in the PEG concentration reduced root growth by two to three times for different genotypes. Seed weight and seed size, and seed weight distribution are key indicators to evaluate the genotypic response to drought stress [84, 85]. A positive correlation between 100-seed weight per plant and seed yield were reported in soybean under water limited conditions. For instance, Habit (soybean drought-tolerant cultivar) exhibited higher 100-seed weight and seed yield under drought stress [29, 86].Water deficit conditions lead to a significant reduction in seed weight and seed size. It also had little effect on seed shape as shrunken and wrinkled, and hard seeds were produced in soybean [84, 85, 87]. Same study pointed out 30–40% reduction in proportion of seed having diameter > 4.8 mm. In contrast, the ratio of seeds of diameter < 3.2 mm was increased by 3–15% [85].

Germination is a complex process that consists of several metabolic events. Numerous studies reported that negative correlation exists between germination percentage and flooding stress [88, 89]. Seeds are usually germinated under optimum conditions within 1 or 2 days. But, seed germination is delayed due to the quick absorption of water, collapse of seed structure, and outflow of internal seed contents under flooding stress. When seeds were flooded for 3 days after imbibition, germination percentage was drastically dropped out and seed injury was observed [90]. Flooding causes mechanical damage on the soybean seeds and prohibits germination. Seed coat and seed weight are fundamental factors to evaluate a positive effect on seed flooding tolerance. For example, germination rate (GR) and normal seedling rate (NS) was higher in pigmented varieties as compared to yellow varieties of soybean (Table 1). These parameters (GR and NS) were negatively correlated with seed weight (SW) in the combined population [91]. Therefore, pigmented seed coat and small seed weight could be key parameters in response to seed-flooding tolerance.

2.2.2. Parameters related to vegetative tissues

Root length, shoot length and leaf area are considered as major determinants to evaluate drought response during vegetative stage. A positive relationship exists between root traits and resistance to drought [52, 92]. At seedling stage, drought stress affects leaf expansion rate, leaf water potential, relative water content of leaves (%RWC) and relative growth. The degradation of chlorophyll contents of soybean leaves was correlated with the different levels of drought stress [75]. Water deficit stress also decreased the number of nodes and intermodal length while the reduction in inter-nodal length depends upon the duration of drought stress. For example, drought stress showed no profound impact on number of internodes in drought tolerant soybean cultivar (C12), whereas drought-susceptible cultivar (C08) showed higher number of internode [93].

Essential traits, root length and shoot length are also important indicators in response to flooding stress. The insufficient allocation of water, minerals, nutrients, and hormones led to root and shoot damage [94]. The first symptom usually appears in soybean is wilting of leaves in response to flooding. Soybean shoot growth under flooded conditions is significantly decreased due to inability of the root system regarding water transport, hormones, nutrients and assimilates [95, 96]. Flooding tolerance in soybean is strongly correlated to root surface area, root length and dry weight [97]. It has been reported that root tips are extremely sensitive to flooding in soybean and pea seedlings [98, 99, 100]. Under complete submergence, soybean root growth is absolutely repressed due to the death of root tips.

2.2.3. Parameters related to adult plants

In soybean, pod number per plant, seed number per pod and 100-seed weight are major determinants of yield under water stress [101], and these yield components are the important sink for assimilates at reproductive stages [102]. Drought stress especially during flowering (R1) and pod-filling stages reduces soybean yield [30] (Table 1). Under water deficit conditions, an increase in rate of abortion has been reported during early pod-filling stage in soybean [54, 103]. Soybean yield is also affected by the occurrence of drought stress during seed filling (R6) period [93]. Water stress at flowering stage decreased the pod number and seed number resulting in yield loss [104]. Kobraei et al. [29] conducted experiment on eight soybean cultivars to asses yield under normal and drought conditions. This study pointed out that drought reduced the yield components resulting in yield loss. In addition, more yield loss was observed during R1 stage as compared to R6 stage [104].

One of the major traits conferring tolerance to waterlogging is yield and production of good quality seeds [105]. A significant decline in pod number, pods per node, branch number, and seed size was observed following 7 days of flooding at different vegetative and regenerative development stages [106]. Sullivan et al. [107] confirmed reduction in pod number and plant height at early vegetative growth stages. Soybean crops flooded with excessive water at early flowering stage showed severe chlorosis and stunting growth [108]. Schöffel et al. [109] showed a decreased number of pods per plant at the reproductive stage (R4) in pot trails. A field experiment was conducted in flooded soil and obtained yield reduction from 20–39% in the different soybean cultivars when subjected during the R5 stage. During flooding, a significant reduction in soybean yield was observed at R5 stage as compared to the R2 stage [110].

2.3. Genetic variation of tolerance to water stress

2.3.1. Cultivated soybean

Considerable genetic variation in seed yield was observed in soybean genotypes under drought stress. A total of 50 soybean genotypes were screened under rain-fed condition in Bangladesh. Among them, genotypes BARI Soybean 5, BARI Soybean 6, Shohag and BD2331 were identified as drought-tolerant genotypes [32]. In another study, response of eight cultivars of soybean (Clark, Hobbit, Pershing, Williams, Hood, DPX, M7 and M9) was investigated in Iran. Williams cultivar was predicted as drought-tolerant, having highest number of nodes and pods/plant in normal and water deficit conditions [29]. Genetically and geographically, diverse soybean germplasm lines i.e. from Korea (PI085355, PI339984, PI407778A, PI407973A, PI423841, PI424460, PI424608A, PI603170, PI458020), China (PI088444, PI567398, PI567561, PI594410, PI578477A), Japan (PI243548, PI417092, PI507066) were screened to examine root response under water deficit condition in clay and sandy soil. Plant Introduction PI578477A, PI088444 (high lateral root number in clay soil) and PI458020 (thick lateral roots in sandy soil) were found to have higher yield under water-limited conditions [50]. Brazilian cultivars BR-4 and Ocepar 4 were considered as drought-tolerant [111]. Several cultivated germplasm lines (Glycine max) including Williams, Jackson, Prima 2000, Jindou 21(C12), PI416937, PI 427136, PI 408105A, PI 471938, PI 424088, PI 081041, N04-9646, DT51 and R02-1325 have promising performance under water deficit conditions and can be used in breeding program [25, 27, 112, 113].

Genetic variation in soybean germplasm was observed in response to flooding tolerance to overcome yield loss. Elite lines conserve genomic regions that can inhibit extensive yield losses during flooding stress. An experiment was conducted to determine genetic variations using 21 soybean varieties for flooding tolerance in both screen-house and field tests. Three soybean germplasm, Nam Vang from Cambodia, VND2 from China and ATF15-1 from Australia were identified as most flood-tolerant varieties which survived better, grew taller, produced more pods/plants and heavier seed weight as compared to sensitive varieties [114]. A total of 192 soybean germplasm lines were screened for flooding tolerance at seedling stage. Among them, Jangbaegkong, Danbaegkong, Sowonkongkong, Socheong2 and Suwon269 were identified as donor line for flooding tolerance, whereas Shillog, T201, T181, NTS1116 and HP-963 exposed flooding sensitivity [115]. Several cultivated germplasm lines (Glycine max) including PI 408105A, PI 561271, PI 567343, PI 407184, PI603910C, PI 567394B, PI 567651, Archer and Misuzudaiz have been identified as a source of potential source for flooding tolerance [112].

2.3.2. Wild soybean

Wild soybean (Glycine soja), is a valuable genetic resource for the tolerance to water stress by reintroducing alleles. Wild soybean PI 483463 (G. soja) had favourable donor alleles for root angle, while PI 468917 predicted to contribute to slow wilting. Hence, it can be used for development of drought-resistant soybean cultivars [112, 116]. In another study, the wild parent, PI 407162 had favourable alleles for fibrous roots, thus enhancing the soybean ability to survive under drought stress. These studies suggested that it is possible to enhance genetic variation in cultivated soybean by introducing alleles from wild soybeans [117]. For flooding, different wild soybean accessions, PI 467162, PI 479751, PI 407229, PI 597459C, PI 424082, PI 378699A, PI 424107A, PI 366124, PI 378699A were identified, which showed tremendous waterlogging tolerance than G. max [112]. Therefore, wild populations can offer useful in breeding program for improving drought and flooding resistance of soybean.


3. Genetic regulation mechanisms for tolerance to water stress

3.1. Drought tolerance

3.1.1. Genetic and QTL structure of morpho-physiological performance

The application of QTL helps in identification of chromosomal regions, detecting phenotypic variation associated with drought-resistance traits and to determine the desirable alleles at these QLs for marker-assisted breeding. Progress towards the identification of drought-related QTLs is needed [118], only a few QTLs have been reported for drought (Table 2). Du et al. [128] identified 19 QTLs associated with seed yield under normal and water-limited conditions and 10 QTLs associated with drought susceptibility index (DSI) in soybean. To develop drought-tolerant varieties, the role of secondary traits associated with yield stability has been accelerated. In crops, under water deficit condition, several secondary traits i.e. early seedling vigor [129], canopy wilting [119, 130], root system architecture (RSA) [117, 131, 132], canopy temperature depression [133], carbon isotope discrimination [134, 135], alterations in photosynthesis [136, 137], and nitrogen fixation [138, 139, 140, 141] have been reported.

Trait QTL Chro. Marker R2 Population Ref.
Canopy wilting Gm02-1 2 ss107913715 0.06–0.12 KJ, BP [119]
Gm02-2 2 ss107912946/satt296 0.06–0.18 AP [119, 120]
Gm02-3 2 Satt296 0.06–0.19 BP, AP [119]
qSW-Gm04 4 Satt646 0.09 BP [120]
Gm05 5 ss107913925/satt276 0.04–0.16 KJ [119, 120]
Gm08 8 Satt177 0.05–0.15 KJ, KN [119, 121]
Leaf wilting Gm09 9 Sat044 0.17 Jackson ×KS4895 [122]
Canopy wilting Gm11 11 ss107913507 0.14–0.39 KJ, KP, AP [119]
qSW-Gm12 12 Satt302 0.27 BP [120]
Gm13 13 Satt362 0.16 KJ [121]
Gm14 14 ss107913401 0.08–0.12 KJ,AP [119, 121]
qSW-Gm17/Gm17–1 17 ss107929993 0.06–0.22 KJ,AP, BP [119, 120, 121]
Gm17-2 17 ss107913610 0.09–0.10 KJ, KP [119]
qSW-Gm19 19 ss107924069 0.11–0.29 KJ, KP, BP [119]
Yield Gm06 6 Satt205-satt489 0.7 Minsoy ×Noir 1 [123]
Yield and wilting Gm13 13 Sat_375 Hutcheson × PI471938, [124]
Gm13-1 13 Sat_074
Gm17 17 Satt226
Water use efficiency Gm19 19 A489H 0.14 S-100 × Tokyo [125]
A063-1 0.8
Gm18 18 B031-1 8.5 Young ×PI416937 [126]
Gm12 12 A089-1 8.7
Gm16 16 cr497-1 13.2
Gm16 16 K375-1 7.5
Gm4 4 A063-1 5
Nitrogen fixation (shoot ureide) Gm09 9 BARC-060299-16,598 0.16 KS4895 × Jackson [127]
Gm19 19 Satt561 0.18
Gm13 13 BARC-014657-01608 0.24
Gm17 17 BARC-057467-14,765 0.12

Table 2.

