Soybean production statistics (FAOSTAT 2010)
1. Introduction
Soil is a dynamic environment due to fluctuations in climatic conditions that affect pH, temperature, water and nutrient availability. These factors, along with agricultural management practices, affect the soil micro-flora health and the capacity for effective plant-microbe interactions. Despite these constant changes, soil constitutes one of the most productive of earth’s ecospheres and is a hub for evolutionary and other adaptive activities.
1.1. Biological nitrogen fixation
Biological nitrogen fixation (BNF) is one of the most important phenomena occurring in nature, only exceeded by photosynthesis [1,2]. One of the most common limiting factors in plant growth is the availability of nitrogen [3]. Although 4/5ths of earth’s atmosphere is comprised of nitrogen, the ability to utilize atmospheric nitrogen is restricted to a few groups of prokaryotes that are able to covert atmospheric nitrogen to ammonia and, in the case of the legume symbiosis, make some of this available to plants. Predominantly, members of the plant family Leguminosae have evolved with nitrogen fixing bacteria from the family Rhizobiaceae. In summary, the plants excrete specific chemical signals to attract the nitrogen fixing bacteria towards their roots. They also give the bacteria access to their roots, allowing them to colonize and reside in the root nodules, where the modified bacteria (bacteroids) can perform nitrogen fixation [1,4,5]. This process is of great interest to scientists in general, and agriculture specifically, since this highly complex recognition and elicitation is co-ordinated through gene expression and cellular differentiation, followed by plant growth and development; it has the potential to minimize the use of artificial nitrogen fertilizers and pesticides in crop management. This biological nitrogen fixation process is complex, but has been best examined in some detail in the context of soybean-
1.2. Soybean – The plant
Soybean (
Soybean originated in China, where it has been under cultivation for more than 5000 years [6]. The annual wild soybean (
Table 1 provides the latest statistics on soybean cultivation and production as available at FAOSTAT [15]
|
|
|
|
|
|
|
|
|
102,386,923 | 1,090,708 | 78,811,779 | 19,713,738 | 2,739,398 | 31,300 | 1,476,800 |
|
25,548 | 13,309 | 28,864 | 14,100 | 17,491 | 19,042 | 29,424 |
|
261,578,498 | 1,451,646 | 227,480,272 | 27,795,578 | 4,791,402 | 59,600 | 4,345,300 |
|
6,983,352 | 43,283 | 4,838,633 | 1,906,313 | 193,870 | 1,252 | 154,300 |
|
39,761,852 | 390,660 | 24,028,558 | 12,442,496 | 2,890,760 | 9,377 | 241,300 |
Soybean is a well-known nitrogen fixer and has been a model plant for the study of BNF. Its importance in BNF led to the genome sequencing of soybean; details of the soybean genome are available at soybase.org (
The efficiency of BNF depends on climatic factors such as temperature and photoperiod [16]; the effectiveness of a given soybean cultivar in fixing atmospheric nitrogen depends on the interaction between the cultivar’s genome and conditions such as soil moisture and soil nutrient availability [17,18]; and the competitiveness of the bacterial strains available, relative to indigenous and less effective strains, plus the amount and type of inoculants applied, and interactions with other, possibly antagonistic, agrochemicals that are used in crop protection [19]. The most important criteria, however, is the selection of an appropriate strain of
1.3. Bradyrhizobium japonicum
Initially attached to the root-hair tips of soybean plants, rhizobia colonize within the roots and are eventually localized within symbiosomes, surrounded by plant membrane. This symbiotic relationship provides a safe niche and a constant carbon source for the bacteria while the plant derives the benefits of bacterial nitrogen fixation, which allows for the use of readily available nitrogen for plant growth. Inoculation of soybean with
1.4. Lipo-chitooligosaccharide (LCO) from Bradyrhizobium japonicum
As mentioned earlier in this review, the process of nodulation in legumes begins with a complex signal exchange between host plants and rhizobia. The first step in rhizobial establishment in plant roots is production of isoflavonoids as plant-to-bacterial signals; the most common in the soybean-
Nodulation and subsequent nitrogen fixation are affected by environmental factors. It has been observed that, under sub-optimal root zone temperatures (for soybean 15-17 ºC), pH stress and in the presence of nitrogen, isoflavanoid signal levels are reduced; while high temperature (39 ºC) increases non-specific isoflavanoid production and reduces
LCOs also positively and directly affect plant growth and development in legumes and non-legumes. The potential role of LCOs in plant growth regulation was first reported by Denarie and Cullimore [47]). Nod genes A and B from
Since the protein quality of soybean plays an important role in overall agricultural and in nutraceuticals production, it is imperative that we study the proteomics of soybean and its symbiont
1.5. Proteomics as a part of integrative systems biology
The “omics” approach to knowledge gain in biology has advanced considerably in the recent years. The triangulation approach of integrating transcriptomics, proteomics and metabolomics is being used currently to study interconnectivity of molecular level responses of crop plants to various conditions of stress tolerance and adaptation of plants, thus improving systems level understanding of plant biology [60, 61].
