Open access peer-reviewed chapter

Climate-Smart Maize Breeding: The Potential of Arbuscular Mycorrhizal Symbiosis in Improving Yield, Biotic and Abiotic Stress Resistance, and Carbon and Nitrogen Sink Efficiency

Written By

Arfang Badji, Issa Diedhiou and Abdoulaye Fofana Fall

Submitted: September 12th, 2021 Reviewed: September 24th, 2021 Published: April 20th, 2022

DOI: 10.5772/intechopen.100626

Chapter metrics overview

28 Chapter Downloads

View Full Metrics


Maize is part of the essential food security crops for which yields need to tremendously increase to support future population growth expectations with their accompanying food and feed demand. However, current yield increases trends are sub-optimal due to an array of biotic and abiotic factors that will be compounded by future negative climate scenarios and continued land degradations. These negative projections for maize yield call for re-orienting maize breeding to leverage the beneficial soil microbiota, among which arbuscular mycorrhizal fungi (AMS) hold enormous promises. In this chapter, we first review the components relevant to maize-AMF interaction, then present the benefits of arbuscular mycorrhizal symbiosis (AMS) to maize growth and yield in terms of biotic and abiotic stress tolerance and improvement of yield and yield components, and finally summarize pre-breeding information related to maize-AMF interaction and trait improvement avenues based on up-to-date molecular breeding technologies.


  • maize
  • climate-smart breeding
  • arbuscular mycorrhizal fungi
  • pre-breeding and Breeding
  • sterss tolerance
  • GWAS
  • genomic selection

1. Introduction

By 2050, around 9.9 billion people will be living on earth, with an expected concurrent doubling of the global food demand; hence agricultural production must increase at the same rate [1, 2]. This exponential population growth comes with an expected doubling of meat consumption; hence, demand for cereals-based feeds such as maize (Zea maysL.) will follow the same trend [3]. Therefore, modern breeding programs must double current genetic gains [2, 4]. However, a 2013 study alerted that current yield increase trends of most staple crops, including maize, are insufficient to meet the 2050 food demands [5]. Several biotic and abiotic factors are determinant limitations to crop yield despite breeding efforts, and climate disturbances will further compound these yield-reducing stressors [2, 6].

With this background, it is apparent that crop improvement programs targeting only the inherent genetic makeups of plants to increase yields are not efficient enough to increase crop production sufficiently to meet future food and feed demands [4]. Furthermore, it is necessary to achieve the desired crop production without increasing production surfaces since land degradation will likely worsen shortly [3]. This alarming situation calls for re-orienting plant breeding programs to adopt new climate-smart breeding approaches to boost crop productivity sufficiently to levels that would match the current and expected population growth rates [4, 7]. Instead of just focusing on increasing crop yields through improving its inherent genetic makeup, plant breeders should explore the immediate growing environment of the crops they seek to improve.

One of the components of the immediate growing environments of crops is the soil microbiota composed of microorganisms including fungi, archaea, and bacteria that have co-evolved with plants, among which some form highly beneficial symbiotic relationships with plants helping them in nutrient uptake, growth regulation, biotic and abiotic resistance, which ultimately results in increased yields [8, 9, 10]. The soil microbiota is relevant since most plant traits of interest, including nutrient use efficiency, tolerance to drought, salt, pest, and diseases, and yield, are part of a system comprising complex plant-associated microorganisms [11]. Plants have developed the ability to modulate the composition and activity of their microbiota through the secretion molecules and other signaling compounds [12]. Plant breeders would greatly benefit from understanding the genetic basis of this interaction and its influence on traits of interest and using this knowledge during selection and stability studies [11].

Among these microorganisms, arbuscular mycorrhizal fungi (AMF) are significant elements of the soil–plant system and constitute 5 to 50% of the microbial biomass of soils (Olsson et al., 1999). Arbuscular mycorrhizal symbiosis (AMS) is the most widespread and oldest terrestrial symbiosis [13], formed by 80–90% of terrestrial vascular plants, including grasses such as maize [14]. Plants benefit from AMS better mineral nutrition, especially phosphorus uptake [15], which improves mycorrhized plants biomass compared to non-mycorrhizal plants [13, 16], through colonization of plant roots, production of large networks of extra-root mycelium in the soil, and aid in the uptake of mineral nutrients by hosts in exchange for carbohydrates [17]. Elements such as nitrogen, magnesium, calcium, potassium, and trace elements such as copper [18], zinc, or even iron, are better absorbed by the plant through the AMF symbiosis [19, 20].

Furthermore, AMF are also a significant component of soil fertility improvement [21], playing an essential role in the soil’s physical, chemical, and biological components. They increase soil water holding capacity by improving its structure and inherent enzymatic activity by activating other microorganisms such as nitrogen-fixing bacteria [22]. AMF also participate in the nitrogen, phosphorus, and carbon cycles while correcting soil acidity [23, 24]. Regarding plant bio-protection, AMF play an essential role [25, 26] through, for instance, helping plants to thwart root-damaging nematodes [27, 28], pathogenic fungi such as verticillium wilt [29], and various pathogenic bacteria [30]. In addition, AMS provides plants with better resistance to abiotic stresses such as water and salt stress or the presence of heavy metals [31, 32].

Maize (Z. maysL.) is one of the essential staple food crops, therefore, essential to food security [33, 34]. Along with rice and wheat, it provides at least 30% of the food calories to more than 4.5 billion people in 100 countries [35, 36]. Maize is grown in more than 166 countries in the world, including tropical, subtropical, and temperate regions from mean sea level to 3000 m AMSL [37], and among cereals, it ranks highest in terms of grain yield per hectare worldwide [38]. Furthermore, besides its revenue generation as a cash crop, maize utilization is diversifying and joining new markets such as biofuel production and livestock feed [33, 34]. Therefore, maize productivity and production need to increase exponentially to support future food and feed demands as a food security crop. This increase will be required to occur under less inorganic input, severed land degradation, and aggravated climate disturbances that will profoundly disadvantage maize in its interaction with its biotic and abiotic environments. Considering the tremendous benefits of AMS to crops such as maize, we believe future maize research and breeding should adopt a more climate-smart approach by focusing more on understanding maize-AMF interaction and improving symbiotic capacity to boost yields. Therefore, in this chapter, we first review the components relevant to maize-AMF interaction, then present benefits of AMS in terms of biotic and abiotic stress tolerance and improvement of yield and yield components, and finally summarize pre-breeding information related to maize-AMF interaction and trait improvement avenues based on up-to-date molecular breeding technologies.


2. Arbuscular mycorrhizal fungi (AMF)

AMF are significant elements of the soil–plant system [13]. Mycorrhizae from the Greek “myco” for fungus and “rhize” for root essentially refers to the symbiotic association between fungi and plants’ roots. AMF constitute 5 to 50% of the microbial biomass of soils. Mycorrhizal hyphae biomass can vary from 54 to 900 kg per hectare [39], or nearly 200 meters of hyphae per gram of soil [40]. AMS is the most widespread and oldest terrestrial symbiosis [41], formed by more than 80–90% of terrestrial vascular plants [14]. AMF inhabit all continents, from the subarctic islands to the Antarctic Peninsula [19, 42]. According to Wang et al. [9], AMF has co-evolved with plants for at least 400 million years, allowing plants the colonization of lands by plants through improved hydro-mineral nutrition.

AMF belong to the phylum of Glomeromycota [43], with a taxonomic classification of AMF originally based on morpho-anatomical observations of spores [44]. However, the advances in biomolecular tools have allowed the use of Polymerase Chain Reaction (PCR) in the classification of AMF through amplification of ribosomal regions (18S), which permits a better definition of species or even molecular taxa [45]. More than 250 species of Glomeromyceta are currently described, with a constantly updated taxonomy updated, resulting in new species and higher taxa being regularly introduced [46, 47]. AMF are obligate symbiont because of their inability to develop without a host plant [48], with a reproductive system that can be either clonal or asexual through spore or coenocyte formation [49]. Several studies have shown the existence of hyphal fusions, called anastomoses which lead to exchanges of nuclei and cytoplasm between species of the same genus [50, 51, 52], hence participating in the conservation of diversity and the complex genetics of AMF [53]. Some AMF species are homokaryotic, with identical nuclei in each spore; thus, the genetic variation is present in each spore, resulting in several different copies of the same gene [54]. Heterokaryotic species are characterized by different nuclei in each spore, resulting in the distribution of the genetic variation among the different nuclei inside a spore. In other words, the existence of several different genomes in each spore helps AMF to adapt to different environments [55]. Furthermore, there are four phases in the life cycle of AMF [56]: the spore germination and hyphae growth in the rhizosphere phase, the root infection phase by hyphae, stimulated by carbon dioxide (CO2), and root exudates, which propagates in the root, the phase of root colonization with the formation of arbuscules and vesicles, and the phase of the development of external hyphae, resulting in an increased volume of soil explored by the roots and production of spores [57].


3. Survey of AMF that colonize maize

Host specificity of AMF is a longtime debate among researchers. Although many authors argued that AMF have no host-plant specificity [58], several studies tend to demonstrate the preference of some AMF genus to some plant species [59]. Crops like maize have a relatively high mycorrhizal dependency for plant growth and nutrient uptake [60]. Mycorrhizal dependency is an intrinsic property of every plant species that depend on the AMS. The type of crop, the soil properties, and the effect of the cropping system characterize mycorrhizal dependency [61]. There are three categories of plant species according to their mycorrhizal dependency. First, non-mycotrophic plants are capable of developing without the intervention of mycorrhizal fungi. Secondly, facultative mycotrophs require that reproduction occurs in the presence of mycorrhizal symbiosis only when the environment in which they grow is nutrient-limited. Lastly, obligate mycotrophs can only complete their development cycle associated with AMF. To study mycorrhizal dependency, the percentage of root colonized by AMF is a critical index. For example, the root colonization rate is 0% for Brassica napusand between 50 and 70% for Z. mays[62].

Furthermore, researchers use different methods such as trap cultures, wet sieving, morphological identification of spores, and molecular tools to determine AMF communities associated with maize. Based on such methods, many authors showed that maize crops could associate with different AMF species belonging to various genera (Table 1). Paraglomeraceae, Aucolosporaceae, Gigasporaceae, Glomeraceae, Archaeosporaceae,and Paraglomeraceaeare the AMF families that associated with maize; however, the Glomus group preponderant [63, 64, 66, 68, 69, 71]. Although it is well established that the genus Glomus has the most widespread dispersion, maize genotypes and agricultural systems influence the mycorrhizal community. Evaluation of maize varieties with different genomes revealed colonization levels depend largely and continuously on maize genotypes within each germplasm [70]. Maize monoculture also reduces AMF diversity [68, 71, 72]. For instance, Archaeosporaceae and Paraglomeraceae group are not colonizers of maize grown in monoculture [69].