A list of reported QTLs in soybean associated with drought tolerance.

KJ = KS4895 × Jackson; BP = Benning × PI 416937; AP = A5959 × PI 416937; KP = KS4895 × PI 424140; KN = Kefeng1 × Nannong1138-2.

In soybean, RSAs, slow canopy wilting and biological nitrogen fixation are promising secondary traits under drought [112]. Under water deficit conditions, a simulation analysis model depicted that slow wilting can improve soybean yield >75% while nitrogen fixation up to 85% [142]. In soybean, less information is available on QTL mapping of drought-associated traits and yield [128, 143], fibrous roots [144] and water-use efficiency (WUE) [123, 125, 126] under water-limited conditions. Several studies have been conducted on QTL mapping for RSA traits in major cereals crops with little information in leguminous crops, especially soybean [145, 146, 147]. Five QTLs were identified on chromosomes 1, 3, 4, 8, and 20 related with fibrous rooting systems in RIL population of soybean derived from a cross between Benning (low fibrous root) and PI 416937 (extensive fibrous root) [144]. These QTLs were detected by using 240 F6 derived recombinant inbred lines (RILs) under rain-fed conditions for 2 years (2001 and 2009). The parent PI 416937 (extensive fibrous root system) contributed favourable alleles for four QTLs, while one QTL had donor alleles from Benning. Moreover, a total of four QTLs related with root surface area and distribution (based on root length and thickness) were identified in an inter-specific mapping population (Glycine max × Glycine soja). Two QTLs on Chr 6 had favourable donor alleles from the wild parent, PI 407162 (G. soja) with R2 value of >10%. As a result, plants enhanced their ability to form fibrous roots. Manavalan et al. [148] identified one QTL cluster associated with root length and lateral root number in 251 BC2F5 backcross inbred lines through linkage mapping with favourable alleles from Dunbar (Table 2).

Slow canopy wilting is a key factor to screen soybean germplasm under water-limited conditions [121]. A total of 13 QTLs associated with slow wilting were detected using five bi-parental populations under water-limited conditions, with phenotypic variation (R2 0.04–0.29). Eleven out of 13 QTLs had favourable alleles from PI 416937 and Jackson [119, 120, 121]. The major QTL associated with slow wilting was mapped on LG K with 17% phenotypic variation [122]. To validate QTL data from different mapping population on same linkage map, ‘Meta-QTL analysis’ has been proposed [149, 150]. In soybean, Meta-QTL analysis was used to refine the confidence interval of eight QTLs using mapping results from five bi-parental population However, these QTLs are complex, unstable and quantitative nature, so breeders find difficulties to utilize them [151]. Considering this problem, confirmation of QTL should be performed by using more advanced progeny or near isogenic lines (BCnF2).

Studies on QTL mapping associated with biological-nitrogen fixation are very few in plants including soybean. Three QTLs for nodule number (LGs B1, E) were identified using the composite interval mapping and explained 13% phenotypic variation [152]. Two QTLs for shoot ureide were detected on Chrs. 9 and 19, and two QTLs associated with shoot nitrogen concentration were mapped on Chrs. 13 and 17 under water stress. These QTLs explained phenotypic variation ranging from 0.11 to 0.31 (Table 2) [127]. Jackson contributed favourable alleles for shoot ureide concentration on Gm 19 and Gm 13 while other two on Gm 09 and Gm17 have favourable alleles from KS4895. Under well-watered conditions, a number of QTLs associated with shoot ureide and nitrogen concentrations were reported. However, not a single QTL was detected under both conditions (stress and control) illustrating that soybean shows diverse mechanisms for regulation of N2-fixation under well-watered and drought conditions [127].

3.1.2. Identification of important genes for drought tolerance

Drought stress-responsive genes are categorized as effectors and regulatory genes [153]. Effectors include gene encoding protein such as LEA proteins, osmolyte biosynthesis (osmotin), aquaporins, chaperons, antioxidants and enzymes involved in different metabolic pathway. Regulatory genes encoding product such as receptors, calmodulin-binding proteins, kinases, phosphatases and transcription factors are involved in signal transduction and gene expression [153]. A number of plant TFs such as ethylene-responsive factor, WRKY, MYB, basic leucine zipper domain (bZIP) and NAC are involved in ABA signalling under drought stress, while dehydration responsible element binding (DREB) protein, are involved in ABA-independent pathway [154, 155, 156]. Major families of TF genes expressed in response to drought stress in plants are summarized in Table 3.

Gene family Gene Studied plant Ref.
R2R3-MYB transcription factor GmMYB84 Soybean [157]
GmMYBJ1 Arabidopsis [158]
bZIP transcription factor GmFDL19 Soybean [159]
GmbZIP1 Arabidopsis [160]
DREB transcription factor GmDREB2 Tobacco [161]
AP2/ERF transcription factor GmDREB2A;2 Soybean [162]
AP2/ERF transcription factor GmERF3 Tobacco [163]
AP2/ERF transcription factor GmERF4 Tobacco [164]
WRKY family GmWRKY54 Arabidopsis [156]
WRKY family GsWRKY20 Arabidopsis [165]
NAC family GmNAC20 Soybean [166]
Homeodomainleucine zipper (HD-Zip) proteins Multiple HD-Zip genes Soybean [167]
C2H2-type Zinc finger protein GmZFP3 Arabidopsis [168]
Trihelix transcription factors GmGT-2B b Arabidopsis [169]
GmGT-2A Arabidopsis

Table 3.

Major families of TF genes expressed in response to drought stress in plants.

In the soybean genome, 5035 TFs models were identified based on in-silico annotation [170]. Among all TFs, the WRKY transcription factor is the largest family in plants. A total of 233 WRKY members have been identified in soybean ( fam=WRKY) [171]. Identification of two WRKY genes (GmWRKY21 and GmWRKY54) and their role in enhancing tolerance to drought, salt and cold has been studied in Arabidopsis [156]. Moreover, the involvement of GmWRKY27 has been characterized under drought and salt stress. Overexpression of GmWRKY27 RNAi and GmWRKY27 in soybeans results in increased tolerance and hypersensitivity to drought and salt stress, respectively. In the same study, the association of GmWRKY27 with GmMYB174 was observed, which binds to neighbouring cis-elements in GmNAC29 promoter and suppressed gene expression of GmNAC29 led to increased tolerance to abiotic stress [172]. In soybean, novel candidates of WRKY genes were detected, which provided the unique function of WRKY transcription factors under water deficit conditions [173].

Another gene family, Homeodomain-leucine zipper (HD-Zip) comprised of 140 HD-Zip genes ( were detected under drought and salt stress. Out of 140, 59 are coding genes while 20 paralogous genes exhibited differential expression under drought and saline environment [174]. In soybean, overexpression of GmDREB3 also enhances tolerance drought tolerance in response to accumulation of proline [175].

3.2. Flooding tolerance

3.2.1. QTL mapping

In recent years, the advent of molecular marker technologies has opened up new opportunities for QTL analyses, fine mapping and cloning of genes for water stress tolerance. The genetic basis of drought and flooding tolerance has been studied by evaluating different component traits in drought and flood-tolerant soybean. Both drought and flooding tolerance are quantitatively inherited and controlled by several genetic loci. Consequently, a large number of QTLs related to flooding tolerance are summarized in Table 4.

Trait QTL Chro. Marker Population Ref.
Grain yield Gm18 18 Sat_064 Archer × Minsoy, Archer × Noir I [176]
Injury score, tolerance index Gm5, Gm13 5, 13 Satt385, Satt269 A5403 × Archer, P9641 × Archer [177]
Flooding tolerance ft1 6 Satt100 Misuzudaizu × Gong 503 [178]
Seed germination Sft1, Sft2 12, 8 Sat_175, Satt 187 Peking × Tamahomare [91]
Sft3, Sft4 4, 2 Satt 338, Sat_279
Flooding toleranceand/or resistance to P. sojae FTS-13 13 Sct_033, BARC-024569-4982 PI 408105A × S99-2281 [179]
FTS-11 11 BARC-016279-02316
Joint waterlogging tolerance index Wt1,wt2 19 Satt229-Satt527 Satt527-Sat_286 Su88-M21 × Xinyixiaoheidou [180]
Root length development/Root surface area Qhti-12-1 12 Satt052-Satt302 Iyodaizu × Tachinagaha [181]

Table 4.

A summary of QTL mapping studies for flood tolerance traits in soybean.

The analysis of quantitative trait loci (QTLs) for water-logging tolerance in soybean is usually challenging. However, several studies have been done on QTLs associated to flooding tolerance, focused on injury score and tolerance index in soybean [91, 176, 177, 178, 179, 182]. For instance, a single QTL located on Chr. 18 (Sat_064) was identified using 208 lines of two recombinant inbred (RI) populations, for soybean growth and grain yields under water-logging conditions [176]. The results indicated that the Sat_064 QTL is unique in response to flooding. The Sat_064 QTL was further confirmed in a southern cultivar Archer using near-isogenic lines (NILs) [183]. In addition, two flooding-tolerance QTLs on Chr. 5 (Satt385) and Chr.13 (Satt269) were identified associated with water-logging tolerance through partial linkage mapping and bulk-segregation analysis using two populations [177]. Seven loci were detected associated with yield in response to flooding in a mapping population between Misuzudaizu and Moshidou Gong 503. Among them, only a large and stable QTL, ft1 tightly linked with flowering was reproducible with high LOD score in 2 years, 2012 and 2013 (15.41 and 7.57) [178].

In another experiment, four QTLs, Sft1, Sft2, Sft3 and Sft4 associated with seed-flooding tolerance, during geminating stage, were detected using population derived from cross between a tolerant ‘Peking’ (black seed coat) × susceptible cultivar ‘Tamahomare’ (yellow seed coat). Among these QTLs, Sft1 located on Chr.12 had great effect on germination rate, whereas sft2 mapped on Chr. 8 had contribution in seed coat pigmentation [91]. Two QTLs, FTS-11 and FTS-13 were mapped on Chr. 11 and Chr.13, respectively, using F7 recombinant inbred lines (RILs) at an early reproductive stage. These QTLs were also related with flooding yield index and flooding injury score. The major QTL FTS-13, with phenotypic variation 18.3% was detected in multiple locations and years [179]. Recently, QTLs for root surface area development (RSAD) and root length development (RLD) on Chr. 12 (between markers Satt052 and Satt302) were identified in relation to hypoxia tolerance using F8:9 RILs derived from a cross between Iyodaizu and Tachinagaha in soybean. For the validation of these major and stable QTLs, NILs with the QTL region were developed derived from Iyodaizu [181].