While transcriptomics is an important tool for studying gene expression, proteomics actually portrays the functionality of the genes expressed. Several techniques are available for studying differential expression of protein profiles, and can be broadly classified as gel-based and MS (mass spectrometry)-based quantification methods. The gel based approach uses conventional, two-dimensional (2-D) gel electrophoresis, and 2-D fluorescence difference gel electrophoresis (2D-DIGE), both based on separation of proteins according to isoelectric point, followed by separation by molecular mass. The separated protein spots are then isolated and subjected to MS analysis for identification. Major drawbacks of these techniques are laborious sample preparation and inability to identify low abundance, hydrophobic and basic proteins.
The MS based approach can be a label-based quantitation, where the plants or cells are grown in media containing 15N metabolite label or using 15N as the nitrogen source. Label-free quantitation, however, is easier and allows analysis of multiple and unlimited samples. This technique, also referred to as MudPIT (multidimensional protein identification technology), is a method used to study proteins from whole-cell lysate and/or a purified complex of proteins [62,63]. The total set of proteins or proteins from designated target sites are isolated and subjected to standard protease digestions (eg. such as tryptic digestion). In brief, flash frozen leaf samples are ground in liquid nitrogen and polyphenols; tannins and other interfering substances such as chlorophyll are removed. The processed tissue is resuspended in a chaotropic reagent to extract proteins in the upper phase, and the plant debris is discarded [64-70]. The total protein set, in the resulting solution, is further quantified using the Lowry method [71]. The protein samples (2 µg of total protein each), once digested with trypsin, can then be loaded onto a microcapillary column packed with reverse phase and strong cation exchange resins. The peptides get separated in the column, based on their charge and hydrophobicity. The columns are connected to a quarternary high-performance liquid chromatography pump and coupled with an ion trap mass spectrometer, to ionize the samples within the column and spray them directly into a tandem mass spectrometer. This allows for a very effective and high level of peptide separation within the mixture, and detects the eluting peptides to produce a mass spectrum. The detected peptide ions, at measured mass-to-charge (m/z) ratios with sufficient intensity, are selected for collision-induced dissociation (CID). This procedure allows for the fragmenting of the peptides to produce a product ion spectrum, the MS/MS spectrum. In addition, the fragmentation occurs preferentially at the amide bonds, to generate N-terminal fragments (b ions) and C-terminal fragments (y ions) at specific m/z ratios, providing structural information about the amino acid sequence and sites of modification. The b ion and y ion patterns are matched to a peptide sequence in a translated genomic database to help identify the proteins present in the sample [72-75]. A variety of database searching and compiling algorithms are used to interpret the data obtained for structure and function of the identified proteins.