AMF familyAMF speciesHabitatReferences
AcaulosporaceaeAcaulospora spBenin, Thailand[63, 64, 65]
AcaulosporaceaeAcaulospora longulaBrazil[66]
AcaulosporaceaeAcaulospora rugosaBrazil[66]
AcaulosporaceaeAcaulospora scrobiculataBrazil[66]
AcaulosporaceaeAcaulospora morrowiaeBrazil[66]
GlomeraceaeGlomus caledoniumJapan[67]
EntrophosporacaeEntrophospora spThailand[65]
GlomeraceaeGlomus spBenin, Hungary, Japan, Thailand[63, 64, 65, 68, 69, 70]
GlomeraceaeGlomus intraradicesGermany, Switzerland[71]
GlomeraceaeScutellospora spBenin, Thailand[63, 65]
ArchaeosporaceaeArchaeospora spHungary[66, 69]
igasporaceaeGigaspora spBenin, Hungary[63, 64, 69]
EntrophosporaceaeEntrophospora schenckiiThailand[65]
GlomeraceaeGlomus mosseaeGermany, Switzerland[65, 71]
ParaglomeraceaeParaglomus spHungary[69, 71]
GigasporaceaeScutellospora fulgidaThailand[65]
GlomeraceaeGlomus geosporumThailand[65]

Table 1.

Examples of AMF species associated with maize.


4. Phenotypic and molecular bases of maize-AMF symbiosis

Most terrestrial plants, including maize, interact with AMF under nutrient-limited conditions, mainly phosphorus. The physiological mechanisms underlying AMS establishment are under intense study using model plants, yet little information is currently available about molecular bases. Several studies have been performed for investigating the effect of AMF on gene expression through several approaches in different plant species over the last few years. Transcriptional analyses of few model plants like rice [73], Petunia [74], Lotus japonicus[75], Medicago truncatula[76], and tomato [77] allowed to identify genes involved in the AMS including genes encoding mycorrhizae-specific transporters. According to Willmann et al. [78], transporter genes are crucial for functional symbiosis. Many authors have defined four distinct stages of AMS based on the morphological analyses of the mutants.

The first step of an AMS is pre-contact signaling. It is characterized by a bi-directional exchange of signaling molecules and metabolic resources between AMF and plants. Indeed, plants produce strigolactone recognized by AMF, which exudes Myc-LCO, leading to deformation of absorbent hairs and nuclear calcium spiking [79]. The calcium oscillations are decoded by calcium and calmodulin-dependent protein kinases (CCaMK/DMI3), activating CYCLOPS/IPD3. These genes induce various micro RNA, transcription factors, and auxin signaling during AMS as documented by Diedhiou and Diouf [80]. Transcription factors regulate the signaling pathway during mycorrhization through interconnections, not yet clearly defined compared to Rhizobium/legume symbiosis.

Molecular recognition between partners is followed by contact between fungal hyphae and plant roots. This contact triggers a chain of events that starts with the hyphae branching, differentiating into hyphopodium or appressorium on the root surface. This structure prepares the penetration of the fungus into plant cells. Then, hydrolases and other molecules probably make the cell wall more flexible and cause the migration of the nucleus towards the appressorium, rearrangements of the cytoskeleton, and endoplasmic reticulum. These events lead to the subsequent formation of a pre-penetration apparatus (PPA) [57]. This apparatus facilitates the invasion of hyphae on epidermal and the first cortical cells [57]. According to some authors, PPA is responsible for forming a symbiotic interface and a new apoplastic compartment separating AMF and plant. During appressorium formation, defense genes are weakly activated in the plant [81]. Several genes such as VAPYRIN, NSP1/NSP2, and Cbf1/Cbf2 are involved in this step, as documented by Diedhiou and Diouf [80]. However, their precise function in root endosymbiosis remains unclear.

After physical contact between the two partners, hyphae fungal penetrate the cortical cells without damaging their plasma membrane, which invaginates and proliferates around the hyphae that develop inside these cells. This event results in forming an intra-radical mycelium. Intra-radical proliferation extends the colonization area to the intercellular space of the cortical parenchyma and inner cortical cells. Very few specific genes are involved in this step [80, 82]. This low expression supports the hypothesis that very few additional plants genes are activated after successful fungal colonization.

Intra-radical proliferation leads to the formation of arbuscules, which represent the final and most intimate step of the AMS. Indeed, intramatricial hyphae perforate the cell wall and penetrate inside the cell. They branch out to achieve a structure reminiscent of a small tree called an arbuscule which surrounds the cytoplasmic membrane to form the peri-arbuscular membrane (PAM). These modifications induce many changes in genes expression patterns even if their activity on the whole root level largely remains the same. Studies carried out on model plants allowed to identify mainly transcription factors and phosphorus transporters require to form arbuscules [21, 83]. The possible interconnections between these genes are described particularly between RAM1 and PT4/STR [84]. For maize, several analyses focused on identifying phosphate transporters whose Pht1;6 localized to arbuscule-containing cells [78]. It plays a criticssl role in the maintening the arbuscule function. Indeed, loss of function of Pht1;6 reduce root colonization with premature degeneration of the arbuscules. In addition, 13 Pi transporters were identified by Liu et al. [21]. Among them is ZmPt9 gene, which is different from members of the PHT1 gene family. Functional analysis indicates that ZmPt9 promotes the Pi transporter gene induction involved in Pi uptake [85]. Overexpression of ZmPt9 in Arabidopsis plant increases primary root length and lateral root formation. Furthermore, phosphorus content is higher in the transgenic plant compared to the wild type [86]. Recently, Wang et al. [87] showed that ZmPt7 regulates Pi acquisition, and its transport is mediated by phosphorylation.


5. Impact of AMF on maize resistance to biotic and abiotic stress

Maize is one of the essential sources of carbohydrate globally [88]; however, abiotic stresses and plant pests and diseases are significant threats in maize production worldwide, and future climate disturbances will further compound these scenarios [89]. AMS improves plant growth, hydro-mineral nutrition, and physiology under various environmental stress conditions like salinity, drought, and the presence of heavy metals [90], as well as resistance to biotic stresses such as pests, diseases, pathogen and weeds [91]. The benefits of AMF to plant partners vary depending on the type of stress [92].

AMF adapt to biotic and abiotic stresses independently of its host plant [14] and respond to stresses such as pests, diseases, pathogen, weeds, drought, extreme temperatures, salinity, and heavy metals [93, 94, 95]. Extensive evidence shows that AMF can control plant fungal, viral, and bacterial diseases (Himaya et al., 2021). The adaptation mechanisms of AMF to these biotic stresses are generally linked to pathogen resistance, including competition for colonization sites and improvement of the defense system of the plants [14]. Gerlach et al. [96] reported changes in leaf’s elemental concentration, resource reallocation, especially for carbohydrates and amino acids, and expression of defense-related genes under maize-AMF symbiosis. Patanita et al. [97] demonstrated the benefits of mycorrhization in the control of Magnaporthiopsis maydisalso called Harpophora maydis[98], the cause of late wilt disease of maize, which causes up to 50% grain yield losses in many countries [99, 100]. In addition, Fusariumand Aspergillusare two of the most dominant fungal pest species of maize, causing acute diseases and yield losses and majorly responsible for deterioration and losses on maize plants [101, 102]. Olawuyi et al. [103] investigated the effect AMF on Aspergillus niger and revealed that Glomus deserticolawas an effective biocontrol agent against Aspergillus niger, the soilborne pathogen of maize. Glomus clarumand Glomus deserticolaa have biocontrol potential against Fusarium verticillioides[104]. Downy mildew disease caused by Peronosclerosporais responsible for decreasing maize production (Soenartiningsih and Talanca 2010). The combination of botanical fungicides (Turmeric rhizome and betel leaves) with AMF (Enthroposporasp., Gigasporasp., and Glomussp.) and Trichoderma asperellumcan reduce the incidence of downy mildew by extending the incubation period and increasing the dry weight of maize shoots [105]. Striga hermonthicais one of the most critical biotic constraints affecting maize crops in sub-Saharan Africa. The high infestation of this parasitic plant has forced many poor farmers to abandon their farms [106]. Several studies have demonstrated that AMF can inhibit or suppress Striga germination, especially on cereal crops such as maize [107, 108]. Othira [109] carried out a study that confirmed the effectiveness of AMF in protecting maize against Striga infestation, promoting crop growth, and reducing Strigaplant incidence, plant biomass, and phosphate content. He evidenced that AMF (Gigaspora margarita) enhanced the performance of the maize plant host, allowing it to resist better Strigadamage [109].

In addition, AMF also helps maize plants cope with abiotic stresses such as salinity, drought, extreme temperature, and heavy metal. Various mechanisms explain abiotic stress biological regulation through AMF, such as increased hydromineral nutrition, ion selectivity, gene regulation, production of osmolytes, and the synthesis of phytohormones and antioxidants [14]. For instance, Rhizophagus irregularis,an AMF species, can improve maize drought tolerance through enhancing apoplastic water flow [110]. According to Mathur and Jajoo [111], Glomus Funneliformiscan help maize resist extreme temperatures by regulating the photosystem (PS) II heterogeneity. Studies carried out by Estrada et al. [94] demonstrated that AMF species such as R. irregularis, Septoglomus constrictum,and Claroideoglomus etunicatumimprove maize tolerance to salinity. The authors showed that these AMF species improve K+ and Na+ homeostasis, shoot and root dry weights, shoot K concentration, and reduced Cl and Na contents in shoots. AMF can also play a role in maize tolerance to heavy metals. Indeed, maize inoculation with some Glomus isolates can improve maize dry weight and contents of essential elements (K, P, and Mg) [93].

Drought is also one of the significant stresses that can reduce maize productivity [112]. Water constraints decrease the photosynthetic activity of plants, which close their stomates to minimize water loss, decreasing productivity [113, 114]. Several studies demonstrated that AMF improves crops performance under drought stress [115]. Mycorrhizal maize deals with water deficit through drought mitigation and drought tolerance [116]. A drought mitigation strategy is mediated by indirect AMF benefits and enhanced water uptake. In contrast, drought tolerance involves a combination of direct AMF benefits that improve the innate ability of the plant to cope with stress [117]. Furthermore, inoculation with AMF improves strigolactone and auxin responses to drought stress Ruiz-Lozano et al. [118]. These two critical hormones in plant resilience to abiotic stress [119].


6. Impact of AMF on maize carbon and nitrogen sink efficiency

Carbon (C) and nitrogen (N) are indispensable mineral elements for plant growth and development. AMF plays a vital role in maintaining soil quality by increasing carbon mineralization. After inoculating by Glomus etunicatum, the contents of dissolved organic carbon (DOC), microbial biomass carbon (MBC), and readily oxidizable carbon (ROC) increase in the soil rhizosphere of maize [120]. Rhizoglomus intraradicescolonization improves the active carbon pools such as water-soluble carbon, hot water-soluble carbon, biomass carbon up to 305 − 1, and passive pools such as soil organic carbon up to 4.31 mg.g − 1 compared to the control [121].

Plants can uptake nitrogen from the soil in the form of organic or chemical fertilizers [122] or establish beneficial associations with microbes that facilitate plant N acquisition [123, 124, 125, 126]. Microbes convert different forms of N that plants can use following chemical reactions carried out by living microorganisms such as bacteria, archaea, and fungi. Bacteria like Rhizobia and Frankia are the leading nitrogen suppliers to legumes and actinorhizal plants, respectively [124, 125, 127]. Symbiotic mycorrhizal associations can also enhance plant N acquisition through endomycorrhizae or ectomycorrhizae [128]. AMF mobilizes N in the surrounding rhizosphere and provides it to the host plant [129, 130]. Indeed, AMF develop interconnected structures such as arbuscules, intraradical and extraradical mycelium that allow the N uptake [131] through up-regulating genes coding for NO3– and NH4+ transporters, including AMT3.1 [132]. ATM3.1 is the primary driver of NH4+ transfer to the plant colonized by AMF.