3.2.2. Transcriptome analysis of soybean under water stress

Transcript abundance analysis is vital functional genomics tools to examine flooding responsive mechanisms and identify genes responsible for flooding tolerance. Recently, genome-wide changes associated with gene-expression are investigated through microarray chip analysis, RNA-seq approach and high-coverage gene expression profiling analysis for better understanding the transcriptional response in relation to flooding stress in soybean (Table 5). Transcripts were examined in the root tip, including the hypocotyl of soybean, using high-coverage gene expression profiling analysis; 5831 out of 29,388 were significantly altered under water stress. Genes relevant to ethylene biosynthesis, alcoholic fermentation and cell wall relaxation are promptly up-regulated in response to flooding. Defence-related genes, haemoglobin, and Kunitz trypsin protease inhibitor and acid phosphatase are responsible for flooding [184].

Stress Tissues Platform DEG*/proteins characterized Ref
Flooding Root and hypocotyl High coverage expression profiling 97 genes and 34 proteins [184]
Flooding Roots including hypocotyl Soybean microarray chip More than 6000 genes [185]
Drought & flooding Leaf tissue Illumina Genome Analyzer (San Die go, CA) platform 2724 genes for drought and 3498 genes for flooding, 289 Transcription Factors [186]
Flooding stress Root tips, root with hypocotyl and cotyledons RNA sequencing-based transcriptomic analysis 31 genes [187]
Drought & flooding Leaf, hypocotyl, and root Gel-free/label-free proteomic technique 17 proteins [188]
Drought & flooding Roots Gel-free proteomic technique 97 proteins in response to flooding and 48 proteins for drought [189]
Drought & flooding Root tip Gel-free/label-free proteomic analysis Three S-adenosylmethionine synthetases (SAMs) proteins [190]
Flooding Root and cotyledon Nano spray LTQ XL Orbitrap mass spectrometry (MS) 146 proteins [191]
Flooding & drought Roots Gel-free proteomic technique 97 proteins to flooding, 48 for drought [189]

Table 5.

Soybean transcriptome and proteome studies under flooding and drought stress.

*Differentially Expressed Gene.

In another study, soybean microarray chip-based transcriptomics technique was used to comprehend the molecular response under flooding. In soybean roots including hypocotyl, more than 6000 flooding-responsive genes were identified. The results revealed that genes associated with glycolysis, photosynthesis, amino acid synthesis (Ser-Gly-Cys group), transcriptional regulation of transcription, degradation of ubiquitin-mediated protein, and cell death were expressively up-regulated, whereas genes relevant to cell organization, secondary metabolism, cell wall synthesis, transport of metabolite and chromatin structure were considerably down-regulated. Furthermore, up-regulation of flooding-responsive genes encoding small proteins plays key roles in acclimation to flooding [185]. It has been reported that a total of 2724 and 3498 genes were differentially expressed in response to drought and flooding stress, respectively, which contain 289 TFs demonstrating ethylene response factors (ERFs), basic helix-loop helix (bHLH), WRKY amino acid motif (WRKY), myeloblastosis (MYB) and no apical meristem (NAC) are involved in stress tolerance mechanism [186].

RNA-seq based transcriptomic analysis resulted in detection of 729 and 255 genes in the flooding-tolerant line and ABA-treated soybean, respectively, which were significantly changed under stress condition. Transcript profiles also revealed that a total of 31 genes included 12 genes involved in the regulation of RNA and protein metabolism were commonly altered between the flooding-tolerant line and ABA-treated soybean under flooding stress [187]. On the basis of the above findings, it can be concluded that transcript profiles can be helpful as an adaptive mechanism for soybean survival under water stress.

3.2.3. Proteomics techniques for identification of water stress-responsive mechanisms

Different proteomics techniques i.e. mass spectroscopy (MS)-based (for identification of a number of environmental stress-responsive proteins), two-dimensional (2D) gel-based (for visual illustration of the proteins) and SDS gel or gel free-based (for detection of the largest number of proteins) are extensively used under water stress (Table 5). The available genomic information in soybean genome database helps to identify water stress-responsive mechanism. Distinct changes in the soybean proteome during water stress lead to different defence mechanisms. Several studies evidently revealed that some proteins regulating sucrose accumulation, glucose degradation, cell wall relaxing, signal transduction and alcohol fermentation were altered under flooding stress [192, 193]. Flooding stress reduced the differential regulation of proteins involved in maintaining the structure of cell and protein folding [99]. Moreover, the application of exogenous calcium on flooded soybeans up-regulated the lipid metabolism, signalling-related proteins, glycolysis-related proteins and fermentation in roots [189]. A reduction in calcium oxalate crystals was found in cotyledon under flooding [188].

Wang et al. identified three S-adenosylmethionine synthetases (SAMs) proteins using gel-free proteomic analysis under water stress in soybean. The SAMs action declined at early-stage flooding but increased in hypocotyls and roots under water deficit. The results recommended that SAMs were involved in response to water stress and it might affect ethylene biosynthesis in soybean. The action of SAMs was different in hypocotyls, root tips and roots under water stress. The down-regulation of SAMs 1 and SAMs 2 were observed in roots under drought and flooding. Moreover, up-regulation of ACC synthase was examined under drought, whereas the expression was down-regulated in root tips under flooding. However, ACC oxidase was increased under both stresses. These findings indicate that SAMs have key role in ethylene biosynthesis in soybean [194]. A quantitative proteomics study has been conducted for the better understanding of flooding responsive mechanisms using flooding-tolerant mutant and abscisic acid (ABA)-treated soybean. A total of 146 proteins were usually altered at the early stage of flooding. Proteins related to protein synthesis such as nascent polypeptide-related complex and chaperonin 20, and RNA regulation-associated proteins were up-regulated both at protein and mRNA expression. However, these identified proteins at early stage of flooding were not meaningfully altered. This study suggested that proteins associated with protein synthesis and RNA regulation can influence in triggering tolerance to flooding stress [195]. Therefore, proteomic approaches can be used to understand the response mechanism to drought and flooding stress at the initial stage of soybean growth.


4. Improvement of soybean tolerance to drought and flooding stress

4.1. Breeding objectives and progress of conventional breeding

The objective of soybean breeding programs is to develop cultivars with enhanced yield (more pods/plant, more seeds/pod, 100-seed weight), seed composition (high protein and oil contents), shattering resistance and tolerance to abiotic and biotic stress. Many important agronomic traits (qualitative or simply inherited) are incorporated into commercial cultivar through conventional breeding. As drought and flooding are complex quantitative traits, breeders face difficulties to improve these traits through conventional breeding. Moreover, conventional breeding is tedious, labour extensive, requires a considerable time (8–9 years) and a large amount of space for evaluation. For example, in China, Jindou 21 is an excellent example of drought-tolerant cultivar developed through selective breeding. Initially, Lin Xian White (higher drought tolerance, low yield soybean cultivar) was crossed with Jindou 2 (drought tolerant and high yield). After six generations, the resulting drought line was selected and further crossed with jindou14. Finally, Jindou 21 was developed after 7 years of selection in arid region of western Shanxi and depicted increased yield under water stress [196]. Xu et al. also identified 463 Chinese strains having high level of drought tolerance through breeding. These strains could be used as a potential source for enhancing drought resistance in soybean [197]. Development of RILs population for flooding tolerance is a long and tedious process. For example, in soybean, to develop F7 population by crossing S992281 X PI4081051 (high yield, flooding tolerant) via single-seed descent method requires 7 years. Hence, conventional breeding approach is less useful [179].

4.2. QTL mapping and marker-assisted selection

To deal with complex nature of drought and flooding, marker-assisted selection to identify QTL can be used as a promising approach. Time consuming phenotypic characterization of large population to get an effective QTL is a major challenge to improve agronomic traits associated with drought and flooding tolerance. If molecular markers are closely linked to the target QTL, it would be possible to transfer character into commercial cultivar through marker-assisted breeding. Marker-assisted selection can be effectively used in soybean having high linkage disequilibrium (low recombinant frequency) [198]. For example, four QTLs associated with root morphology were detected by using 629 SSR markers, indicating that fibrous roots QTL may be related with drought tolerance and seed yield in soybean [144]. In another study, three QTLs for flooding tolerance were detected using 360 SSR markers in soybean. Among three QTLs, one major QTL exhibited large impact on flooding tolerance environments [178].

4.3. Genetic engineering

Genetic engineering in the twenty-first century is a perquisite tool in cell and molecular biology that will provide additional approaches for genetic modification by overexpression or gene silencing, protein sub-cellular localization, transposon mutagenesis and promoter characterization for permitting the development of novel and genetically diverse genotypes. These techniques have become profound strategies in soybean breeding which provide unique chances to modify the genetic makeup of soybean. Recent advancement in genetic mapping and the identification of new drought and flooding stress-responsive genes from various organisms allow researchers to modify plants using several genetic strategies. Genetic transformation in soybean was first reported in 1988 [199, 200], but the stable transformation of soybeans is still a challenging task. Several studies reported on soybean transformation by Agrobacterium-mediated transformation and particle bombardment methods [201, 202]. Both approaches have been used successfully for genetic transformation of soybean. The success is mainly dependent on the efficient delivery of transforming DNA and the recovery of transgenic lines from a transformed cell. Transgenic soybean expressing GMFDL19 gene enhanced tolerance towards drought stress [159] .

4.4. Other new breeding techniques

Over the past 20 years, several new breeding techniques have been developed and are being implemented to facilitate breeding for the crop improvement. New breeding techniques (NBTs) give the ability to accurately modify DNA by editing DNA and genes on or off. Gene or genome editing including CRISPR/Cas9 is a broad category that offers an inexpensive, quick and easy technique to manipulate DNA and lessen the time and effort as compared to traditional breeding. Now-a-days, researchers are working on CRISPR/Cas9-edited versions to improve the different crops such as soybeans, rice, corn, canola and wheat with new traits like drought and flooding resistance and higher yields. Recently, various new plant breeding techniques such as zinc finger nuclease (ZFN) technology, acetate-mediated approach, oligonucleotide-directed mutagenesis (ODM), RNA-dependent DNA methylation (RdDM), cisgenesis, intragenesis, grafting (on GM rootstock) and reverse breeding allow the faster and more efficient improvement of crop varieties.

4.5. Agronomic practices to mitigate the effects of water stress

Agronomic practices can be mitigated the adverse effects of drought and flooding stresses by adopting various strategies. Seed priming is an effective and pragmatic technique to mitigate drought in which seeds are moderately hydrated. In this technique, germination rate, germination percentage and germination uniformity of primed seed increased [11, 203]. This approach has been useful to counteract the effects of drought stress in a range of crop species. Foliar application of plant growth regulators is another technique for improving growth against drought stress. Exogenously applied abscisic acid, uniconazole and brassinolide increased yields both under well-watered and drought conditions in soybean. Plant growth regulator treatments meaningfully increased water potential and chlorophyll contents under water stress conditions [204]. Traditional irrigation system causes >50% loss of irrigated water because of uncovered and unlined ditches. Therefore, a well-managed pipe system is required to avoid losses from traditional irrigation system as it can enhance the conveyance efficiency >90% [205]. Mulching involving covering of soil by using straw or plastic sheets, is another best strategy to retain moisture in soil. For instance, in China, soybean yield increased up to 23.4 and 50.6% by using mulching along with hole sowing and row sowing, respectively [206].