2. Analyses of soybean proteomics
2.1. Physiological and biological changes in the soybean proteome
2.1.1. Whole plant organs
The various tissues of soybean have specific groups of associated proteins at each developmental stage. While leaves at various developmental stages showed 26 differentially expressed proteins, the first trifoliate stage manifested the greatest increase in protein types of the outer/inner envelope of choloroplast membrane and also of the protein transport machineries. Young leaves showed abundant chaperonin-60, while HSP 70 and TP-synthase b were present in all the tissues analyzed. Age dependent correlation was observed in net photosynthesis rate, chlorophyll content and carbon assimilation. During the flowering stage, flower tissue expressed 29 proteins that were exclusively involved in protein transport and assembly of mitochondria, secondary metabolism and pollen tube growth (Ahsan and Komatsu., 2009 [76]. Soybean peroxisomal adenine nucleotide carrier (GmPNC1) is associated with the peroxisomal membrane and facilitates ATP and ADP importing activities. The proteins At PNC1 and At PNC2 are arabidopsis orthologs of Gm PNC1. Under constant darkness, Gm PNC1 increased in cotyledons up to 5 days post germination and the levels were rapidly reduced when the seedlings were exposed to light. RNA interference studies on arabidopsis At PNC1 and At PNC2 suggests that PNC1 assists with transport of ATP/ADP in the peroxisomal fatty acid-b oxidation pathway post germination (Arai et al., 2008 [77]. This probably helps the seedling establish vigour for future growth.
In order to establish if xylem proteins and the apoplast conduit are involved in long distance signalling in autoregulation of nodulation (AON) in the soybean-
Proteomic studies on chasmogamous (CH) CH cv. Toyosuzu and cleistogamous (CL) CL cv. Karafuto-1 flowerbuds using 2D gel revealed differential protein levels of β-galactosidase and protein disulfide isomerase. Cleistogamy occurs in plants under diverse stress conditions, such as drought and cold, and can also vary with temperature and light [79]. Soybean cv Maverick was used to study proteomics during seed filling stages, at 2, 3, 4, 5 and 6 weeks after flowering, using 2D and MALDI-TOF-MS. Storage proteins, proteins involved in metabolism and metabolite transport and defense related proteins were the most abundant, along with cysteine and methionine biosynthesis proteins, lipoxygenases and 14-3-3-like proteins [80,81].
Based on these findings, it is clear that the plant partitions its proteomics based on ontogeny and this specificity probably plays a crucial role in organ maturation and transition from one stage to another in the plants life cycle. Understanding this is of fundamental importance in agriculture, global food production, biofuel production and issues such as plant responses to climate change.
2.1.2. Seeds
Both 2D gel and peptide mass fingerprinting techniques (MALDI-TOF-MS) were used to study the proteins of mature and dry soybean (cv. Jefferson) seeds. Sucrose binding proteins, alcohol dehydrogenase and seed maturation proteins were some of the key proteins identified (Mooney and Thelen 2004 [82]. A comparison of four methods for protein isolation and purification from soybean seed was one of the first reports on soybean proteomics; thiourea/urea and TCA protocols were found to be the best. Proteins extracted with these two methods and further characterized by MALDI-TOF-MS and LC-MS helped identify proteins such as β-conglycinin, glycinin, Kunitz trypsin inhibitor, alcohol dehydrogenase, Gm Bd 28K allergen and sugar binding proteins in seeds [83]. The two major soybean storage proteins are α-conglycinin and glycinin. While the α-conglycinin subunits separated well in the pH range 3.0-10.0, glycinin polypeptides could be separated in pH ranges 4.0-7.0 and 6.0-11.0. Apart from these major storage proteins, this combined proteomic approach (2D-PAGE and immobilized pH gradient strips) also identified 44 storage proteins in wild soybean (
Synthesis of soybean glycinin and conglycinin, was suppressed by RNA interference. The storage protein knockdown (SP2) seeds were very similar to the wild type during development and at maturity. Proteomic analysis of the SP2 soybean genotypes and next-generation transcript sequencing (RNA-Seq) suggested that the seeds could rebalance their transcriptome and metabolome in the face of at least some alterations. GFP quantification for glycinin allele mimics further revealed that glycinin was not involved in proteome rebalance and that seeds are capable of compensating through increases in other storage proteins, to maintain normal protein content, even if the major storage proteins were not available [86].