Another way to enhance plant nutrition, particularly N uptake, is to develop tripartite associations with bacteria and mycorrhizal fungi, even if they are not well characterized yet [133]. Indeed, bacteria of the genus Paenibacillus have been identified inside Laccaria bicolor cells and can stimulate in vitro production of R. irregularisspore and mycorrhizal plant colonization by Glomus mossea[134, 135, 136]. This stimulating effect enhances fungal growth that could favor the establishment of more efficient fungal and N2-fixing symbioses. Nevertheless, the contributions of AMF to nitrogen acquisition are little be known, even intercropping system between maize and nitrogen-fixing plant. In an intercropping between maize and soybean, common mycorrhizal networks (CMNs) regulate Nitrogen allocation to plant roots [137]. Co-inoculation with AMF and rhizobia transferred more than 54% more nitrogen from soybean to maize than inoculation with AMF alone [137]. Furthermore, a recent study questioned the relevance of the chitin-like N source, an organic N source for the AMF, in the N supply to plants. Experiments showed that only R. irregularishyphae can access a significant fraction (>20%) of the organic N supplied as chitin into a pot zone but not Andropogon gerardiiroots, and this Ni was transferred to the plants within as little time as five weeks [138].

Overall, the presented evidence suggests that AMF significantly impacts N use efficiency by mycorrhizal/rhizobial plants, and carbon allocation is effective even with a cereal-legume cropping system. Understanding these mechanisms in a climate change context is critical for introducing symbiotic microorganisms as organic fertilizer in both croplands and forests while taking care of the ecosystem services rendered by microbial symbionts. Moreover, there are few evience that AMS could mitigate greenhouse gase emission in several cropping systems through diverse mechanisms [139, 140, 141, 142, 143, 144, 145], opening avenues for breeding of climate-considerate crop varieties. In that regard, AMS was reported to mitigate N2O emissions in several crop-soil systems such as maize [139], tomato [143, 144], rice [145], and grassland [142, 144].


7. Impact of AMF on maize yield and allied traits

Currently, AMF are critical organic components in cropping systems. Their interaction with crops increases yields by promoting plant growth and nutrition capacity [10]. Several experiments investigated the effects of AMF inoculation on maize yield. According to Cozzolino et al. [146], inoculation by Rhizophagus irregularisincreases maize stalk and leaf dry weight and grain yields compared to non-inoculated plants. They also found that colonization of maize by R. irregularisincreases available soil phosphorus (P) concentrations suggesting that inoculated roots mobilize more P and water than wild type. Recently, Assogba et al. [147] revealed mixed effects of Glomeraceae and Acaulosporaceae groups on the growth of maize seedlings under greenhouse conditions. Glomeraceae group improve significantly fresh above and underground biomass to 54.97% and 42.94%, respectively, and 55.23% for the leaf area compared to the control. Moreover, maximum plant heights and number of leaves were obtained with the Acaulosporaceae group, having 20.55% and 17.04%, respectively, compared to 11.77% for the control.

Studies were also conducted to reveal the effects of AMF on maize yield under abiotic stresses such as drought, salinity, heavy metals. Drought is one of the significant stresses that negatively affect maize yield [112]. AMF applications under water deficit improve the maize yield in different irrigation regimes. Rhizophagus irregularisenhances shoot dry weight (SDW) between 26 and 35% under drought conditions [148, 149]. Limited irrigation causes a two-fold decrease of the dry shoot weight (SDW) in AMF-maize plants as compared to non-AMF plants (17% vs. 37%, respectively) [149]. Furthermore, co-inoculation of Funneliformis mosseaeand Pseudomonas fluorescens(phosphate solubilizing bacteria) on maize improves vegetative and reproductive traits, root colonization, grain yield under water deficit while preserving natural resources such as P stocks [150]. According to Celebi et al. [151], R. irregularissignificantly improves agro-morphological parameters even in restricted irrigation conditions and increases leaf and stem ratios. Like for drought, AMF can increase resistance to salinity through several mechanisms, thus improving yield. Zhang et al. [152] reported that Trichoderma and Stachybotrys could promote maize growth in saline soil. Indigenous AMF improve maize growth in saline fields by significantly increasing biomass production and promoting leaf proline accumulation and a higher K+/Na + ratio [21]. Besides, Glomus tortuosumremarkably ameliorates dry mass and leaf area and enhances photosynthetic capacity by improving chlorophyll content and efficiently allowing light energy utilization, gas exchange, and rubisco activity under salinity stress [153].

Furthermore, several studies indicate that AMF can facilitate the revegetation of heavy metal contaminated soils and improve yields. Inoculation of maize by Claroideoglomus etunicatumin soils spiked with Lanthanum (La) significantly enhanced dry shoot weight and increased K, P, Ca, and Mg content in maize shoots between 27.40 and 441.77% [154]. Also, C. etunicatumdecreased shoot La concentration by 51.53% in maize while root La concentration increased by 30.45%.


8. Pre-breeding and breeding perspectives to maize-AMF symbiosis

One of the pivotal paths towards climate resilience and reversing the predicted negative impacts on food security is the adoption of climate-smart breeding approaches to design of high-yielding crops adapted to climate disturbances, such as increased abiotic and biotic stress [155, 156, 157]. Considering the tremendous positive impact of AMF symbiosis on maize yield, biotic and abiotic stress tolerance, Carbon and Nitrogen sink capacity, greenhouse gas mitigation [10, 14, 90, 91, 141, 158, 159, 160, 161], it is crucial to improve the symbiotic response capacity in the crop as a contribution to food security in the face of the changing climate scenarios and continuous land degradation [117, 162]. Besides, beneficial microorganisms such as AMF are not just traits influencers but rather are part of the phenotypic expression of plants in an integrated system started from nutrient mobilization to resource allocation to different plant functions, including resistance to biotic and abiotic tolerance, and nutrient efficiency and accumulation of assimilates in plant reserve organs which translates into yield [11, 163]. The current scientific information is more inclined towards a non-antagonistic impact of modern breeding activities on the mycorrhizal symbiotic capacity of maize [70, 96, 164, 165, 166], indicating the feasibility of efficient incorporating AMF-maize collaboration into ongoing breeding programs [165, 167, 168]. Therefore, the necessary continuous increase in crop yield to meet future food demands requires breeding efforts to improve symbiosis between critical crops such as maize with AMF [11, 166, 168].

For breeding to be efficient and achieve the expected genetic gains and progress, it is necessary to generate a host of useful pre-breeding information and devise breeding strategies based on state-of-art technologies selected through careful consideration of the factors that control maize-AMF interactions. In the coming sections, we review the critical pre-breeding information generated so far regarding maize symbiotic response to and interaction with AMF and identify areas necessitating further research to support breeding activities. We also devise breeding strategies to improve maize varieties’ symbiotic response and interaction to AMF based on the current knowledge of maize-AMF interactions.

8.1 Genetic diversity and inheritance of maize response to AMF symbiosis

The first and foremost step towards climate-smart crops is harnessing genetic diversity to allow the selection of superior material for breeding [169]. The maize genotype affects AMF abundance in the soil [170]. Maize has high genetic variance in response to AMF colonization [11, 70, 164, 170], indicating the possibility of selection in breeding. However, little information is available regarding the type of gene action controlling the maize response to AMP symbiosis, hence the need for more research in this area to judge opportunities for trait improvement through breeding. The high genetic diversity revealed by the few studies that investigated this pre-breeding characteristic of the maize-AMF interaction should be verified in several other genetic and environmental backgrounds to confirm promises of fast breeding progress. However, breeding progress might be hampered by the generally low to moderate heritability of maize responsiveness to AMF colonization [171].

Expectations of slow breeding progress are especially true for the traditional phenotypic selection, which strongly relies on phenotyping, increasing cost and time for budget-constrained breeding programs. Also, information related to the genetic control of maize-AMF interactions as to the proportion of additive and non-additive gene action involved in maize symbiotic response to AMF colonization [11]. Understanding the genetic control of any trait is crucial to designing effective breeding strategies for its improvement [172]. Therefore, besides the need to conduct more studies targeting maize levels of genetic diversity in response to AMF colonization, determining the preponderance of additive vs. dominance or epistasis genetic control on the trait needs to be elucidated better to inform future breeding strategies. New breeding approaches, especially those relying on advances in marker technologies such as marker-assisted selection (MAS) and genomic selection (GS), but also transgenic and genome editing (GE) techniques, could help to accelerate the improvement of maize responsiveness to AMF colonization and increase yield and stress tolerance [173, 174, 175, 176].

8.2 Genetic architecture of maize response to AMF

One of the first steps into implementing molecular breeding for maize response to AMF to increase yield performance is identifying genetic polymorphisms controlling the final maize benefit from the symbiosis [177]. However, very few studies undertook to map genomic regions associated with maize response to AMF symbiosis [168, 171]. Kaeppler et al. [164] conducted the first quantitative trait loci (QTL) mapping for maize interaction with AMF in a population generated from a cross between B73 and Mo17. They identified one QTL controlling maize responsiveness to AMF, and such a low number of QTL was attributable to the low heritability of the trait in their study. Twenty years later, Ramírez-Flores et al. [161] undertook another study to identify QTL that determined maize benefits from AMF symbiosis. Several QTL were identified in this study, suggesting a polygenic nature in the control of the trait, contrary to the monogenetic direction indicated by the earlier study [168, 171]. Considering the molecular complexity involved in the symbiosis process, from the recognition between AMF and plant to the effective establishment of the symbiotic relationship [158], the polygenic nature of Maize-AMF interaction is more plausible. However, more studies are required to confirm this hypothesis further.

Confirming the genetic architecture of maize-AMF interaction is pivotal since effective conventional or molecular breeding strategy design will depend on the number, siege of QTL controlling the traits and their interactions [178, 179]. These studies should be conducted in a wide variety of germplasm and geographical backgrounds to discover a comprehensive number of QTL that could accurately determine the genetic architecture of the trait through meta-analyses and other integrative studies [180].

8.3 Research perspectives and breeding strategies for improved maize response to AMS

Plant breeders generally are biased towards direct phenotypes, ignoring that most of these traits are mediated by beneficial microorganisms [11, 163, 167]. Although evidence points more towards a positive co-existence between modern plant breeding activities and practices, it is necessary to ascertain this status on target environments and maize populations. It is evident that response to AMF colonization is dependent on available resources such as soil phosphorus, crop species, and genotype [181]. The quantity and quality of soil phosphorus available to a particular crop are parameters that determine the maintenance of the diversity and quantity of the AMF community and their symbiotic capacity with maize [182]. Reports exist about the possibility of inhibition of the symbiosis between maize and AMF after artificial fertilization through the addition of external Phosphorus [183], making it necessary to adapt crop improvement for symbiotic capacity to target environments and cropping systems. Figure 1 shows the cascade of pre-breeding and breeding activities that should be involved in a strategic crop improvement program targeting improved maize response to AMF colonization and symbiosis.

Figure 1.

Pre-breeding and breeding pipeline for improved maize-AMF symbiosis.