Several management practices have been tried to overcome completely or partially flooding injuries. Flooding induces nitrogen deficiencies resulting in a significant decrease in the uptake of nitrogen. As a result, yellowing of leaves occurred following 2–3 days of flooding. It has been reported that the application of nitrogen fertilizer i.e. polymer-coated urea (PCU) is effective to reduce nitrogen loss and recover flood damage in corn. It also helps to overcome oxygen deficiency in response to flooding stress preferentially [207]. Hypoxia also reduces the capacity of plant to absorb potassium (K). K plays a vital role in alleviating both biotic and abiotic stresses [208]. Indeed, K+ ions are involved in detoxification of ammonium and ammonia [209], promoting photosynthesis which helps plant recovery and nutrient uptake. Foliar and soil applications oxygen-containing fertilizers lessen the drastic effects of flooding stress [210]. For example, under flooding, oxygen-containing fertilizers considerably retained chlorophyll content and biomass in Italian basil [211].

Under flooding stress, 1-aminocyclopropane-1-carboxylate (ACC) synthase enzyme along with several stress proteins were synthesized [212].The stressed plant consequently produces more ACC in their roots. In roots, ACC cannot be converted into ethylene due to insufficient oxygen. This ACC transferred from roots to shoots converting ACC to ethylene (sufficient oxygen environment) in shoots [213]. In soybean, phytohormone indole acetic acid (IAA) prompts the production of ethylene which prevents the inhibitory effects of high IAA on root growth [214]. Elevation in ethylene production by waterlogged plants results in wilting, necrosis, chlorosis and reduced biomass yield. The application of ACC deaminase-producing plant growth-promoting rhizobacteria (PGPR) can protect plants from these damages [215, 216]. PGPR produce ACC deaminase, which converts ACC into α-ketobutyrate and ammonia, thus reducing the levels of ethylene under water stress conditions. A combination of PGPRs, along with arbuscular mycorrhizal (AM) fungi, including ACC deaminase-producing bacteria, Pseudomonas, Azospirillum, Rhizobium and Bradyrhizobium, could be a novel step in the alleviation of flooding-impacted plants.


5. Conclusions

Water stress has become major abiotic limitation factor on soybean production under warming climate. To combat drought and flooding stress, there is need to explore the resilient genetic resources and their utilization in breeding program. With the advancement in transcriptomics, proteomics, metabolomics, structural genomics and epigenetics, the production of soybean can be enhanced under water stress by integrating all disciplines. Recent advances in breeding system and agronomic practices will offer an opportunity for significant and predictable incremental improvements in soybean under water stress.



This work is supported by the National Key R & D Program for Crop Breeding (2016YFD0100201), the Natural Science Foundation of China (31571691, 31771821), the MOE Program for Changjiang Scholars and Innovative Research Team in University (IRT_17R55), and the Jiangsu JCIC-MCP program.