Transgenic soybean seeds have higher amounts of malondialdehyde, ascorbate peroxidase, glutathione reductase, and catalase (29.8, 30.6, 71.4, and 35.3%, respectively) than non-transgenic seeds. Precursors of glycinin, allergen Gly m Bd 28k, actin and sucrose binding proteins were the other proteins identified [87,88]. High protein accessions of soybean (with 45 % or more protein in seeds) were compared with soybean cultivar Williams 82. 2-DE-MALDI-TOF-MS followed by Delta2D image analysis showed huge differences in 11S storage globulins amongst the accessions. In addition, the trait for high protein from PI407788A was moved to experimental line LG99-469 and was stable upon transformation [89,90].
2.1.3. Roots, root hairs and nodules
Since the root apical meristem (RAM) is responsible for the growth of the plant root system and root architecture plays and important role in determining the performance of crop plants, a proteome reference map of the soybean root apex and the differentiated root zone was established. The root apex samples comprised of 1 mm of the root apex, encasing the RAM, the quiescent center and the root cap. The predominant proteins in the root belonged to those of stress response, glycolysis, redox homeostasis and protein processing machinery. The root apex contained key proteins, such as those involved in redox homeostasis and flavonoid biosynthesis, but was underrepresented in glycolysis, stress response and TCA cycle related proteins [91]. Analysis of the proteome of isolated soybean root hair cells using 2-D gel and shotgun proteomics approaches identified proteins involved in basic cell metabolism, those whose functions are specific to root hair cell activities, including water and nutrient uptake, vesicle trafficking, and hormone and secondary metabolism [92, 93]. Proteomic studies of soybean roots and root hairs after
2.2. Soybean proteomics under stress conditions
Like all plants, soybean also encounters various stressors during its life cycle. Work related to flooding, drought, salt, heat, biotic stressors, metal toxicity, ozone, phosphorous deficiency and seed protein allergens are reviewed here.
2.2.1. Flooding stress
Plasma membrane proteins from the root and hypocotyl of soybean seedlings were purified and subjected to 2-D gel electrophoresis, followed by MS and protein sequencing, and also using nanoliquid chromatography followed by nano-LC-MS/MS based proteomics. The two techniques were used to compare the proteins present, and this indicated that during flooding stress proteins typically found in the cell wall were up-regulated in the plasma membrane. Also, the anti-oxidative proteins were up-regulated to protect the cells from oxidative damage, heat shock proteins to protect protein degradation and signaling proteins to regulate ion homeostasis [97]. MS based proteomics applied to root tips of two-day-old seedlings flooded for 1 day showed increased levels of proteins involved in energy production. Proteins involved in cell structure maintenance and protein folding were negatively affected, as was their phosphorylation status [98].
Two-day-old germinated soybean seeds were subjected to water logging for 12 h and total RNA and proteins were analyzed from the root and hypocotyl. At the transcriptional level, the expression of genes for alcohol fermentation, ethylene biosynthesis, pathogen defense, and cell wall loosening were all significantly up-regulated, while scavengers and chaperons of reactive oxygen species were seen to change only at the translational level. Transcriptional and translational level changes were observed for hemoglobin, acid phosphatase, and Kunitz trypsin protease inhibitors. This adaptive strategy might be for both hypoxia and more direct damage of cells by excessive water [99]). Proteins from 2-day-old soybean seedlings flooded for 12 h were analyzed using 2-D gel MS, 2-D fluorescence difference gel electrophoresis, and nanoliquid chromatography. Early responses to flooding involved proteins related to glycolysis and fermentation, and inducers of heat shock proteins. Glucose degradation and sucrose accumulation increased due to activation of glycolysis and down-regulation of sucrose degrading enzymes, in addition the methylglyoxal pathway, a detoxification system linked to glycolysis, was up-regulated. 2-D gel based phosphoproteomic analysis showed that proteins involved in protein synthesis and folding were dephosphorylated under flooding conditions [100]. Water logging stress imposed on very early soybean seedlings (V2 stage) resulted in a gradual increase of lipid peroxidation and
Soybean seeds germinated for 48 h were subjected to water logging stress for 6-48 h. In addition to general stress responses due to increases in reactive oxygen species scavengers, several glycolytic enzymes were up-regulated, suggesting changes in energy generation [103].