A typical breeding program for any trait should identify adequate germplasm, possibly including wild relatives, exotic accessions, and landraces, as a base population for breeding through careful mating designs and accelerate genetic gains towards possible variety release [184, 185]. The base population should be both phenotyped for target traits and genotyped with molecular markers to allow measuring phenotype and marker-based genetic diversity and population structure to optimize downstream research and breeding activities such as parent selection and cross designs for pre-breeding activities such as inheritance and genetic control studies, QTL mapping, and selection techniques such as phenotypic selection (PS), MAS, GS [186, 187, 188, 189]. Phenotypic selection is a group of breeding methods basing the selection of superior genotypes for the next generation of for variety release on their observed phenotypic values. Phenotypic selection is best for highly heritable and easy-to-measure traits. Both MAS and GS are based on selecting genotypes using molecular markers, albeit they are essentially different. MAS relies on mapped QTLs for a particular trait, of which it uses associated markers to select desired phenotypically unobserved lines. MAS works best when the trait is monogenic or oligogenic (controlled by one or a few large-effect QTL) [178, 190]. GS uses whole-genome markers to compute genomic-estimated breeding values of phenotypically unobserved genotypes as a basis for selection. GS performs best on polygenic traits that are controlled by multiple small-effect QTL, which characterizes most traits that plant breeders investigate [191, 192, 193].

In the case of maize interaction with AMF, phenotyping should be done with a control (non-mycorrhized plants) experiment to allow direct estimation of benefits offered by AMF symbiosis on traits of interest as in several studies [109, 194, 195, 196]. A comprehensive number of phenotypic, biochemical, and omic traits should be selected for phenotyping based on their direct or indirect involvement in or them being influenced by maize-AMF interactions to run univariate and multivariate analyses for genotype ranking, estimation of AMS effect on target traits, and strength and direction of relationships among traits [197]. Where possible, high-throughput phenotyping (HTP) techniques should be used to precisely measure and allow the accurate estimation of genetic and genomic parameters, including genetic control and inheritance, marker-trait association, and genomic prediction accuracies [198, 199, 200]. During the last decade, HTP technologies served to precisely measure the shoot biomass of tomato, barley [201], and Medicago [201, 202] growth trends under AMF colonization and to estimate nitrogen use efficiency of tomato, barley, and Medicago plants [203].

It is noteworthy that the inherent low allele diversity and low recombination rates arising from the bi-parental nature of such mapping populations and the short timespan from their generation to advanced stages used for mapping are critical limits to most of these studies based on genetic linkage based QTL mapping methods [204, 205, 206, 207]. The low statistical power is because all the genetic and allele diversity only comes from the two parents crossed to generate the mapping population. The low resolution of QTL is caused by the short time for creating such populations, which, even with recombinant inbred lines, is still too little to allow enough recombination in the genome of the lines [206, 207]. These limitations lead to low statistical power for QTL discovery and low resolution of the genomic regions mapped [206, 207]. These shortcomings could have partly explained the low QTL number mapped by Kaeppler et al. [164], and that results from Ramírez-Flores et al. [161] might not have comprehensively captured the genetic architecture of maize-AF interaction. Genome-wide association studies (GWAS) is an alternative and complementary technique to pipe rental population-based QTL mapping from which it differs by the reliance on populations composed of diverse lines with historical recombination events. Consideration of genome-wide association studies (GWAS) should allow complementing traditional bi-parental QTL analyses, especially in Joint Linkage Association Mapping (JLAM), a technique that combines the strengths of both GWAS and biparental QTL mapping to alleviate their respective weaknesses [205]. Also, GWAS will increase the statistical power and resolution of the resulting QTL [204, 205, 208].

One of the main challenges breeders face is combining several traits of interest in elite lines due to the pervasive pleiotropic effect and close-linkage of genes controlling these traits, two genetic phenomena that yield similar phenotypic outcomes but are difficult to distinguish between each other unless specific analyses are performed [185, 209]. A prerequisite for efficiently achieving multiple-trait selection is delineating the genetic basis of the correlations among traits through multivariate analyses [210]. Several multivariate GWAS and GS exist in the perspective of genomics-aided multi-trait selection for maize response to AMF symbiosis. Multivariate methods allow leveraging shared genetic information among traits and possibly environments to increase statistical power and accuracy [210, 211]. Also, GWAS could complement GS by including GWAS-discovered QTL as fixed effects in GS models, which is reported to improve prediction accuracy, thereby increasing genetic gains per unit time [173].

Since its invention, GWAS has evolved, moving from single-locus single-trait mixed linear models proposed by Yu et al. [212] to multi-locus multi-traits algorithms, which, unlike the former, jointly test associations between several traits and all genome-wide markers [213, 214]. Single-trait mixed linear models suffer from several weaknesses, including high rates of false-negative associations caused by multiple testing issues that require stringent Bonferroni thresholds [215]. In contrast, multi-locus multi-traits algorithms have better statistical power by avoiding correcting for multiple testing [214, 216]. However, these methods are still inefficient in differentiating between the two causes of trait correlations [216]; instead, integration of structural equation modeling (SEM) to GWAS is necessary [217]. Several GWAS packages that incorporate SEM are available for use in the case of maize-AMF interactions, for instance, GW-SEM [218], SEM-GWAS [219], GenomicSEM [220]. A more advanced software package is the multi-trait multi-locus Structural Equation Modeling (mtmlSEM) that considers, besides the multi-trait framework, a multi-locus approach to model associations between multiple traits and all loci simultaneously using SEM [221]. Also, GWAS results should be complemented with a robust candidate gene discovery and In Silico and lad-based prioritization steps to allow selection of high-confidence trait-associated genes that could be used in molecular breeding techniques such as MAS GE [222, 223, 224, 225]. GE is a novel molecular breeding technique that, after mapping a genome region with an unfavorable genetic effect or with the potential of improving a trait, is used to precisely modify, insert, replace, or delete DNA in a genome [226].

Determining the genetic architecture of maize-AMF interactions will allow breeders to decide what selection approach would yield better genetic gains in a shorter time with a competitive budget requirement. However, considering the complexity of the molecular basis of symbiosis (see Section 7 of this chapter) and the probable polygenic nature of the phenomenon [168], it is expected that PS or MAS might not be efficient [227, 228, 229, 230]. GS, especially combined with HTP technologies, should accelerate genetic gains while reducing overall variety development costs [231]. For complex and polygenic traits such as maize-AMF interactions subject to several non-genetic influences, multi-trait GS models, especially those considering multi-environment trials (MET) such as R packages BMTME [232], would be of tremendous benefit. Multi-trait multi-environment GS methods are being routinely used for diverse traits of diverse crops, including maize [233, 234, 235, 236].



The Authors thank the Carnegie Corporation of New York for funding the Post-Doctoral Fellowship of A.B. through the Regional Universities Forum for Capacity Building in Agriculture (RUFORUM), Grant number: RU-NARO/2020/Post-Doc/02. A.F.F is supported by the Regional Academic Exchanged for Enhanced Skills in Fragile Ecosystem Management (REFORM) Program. I.D is supported by DST-FICCI sponsored by CV Raman International Fellowship for African Researchers.


Conflict of interest

The authors declare no conflict of interest.