  1. 1. Wilcox JR. World distribution and trade of soybean. In: Boerma HG, Specht JE, editors. Soybeans: Improvement, Production, and Uses. Vol. 16. Agronomy Monographs. 3rd ed. Madison, WI, USA: ASA-CSSA-SSSA; 2004. pp. 1-14
  2. 2. Koberg M, Abu-Much R, Gedanken A. Optimization of bio-diesel production from soybean and wastes of cooked oil: Combining dielectric microwave irradiation and a SrO catalyst. Bioresource Technology. 2011;102:1073-1078. DOI: 10.1016/j.biortech.2010.08.055
  3. 3. Jooyandeh H. Soy products as healthy and functional foods. Middle-East Journal of Scientific Research. 2011;7:71-80
  4. 4. Goldsmith PD. Economics of soybean production, marketing and utilization. In: Johnson LA, White PJ, Galloway R, editors. Soybeans: Chemistry, Production Processing and Utilization. Urbana: AOCS Press; 2008. pp. 117-150
  5. 5. Boyer JS. Plant productivity and environment. Science. 1982;218:443-448. DOI: 10.1126/science.218.4571.443
  6. 6. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al. Extinction risk from climate change. Nature. 2004;427:145-148. DOI: 10.1038/nature02121
  7. 7. Ahmed F, Rafii M, Ismail MR, Juraimi AS, Rahim H, Asfaliza R, et al. Waterlogging tolerance of crops: Breeding, mechanism of tolerance, molecular approaches, and future prospects. BioMed Research International. 2013;2013:1-10. DOI: 10.1155/2013/963525
  8. 8. Valliyodan B, Nguyen HT. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinion in Plant Biology. 2006;9:189-195. DOI: 10.1016/j.pbi.2006.01.019
  9. 9. Szilagyi L. Influence of drought on seed yield components in common bean. Bulgarian Journal of Plant Physiology 2003;2003:320-330
  10. 10. Hirt H, Shinozaki K. Topics in Current Genetics, Plant Responses to Abiotic Stress. Heildelberg: Springer Science & Business Media Berlin; 2004
  11. 11. Kaya MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı Ö. Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). European Journal of Agronomy. 2006;24:291-295. DOI: 10.1016/j.eja.2005.08.001
  12. 12. Okçu G, Kaya MD, Atak M. Effects of salt and drought stresses on germination and seedling growth of pea (Pisum sativum L.). Turkish Journal of Agriculture and Forestry. 2005;29:237-242
  13. 13. Zeid I, Shedeed Z. Response of alfalfa to putrescine treatment under drought stress. Biologia Plantarum. 2006;50:635-640. DOI: 10.1007/s10535-006-0099-9
  14. 14. Boyer JS. Subcellular mechanisms of plant response to low water potential. Agricultural Water Management. 1983;7:239-248. DOI: 10.1016/0378-3774(83)90087-2
  15. 15. Turner NC, Wright GC, Siddique K. Adaptation of grain legumes (pulses) to water-limited environments. Advances in Agronomy. 2001;71:193-231. DOI: 10.1016/S0065-2113[01]71015-2
  16. 16. Boerma HR, Specht JE. Soybeans: improvement, production and uses. Agronomy Monographs. Vol. 16, 3rd ed. Madison, WI, USA: ASA-CSSA-SSSA; 2004
  17. 17. Purcell LC, Specht JE. Physiological traits for ameliorating drought stress. In: Boerma HG, Specht JE, editors. Soybeans: Improvement, Production, and Uses. Vol. 16. Agronomy Monographs. 3rd ed. Madison, WI, USA: ASA-CSSA-SSSA; 2004. pp. 559-620. DOI: 10.2134/agronmonogr16.3ed.c12
  18. 18. Kavar T, Maras M, Kidrič M, Šuštar-Vozlič J, Meglič V. Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Molecular Breeding. 2008;21:159-172. DOI: 10.1007/s11032-007-9116-8
  19. 19. Nguyen HT, Babu RC, Blum A. Breeding for drought resistance in rice: Physiology and molecular genetics considerations. Crop Science. 1997;37:1426-1434. DOI: 10.2135/cropsci1997.0011183X003700050002x
  20. 20. Mittler R. Abiotic stress, the field environment and stress combination. Trends in Plant Science. 2006;11:15-19. DOI: 10.1016/j.tplants.2005.11.002
  21. 21. Valliyodan B, Van Toai TT, Alves JD, de Fátima P, Goulart P, Lee JD, Fritschi FB, et al. Expression of root-related transcription factors associated with flooding tolerance of soybean (Glycine max). International Journal of Molecular Sciences. 2014;15:17622-17643. DOI: 10.3390/ijms151017622
  22. 22. Kokubun M. Genetic and cultural improvement of soybean for waterlogged conditions in Asia. Field Crops Research. 2013;152:3-7. DOI: 10.1016/j.fcr.2012.09.022
  23. 23. Kosturkova G, Todorova R, Sakthivelu G, Akitha Devi M, Giridhar P, Rajasekaran T, et al. Response of bulgarian and indian soybean genotypes to drought and water deficiency in field and laboratory conditions. General and Applied Plant Physiology. 2008;34:239-250
  24. 24. Rasaei B, Ghobadi M-E, Khas-Amiri M, Ghobadi M. Effect of osmotic potential on germination and seedling characteristics of soybean seeds. International Journal of Agriculture and Crop Sciences. 2013;5:1265
  25. 25. Hossain MM, Liu X, Qi X, Lam H-M, Zhang J. Differences between soybean genotypes in physiological response to sequential soil drying and rewetting. The Crop Journal. 2014;2:366-380
  26. 26. Hossain MM, Lam H-M, Zhang J. Responses in gas exchange and water status between drought-tolerant and-susceptible soybean genotypes with ABA application. The Crop Journal. 2015;3:500-506. DOI: 10.1016/j.cj.2014.08.001
  27. 27. Fenta BA, Beebe SE, Kunert KJ, Burridge JD, Barlow KM, Lynch JP, et al. Field phenotyping of soybean roots for drought stress tolerance. Agronomy. 2014;4:418-435. DOI: 10.3390/Agronomy4030418
  28. 28. Sepanlo N, Talebi R, Rokhzadi A, Mohammadi H. Morphological and physiological behavior in soybean (Glycine max) genotypes to drought stress implemented at pre-and post-anthesis stages. Acta Biologica Szegediensis. 2014;58:109-113
  29. 29. Kobraei S, Etminan A, Mohammadi R, Kobraee S. Effects of drought stress on yield and yield components of soybean. Annals of Biological Research. 2011;2:504-509
  30. 30. Kobraee S, Shamsi K, Rasekhi B. Soybean production under water deficit conditions. Annals of Biological Research. 2011;2:423-434
  31. 31. Prince SJ, Murphy M, Mutava RN, Durnell LA, Valliyodan B, Shannon JG, et al. Root xylem plasticity to improve water use and yield in water-stressed soybean. Journal of Experimental Botany. 2017;68:2027-2036. DOI: 10.1093/jxb/erw472
  32. 32. Chowdhury J, Karim M, Khaliq Q, Solaiman A, Ahmed J. Screening of soybean (Glycine max L.) genotypes under water stress condition. Bangladesh Journal of Agricultural Research. 2016;41:441-450. DOI: 10.3329/bjar.v41i3.29716
  33. 33. Shimamura S, Mochizuki T, Nada Y, Fukuyama M. Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean (Glycine max) under flooded conditions. Plant and Soil. 2003;251:351-359. DOI: 10.1023/A:1023036720537
  34. 34. Henshaw T, Gilbert R, Scholberg J, Sinclair T. Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: I. Root and nodule development. Journal of Agronomy and Crop Science. 2007;193:177-188. DOI: 10.1111/j.1439-037X.2007.00257.x
  35. 35. Henshaw T, Gilbert R, Scholberg J, Sinclair T. Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: II. Aboveground growth and biomass. Journal of Agronomy and Crop Science. 2007;193:189-197. DOI: 10.1111/j.1439-037X.2007.00258.x
  36. 36. Oh K-W, Lim S-G, Kim S-R, Ko J-M, Han W-Y, Kim H-T, et al. Flooding affects root morphology and photosynthesis in soybean (Glycine max [L.] Merr.). Journal of the Korean Society of the Crop Science. 2008;120:1
  37. 37. Sakazono S, Nagata T, Matsuo R, Kajihara S, Watanabe M, Ishimoto M, et al. Variation in root development response to flooding among 92 soybean lines during early growth stages. Plant Production Science. 2014;17:228-236. DOI: 10.1626/pps.17.228
  38. 38. Borella J, do Amarante L, de Oliveira, DDC, de Oliveira, ACB, Braga EJB. Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes. Scientia Agricola 2014;71:499-508. DOI: 10.1590/0103-9016-2014-0044
  39. 39. Nguyen VL, Binh VT, Hoang DT, Mochizuki T, Nguyen VL. Genotypic variation in morphological and physiological response of soybean to waterlogging at flowering stage. International Journal of Agricultural Science Research. 2015;4:150-157
  40. 40. Suematsu K, Abiko T, Nguyen VL, Mochizuki T. Phenotypic variation in root development of 162 soybean accessions under hypoxia condition at the seedling stage. Plant Production Science. 2017;20:323-335. DOI: 10.1080/1343943X.2017.1334511
  41. 41. Oosterhuis D, Scott H, Hampton R, Wullschleger S. Physiological responses of two soybean (Glycine max [L.] Merr) cultivars to short-term flooding. Environmental and Experimental Botany. 1990;30:85-92
  42. 42. Colmer T, Voesenek L. Flooding tolerance: Suites of plant traits in variable environments. Functional Plant Biology. 2009;36:665-681. DOI: 10.1016/0098-8472[90]90012-S
  43. 43. van Veen H, Mustroph A, Barding GA, Vergeer-van Eijk M, Welschen-Evertman RA, Pedersen O, et al. Two Rumex species from contrasting hydrological niches regulate flooding tolerance through distinct mechanisms. The Plant Cell. 2013;25:4691-6707. DOI: 10.1105/tpc.113.119016
  44. 44. Bailey-Serres J, Voesenek L. Flooding stress: Acclimations and genetic diversity. Annual Review of Plant Biology. 2008;59:313-339. DOI: 10.1146/annurev.arplant.59.032607.092752
  45. 45. Bengough AG, McKenzie B, Hallett P, Valentine T. Root elongation, water stress, and mechanical impedance: A review of limiting stresses and beneficial root tip traits. Journal of Experimental Botany. 2011;62:59-68. DOI: 10.1093/jxb/erq350
  46. 46. Fehr WR, Caviness CE, Burmood D, Pennington J. Stage of development descriptions for soybeans, Glycine max [L.] Merrill. Crop Science. 1971;11:929-931
  47. 47. Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, et al. Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. Journal of Experimental Botany. 2014;65:1497-1512. DOI: 10.1093/jxb/eru014
  48. 48. Vadez V. Root hydraulics: The forgotten side of roots in drought adaptation. Field Crops Research. 2014;165:15-24. DOI: 10.1016/j.fcr.2014.03.017
  49. 49. Serraj R, Bona S, Purcell LC, Sinclair TR. Nitrogen accumulation and nodule activity of field-grown ‘Jackson’soybean in response to water deficits. Field Crops Research. 1997;52:109-116. DOI: 10.1016/S0378-4290[96]01068-4
  50. 50. Prince SJ, Murphy M, Mutava RN, Zhang Z, Nguyen N, Kim YH, et al. Evaluation of high yielding soybean germplasm under water limitation. Journal of Integrative Plant Biology. 2016;58:475-491. DOI: 10.1111/jipb.12378
  51. 51. Garay A, Wilhelm W. Root system characteristics of two soybean isolines undergoing water stress conditions. Agronomy Journal. 1983;75:973-977. DOI: 10.2134/agronj1983.00021962007500060026x
  52. 52. Liu Y, Gai J-Y, Lu H, Wang Y-J, Chen S-Y. Identification of drought tolerant germplasm and inheritance and QTL mapping of related root traits in soybean (Glycine max [L.] Merr). Acta Genetica Sinica. 2005;32:855-863
  53. 53. He J, Jin Y, Y-L D, Wang T, Turner NC, Yang R-P, et al. Genotypic variation in yield, yield components, root morphology and architecture, in soybean in relation to water and phosphorus supply. Frontiers in Plant Science. 2017;8:1499. DOI: 10.3389/fpls.2017.01499
  54. 54. Liu F, Andersen MN, Jensen CR. Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Functional Plant Biology. 2003;30:271-280. DOI: 10.1071/FP02185
  55. 55. Stolf-Moreira R, Medri M, Neumaier N, Lemos N, Pimenta J, Tobita S, et al. Soybean physiology and gene expression during drought. Genetics and Molecular Research. 2010;9:1946-1956. DOI: 10.4238/vol9-4gmr851
  56. 56. Laan P, Berrevoets M, Lythe S, Armstrong W, Blom C. Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species. The Journal of Ecology. 1989;77:693-703. DOI: 10.2307/2260979