2.2.2. Water stress – Drought
Soybean root activities are affected during water stress. The root can be partitioned into zones 1 (apical 4 mm zone) and 2 (4-8 mm zone), based on maximum elongation during well watered conditions. Soluble proteins from these regions, studied under both well-watered and water deficit stress conditions, revealed region-specific regulation of the phenylpropanoid pathway. Zone 1 of roots manifested increases in isoflavanoid biosynthesis related enzymes and proteins that contribute to growth and maintenance of the roots under water stress conditions. However, zone 2 of water stressed roots manifested up-regulation of caffeoyl-CoA
2.2.3. High temperature stress
Tissue specific proteomics under high temperature stress revealed 54, 35 and 61 differentially expressed proteins in the leaves, stems and roots, respectively. Heat shock proteins and those involved in antioxidant defense were up-regulated while proteins for photosynthesis, amino acid and protein synthesis and secondary metabolism were down- regulated. HSP70 and other low molecular weight HSPs were seen in all the tissues analyzed. ChsHSP and CPN-60 were tissue specific and the sHSPs were found only in tissues under heat stress, and were not induced by other stresses such as cold or hydrogen peroxide exposure [107].
2.2.4. Salt stress
Salt stress is also an important abiotic stressor that affects crop growth and productivity. Of the 20% of agricultural land available globally, 50% of the cropland is estimated by the United Nations Environment Program (The UNEP) to be salt-stressed [108]. As the plant grows under salt stresses conditions, depending on the severity of the stress, the plants can experience reduced photosynthesis, protein and energy production, and changes in lipid metabolism [109,110]. As soil salinity increase, the effects on seed germination and germinating seedlings are profound. Responses to salinity and drought stress are similar; they affect the osmotic activity of the root system, thereby affecting the movement of water and nutrients into the plants. In Canadian soils, salinity varies between spring and fall and the most saline conditions are seen at the soil surface just after spring thaw. In the Canadian prairies, the dominant salts of saline seeps include calcium (Ca), magnesium (Mg) and sodium (Na) cations, and sulphate (SO4-) anions [111]. Soybean is very sensitive to Cl-, but not greatly affected by Na+, because of its ability to restrict movement of Na+ to leaves [112].
This first report regarding soybean seedling proteomic responses to salt stress evaluated length and fresh weight of the hypocotyl and roots of soybean exposed to a series of NaCl concentrations. At 200 mM NaCl, the length and fresh weight of hypocotyl and roots were greatly reduced, with a simultaneous increase in proline content, suggesting activation of mechanisms for coping with salt stress. In addition, hypocotyl and root samples from 100 mM NaCl treated seedlings up-regulated seven key proteins, such as late embryogenesis-abundant protein, b-conglycinin, elicitor peptide three precursor, and basic/helix-loop-helix protein. The same treatment caused down-regulation of protease inhibitor, lectin, and stem 31-kDa glycoprotein precursor. This combination of up- and down-regulated proteins indicates a metabolic shift and could represent a strategy used by soybean seedlings to enhance tolerance of, or adapt to, salt stress [113].
Sobhanian et al. [110,114] found that treatment of soybean seedlings with 80 mM NaCl arrests the growth and development of both hypocotyl and roots. This study assessed effects on leaf, hypocotyl and root proteomics of salt treated soybean seedlings and found that reduction of glyceraldehyde-3-phospahte dehydrogenase was indicative of reduction in ATP production, and down-regulation of calreticulin was associated with disruption in the calcium signalling pathway, both of which are associated with decreased plant growth. The levels of other proteins, such as kinesin motor protein, trypsin inhibitor, alcohol dehydrogenase and annexin, were also found to change, suggesting that these proteins might play different roles in soybean salt tolerance and adaptation [110,114].