  1. 1. Islam SMF, Karim Z. World’s Demand for Food and Water: The Consequences of Climate Change. In: Desalination - Challenges and Opportunities [Internet]. IntechOpen; 2020. p. 13. Available from:
  2. 2. Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, Mueller ND, et al. Climate Change and Global Food Systems: Potential Impacts on Food Security and Undernutrition. Annu Rev Public Health. 2017;38:259-77.
  3. 3. Raimondo M, Nazzaro C, Marotta G, Caracciolo F. Land degradation and climate change: Global impact on wheat yields. L Degrad Dev. 2021;32(1):387-98.
  4. 4. Voss-Fels KP, Stahl A, Hickey LT. Q&A: Modern crop breeding for future food security. BMC Biol. 2019;17(1):1-7.
  5. 5. Ray DK, Mueller ND, West PC, Foley JA. Yield Trends Are Insufficient to Double Global Crop Production by 2050. PLoS One. 2013;8(6).
  6. 6. Raza A, Razzaq A, Mehmood S, Zou X, Zhang X, Lv Y, et al. Impact of Climate Change on Crops Adaptation and Strategies to Tackle Its Outcome: A Review. Plants [Internet]. 2019;8(2):34. Available from:
  7. 7. Mba C, Ghosh K, Guimaraes EP. Re-orienting crop improvement for the changing climatic conditions of the 21st century [electronic resource]. Agric food Secur [Internet]. 2012;1(1):6. Available from:
  8. 8. Compant S, Samad A, Faist H, Sessitsch A. A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J Adv Res. 2019;19:29-37.
  9. 9. Wang B, Yeun LH, Xue J, Liu Y, Ané J, Qiu Y. Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol [Internet]. 2010 Apr 6;186(2):514-25. Available from:
  10. 10. Real-Santillán RO, del-Val E, Cruz-Ortega R, Contreras-Cornejo HÁ, González-Esquivel CE, Larsen J. Increased maize growth and P uptake promoted by arbuscular mycorrhizal fungi coincide with higher foliar herbivory and larval biomass of the Fall ArmywormSpodoptera frugiperda. Mycorrhiza. 2019;29(6):615-22.
  11. 11. Hohmann P, Messmer MM. Breeding for mycorrhizal symbiosis: focus on disease resistance. Euphytica. 2017;213(5).
  12. 12. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 2013;37(5):634-63.
  13. 13. Duponnois R, Ouahmane L, Kane A, Thioulouse J, Hafidi M, Boumezzough A, et al. Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biol Biochem. 2011;43(10):2160-8.
  14. 14. Diagne N, Ngom M, Djighaly PI, Fall D, Hocher V, Svistoonoff S. Roles of arbuscular mycorrhizal fungi on plant growth and performance: importance in biotic and abiotic stressed regulation. Diversity. 2020;12(10):1-25.
  15. 15. Smith SE, Jakobsen I, Grønlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 2011;156(3):1050-7.
  16. 16. Egerton-Warburton LM, Querejeta JI, Allen MF. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot. 2007;58(6):1473-83.
  17. 17. Alvarado-López CJ, Dasgupta-Schubert N, Ambriz JE, Arteaga-Velazquez JC, Villegas JA. Lead uptake by the symbioticDaucus carotaL.–Glomus intraradices system and its effect on the morphology of extra- and intraradical fungal microstructures. Environ Sci Pollut Res. 2019;26(1):381-91.
  18. 18. Facelli E, Smith SE, Smith FA. Mycorrhizal symbiosis overview and new insights into roles of arbuscular mycorrhizas in agro- and natural ecosystems. Australas Plant Pathol. 2009;38(4):338-44.
  19. 19. Smith SE, Read D. Mycorrhizal Symbiosis. Third. Vol. 137, Soil Science. 2010. 204 p.
  20. 20. Ercoli L, Schüßler A, Arduini I, Pellegrino E. Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities. Plant Soil. 2017;419(1-2):153-67.
  21. 21. Liu F, Xu Y, Jiang H, Jiang C, Du Y, Gong C, et al. Systematic identification, evolution and expression analysis of theZea maysPHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci. 2016;17(6):1-18.
  22. 22. Sadhana B. Review Article Arbuscular Mycorrhizal Fungi (AMF) as a Biofertilizer- a Review. IntJCurrMicrobiolAppSci [Internet]. 2014;3(4):384-400. Available from:
  23. 23. Jamiołkowska A, Ksiȩzniak A, Gałązka A, Hetman B, Kopacki M, Skwaryło-Bednarz B. Impact of abiotic factors on development of the community of arbuscular mycorrhizal fungi in the soil: A Review. Int Agrophysics. 2018;32(1):133-40.
  24. 24. Parihar M, Rakshit A, Meena VS, Gupta VK, Rana K, Choudhary M, et al. The potential of arbuscular mycorrhizal fungi in C cycling: a review. Arch Microbiol [Internet]. 2020;202(7):1581-96. Available from:
  25. 25. Eke P, Chatue Chatue G, Wakam LN, Kouipou RMT, Fokou PVT, Boyom FF. Mycorrhiza consortia suppress the fusarium root rot (Fusarium solani f. sp. Phaseoli) in common bean (Phaseolus vulgarisL.). Biol Control [Internet]. 2016;103:240-50. Available from:
  26. 26. Smms H, Sivasubramaniam N, Smms A. A Review on Role of Mycorrhizal Fungi in Plant Disease Management. 2021;41-50.
  27. 27. Ceustermans A, Van Hemelrijck W, Van Campenhout J, Bylemans D. Effect of arbuscular mycorrhizal fungi on pratylenchus penetrans infestation in apple seedlings under greenhouse conditions. Pathogens. 2018;7(4).
  28. 28. Schouteden N, Waele D De, Panis B, Vos CM. Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: A review of the mechanisms involved. Front Microbiol. 2015;6(NOV):1-12.
  29. 29. Zhang W, Zhao F, Jiang L, Chen C, Wu L, Liu Z. Different Pathogen Defense Strategies in Arabidopsis: More than Pathogen Recognition. Cells [Internet]. 2018 Dec 7;7(12):252. Available from:
  30. 30. Singh I, Giri B. Arbuscular mycorrhiza mediated control of plant pathogens. Mycorrhiza - Nutr Uptake, Biocontrol, Ecorestoration Fourth Ed. 2018;131-60.
  31. 31. Abd-Alla MH, Nafady NA, Bashandy SR, Hassan AA. Mitigation of effect of salt stress on the nodulation, nitrogen fixation and growth of chickpea (Cicer arietinumL.) by triple microbial inoculation. Rhizosphere [Internet]. 2019;10(January):100148. Available from:
  32. 32. Bothe H. Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis. 2012;58(1-3):7-16.
  33. 33. Renzaho AMN, Kamara JK, Toole M. Biofuel production and its impact on food security in low and middle income countries: Implications for the post-2015 sustainable development goals. Renew Sustain Energy Rev [Internet]. 2017;78(May 2016):503-16. Available from:
  34. 34. James A, Zikankuba VL. Mycotoxins contamination in maize alarms food safety in sub-Sahara Africa. Food Control [Internet]. 2018;90:372-81. Available from:
  35. 35. Shiferaw B, Prasanna BM, Hellin J, Bänziger M. Crops that feed the world 6. Past successes and future challenges to the role played by maize in global food security. Food Secur. 2011;3(3):307-27.
  36. 36. Cairns JE, Hellin J, Sonder K, Araus JL, MacRobert JF, Thierfelder C, et al. Adapting maize production to climate change in sub-Saharan Africa. Food Secur. 2013;5(3):345-60.
  37. 37. Kumar P, Singh R, Jaswinder SBS, Sekhar KJC, Soujanya PL. An overview of crop loss assessment in maize. 2018;(August 2019).
  38. 38. Amissah S, Osekre EA, Nyadanu D, Akromah R, Afun JVK, Adu Amoah R, et al. Inheritance and combining ability studies on grain yield and resistance to maize weevil (sitophilus zeamais, motschulsky) among extra early quality protein maize inbred lines. Ecol Genet Genomics [Internet]. 2019 Oct;12:100043. Available from:
  39. 39. Zhu Y-G, Miller MR. Carbon cycling by arbuscular mycorrhizal fungi in soil–plant systems. Trends Plant Sci [Internet]. 2003 Sep;8(9):407-9. Available from:
  40. 40. Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. Networks of power and influence: The role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot. 2004;82(8):1016-45.
  41. 41. Fitter A, Gilligan C, Hollingworth K, Kleczkowski A, Twyman R, Pitchford J. Biodiversity and ecosystem function in soil. Funct Ecol. 2005;369-77.
  42. 42. Newsham KK, Upson R, Read DJ. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol [Internet]. 2009;2(1):10-20. Available from:
  43. 43. Stürmer SL. A history of the taxonomy and systematics of arbuscular mycorrhizal fungi belonging to the phylum Glomeromycota. Mycorrhiza. 2012;22(4):247-58.
  44. 44. Morton JB, Benny GL. Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon (USA). 1990;
  45. 45. Young JPW. A molecular guide to the taxonomy of arbuscular mycorrhizal fungi. New Phytol. 2012;193(4):823-6.
  46. 46. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol. 2012;193(4):970-84.
  47. 47. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza. 2013;23(7):515-31.
  48. 48. Berruti A, Lumini E, Balestrini R, Bianciotto V. Arbuscular mycorrhizal fungi as natural biofertilizers: Let’s benefit from past successes. Front Microbiol. 2016;6(JAN):1-13.
  49. 49. Kuhn G, Hijri M, Sanders IR. Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature. 2001;414(6865):745-8.
  50. 50. Giovannetti M. Structure, extent and functional significance of belowground arbuscular mycorrhizal networks. Mycorrhiza State Art, Genet Mol Biol Eco-Function, Biotechnol Eco-Physiology, Struct Syst (Third Ed. 2008;59-72.
  51. 51. De La Providencia IE, De Souza FA, Fernández F, Delmas NS, Declerck S. Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol. 2005;165(1):261-71.
  52. 52. Chagnon PL. Ecological and evolutionary implications of hyphal anastomosis in arbuscular mycorrhizal fungi. FEMS Microbiol Ecol. 2014;88(3):437-44.
  53. 53. Cárdenas-Flores A, Draye X, Bivort C, Cranenbrouck S, Declerck S. Impact of multispores in vitro subcultivation of Glomus sp. MUCL 43194 (DAOM 197198) on vegetative compatibility and genetic diversity detected by AFLP. Mycorrhiza. 2010;20(6):415-25.
  54. 54. Hijri M, Sanders IR. Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature. 2005;433(7022):160-3.
  55. 55. Croll D, Sanders IR. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evol Biol. 2009;9(1):1-11.
  56. 56. Dickson S, Smith SE. Cross walls in arbuscular trunk hyphae form after loss of metabolic activity. New Phytol. 2001;151(3):735-42.
  57. 57. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus inMedicago truncatularoot epidermal cells before infection. Plant Cell. 2005;17(12):3489-99.
  58. 58. Sanders IR. Specificity in the Arbuscular Mycorrhizal Symbiosis. 2002;157:415-37.
  59. 59. Jacquemyn H, Merckx V, Brys R, Tyteca D, Cammue BPA, Honnay O, et al. Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). New Phytol. 2011;192(2):518-28.
  60. 60. Hao Z, Xie W, Chen B. viruses Arbuscular Mycorrhizal Symbiosis A ff ects Plant. Viruses. 2019;11(534):1-12.
  61. 61. Chifflot V, Rivest D, Olivier A, Cogliastro A, Khasa D. Molecular analysis of arbuscular mycorrhizal community structure and spores distribution in tree-based intercropping and forest systems. Agric Ecosyst Environ. 2009;131(1-2):32-9.
  62. 62. Tawaraya K. Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr. 2003;49(5):655-68.
  63. 63. Bossou LR, Houngnandan HB, Adandonon A, Zoundji C. Diversité des champignons mycorhiziens arbusculaires associés à la culture du maïs (Zea maysL .) au Bénin Diversity of arbuscular mycorrhizal fungi associated with maize cropping (Zea maysL .) in Benin. 2019;13(April):597-609.
  64. 64. Sukmawati S, Adnyana A, Suprapta DN, Proborini M, Soni P, Adinurani PG. Multiplication arbuscular mycorrhizal fungi in Corn (Zea maysL.) with pots culture at greenhouse. E3S Web Conf. 2021;226:1-10.
  65. 65. Na Bhadalung N, Suwanarit A, Dell B, Nopamornbodi O, Thamchaipenet A, Rungchuang J. Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize cropping system. Plant Soil. 2005;270(1):371-82.