  57. 57. Smirnoff N, Crawford R. Variation in the structure and response to flooding of root aerenchyma in some wetland plants. Annals of Botany. 1983;51:237-249. DOI: 10.1093/oxfordjournals.aob.a086462
  58. 58. Kawai M, Samarajeewa P, Barrero R, Nishiguchi M, Uchimiya H. Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta. 1998;204:277-287. DOI: 10.1007/s004250050257
  59. 59. Seago JRJL, Marsh LC, Stevens KJ, Soukup A, Votrubova O, Enstone DE. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany. 2005;96:565-579. DOI: 10.1093/aob/mci211
  60. 60. Drew MC, He C-J, Morgan PW. Programmed cell death and aerenchyma formation in roots. Trends in Plant Science. 2000;5:123-127. DOI: 10.1016/S1360-1385(00)01570-3
  61. 61. Steffens B, Kovalev A, Gorb SN, Sauter M. Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling. The Plant Cell. 2012;24:3296-3306. DOI: 10.1105/tpc.112.101790
  62. 62. Thomas A, Guerreiro S, Sodek L. Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Annals of Botany. 2005;96:1191-1198. DOI: 10.1093/aob/mci272
  63. 63. Bacanamwo M, Purcell LC. Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. Journal of Experimental Botany. 1999;50:689-696. DOI: 10.1093/jexbot/50.334.689
  64. 64. Shimamura S, Yamamoto R, Nakamura T, Shimada S, Komatsu S. Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Annals of Botany. 2010;106:277-284. DOI: 10.1093/aob/mcq123
  65. 65. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P. Hormonal interplay during adventitious root formation in flooded tomato plants. The Plant Journal. 2010;63:551-562. DOI: 10.1111/j.1365-313X.2010.04262.x
  66. 66. Tamang BG, Magliozzi JO, Maroof MS, Fukao T. Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings. Plant, cell & Environment. 2014;37:2350-2365. DOI: 10.1111/pce.12277
  67. 67. Evans DE. Aerenchyma formation. New Phytologist. 2004;161:35-49. DOI: 10.1046/j.1469-8137.2003.00907.x
  68. 68. Phukan UJ, Mishra S, Timbre K, Luqman S, Shukla RK. Mentha arvensis exhibit better adaptive characters in contrast to Mentha piperita when subjugated to sustained waterlogging stress. Protoplasma. 2014;251:603-614. DOI: 10.1007/s00709-013-0561-4
  69. 69. Makbul S, Guler NS, Durmus N, Guven S. Changes in anatomical and physiological parameters of soybean under drought stress. Turkish Journal of Botany. 2011;35:369-377. DOI: 10.3906/bot-1002-7
  70. 70. Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F. Antioxidant systems and O2.−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiology. 2001;127:817-831. DOI: 10.1104/pp.010188
  71. 71. Türkan İ, Bor M, Özdemir F, Koca H. Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science. 2005;168:223-231. DOI: 10.1016/j.plantsci.2004.07.032
  72. 72. Clement M, Lambert A, Herouart D, Boncompagni E. Identification of new up-regulated genes under drought stress in soybean nodules. Gene. 2008;426:15-22. DOI: 10.1016/j.gene. 2008.08.016
  73. 73. Creissen GP, Mullineaux PM. The molecular biology of the ascorbate-glutathione cycle in higher plants. In: Inzé D, Montgan MV, editors. Oxidative Stress in Plants. UK: Taylor & Francis; 2002. pp. 247-270
  74. 74. Aroca R, Irigoyen JJ, Sánchez-Díaz M. Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiologia Plantarum. 2003;117:540-549. DOI: 10.1034/j.1399-3054.2003.00065.x
  75. 75. Masoumi H, Masoumi M, Darvish F, Daneshian J, Nourmohammadi G, Habibi D. Change in several antioxidant enzymes activity and seed yield by water deficit stress in soybean (Glycine max L.) cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2010;38:86-94. DOI: 10.15835/nbha3834936
  76. 76. Else MA, Coupland D, Dutton L, Jackson MB. Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiologia Plantarum. 2001;111:46-54. DOI: 10.1034/j.1399-3054.2001.1110107.x
  77. 77. Jackson M, Hall K. Early stomatal closure in waterlogged pea plants is mediated by abscisic acid in the absence of foliar water deficits. Plant, Cell & Environment. 1987;10:121-130. DOI: 10.1111/1365-3040.ep11602085
  78. 78. Malik AI, Colmer TD, Lambers H, Schortemeyer M. Changes in physiological and morphological traits of roots and shoots of wheat in response to different depths of waterlogging. Functional Plant Biology. 2001;28:1121-1131. DOI: 10.1071/PP01089
  79. 79. Boru G, Vantoai T, Alves J, Hua D, Knee M. Responses of soybean to oxygen deficiency and elevated root-zone carbon dioxide concentration. Annals of Botany. 2003;91:447-453. DOI: 10.1093/aob/mcg040
  80. 80. Fukao T, Xu K, Ronald PC, Bailey-Serres J. A variable cluster of ethylene response factor–like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell. 2006;18:2021-2034. DOI: 10.1105/tpc.106.043000
  81. 81. Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJ. Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiology. 2005;139:497-508. DOI: 10.1104/pp.105.064725
  82. 82. Jackson MB, Attwood PA. Roots of willow [Salix viminalis L.] show marked tolerance to oxygen shortage in flooded soils and in solution culture. Plant and Soil. 1996;187:37-45
  83. 83. Yordanova RY, Christov KN, Popova LP. Antioxidative enzymes in barley plants subjected to soil flooding. Environmental and Experimental Botany. 2004;51:93-101. DOI: 10.1016/S0098-8472[03]00063-7
  84. 84. Vieira RD, Tekrony D, Egli D. Effect of drought and defoliation stress in the field on soybean seed germination and vigor. Crop Science. 1992;32:471-475
  85. 85. Dornbos Jr D, Mullen R. Influence of stress during soybean seed fill on seed weight, germination, and seedling growth rate. Canadian Journal of Plant Science. 1991;71:373-383. DOI: 10.4141/cjps91-052
  86. 86. Maleki A, Naderi A, Naseri R, Fathi A, Bahamin S, Maleki R. Physiological performance of soybean cultivars under drought stress. Bulletin of environment, pharmacology and. Life Sciences. 2013;2:38-44
  87. 87. Guffy R, Hesketh J, Nelson R, Bernard R. Seed growth rate, growth duration, and yield in soybean. Biotronics: Reports of Biotron Institute, Kyushu University. 1991;20:19-30
  88. 88. Maryam A, Nasreen SA. Review: Water logging effects on morphological, anatomical, physiological and biochemical attributes of food and cash crops. International Journal of Water Resources and Environmental Sciences. 2012;1:113-120. DOI: 10.5829/idosi.ijwres.2012.1.4.11119
  89. 89. Yaklich RW, Abdul-Baki AA. Variability in metabolism of individual axes of soybean seeds and its relationship to vigor. Crop Science. 1975;15:424-426. DOI: 10.2135/cropsci1975.0011183X001500030042x
  90. 90. Wuebker EF, Mullen RE, Koehler K. Flooding and temperature effects on soybean germination. Crop Science. 2001;41:1857-1861. DOI: 10.2135/cropsci2001.1857
  91. 91. Sayama T, Nakazaki T, Ishikawa G, Yagasaki K, Yamada N, Hirota N, et al. QTL analysis of seed-flooding tolerance in soybean (Glycine max [L.] Merr.). Plant Science. 2009;176:514-521. DOI: 10.1016/j.plantsci.2009.01.007
  92. 92. Manavalan LP, Guttikonda SK, Phan Tran L-S, Nguyen HT. Physiological and molecular approaches to improve drought resistance in soybean. Plant and Cell Physiology. 2009;50:1260-1276. DOI: 10.1093/pcp/pcp082
  93. 93. Desclaux D, Huynh TT, Roumet P. Identification of soybean plant characteristics that indicate the timing of drought stress. Crop Science. 2000;40:716-722. DOI: 10.2135/cropsci2000.403716x
  94. 94. Jackson M, Ricard B. Physiology, biochemistry and molecular biology of plant root systems subjected to flooding of the soil. In: Visser EJW, de Kroon H, editors. Root Ecology. Heidelberg: Springer-Verlag; 2003. pp. 193-213. DOI: 10.1007/978-3-662-09784-78
  95. 95. Jackson MB, Drew MC, Kozlowski T. Effect of flooding on growth and metabolism of herbaceous plants. In: Kozlowski TT, editor. Flooding and Plant Growth. New York: Academic Press; 1984. pp. 47-128. DOI: 10.1093/aob/mcg014
  96. 96. Kramer PJ. Causes of injury to plants resulting from flooding of the soil. Plant Physiology. 1951;26:722. DOI: 10.1104/pp.26.4.722
  97. 97. Sallam A, Scott H. Effects of prolonged flooding on soybeans during early vegetative growth. Soil Science. 1987;144:61-66. DOI: 10.1080/01904168709363593
  98. 98. Gladish DK, Xu J, Niki T. Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Annals of Botany. 2006;97:895-902. DOI: 10.1093/aob/mcl040
  99. 99. Nanjo Y, Nakamura T, Komatsu S. Identification of indicator proteins associated with flooding injury in soybean seedlings using label-free quantitative proteomics. Journal of Proteome Research. 2013;12:4785-4798. DOI: 10.1021/pr4002349
  100. 100. Subbaiah CC, Sachs MM. Molecular and cellular adaptations of maize to flooding stress. Annals of Botany. 2003;91:119-127. DOI: 10.1093/aob/mcf210
  101. 101. Ohashi Y, Nakayama N, Saneoka H, Mohapatra PK, Fujita K. Differences in the responses of stem diameter and pod thickness to drought stress during the grain filling stage in soybean plants. Acta Physiologiae Plantarum. 2009;31:271-277. DOI: 10.1007/s11738-008-0229-4
  102. 102. Nobuyasu H, Liu S, Adu-Gyamfi J, Mohapatra P, Fujita K. Variation in the export of 13 C and 15 N from soybean leaf: The effects of nitrogen application and sink removal. Plant and Soil. 2003;253:331-339. DOI: 10.1023/A:1024836600725
  103. 103. Westgate M, Peterson C. Flower and pod development in water-deficient soybeans (Glycine max L. Merr). Journal of Experimental Botany. 1993;44:109-117. DOI: 10.1093/jxb/44.1.109
  104. 104. Ekhtiari S, Kobraee S, Shamsi K. Soybean yield under water deficit conditions. Journal of biodiversity and environment. Science. 2013;3:46-52
  105. 105. VanToai T, Beuerlein A, Schmitthenner S, St Martin S. Genetic variability for flooding tolerance in soybeans. Crop Science. 1994;34:1112-1115. DOI: 10.2135/cropsci1994.0011183X003400040051x
  106. 106. Linkemer G, Board JE, Musgrave ME. Waterlogging effects on growth and yield components in late-planted soybean. Crop Science. 1998;38:1576-1584. DOI: 10.2135/cropsci1998.0011183X003800060028x
  107. 107. Sullivan M, VanToai T, Fausey N, Beuerlein J, Parkinson R, Soboyejo A. Evaluating on-farm flooding impacts on soybean. Crop Science. 2001;41:93-100. DOI: 10.2135/cropsci2001.41193x
  108. 108. Griffin JL, Saxton AM. Response of solid-seeded soybean to flood irrigation. II. Flood duration. Agronomy Journal. 1988;80:885-888. DOI: 10.2134/agronj1988.00021962008000060009x
  109. 109. Schöffel ER, Saccol AV, Manfron PA, Medeiros SLP. Excesso hídrico sobre os componentes do rendimento da cultura da soja. Ciência Rural. 2001;31:7-12. DOI: 10.1590/S0103-84782001000100002
  110. 110. Rhine MD, Stevens G, Shannon G, Wrather A, Sleper D. Yield and nutritional responses to waterlogging of soybean cultivars. Irrigation Science. 2010;28:135-142. DOI: 10.1007/s00271-009-0168-x
  111. 111. Neumaier N, Farias JR, Nepomuceno AL. Índice de tolerância à seca em quatro cultivares de soja. In: Sociedade Brasileira de Agrometeorologia, Anais. Congresso Brasileiro de Agrometeorologia. Campina Grande, PB; 1995. p. 80-82
  112. 112. Valliyodan B, Ye H, Song L, Murphy M, Shannon JG, Nguyen HT. Genetic diversity and genomic strategies for improving drought and waterlogging tolerance in soybeans. Journal of Experimental Botany. 2016;68:1835-1849. DOI: 10.1093/jxb/erw433
  113. 113. Thu NBA, Nguyen QT, Hoang XLT, Thao NP, Tran L-SP. Evaluation of drought tolerance of the Vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering. BioMed Research International. 2014;2014:1-9. DOI: 10.1155/2014/809736