Soybean cultivars Lee68 and N2899 are salt-tolerant and salt-sensitive, respectively. The percentage germination was not affected when exposed to 100 mmol L-1 NaCl, however, the mean germination time for Lee68 (0.3 days) and N2899 (1.0 day) was delayed, compared with control plants. Hormonal responses to salt stress differed between these cultivars. Both cultivars, increased abscisic acid levels and decreased giberrelic acid (GA 1, 3) and isopentyladenosine concentrations; auxin (IAA) increased in Lee68, but remained unchanged in N2899. 2-D gel electrophoresis, followed by MALDI-TOF-MS analysis, of the proteins from germinated seeds suggested increases in ferritin and the 20S proteasome subunit β-6 in both the cultivars. Glyceraldehyde 3-phosphate dehydrogenase, glutathione
2.2.5. Biotic stress
The soybean-
Soybean mosaic virus (SBMV) causes one of the most serious viral infections of soybean; leaves of infected plants were studied at a series of time points using 2-D gel electrophoresis, followed by MALDI-TOF-MS and tandem TOF/TOF-MS. Proteins expressed in the inoculated leaves were identified and were seen to be involved in protein degradation, defense signalling, coping with changes in the levels of reactive oxygen species, cell wall reinforcement, and energy and metabolism regulation. Quantitative real time PCR was used to focus on gene expression related to some of these proteins. Photosynthesis and metabolism related genes were down-regulated at all the time points, while most of the energy related genes (respiration in this case) were up-regulated for at least five of the six time points studied [117]. At the time of this writing, this report is the only one addressing the proteomic approach to molecular understanding of soybean-SBMV interaction.
2.2.6. Other miscellaneous stress related reports
Aluminium toxicity is often observed in acidic soils and Baxi 10 (BX10) is an Al-resistant cultivar. One-week-old soybean seedlings treated with 50 mM AlCl3 for 24, 48 and 72 h were studied for characterization of root proteins in response to Al; and 2-D gel electrophoresis followed by MS revealed 39 proteins expressed differentially following Al treatment. Of these 21 were up-regulated (such as heat shock proteins, glutathione S-transferase, chalcone related synthetase, GTP-binding protein, ABC transporters and ATP binding proteins). Five proteins were also down-regulated and 15 newly induced proteins were present following AL treatment [118].
The process of nitrogen fixation demands large amounts of phosphorus [119]. When soybean plants are starved of phosphorus, 44 phosphate starvation proteins are expressed in soybean nodules [120].
Label free proteomics, coupled with multiple reaction monitoring (MRM) with synthetic isotope labelled peptides, was used to study 10 allergens from 20 non-genetically modified commercial varieties of soybean. The concentration of these allergens varied between 0.5-5.7
The responses of soybean plants exposed to 116 ppb O3 involved significant changes to carbon metabolism, photosynthesis, amino acid, flavanoid and isoprenoid biosynthesis, signaling, homeostasis, anti-oxidant and redox pathways [122], as indicated by shifts in expression of the relevant proteins.
More information regarding soybean functional genomics and proteomics is available at the publicly accessible Soybean Knowledgebase (SoyKB) http://soykb.org/ [123].
3. Bradyrhizobium japonicum and its proteomics/exoproteomics
Culturing bacteria
Since competitiveness plays an important role in this symbiotic relationship, 2-D gel electrophoresis, image and data analysis, and in-gel digestion proteomic studies, were conducted on
A study of 2-D gel electrophoresis combined with MALDI-TOF MS for the identification of
4. Other dimensions to soybean-rhizobacteria interactions
Apart from
Bacteriocins are grouped into four distinct classes based on the peptide characteristics such as post translational modifications, side chains, heat stability, N-terminal sequence homology and molecular weight [140].
Proteomic profiling of both these bacteria are underway in our laboratory and we hope to acquire some indications of plant proteomic shifts related to biological nitrogen fixation through these experiments over the next few months.
5. Conclusions and future perspectives
Soybean is an important protein and oil seed crop and BNF is an important source of nitrogen for the crop. Considerable work has been conducted regarding soybean proteomics, facilitated by recent advancements in technology, but a more systematic approach to this method is required in order to understand the intricacies of plant growth and development in the face of interactions with various symbionts. There is wide variation in the ability of
References
- 1.
Vance CP. Legume symbiotic nitrogen fixation: agronomic aspects 1998. In The Rhizobiaceae: Molecular biology of model Plant-Associated bacteria, eds., Spaink HP, Kondorosi A, Hooykaas PJJ, Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 509-530. - 2.