  66. 66. Oliveira CA, Sá NMH, Gomes EA, Marriel IE, Scotti MR, Guimarães CT, et al. Assessment of the mycorrhizal community in the rhizosphere of maize (Zea maysL.) genotypes contrasting for phosphorus efficiency in the acid savannas of Brazil using denaturing gradient gel electrophoresis (DGGE). Appl Soil Ecol [Internet]. 2009 Mar;41(3):249-58. Available from:
  67. 67. Isobe K, Aizawa E, Iguchi Y, Ishii R. Distribution of arbuscular mycorrhizal fungi in upland field soil of Japan 1. Relationship between spore density and the soil environmental factor. Plant Prod Sci. 2007;10(1):122-8.
  68. 68. Toljander JF, Santos-González JC, Tehler A, Finlay RD. Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol. 2008;65(2):323-38.
  69. 69. Sasvári Z, Hornok L, Posta K. The community structure of arbuscular mycorrhizal fungi in roots of maize grown in a 50-year monoculture. Biol Fertil Soils. 2011;47(2):167-76.
  70. 70. An GH, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, et al. How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil. 2010;327(1):441-53.
  71. 71. Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, et al. Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol. 2006;15(8):2277-89.
  72. 72. Alguacil M, Lumini E, Roldan A, Salinas-Garcia J, Bonfante P, Biaciotto V. the Impact of Tillage Practices on Arbuscular Mycorrhizal. Ecol Appl. 2008;18(2):527-36.
  73. 73. Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, et al. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci U S A. 2005;102(22):8066-70.
  74. 74. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, et al. Phosphate systemically inhibits development of arbuscular mycorrhiza inPetunia hybridaand represses genes involved in mycorrhizal functioning. Plant J. 2010;64(6):1002-17.
  75. 75. Xue L, Cui H, Buer B, Vijayakumar V, Delaux PM, Junkermann S, et al. Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol. 2015;167(3):854-71.
  76. 76. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J. 2012;69(3):510-28.
  77. 77. Ruzicka D, Chamala S, Barrios-Masias FH, Martin F, Smith S, Jackson LE, et al. Inside Arbuscular Mycorrhizal Roots – Molecular Probes to Understand the Symbiosis. Plant Genome. 2013;6(2):1-13.
  78. 78. Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, Koebke E, et al. Mycorrhizal phosphate uptake pathway in maize: Vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front Plant Sci. 2013;4(DEC):1-6.
  79. 79. Akiyama K, Ogasawara S, Ito S, Hayashi H. Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 2010;51(7):1104-17.
  80. 80. Hogekamp C, Küster H. A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis. BMC Genomics. 2013;14(1).
  81. 81. Blilou I, Bueno P, Ocampo JA, Garcia-Garrido JM. Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae. Mycol Res. 2000;104(6):722-5.
  82. 82. Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Küster H. Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-Box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol. 2011;157(4):2023-43.
  83. 83. Diédhiou I, Diouf D. Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol [Internet]. 2018;34(3):0. Available from:
  84. 84. Rich MK, Courty PE, Roux C, Reinhardt D. Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza inPetunia hybrida. BMC Genomics. 2017;18(1):1-14.
  85. 85. Liu F, Xu Y, Han G, Wang W, Li X, Cheng B. Identification and functional characterization of a maize phosphate transporter induced by mycorrhiza formation. Plant Cell Physiol. 2018;59(8):1683-94.
  86. 86. Xu Y, Liu F, Li X, Cheng B. The mycorrhiza-induced maize ZmPt9 gene affects root development and phosphate availability in nonmycorrhizal plant. Plant Signal Behav [Internet]. 2018;13(12):1-3. Available from:
  87. 87. Wang F, Cui PJ, Tian Y, Huang Y, Wang HF, Liu F, et al. Maize ZmPT7 regulates Pi uptake and redistribution which is modulated by phosphorylation. Plant Biotechnol J. 2020;18(12):2406-19.
  88. 88. Rouf Shah T, Prasad K, Kumar P. Maize—A potential source of human nutrition and health: A review. Cogent Food Agric. 2016;2(1).
  89. 89. Chávez-Arias CC, Ligarreto-Moreno GA, Ramírez-Godoy A, Restrepo-Díaz H. Maize Responses Challenged by Drought, Elevated Daytime Temperature and Arthropod Herbivory Stresses: A Physiological, Biochemical and Molecular View. Front Plant Sci. 2021;12(July):1-14.
  90. 90. Kapoor R, Evelin H, Mathur P, Giri B. Arbuscular Mycorrhiza: Approaches for Abiotic Stress Tolerance in Crop Plants for Sustainable Agriculture. In: Plant Acclimation to Environmental Stress [Internet]. New York, NY: Springer New York; 2013. p. 359-401. Available from:
  91. 91. Pozo MJ, Jung SC, Martínez-Medina A, López-Ráez JA, Azcón-Aguilar C, Barea J-M. Root Allies: Arbuscular Mycorrhizal Fungi Help Plants to Cope with Biotic Stresses. In 2013. p. 289-307. Available from:
  92. 92. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett. 2010;13(3):394-407.
  93. 93. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H. Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol. 1999;154(5-6):718-28.
  94. 94. Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant, Cell Environ. 2013;36(10):1771-82.
  95. 95. Lenoir I, Fontaine J, Lounès-Hadj Sahraoui A. Arbuscular mycorrhizal fungal responses to abiotic stresses: A review. Phytochemistry [Internet]. 2016;123:4-15. Available from:
  96. 96. Gerlach N, Schmitz J, Polatajko A, Schlüter U, Fahnenstich H, Witt S, et al. An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. Plant, Cell Environ. 2015;38(8):1591-612.
  97. 97. Patanita M, Campos MD, Félix MDR, Carvalho M, Brito I. Effect of tillage system and cover crop on maize mycorrhization and presence of Magnaporthiopsis maydis. Biology (Basel). 2020;9(3).
  98. 98. Klaubauf S, Tharreau D, Fournier E, Groenewald JZ, Crous PW, de Vries RP, et al. Resolving the polyphyletic nature of Pyricularia (Pyriculariaceae). Stud Mycol [Internet]. 2014;79(1):85-120. Available from:
  99. 99. Molinero-Ruiz L, Melero-Vara J, Mateos A. Cephalosporium maydis, the Cause of Late Wilt in Maize, a Pathogen New to Portugal and Spain. Plant Dis - PLANT DIS. 2010 Mar 1;94:379.
  100. 100. Drori R, Sharon A, Goldberg D, Rabinovitz O, Degani O, Mediterranea SP, et al. Molecular diagnosis for Harpophora maydis, the cause of maize late wilt in Israel Published by: Firenze University Press on behalf of the Mediterranean Phytopathological Union Stable URL: Ha. 2013;52(1):16-29.
  101. 101. Owolade OF, Alabi BS, Enikuomehin OA, Atungwu JJ. Effect of harvest stage and drying methods on germination and seed-borne fungi of maize (Zea maysL.) in South West Nigeria. African J Biotechnol. 2005;4(12):1384-9.
  102. 102. Hussain N, Hussain A, Ishtiaq M, Azam S, Hussain T. Pathogenicity of two seed-borne fungi commonly involved in maize seeds of eight districts of Azad Jammu and Kashmir, Pakistan. African J Biotechnol. 2013;12(12):1363-70.
  103. 103. Olawuyi OJ, Odebode AC, Olakojo SA, Popoola OO, Akanmu AO, Izenegu JO. Host-pathogen interaction of maize (Zea maysL.) and Aspergillus niger as influenced by arbuscular mycorrhizal fungi (Glomus deserticola). Arch Agron Soil Sci [Internet]. 2014;60(11):1577-91. Available from:
  104. 104. Olowe OM, Olawuyi OJ, Sobowale AA, Odebode AC. Role of arbuscular mycorrhizal fungi as biocontrol agents against Fusarium verticillioides causing ear rot ofZea maysL. (Maize). Curr Plant Biol [Internet]. 2018;15(November):30-7. Available from:
  105. 105. Prasetyo J, Ginting C, Akin HM, Suharjo R, Niswati A, Afandi A, et al. The effect of biological agent and botanical fungicides on maize downy mildew. Biodiversitas. 2021;22(4):1652-7.
  106. 106. Atera EA, Itoh K, Azuma T, Ishii T. Farmers’ perspectives on the biotic constraint ofStriga hermonthicaand its control in western Kenya. Weed Biol Manag. 2012;12(1):53-62.
  107. 107. Lendzemo VW, Van Ast A, Kuyper TW. Can arbuscular mycorrhizal fungi contribute to Striga management on cereals in Africa? Outlook Agric. 2006;35(4):307-11.
  108. 108. Manjunatha PH, Nirmalnath PJ, Ht C. Field evalualtion of native arbuscular mycorrhizal fungi in the management of Striga in sugarcane (Saccharum officinarumL .). J Pharmacogn Phytochem. 2018;7(2):2496-500.
  109. 109. Othira, J. O. Effectiveness of arbuscular mycorrhizal fungi in protection of maize (Zea maysL.) against witchweed (Striga hermonthicaDel Benth) infestation. J Agric Biotechnol Sustain Dev. 2012;4(3):37-44.
  110. 110. Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, et al. Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot. 2012;109(5):1009-17.
  111. 111. Mathur S, Jajoo A. Arbuscular mycorrhizal fungi protects maize plants from high temperature stress by regulating photosystem II heterogeneity. Ind Crops Prod [Internet]. 2020;143(November):111934. Available from:
  112. 112. Wossen T, Abdoulaye T, Alene A, Feleke S, Menkir A, Manyong V. Measuring the impacts of adaptation strategies to drought stress: The case of drought tolerant maize varieties. J Environ Manage [Internet]. 2017;203:106-13. Available from:
  113. 113. Mangena P. Water Stress: Morphological and Anatomical Changes in Soybean (Glycine maxL.) Plants. Plant, Abiotic Stress Responses to Clim Chang. 2018;
  114. 114. Brodribb TJ, Sussmilch F, McAdam SAM. From reproduction to production, stomata are the master regulators. Plant J. 2020;101(4):756-67.
  115. 115. Bahadur A, Batool A, Nasir F, Jiang S, Mingsen Q, Zhang Q, et al. Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int J Mol Sci. 2019;20(17):1-18.
  116. 116. Begum N, Ahanger MA, Su Y, Lei Y, Mustafa NSA, Ahmad P, et al. Improved Drought Tolerance by AMF Inoculation in Maize (Zea mays) Involves Physiological and Biochemical Implications. Plants [Internet]. 2019 Dec 6;8(12):579. Available from:
  117. 117. Posta K, Hong Duc N. Benefits of Arbuscular Mycorrhizal Fungi Application to Crop Production under Water Scarcity. In: Drought - Detection and Solutions [Internet]. IntechOpen; 2020. p. 13. Available from:
  118. 118. Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, et al. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ. 2016;39(2):441-52.
  119. 119. Saeed W, Naseem S, Ali Z. Strigolactones biosynthesis and their role in abiotic stress resilience in plants: A critical review. Front Plant Sci. 2017;8(August):1-13.
  120. 120. Xu H, Shao H, Lu Y. Arbuscular mycorrhiza fungi and related soil microbial activity drive carbon mineralization in the maize rhizosphere. Ecotoxicol Environ Saf [Internet]. 2019;182(June):109476. Available from:
  121. 121. Subramanian KS, Vivek PN, Balakrishnan N, Nandakumar NB, Rajkishore SK. Effects of arbuscular mycorrhizal fungus Rhizoglomus intraradices on active and passive pools of carbon in long-term soil fertility gradients of maize based cropping system. Arch Agron Soil Sci [Internet]. 2019;65(4):549-65. Available from:
  122. 122. Landberg R, Hanhineva K, Tuohy K, Garcia-Aloy M, Biskup I, Llorach R, et al. Biomarkers of cereal food intake. Genes Nutr. 2019;14(1):1-16.
  123. 123. Chen A, Gu M, Wang S, Chen J, Xu G. Transport properties and regulatory roles of nitrogen in arbuscular mycorrhizal symbiosis. Semin Cell Dev Biol [Internet]. 2018;74:80-8. Available from:
  124. 124. Santi C, Bogusz D, Franche C. Biological nitrogen fixation in non-legume plants. Ann Bot. 2013;111(5):743-67.
  125. 125. Udvardi M, Poole PS. Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol. 2013;64:781-805.