  114. 114. VanToai TT, Hoa TTC, Hue NTN, Nguyen HT, Shannon JG, Rahman MA. Flooding tolerance of soybean (Glycine max [L.] Merr.) germplasm from Southeast Asia under field and screen-house environments. The Open Agriculture Journal. 2010;4:38-46. DOI: 10.2174/1874331501004010038
  115. 115. Koo SC, Kim HT, Kang BK, Lee YH, Oh KW, Kim HY, et al. Screening of flooding tolerance in soybean germplam collection. Korean Journal of Breeding Science. 2014;46:129-135. DOI: 10.9787/KJBS.2014.46.2.129
  116. 116. Seversike TM, Sermons SM, Sinclair TR, Carter TE, Rufty TW. Physiological properties of a drought-resistant wild soybean genotype: Transpiration control with soil drying and expression of root morphology. Plant and Soil. 2014;374:359-370. DOI: 10.1007/s11104-013-1757-2
  117. 117. Prince SJ, Song L, Qiu D, dos Santos JVM, Chai C, Joshi T, et al. Genetic variants in root architecture-related genes in a Glycine soja accession, a potential resource to improve cultivated soybean. BMC Genomics. 2015;16:132. DOI: 10.1186/s12864-015-1334-6
  118. 118. Pathan MS, Lee JD, Shannon JG, Nguyen HT. Recent advances in breeding for drought and salt stress tolerance in soybean. In: Jenks MA, Hasegawa PM, Jain S, editors. Advances in molecular breeding toward drought and salt tolerant crops. Germany: Springer; 2007. pp. 739-773. DOI: 10.1007/978-1-4020-5578-230
  119. 119. Hwang S, King CA, Ray JD, Cregan PB, Chen P, Carter TE, et al. Confirmation of delayed canopy wilting QTLs from multiple soybean mapping populations. Theoretical and Applied Genetics. 2015;128:2047-2065. DOI: 10.1007/s00122-015-2566-1
  120. 120. Abdel-Haleem H, Carter TE, Purcell LC, King CA, Ries LL, Chen P, et al. Mapping of quantitative trait loci for canopy-wilting trait in soybean (Glycine max L. Merr). Theoretical and Applied Genetics. 2012;125:837-846. DOI: 10.1007/s00122-012-1876-9
  121. 121. Charlson DV, Bhatnagar S, King CA, Ray JD, Sneller CH, Carter TE, et al. Polygenic inheritance of canopy wilting in soybean (Glycine max [L.] Merr.). Theoretical and Applied Genetics. 2009;119:587-594. DOI: 10.1007/s00122-009-1068-4
  122. 122. Bhatnagar S, King CA, Purcell L, Ray JD. Identification and mapping of quantitative trait loci associated with crop responses to water-deficit stress in soybean (Glycine max [L.] Merr.). The ASACSSA-SSSA International Annual Meeting Poster Abstract; Salt Lake City, UT, USA. November 6-10, 2005
  123. 123. Specht J, Chase K, Macrander M, Graef G, Chung J, Markwell J, et al. Soybean response to water. Crop Science. 2001;41:493-509. DOI: 10.2135/cropsci2001.412493x
  124. 124. Monteros M, Lee G, Missaoui AM, Carter TE, Boerma HR Identification and confirmation of QTL conditioning drought tolerance in Nepalese soybean PI471938. In: The 11th Biennial Conference on the Molecular and Cellular Biology of the Soybean; Lincoln, Nebraska. August 5-8, 2006
  125. 125. Mian M, Ashley D, Boerma H. An additional QTL for water use efficiency in soybean. Crop Science. 1998;38:390-393. DOI: 10.2135/cropsci1998.0011183X003800020020x
  126. 126. Mian MA, Bailey MA, Ashley DA, Wells R, Carter TE, Parrott WA, Boerma HR. Molecular markers associated with water use efficiency and leaf ash in soybean. Crop Science. 1996;36:1252-1257
  127. 127. Hwang S, King CA, Davies MK, Ray JD, Cregan PB, Purcell LCQTL. Analysis of shoot Ureide and nitrogen concentrations in soybean (Glycine max [L.] Merr.). Crop Science. 2013;53:2421-2433. DOI: 10.2135/cropsci2012.11.0641
  128. 128. Du W, Wang M, Fu S, Mapping YD. QTLs for seed yield and drought susceptibility index in soybean (Glycine max L.) across different environments. Journal of Genetics and Genomics. 2009;36:721-731. DOI: 10.1016/S1673-8527[08]60165-4
  129. 129. Anandan A, Anumalla M, Pradhan SK, Ali J. Population structure, diversity and trait association analysis in rice (Oryza sativa L.) germplasm for early seedling vigor (ESV) using trait linked SSR markers. PLoS One. 2016;11:e0152406. DOI: 10.1371/journal.pone.0152406
  130. 130. Carter Jr TE, De Souza PI, Purcell LC, editors. Recent advances in breeding for drought and aluminum resistance in soybean. In: Proceedings of the World Soybean Conference VI Chicago, IL; August 4, 1999. pp. 4-7. DOI: 10.1007/978-1-4020-5578-230
  131. 131. Aceves-García P, Álvarez-Buylla ER, Garay-Arroyo A, García-Ponce B, Muñoz R, de la Paz Sánchez M. Root architecture diversity and meristem dynamics in different populations of Arabidopsis thaliana. Frontiers in Plant Science. 2016;7:858. DOI: 10.3389/fpls.2016.00858
  132. 132. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, et al. Control of root system architecture by Deeping rooting 1 increases rice yield under drought conditions. Nature Genetics. 2013;45:1097-1102
  133. 133. Pinto RS, Reynolds MP. Common genetic basis for canopy temperature depression under heat and drought stress associated with optimized root distribution in bread wheat. Theoretical and Applied Genetics. 2015;128:575-585. DOI: 10.1007/s00122-015-2453-9
  134. 134. Ellsworth PZ, Cousins AB. Carbon isotopes and water use efficiency in C4 plants. Current Opinion in Plant Biology. 2016;31:155-161. DOI: 10.1016/j.pbi.2016.04.006
  135. 135. Tambussi EA, Bort J, Guiamet JJ, Nogués S, Araus JL. The photosynthetic role of ears in C3 cereals: Metabolism, water use efficiency and contribution to grain yield. Critical Reviews in Plant Sciences. 2007;26:1-16
  136. 136. Feller U. Drought stress and carbon assimilation in a warming climate: Reversible and irreversible impacts. Journal of Plant Physiology. 2016;203:84-94. DOI: 10.1016/j.jplph.2016.04.002
  137. 137. Tuinstra M, Ejeta G, Goldsbrough P. Evaluation of near-isogenic sorghum lines contrasting for QTL markers associated with drought tolerance. Crop Science. 1998;38:835-842
  138. 138. Djekoun A, Planchon C. Water status effect on dinitrogen fixation and photosynthesis in soybean. Agronomy Journal. 1991;83:316-322. DOI: 10.2134/agronj1991.00021962008300020011x
  139. 139. Sadras VO, Lake L, Li Y, Farquharson EA, Sutton T. Phenotypic plasticity and its genetic regulation for yield, nitrogen fixation and δ13C in chickpea crops under varying water regimes. Journal of Experimental Botany. 2016;67:4339-4351
  140. 140. Sinclair T, Serraj R. Legume nitrogen-fixation and drought. Nature. 1995;378:344. DOI: 10.1038/378344a0
  141. 141. Sulieman S, Ha CV, Nasr Esfahani M, Watanabe Y, Nishiyama R, Pham CTB, et al. DT2008: A promising new genetic resource for improved drought tolerance in soybean when solely dependent on symbiotic N2 fixation. BioMed Research International. 2015;2015:687213. DOI: 10.1155/2015/687213
  142. 142. Sinclair TR, Messina CD, Beatty A, Samples M. Assessment across the United States of the benefits of altered soybean drought traits. Agronomy Journal. 2010;102:475-482. DOI: 10.2134/agronj2009.0195
  143. 143. Specht J, Hume D, Kumudini S. Soybean yield potential – A genetic and physiological perspective. Crop Science. 1999;39:1560-1570. DOI: 10.2135/cropsci1999.3961560x
  144. 144. Abdel-Haleem H, Lee GJ, Boerma RH. Identification of QTL for increased fibrous roots in soybean. Theoretical and Applied Genetics. 2011;122:935-946. DOI: 10.1007/s00122-010-1500-9
  145. 145. Atkinson JA, Wingen LU, Griffiths M, Pound MP, Gaju O, Foulkes MJ, et al. Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat. Journal of Experimental Botany. 2015;66:2283-2292. DOI: 10.1093/jxb/erv006
  146. 146. Courtois B, Ahmadi N, Khowaja F, Price AH, Rami J-F, Frouin J, et al. Rice root genetic architecture: Meta-analysis from a drought QTL database. Rice. 2009;2:115-128. DOI: 10.1007/s12284-009-9028-9
  147. 147. Giuliani S, Sanguineti MC, Tuberosa R, Bellotti M, Salvi S, Landi P. Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. Journal of Experimental Botany. 2005;56:3061-3070. DOI: 10.1093/jxb/eri303
  148. 148. Manavalan LP, Prince SJ, Musket TA, Chaky J, Deshmukh R, Vuong TD, et al. Identification of novel QTL governing root architectural traits in an interspecific soybean population. PLoS One. 2015;10:e0120490. DOI: 10.1371/journal.pone.0120490
  149. 149. Deshmukh RK, Sonah H, Kondawar V, Singh Tomar RS, Deshmukh NK. Identification of meta quantitative trait loci for agronomical traits in rice (Oryza sativa). Indian Journal of Genetics and Plant Breeding. 2012;72:264-270
  150. 150. Sosnowski O, Charcosset A, Joets J. BioMercator V3: An upgrade of genetic map compilation and quantitative trait loci meta-analysis algorithms. Bioinformatics. 2012;28:2082-2083. DOI: 10.1093/bioinformatics/bts313
  151. 151. Hwang S, King CA, Chen P, Ray JD, Cregan PB, Carter Jr TE, et al. Meta-analysis to refine map position and reduce confidence intervals for delayed-canopy-wilting QTLs in soybean. Molecular Breeding. 2016;36:1-14. DOI: 10.1007/s11032-016-0516-5
  152. 152. Santos MA, Geraldi IO, Garcia AAF, Bortolatto N, Schiavon A, Hungria M. Mapping of QTLs associated with biological nitrogen fixation traits in soybean. Hereditas. 2013;150:17-25. DOI: 10.1111/j.1601-5223.2013.02275.x
  153. 153. Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology. 2006;57:781-803. DOI: 10.1146/annurev.arplant.57.032905.105444
  154. 154. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, et al. Overexpressing a NAM, ATAF, and CUC [NAC] transcription factor enhances drought resistance and salt tolerance in rice. Proceedings of the National Academy of Sciences. 2006;103:12987-12992. DOI: 10.1073/pnas.0604882103
  155. 155. Liao Y, Zou H-F, Wei W, Hao Y-J, Tian A-G, Huang J, et al. Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta. 2008;228:225-240. DOI: 10.1007/s00425-008-0731-3
  156. 156. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, et al. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal. 2008;6:486-503. DOI: 10.1111/j.1467-7652.2008.00336.x
  157. 157. Wang N, Zhang W, Qin M, Li S, Qiao M, Liu Z, et al. Drought tolerance conferred in soybean (Glycine max. L) by GmMYB84, a novel R2R3-MYB transcription factor. Plant and Cell Physiology. 2017;58:1764-1776. DOI: 10.1093/pcp/pcx111
  158. 158. Su L-T, Li J-W, Liu D-Q, Zhai Y, Zhang H-J, Li X-W, et al. A novel MYB transcription factor, GmMYBJ1, from soybean confers drought and cold tolerance in Arabidopsis thaliana. Gene. 2014;538:46-55. DOI: 10.1016/j.gene.2014.01.024
  159. 159. Li Y, Chen Q, Nan H, Li X, Lu S, Zhao X, et al. Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean. PLoS One. 2017;12:e0179554. DOI: 10.1371/journal.pone.0179554
  160. 160. Gao S-Q, Chen M, Xu Z-S, Zhao C-P, Li L, Xu H-J, et al. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Molecular Biology. 2011;75:537-553. DOI: 10.1007/s11103-011-9738-4
  161. 161. Tan DX, Tuong HM, Thuy VTT, Son LV, Mau CH. Cloning and overexpression of GmDREB2 gene from a vietnamese drought-resistant soybean variety. Brazilian Archives of Biology and Technology. 2015;58:651-657. DOI: 10.13140/RG.2.1.3642.3126
  162. 162. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta Gene Regulatory Mechanisms. 2012;1819:86-96. DOI: 10.1016/j.bbagrm.2011.08.004
  163. 163. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, et al. Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. Journal of Experimental Botany. 2009;60:3781-3796. DOI: 10.1093/jxb/erp214