Graham PH, Vance CP. Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Research 2000;65: 93-106. - 3.
Newbould P. The use of nitrogen fertilizers in agriculture. Where do we go practically and ecologically? Plant Soil 1989;115: 297-311. - 4.
Sadowsky MJ, Graham PH. Soil biology of the Rhizobiaceae 1998. In: (Spaink HP, Kondorosi A, Hooykaas PJJ. ed. The Rhizobiaceae, 155-172. (Kluwer: Dordrecht, The Netherlands). - 5.
Graham PH, Vance CP. Legumes: Importance and constraints to greater use. Plant Physiology 2003;131: 872-877. - 6.
Cui Z, Carter TE, Gai J, Qui J, Nelson RL. Origin, description, and pedigree of Chinese soybean cultivars released from 1923 to 1995. U.S. Department of Agriculture, Agricultural Research Service, Tech. Bull 1999; No. 1871. - 7.
Hymowitz T, Harlan JR. Introduction of soybean to North America by Samuel Bowen in 1765. Economic Botany 1983;37:371-379. - 8.
Qui L-J, Chang R-Z: The origin and history of soybean 2010. In The soybean : botany, production and uses / edited by Guriqbal Singh. Pp- 1-23, CAB International. - 9.
Lui K. Soybeans as a powerhouse of nutrients and phytochemicals. In Soybeans as functional foods and ingredients; Lui K., Ed.;AOCS Press: Champaign, IL 2004;p1-53. - 10.
Mandal KG, Sahab KP, Ghosha PH, Hatia KM and Bandyopadhyaya KK. Bioenergy and economic analysis of soybean-based crop production systems in central India. Biomass and Bioenergy 2002; 23:337-345. - 11.
Du W, Xu Y, Liu D. Lipase-catalysed transesterification of soya bean oil for biodiesel production during continuous batch operation. Biotechnology and Applied Biochemistry 2003;38(Pt 2):103-6. - 12.
Mushrush GW, Wynne JH, Willauer HD, Lloyd CL. Soybean-derived biofuels and home heating fuels. Journal of Environmental Science and Health. Part A-Toxic/Hazardous Substances and Environmental Engineering 2006;41(11):2495-502. - 13.
Huo H, Wang M, Bloyd C, Putsche V. Life-cycle assessment of energy use and greenhouse gas emissions of soybean-derived biodiesel and renewable fuels. Environmental Science and Technology 2009;43(3):750-6. - 14.
Pestana-Calsa MC, Pacheco CM, de Castro RC, de Almeida RR, de Lira NP, Junior TC. Cell wall, lignin and fatty acid-related transcriptome in soybean: Achieving gene expression patterns for bioenergy legume. Genetics and Molecular Biology 2012;35(1 (suppl)):322-330. - 15.
FAO (2009) FAOSTAT . Food and Agriculture Organization of the United Nations, Rome, Italy. Available at: http://faostat.fao.org (last accessed 8 July 2012). - 16.
Shiraiwa T, Sakashita M, Yagi Y, Horie T. Nitrogen fixation and seed yield in soybean under moderate high-temperature stress. Plant Production Science 2006;9: 165–167. - 17.
Sridhara S, Thimmegowda S, Prasad TG. Effect of water regimes and moisture stress at different growth stages on nodule dynamics, nitrogenase activity and nitrogen fixation in soybean [ Glycine max (L.) Merrill]. Journal of Agronomy and Crop Science 1995;174: 111-115. - 18.
Jung G, Matsunami T, Oki Y, Kokubun M. Effects of water logging on nitrogen fixation and photosynthesis in supernodulating soybean cultivar Kanto 100. Plant Production Science 2008;11: 291-297. - 19.
Campo RJ, Hungria M. Sources of nitrogen to reach high soybean yields 2004: In: Proceedings of VII World Soybean Research Conference ,IV International Soybean Processing and Utilization Conference ,III Congresso Brasileiro de Soja Brazilian Soybean Congress , Foz do Iguassu, PR, Brazil, 29 February–5 March 2004, pp. 1275-1280. - 20.