  126. 126. Courty PE, Smith P, Koegel S, Redecker D, Wipf D. Inorganic Nitrogen Uptake and Transport in Beneficial Plant Root-Microbe Interactions. CRC Crit Rev Plant Sci. 2015;34(November 2014):4-16.
  127. 127. van Velzen R, Holmer R, Bu F, Rutten L, van Zeijl A, Liu W, et al. Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. Proc Natl Acad Sci U S A. 2018;115(20):E4700-9.
  128. 128. Dellagi A, Quillere I, Hirel B. Beneficial soil-borne bacteria and fungi: A promising way to improve plant nitrogen acquisition. J Exp Bot. 2020;71(15):4469-79.
  129. 129. Ferlian O, Biere A, Bonfante P, Buscot F, Eisenhauer N, Fernandez I, et al. Growing Research Networks on Mycorrhizae for Mutual Benefits. Trends Plant Sci [Internet]. 2018;23(11):975-84. Available from:
  130. 130. Jansa J, Forczek ST, Rozmoš M, Püschel D, Bukovská P, Hršelová H. Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chem Biol Technol Agric [Internet]. 2019;6(1):1-10. Available from:
  131. 131. Ferrol N, Azcón-Aguilar C, Pérez-Tienda J. Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. Plant Sci [Internet]. 2019;280(June):441-7. Available from:
  132. 132. Koegel S, Mieulet D, Baday S, Chatagnier O, Lehmann MF, Wiemken A, et al. Phylogenetic, structural, and functional characterization of AMT3;1, an ammonium transporter induced by mycorrhization among model grasses. Mycorrhiza. 2017;27(7):695-708.
  133. 133. Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, et al. Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: Research strategies for the selection of the best performing inocula. Agronomy. 2020;10(1).
  134. 134. Bertaux J, Schmid M, Prevost-Boure NC, Churin JL, Hartmann A, Garbaye J, et al. In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Appl Environ Microbiol. 2003;69(7):4243-8.
  135. 135. Budi SW, Van Tuinen D, Martinotti G, Gianinazzi S. Isolation from theSorghum bicolormycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Appl Environ Microbiol. 1999;65(11):5148-50.
  136. 136. Hildebrandt U, Ouziad F, Marner FJ, Bothe H. The bacteriumPaenibacillus validusstimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett. 2006;254(2):258-67.
  137. 137. Wang C, White PJ, Li C. Colonization and community structure of arbuscular mycorrhizal fungi in maize roots at different depths in the soil profile respond differently to phosphorus inputs on a long-term experimental site. Mycorrhiza [Internet]. 2016; Available from:
  138. 138. Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Hujslová M, Püschel D, et al. Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers? Mycorrhiza. 2018;28(5-6):465.
  139. 139. Gui H, Gao Y, Wang Z, Shi L, Yan K, Xu J. Arbuscular mycorrhizal fungi potentially regulate N2O emissions from agricultural soils via altered expression of denitrification genes. Sci Total Environ [Internet]. 2021;774:145133. Available from:
  140. 140. Storer K, Coggan A, Ineson P, Hodge A. Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol. 2018;220(4):1285-95.
  141. 141. Shen Y, Zhu B. Arbuscular mycorrhizal fungi reduce soil nitrous oxide emission. Geoderma [Internet]. 2021;402(April):115179. Available from:
  142. 142. Bender SF, Conen F, Van der Heijden MGA. Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem [Internet]. 2015;80:283-92. Available from:
  143. 143. Lazcano C, Barrios-Masias FH, Jackson LE. Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biol Biochem [Internet]. 2014;74:184-92. Available from:
  144. 144. Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Köhl L, et al. Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J. 2014;8(6):1336-45.
  145. 145. Zhang X, Wang L, Ma F, Shan D. Effects of Arbuscular Mycorrhizal Fungi on N2O Emissions from Rice Paddies. Water Air Soil Pollut. 2015;226(7):1-10.
  146. 146. Cozzolino V, Di Meo V, Piccolo A. Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochemical Explor [Internet]. 2013;129:40-4. Available from:
  147. 147. Assogba SA, Adjovi NRA, Agbodjato NA, Sina H, Adjanohoun A, Baba-Moussa L. Evaluation of the Mixed Effects of Some Indigenous Strains of Arbuscular Mycorrhizal Fungi on the Growth of Maize Seedlings Under Greenhouse Conditions. Eur Sci J ESJ. 2020;16(3):275-94.
  148. 148. Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM. New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Interact. 2014;27(4):349-63.
  149. 149. Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci. 2017;8(June):1-15.
  150. 150. Ghorchiani M, Etesami H, Alikhani HA. Improvement of growth and yield of maize under water stress by co-inoculating an arbuscular mycorrhizal fungus and a plant growth promoting rhizobacterium together with phosphate fertilizers. Agric Ecosyst Environ [Internet]. 2018;258(February):59-70. Available from:
  151. 151. Celebi SZ, Demir S, Celebi R, Durak ED, Yilmaz IH. The effect of Arbuscular Mycorrhizal Fungi (AMF) applications on the silage maize (Zea maysL.) yield in different irrigation regimes. Eur J Soil Biol [Internet]. 2010;46(5):302-5. Available from:
  152. 152. Zhang W, Cao J, Zhang S, Wang C. Effect of earthworms and arbuscular mycorrhizal fungi on the microbial community and maize growth under salt stress. Appl Soil Ecol [Internet]. 2016;107:214-23. Available from:
  153. 153. Xu H, Lu Y, Tong S. Effects of arbuscular mycorrhizal fungi on photosynthesis and chlorophyll fluorescence of maize seedlings under salt stress. Emirates J Food Agric. 2018;30(3):199-204.
  154. 154. Hao L, Zhang Z, Hao B, Diao F, Zhang J, Bao Z, et al. Arbuscular mycorrhizal fungi alter microbiome structure of rhizosphere soil to enhance maize tolerance to La. Ecotoxicol Environ Saf [Internet]. 2021;212:111996. Available from:
  155. 155. He T, Li C. Harness the power of genomic selection and the potential of germplasm in crop breeding for global food security in the era with rapid climate change. Crop J [Internet]. 2020;8(5):688-700. Available from:
  156. 156. Kinghorn BP, Cowling WA, Li L, Siddique KHM, Banks RG. Modeling crop breeding for global food security during climate change. 2019;(July 2018):1-10.
  157. 157. Yadav SS, Redden RJ, Hatfield JL, Ebert AW, Hunter D, Ortiz R. Role of Plant Breeding to Sustain Food Security under Climate Change. Food Secur Clim Chang. 2018;(December):145-58.
  158. 158. Ramírez-flores MR, Perez-limón S, Li M, Barrales-gamez B. The genetic architecture of host response suggests a trade-off between mycorrhizal and non-mycorrhizal performance in field-grown maize. 2020;
  159. 159. Fasusi OA, Amoo AE, Babalola OO. Propagation and characterization of viable arbuscular mycorrhizal fungal spores within maize plant (Zea maysL.). J Sci Food Agric. 2021;(March).
  160. 160. Ren AT, Mickan BS, Li JY, Zhou R, Zhang XC, Ma MS, et al. Soil labile organic carbon sequestration is tightly correlated with the abundance and diversity of arbuscular mycorrhizal fungi in semiarid maize fields. L Degrad Dev. 2021;32(3):1224-36.
  161. 161. Al-Maliki S, Al-Amery A, Sallal M, Radhi A, Al-Taey DKA. Effects of arbuscular mycorrhiza and organic wastes on soil carbon mineralisation, actinomycete sand nutrient content in maize plants (Zea maysl.). Malaysian J Soil Sci. 2021;25(December 2020):107-24.
  162. 162. Vosátka M, Albrechtová J. Benefits of Arbuscular Mycorrhizal Fungi to Sustainable Crop Production. In: Microbial Strategies for Crop Improvement [Internet]. Berlin, Heidelberg: Springer Berlin Heidelberg; 2009. p. 205-25. Available from:
  163. 163. Jacott CN. Trade-Offs in Arbuscular Mycorrhizal Symbiosis: Disease Resistance, Growth Responses and Perspectives for Crop Breeding. 2017;1-18.
  164. 164. Li X, Quan X, Mang M, Neumann G, Melchinger A, Ludewig U. Flint maize root mycorrhization and organic acid exudates under phosphorus deficiency: Trends in breeding lines and doubled haploid lines from landraces. J Plant Nutr Soil Sci. 2021;184(3):346-59.
  165. 165. Wang XX, van der Werf W, Yu Y, Hoffland E, Feng G, Kuyper TW. Field performance of different maize varieties in growth cores at natural and reduced mycorrhizal colonization: yield gains and possible fertilizer savings in relation to phosphorus application. Plant Soil. 2020;450(1-2):613-24.
  166. 166. Chu Q, Wang X, Yang Y, Chen F, Zhang F, Feng G. Mycorrhizal responsiveness of maize (Zea maysL.) genotypes as related to releasing date and available P content in soil. Mycorrhiza. 2013;23(6):497-505.
  167. 167. Eduardo Contreras-Liza S. Plant Breeding and Microbiome. Plant Breed - Curr Futur Views. 2021;(May).
  168. 168. Ramírez-Flores MR, Perez-Limon S, Li M, Barrales-Gamez B, Albinsky D, Paszkowski U, et al. The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation. Elife [Internet]. 2020 Nov 19;9:1-18. Available from:
  169. 169. Galluzzi G, Seyoum A, Halewood M, Noriega IL, Welch EW. The role of genetic resources in breeding for climate change: The case of public breeding programmes in eighteen developing countries. Plants. 2020;9(9):1-19.
  170. 170. Aguilar R, Carreón-Abud Y, López-Carmona D, Larsen J. Organic fertilizers alter the composition of pathogens and arbuscular mycorrhizal fungi in maize roots. J Phytopathol. 2017;165(7-8):448-54.
  171. 171. Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF. Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci. 2000;40(2):358-64.
  172. 172. Ortiz R. Role of Plant Breeding to Sustain Food Security under Climate Change. Food Secur Clim Chang. 2018;(December):145-58.
  173. 173. Xu Y, Liu X, Fu J, Wang H, Wang J, Huang C, et al. Enhancing Genetic Gain through Genomic Selection: From Livestock to Plants. Plant Commun [Internet]. 2020;1(1):100005. Available from:
  174. 174. Mores A, Borrelli GM, Laid G, Petruzzino G, Pecchioni N, Giuseppe L, et al. Genomic Approaches to Identify Molecular Bases of Crop Resistance to Diseases and to Develop Future Breeding Strategies. 2021;
  175. 175. Singh RK, Prasad A, Muthamilarasan M, Parida SK, Prasad M. Breeding and biotechnological interventions for trait improvement: status and prospects. Planta [Internet]. 2020;252(4):1-18. Available from:
  176. 176. Ahmar S, Gill RA, Jung KH, Faheem A, Qasim MU, Mubeen M, et al. Conventional and molecular techniques from simple breeding to speed breeding in crop plants: Recent advances and future outlook. Int J Mol Sci. 2020;21(7):1-24.
  177. 177. Berger F, Gutjahr C. Factors affecting plant responsiveness to arbuscular mycorrhiza. Curr Opin Plant Biol [Internet]. 2021 Feb;59:101994. Available from:
  178. 178. Jiang G-L. Molecular Markers and Marker-Assisted Breeding in Plants. In: Plant Breeding from Laboratories to Fields [Internet]. InTech; 2013. p. 45-83. Available from:
  179. 179. Collard BCY, Mackill DJ. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B Biol Sci. 2008;363(1491):557-72.
  180. 180. Badji A, Otim M, Machida L, Odong T, Kwemoi DB, Okii D, et al. Maize Combined Insect Resistance Genomic Regions and Their Co-localization With Cell Wall Constituents Revealed by Tissue-Specific QTL Meta-Analyses. Front Plant Sci [Internet]. 2018;9(July). Available from:
  181. 181. Sendek A, Karakoç C, Wagg C, Domínguez-Begines J, do Couto GM, van der Heijden MGA, et al. Drought modulates interactions between arbuscular mycorrhizal fungal diversity and barley genotype diversity. Sci Rep. 2019;9(1):1-15.
  182. 182. Chu Q, Zhang L, Zhou J, Yuan L. Soil plant-available phosphorus levels and maize genotypes determine the phosphorus acquisition efficiency and contribution of mycorrhizal pathway. 2020;