  164. 164. Zhang G, Chen M, Chen X, Xu Z, Li L, Guo J, et al. Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Molecular Biology Reports. 2010;37:809-818. DOI: 10.1007/s11033-009-9616-1
  165. 165. Luo X, Bai X, Sun X, Zhu D, Liu B, Ji W, et al. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. Journal of Experimental Botany. 2013;64:2155-2169. DOI: 10.1093/jxb/ert073
  166. 166. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, et al. Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. The Plant Journal. 2011;68:302-313. DOI: 10.1111/j.1365-313X.2011.04687.x
  167. 167. Chen X, Chen Z, Zhao H, Zhao Y, Cheng B, Xiang Y. Genome-wide analysis of soybean HD-zip gene family and expression profiling under salinity and drought treatments. PLoS One. 2014;9:e87156. DOI: 10.1371/journal.pone.0087156
  168. 168. Zhang D, Tong J, Xu Z, Wei P, Xu L, Wan Q, et al. Soybean C2H2-type zinc finger protein GmZFP3 with conserved QALGGH motif negatively regulates drought responses in transgenic Arabidopsis. Frontiers in Plant Science. 2016;7:325. DOI: 10.3389/fpls.2016.00325
  169. 169. Xie Z-M, Zou H-F, Lei G, Wei W, Zhou Q-Y, Niu C-F, et al. Soybean trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic Arabidopsis. PLoS One. 2009;4:e6898. DOI: 10.1371/journal.pone.0006898
  170. 170. Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K. Tran L-SP. In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Research. 2009;16:3533-3569. DOI: 10.1093/dnares/dsp023
  171. 171. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2009;463:178-183. DOI: 10.1038/nature08670
  172. 172. Wang F, Chen HW, Li QT, Wei W, Li W, Zhang WK, et al. GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. The Plant Journal. 2015;83:224-236. DOI: 10.1111/tpj.12879
  173. 173. Tripathi P, Rabara RC, Shen QJ, Rushton PJ. Transcriptomics analyses of soybean leaf and root samples during water-deficit. Genomics Data. 2015;5:164-166. DOI: 10.1016/j.gdata.2015.05.036
  174. 174. Jin J, Zhang H, Kong L, Gao G, Luo J. PlantTFDB 3.0: A portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Research. 2013;42:1182-1187. DOI: 10.1093/nar/gkt1016
  175. 175. Qi Q. Effect of transgenic DREB3 drought resistant soybean on soil enzyme activity and soil functional microorganism [thesis]. Northeast Agricultural University. 2011
  176. 176. VanToai TT, St Martin SK, Chase K, Boru G, Schnipke V, Schmitthenner AF, et al. Identification of a QTL associated with tolerance of soybean to soil waterlogging. Crop Science. 2001;41:1247-1252
  177. 177. Cornelious B, Chen P, Chen Y, De Leon N, Shannon J, Wang D. Identification of QTLs underlying water-logging tolerance in soybean. Molecular Breeding. 2005;16:103-112. DOI: 10.1007/s11032-005-5911-2
  178. 178. Githiri S, Watanabe S, Harada K, Takahashi R. QTL analysis of flooding tolerance in soybean at an early vegetative growth stage. Plant Breeding. 2006;125:613-618. DOI: 10.1111/j.1439-0523.2006.01291.x
  179. 179. Nguyen V, Vuong T, VanToai T, Lee J, Wu X, Mian M, et al. Mapping of quantitative trait loci associated with resistance to and flooding tolerance in soybean. Crop Science. 2012;52:2481-2493. DOI: 10.2135/cropsci2011.09.0466
  180. 180. Sun H, Zhao T, Gai J. Inheritance and QTL mapping of waterlogging tolerance at seedling stage of soybean. Acta Agronomica Sinica. 2010;36:590-595. DOI: 10.3724/SP.J.1006.2010.00590
  181. 181. Van Nguyen L, Takahashi R, Githiri SM, Rodriguez TO, Tsutsumi N, Kajihara S, et al. Mapping quantitative trait loci for root development under hypoxia conditions in soybean (Glycine max L. Merr.). Theoretical and Applied Genetics. 2017;130:743-755. DOI: 10.1007/s00122-016-2847-3
  182. 182. Reyna N, Cornelious B, Shannon J, Sneller C. Evaluation of a QTL for waterlogging tolerance in southern soybean germplasm. Crop Science. 2003;43:2077-2082. DOI: 10.1007/s11032-005-5911-2
  183. 183. Cornelious B, Chen P, Hou A, Shi A, Shannon J. Yield potential and waterlogging tolerance of selected near-isogenic lines and recombinant inbred lines from two southern soybean populations. Journal of Crop Improvement. 2006;16:97-111. DOI: 10.1300/J411v16n0107
  184. 184. Komatsu S, Yamamoto R, Nanjo Y, Mikami Y, Yunokawa H, Sakata K. A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. Journal of Proteome Research. 2009;8:4766-4778. DOI: 10.1021/pr900460x
  185. 185. Nanjo Y, Maruyama K, Yasue H, Yamaguchi-Shinozaki K, Shinozaki K, Komatsu S. Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Molecular Biology. 2011;77:129-144. DOI: 10.1007/s11103-011-9799-4
  186. 186. Chen W, Yao Q, Patil GB, Agarwal G, Deshmukh RK, Lin L, et al. Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and flooding stress revealed by RNA-Seq. Frontiers in Plant Science. 2016;7:1044. DOI: 10.3389/fpls.2016.01044
  187. 187. Yin X, Hiraga S, Hajika M, Nishimura M, Komatsu S. Transcriptomic analysis reveals the flooding tolerant mechanism in flooding tolerant line and abscisic acid treated soybean. Plant Molecular Biology. 2017;93:479-496. DOI: 10.1007/s11103-016-0576-2
  188. 188. Komatsu S, Han C, Nanjo Y, Altaf-Un-Nahar M, Wang K, He D, et al. Label-free quantitative proteomic analysis of abscisic acid effect in early-stage soybean under flooding. Journal of Proteome Research. 2013;12:4769-4784. DOI: 10.1021/pr4001898
  189. 189. Oh M, Komatsu S. Characterization of proteins in soybean roots under flooding and drought stresses. Journal of Proteomics. 2015;114:161-181. DOI: 10.1016/j.jprot.2014.11.008
  190. 190. Wang X, Oh M, Sakata K, Komatsu S. Gel-free/label-free proteomic analysis of root tip of soybean over time under flooding and drought stresses. Journal of Proteomics. 2016;130:42-55. DOI: 10.1016/j.jprot.2015.09.007
  191. 191. Yin X, Komatsu S. Nuclear proteomics reveals the role of protein synthesis and chromatin structure in root tip of soybean during the initial stage of flooding stress. Journal of Proteome Research. 2016;15:2283-2298. DOI: 10.1021/acs.jproteome.6b00330
  192. 192. Komatsu S, Sakata K, Nanjo Y. ‘Omics’ techniques and their use to identify how soybean responds to flooding. Journal of Analytical Science and Technology. 2015;6:9. DOI: 10.1186/s40543-015-0052-7
  193. 193. Komatsu S, Nanjo Y, Nishimura M. Proteomic analysis of the flooding tolerance mechanism in mutant soybean. Journal of Proteomics. 2013;79:231-250. DOI: 10.1016/j.jprot.2012.12.023
  194. 194. Wang Z, Li P, Yang Y, Chi Y, Fan B, Chen Z. Expression and functional analysis of a novel Group of Legume-Specific WRKY and Exo70 protein variants from soybean. Scientific Reports. 2016;6:32090. DOI: 10.1038/srep32090
  195. 195. Yin X, Nishimura M, Hajika M, Komatsu S. Quantitative proteomics reveals the flooding-tolerance mechanism in mutant and abscisic acid-treated soybean. Journal of Proteome Research. 2016;15:2008-2025. DOI: 10.1021/acs.jproteome.6b00196
  196. 196. Chang R, Qiu L. Evaluation and utilization of soybean germplasm in China. In: Lam HM, Chang R, Shao G, Liu Z, editors. Research on Tolerance to Stresses in Chinese Soybean. Beijing: China Agricultural Press; 2009
  197. 197. Xu Z, Chang R, Qiu L, Sun J, Li X, editors. Evaluation of soybean germplasm in China. In: Proceedings of the World Soybean Research Conference VI, Chicago; August 1999. pp. 4-7
  198. 198. Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics. 2010;42:1053-1059. DOI: 10.1038/ng.715
  199. 199. Christou P, McCabe DE, Swain WF. Stable transformation of soybean callus by DNA-coated gold particles. Plant Physiology. 1988;87:671-674
  200. 200. Hinchee MA, Connor-Ward DV, Newell CA, McDonnell RE, Sato SJ, Gasser CS, et al. Production of transgenic soybean plants using agrobacterium-mediated DNA transfer. Biotechnology. 1988;6:915-922. DOI: 10.1038/nbt0888-915
  201. 201. Dang W, Z-m W. An optimized agrobacterium-mediated transformation for soybean for expression of binary insect resistance genes. Plant Science. 2007;173:381-389. DOI: 10.1016/j.plantsci.2007.06.010
  202. 202. Paz MM, Shou H, Guo Z, Zhang Z, Banerjee AK, Wang K. Assessment of conditions affecting agrobacterium-mediated soybean transformation using the cotyledonary node explant. Euphytica. 2004;136:167-179. DOI: 10.1007/s00299-005-0113-2
  203. 203. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S. Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development. 2009;29:185-212. DOI: 10.1051/agro:2008021
  204. 204. Zhang M, Duan L, Zhai Z, Li J, Tian X, Wang B, et al., editors. Effects of plant growth regulators on water deficit-induced yield loss in soybean. In: Proceedings of the 4th International Crop Science Congress, Brisbane, Australia. September 26, 2004. pp. 252-256
  205. 205. Barta R, Broner I, Schneekloth J, Waskom R. Colorado high plains irrigation practices guide: Water saving options for irrigators in Eastern Colorado. Colorado Water Resources Research Institute Special Report No 14. 2004
  206. 206. Guo ZL, Sun CQ, Liang N. Impacts of plastic mulching on water saving and yield increasing of dry land spring soybean and its density effect. Chinese Journal of Eco-Agriculture. 2007;1:053
  207. 207. Zurweller BA. Nitrogen Fertilizer Management of Temporarily Waterlogged Soils to Improve Corn Production and Reduce Environmental Nitrogen Loss. Columbia: University of Missouri; 2014
  208. 208. Wang M, Zheng Q, Shen Q, Guo S. The critical role of potassium in plant stress response. International Journal of Molecular Sciences. 2013;14:7370-7390. DOI: 10.3390/ijms14047370
  209. 209. Martinelle K, Häggström L. Mechanisms of ammonia and ammonium ion toxicity i3n animal cells: Transport across cell membranes. Journal of Biotechnology. 1993;30:339-350. DOI: 10.1016/0168-1656[93]90148-G
  210. 210. Ashraf MA, Ahmad MSA, Ashraf M, Al-Qurainy F, Ashraf MY. Alleviation of waterlogging stress in upland cotton [Gossypium hirsutum L.] by exogenous application of potassium in soil and as a foliar spray. Crop and Pasture Science. 2011;62:25-38. DOI: 10.1071/CP09225
  211. 211. Liu G, Li Y, Migliaccio K, Olczyk T, Alva A. Oxygen amendment on growth and nitrogen use efficiency of flooded Italian basil. International Journal of Vegetable Science. 2013;19:217-227. DOI: 10.1080/19315260.2012.713451
  212. 212. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, et al. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLOS Genetics. 2012;8:e1002767. DOI: 10.1371/journal.pgen.1002767
  213. 213. Else MA, Jackson MB. Transport of 1-aminocyclopropane-1-carboxylic acid [ACC] in the transpiration stream of tomato (Lycopersicon esculentum) in relation to foliar ethylene production and petiole epinasty. Functional Plant Biology. 1998;25:453-458. DOI: 10.1071/PP97105
  214. 214. Grichko VP, Glick BR. Amelioration of flooding stress by ACC deaminase-containingplant growth-promoting bacteria. Plant Physiology and Biochemistry. 2001;39:11-17. DOI: 10.1016/S0981-9428[00]01212-2
  215. 215. Barnawal D, Bharti N, Maji D, Chanotiya CS, Kalra A. 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiology and Biochemistry. 2012;58:227-235. DOI: 10.1016/j.plaphy.2012.07.008
  216. 216. Li J, McConkey BJ, Cheng Z, Guo S, Glick BR. Identification of plant growth-promoting bacteria-responsive proteins in cucumber roots under hypoxic stress using a proteomic approach. Journal of Proteomics. 2013;84:119-131. DOI: 10.1016/j.jprot.2013.03.011

Written By

Tuanjie Zhao, Muqadas Aleem and Ripa Akter Sharmin

Submitted: October 9th, 2017 Reviewed: November 6th, 2017 Published: December 20th, 2017