  183. 183. Nouri E, Surve R, Bapaume L, Stumpe M, Chen M, Zhang Y, et al. Phosphate Suppression of Arbuscular Mycorrhizal Symbiosis Involves Gibberellic Acid Signaling. Plant Cell Physiol. 2021;1-34.
  184. 184. Allier A, Teyssèdre S, Lehermeier C, Moreau L, Charcosset A. Optimized breeding strategies to harness genetic resources with different performance levels. BMC Genomics. 2020;21(1):1DUMM.
  185. 185. Breseghello F, Coelho ASG. Traditional and modern plant breeding methods with examples in rice (Oryza sativaL.). J Agric Food Chem. 2013;61(35):8277-86.
  186. 186. Govindaraj M, Vetriventhan M, Srinivasan M. Importance of genetic diversity assessment in crop plants and its recent advances: An overview of its analytical perspectives. Genet Res Int. 2015;2015(Figure 1).
  187. 187. Pradhan SK, Barik SR, Sahoo A, Mohapatra S, Nayak DK, Mahender A, et al. Population structure, genetic diversity and molecular marker-trait association analysis for high temperature stress tolerance in rice. PLoS One. 2016;11(8):1-23.
  188. 188. Varshney RK, Bohra A, Yu J, Graner A, Zhang Q, Sorrells ME. Designing Future Crops: Genomics-Assisted Breeding Comes of Age. Trends Plant Sci [Internet]. 2021;26(6):631-49. Available from:
  189. 189. Nadeem MA, Nawaz MA, Shahid MQ, Doğan Y, Comertpay G, Yıldız M, et al. DNA molecular markers in plant breeding: current status and recent advancements in genomic selection and genome editing. Biotechnol Biotechnol Equip [Internet]. 2017;2818:1-25. Available from:
  190. 190. Collard BCY, Mackill DJ. Marker-assisted selection : an approach for precision plant breeding in the twenty-first century Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B. 2008;363(8):557-72.
  191. 191. Wang X, Xu Y, Hu Z, Xu C. Genomic selection methods for crop improvement: Current status and prospects. Crop J [Internet]. 2018;6(4):1-11. Available from:
  192. 192. Jannink J, Lorenz AJ, Iwata H. Genomic selection in plant breeding: from theory to practice. Brief Funct Genomics. 2010;9(2):166-77.
  193. 193. Nakaya A, Isobe SN. Will genomic selection be a practical method for plant breeding ? Ann Bot. 2012;1303-16.
  194. 194. Lang M, Li X, Zheng C, Li H, Zhang J. Shading mediates the response of mycorrhizal maize (Zea maysL.) seedlings under varying levels of phosphorus. Appl Soil Ecol [Internet]. 2021;166(October):104060. Available from:
  195. 195. Liu S, Guo X, Feng G, Maimaitiaili B, Fan J, He X. Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant Soil. 2016;398(1-2):195-206.
  196. 196. Wang H, Liang L, Liu B, Huang D, Liu S, Liu R, et al. Arbuscular mycorrhizas regulate photosynthetic capacity and antioxidant defense systems to mediate salt tolerance in maize. Plants. 2020;9(11):1-17.
  197. 197. Barber NA, Kiers ET, Theis N, Hazzard R V., Adler LS. Linking agricultural practices, mycorrhizal fungi, and traits mediating plant-insect interactions. Ecol Appl. 2013;23(7):1519-30.
  198. 198. Araus JL, Kefauver SC, Zaman-Allah M, Olsen MS, Cairns JE. Translating High-Throughput Phenotyping into Genetic Gain. Trends Plant Sci. 2018;23(5):451-66.
  199. 199. Chawade A, Van Ham J, Blomquist H, Bagge O, Alexandersson E, Ortiz R. High-throughput field-phenotyping tools for plant breeding and precision agriculture. Agronomy. 2019;9(5):1-18.
  200. 200. Li D, Quan C, Song Z, Li X, Yu G, Li C, et al. High-Throughput Plant Phenotyping Platform (HT3P) as a Novel Tool for Estimating Agronomic Traits From the Lab to the Field. Front Bioeng Biotechnol. 2021;8(January):1-24.
  201. 201. Watts-Williams SJ, Jewell N, Brien C, Berger B, Garnett T, Cavagnaro TR. Using high-throughput phenotyping to explore growth responses to mycorrhizal fungi and zinc in three plant species. Plant Phenomics. 2019;2019.
  202. 202. Tran BTT, Cavagnaro TR, Jewell N, Brien C, Berger B, Watts-Williams SJ. High-throughput phenotyping reveals growth ofMedicago truncatulais positively affected by arbuscular mycorrhizal fungi even at high soil phosphorus availability. Plants, People, Planet. 2021;3(5):600-13.
  203. 203. Berger B, de Regt B, Tester M. Applications of High-Throughput Plant Phenotyping to Study Nutrient Use Efficiency. In: Plant Mineral Nutrients [Internet]. 2013. p. 277-90. Available from: internal-pdf:// for xylem sap collection3.pdf internal-pdf://0036760810/Alexou-2013-Methods for xylem sap collection.pdf internal-pdf://1843399444/Alexou-2013-Methods for xylem sap collection1.pdf internal-pdf://164926113
  204. 204. Xu Y, Li P, Yang Z, Xu C. Genetic mapping of quantitative trait loci in crops. Crop J [Internet]. 2017;5(2):175-84. Available from:
  205. 205. Kibe M, Nyaga C, Nair SK, Beyene Y, Das B, Suresh LM, et al. Combination of Linkage Mapping, GWAS , and GP to Dissect the Genetic Basis of Common Rust Resistance in Tropical Maize Germplasm. Int J Mol Sci. 2020;21(6518).
  206. 206. Arrones A, Vilanova S, Plazas M, Mangino G, Pascual L, Díez MJ, et al. The dawn of the age of multi-parent magic populations in plant breeding: Novel powerful next-generation resources for genetic analysis and selection of recombinant elite material. Biology (Basel). 2020;9(8):1-25.
  207. 207. Gage JL, Monier B, Giri A, Buckler ES. Ten years of the maize nested association mapping population: Impact, limitations, and future directions. Plant Cell. 2020;32(7):2083-93.
  208. 208. Korte A, Farlow A. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods [Internet]. 2013;9(1):1-9. Available from: Plant Methods
  209. 209. Stearns FW. One hundred years of pleiotropy: A retrospective. Genetics. 2010;186(3):767-73.
  210. 210. Jia Y, Jannink JL. Multiple-trait genomic selection methods increase genetic value prediction accuracy. Genetics. 2012;192(4):1513-22.
  211. 211. Maier RM, Zhu Z, Lee SH, Trzaskowski M, Ruderfer DM, Stahl EA, et al. Improving genetic prediction by leveraging genetic correlations among human diseases and traits. Nat Commun [Internet]. 2018;9(1):1-17. Available from:
  212. 212. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006;38(2):203-8.
  213. 213. Jaiswal V, Gahlaut V, Meher PK, Mir RR, Jaiswal JP, Rao AR, et al. Genome wide single locus single trait, multi-locus and multi-trait association mapping for some important agronomic traits in common wheat (T. aestivumL.). PLoS One. 2016;11(7):e0159343.
  214. 214. Gupta PK, Kulwal PL, Jaiswal V. Association mapping in plants in the post-GWAS genomics era. In: Advances in Genetics [Internet]. 1st ed. Elsevier Inc.; 2019. p. 1-80. Available from:
  215. 215. Zhang Y, Jia Z, Dunwell JM. Editorial: The Applications of New Multi-Locus GWAS Methodologies in the Genetic Dissection of Complex Traits. 2019;10(February):1-6.
  216. 216. Fernandes SB, Zhang KS, Jamann TM, Lipka AE. How Well Can Multivariate and Univariate GWAS Distinguish Between True and Spurious Pleiotropy? Front Genet. 2021;11(January):1-11.
  217. 217. Momen M, Mehrgardi AA, Roudbar MA, Kranis A, Pinto RM, Valente BD, et al. Including phenotypic causal networks in genome-wide association studies using mixed effects structural equation models. bioRxiv [Internet]. 2018 Oct 9;9(October):251421. Available from:
  218. 218. Verhulst B, Maes HH, Neale MC. GW - SEM: A Statistical Package to Conduct Genome - Wide Structural Equation Modeling. Behav Genet. 2017;0(0):0.
  219. 219. Momen M, Campbell MT, Walia H, Morota G. Utilizing trait networks and structural equation models as tools to interpret multi-trait genome-wide association studies. Plant Methods [Internet]. 2019;15(1):1-14. Available from:
  220. 220. Grotzinger AD, Rhemtulla M, de Vlaming R, Ritchie SJ, Mallard TT, Hill WD, et al. Genomic SEM Provides Insights into the Multivariate Genetic Architecture of Complex Traits. bioRxiv [Internet]. 2018; Available from:
  221. 221. Igolkina AA, Meshcheryakov G, Gretsova M V., Nuzhdin S V., Samsonova MG. Multi-trait multi-locus SEM model discriminates SNPs of different effects. BMC Genomics [Internet]. 2020;21(Suppl 8):1-11. Available from:
  222. 222. Badji A, Kwemoi DB, Machida L, Okii D, Mwila N, Agbahoungba S, et al. Genetic Basis of Maize Resistance to Multiple Insect Pests: Integrated Genome-Wide Comparative Mapping and Candidate Gene Prioritization. Genes (Basel) [Internet]. 2020 Jun 24;11(6):689. Available from:
  223. 223. Hassani-Pak K, Rawlings C. Knowledge Discovery in Biological Databases for Revealing Candidate Genes Linked to Complex Phenotypes. J Integr Bioinform. 2017;14(1):1-9.
  224. 224. Muthuramalingam P, Krishnan SR, Pothiraj R. Global Transcriptome Analysis of Combined Abiotic Stress Signaling Genes Unravels Key Players inOryza sativaL.: An In silico Approach. 2017;8(May):1-13.
  225. 225. Woldesemayat AA, Modise DM, Gemeildien J, Ndimba BK, Christoffels A. Cross-species multiple environmental stress responses: An integrated approach to identify candidate genes for multiple stress tolerance in sorghum (Sorghum bicolor(L.) Moench) and related model species. PLoS One. 2018;13(3):1-30.
  226. 226. Qaim M. Role of New Plant Breeding Technologies for Food Security and Sustainable Agricultural Development. Appl Econ Perspect Policy. 2020;42(2):129-50.
  227. 227. Andersen EJ, Ali S, Byamukama E, Yen Y. Disease Resistance Mechanisms in Plants. 2018;
  228. 228. Erb M, Reymond P. Molecular Interactions Between Plants and Insect Herbivores. Annu Rev Plant Biol. 2019;70(1):527-57.
  229. 229. Hickey JM, Chiurugwi T, Mackay I, Powell W. Genomic prediction unifies animal and plant breeding programs to form platforms for biological discovery. Nat Genet. 2017;49(9):1297-303.
  230. 230. Azodi CB, McCarren A, Roantree M, Campos G de los, Shiu S-H. Benchmarking algorithms for genomic prediction of complex traits. bioRxiv [Internet]. 2019;614479. Available from:
  231. 231. Moeinizade S, Hu G, Wang L, Schnable PS. Optimizing Selection and Mating in Genomic Selection with a Look-Ahead Approach: An Operations Research Framework. G3: Genes|Genomes|Genetics. 2019;9(7):2123-33.
  232. 232. Montesinos-López OA, Montesinos-López A, Crossa J, Toledo FH, Pérez-Hernández O, Eskridge KM, et al. A Genomic Bayesian Multi-trait and Multi-environment Model. G3: Genes|Genomes|Genetics [Internet]. 2016 Sep;6(9):2725-44. Available from:
  233. 233. Gill HS, Halder J, Zhang J, Brar NK, Rai TS, Hall C, et al. Multi-Trait Multi-Environment Genomic Prediction of Agronomic Traits in Advanced Breeding Lines of Winter Wheat. Front Plant Sci. 2021;12(August):1-14.
  234. 234. Montesinos-López OA, Montesinos-López A, Tuberosa R, Maccaferri M, Sciara G, Ammar K, et al. Multi-Trait, Multi-Environment Genomic Prediction of Durum Wheat With Genomic Best Linear Unbiased Predictor and Deep Learning Methods. Front Plant Sci [Internet]. 2019;10(November):1311. Available from:
  235. 235. Montesinos-López OA, Montesinos-López A, Crossa J, Gianola D, Hernández-Suárez CM, Martín-Vallejo J. Multi-trait, multi-environment deep learning modeling for genomic-enabled prediction of plant traits. G3 Genes, Genomes, Genet. 2018;8(12):3829-40.
  236. 236. de Oliveira AA, Resende MFR, Ferrão LFV, Amadeu RR, Guimarães LJM, Guimarães CT, et al. Genomic prediction applied to multiple traits and environments in second season maize hybrids. Heredity (Edinb) [Internet]. 2020;125(1-2):60-72. Available from:

Written By

Arfang Badji, Issa Diedhiou and Abdoulaye Fofana Fall

Submitted: September 12th, 2021 Reviewed: September 24th, 2021 Published: April 20th, 2022