Hughes RM, Herridge DF. Effect of tillage on yield, nodulation and nitrogen fixation of soybean in far north-coastal New South Wales. Australian Journal of Experimental Agriculture 1989;29: 671-677. - 21.
Alves BJR, Boddey RM, Urquiaga S. The success of BNF in soybean in Brazil. Plant and Soil 2003;252: 1-9. - 22.
Abaidoo RC, Keyser HH, Singleton PW, Dashiell KE, Sanginga N. Population size, distribution, and symbiotic characteristics of indigenous Bradyrhizobium spp. that nodulate TGx soybean genotypes in Africa. Applied Soil Ecology 2007;35: 57-67. - 23.
Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A. Nitrogen uptake, fixation and response to fertilizer N in soybeans: A review. Field Crops Research 2008;108: 1-13. - 24.
Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Research 2002a; 9:189-197. - 25.
Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (supplement). DNA Research 2002b;9: 225-256. - 26.
Ndakidemi PA, Dakora FD, Nkonya EM, Ringo D, Mansoor H. Yield and economic benefits of common bean ( Phaseolus vulgaris ) and soybean (Glycine max ) inoculation in northern Tanzania. Australian Journal of Experimental Agriculture2006;46: 571-577. - 27.
Mateos PF, Baker DL, Petersen M, Velázquez E, Jiménez-Zurdo JI, Martínez-Molina E, Squartini A, Orgambide G, Hubbell DH, Dazzo FB. Erosion of root epidermal cell walls by rhizobium polysaccharide-degrading enzymes as related to primary host infection in the rhizobium–legume symbiosis. Canadian Journal of Microbiology 2001;47: 475-487. - 28.
Salminen SO, Streeter JG. Uptake and metabolism of carbohydrates by Bradyrhizobium japonicum bacteroids. Plant Physiology 1986; 83: 535-540. - 29.
Müller J, Boller T, Wiemken A. Trehalose becomes the most abundant non-structural carbohydrate during senescence of soybean nodules. Journal of Experimental Botany 2001;52(358):943-7. - 30.
Streeter JG, Gomez ML. Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroids from soybean nodules. Applied and Environmental Microbiology 2006;72(6):4250-5. - 31.
Sugawara M, Cytryn EJ, Sadowsky MJ. Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Applied and Environmental Microbiology 2010;76(4):1071-81. - 32.
Rao JR, Cooper JE () Rhizobia catabolize gene-inducing flavanoid via C-ring fission mechanisms. Journal of Bacteriology 1994;176: 5409-5413. - 33.
Mabood F, Souleimanov A, Khan W and Smith DL. Jasmonates induce Nod factor production by Bradyrhizobium japonicum . Plant Physiology and Biochemistry 2006a;44:759–765. - 34.
Mabood F, Zhou X and Smith DL. Pre-incubation of Bradyrhizobium japonicum cells with methyl jasmonate (MeJA) increases soybean nodulation and nitrogen fixation under short season field conditions. Agronomy Journal 2006b;98:289–294. - 35.
Mabood F, Zhou X, Lee KD, Smith DL. Methyl jasmonate, alone or in combination with genistein, and Bradyrhizobium japonicum increases soybean (Glycine max L.) plant dry matter production and grain yield under short season conditions. Field Crops Research 2006c;95:412-419. - 36.
Mabood F and Smith DL. Pre-incubation of Bradyrhizobium japonicum with jasmonates accelerates nodulation and nitrogen fixation in soybean (Glycine max ) at optimal and suboptimal root zone temperatures. Physiologia Plantarum 2005;125:311-325. - 37.
Spaink H, Wijfjes A, Lugtenberg B. Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides. Journal of Bacteriology 1995;177: 6276-6281. - 38.
Perret X, Staehelin C, Broughton WJ. Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews 2000;64: 180-201. - 39.
Kamst E, Spaink HP, Kafetzopoulos D (1998) Biosynthesis and secretion of rhizobial lipochitin-oligosaccharide signal molecules. Pages 29-71 in: Subcellular Biochemistry 29: Plant-Microbe Interactions. B. B. Biswas and H. K. Das, eds. Plenum Press, New York - 40.
Vazquez M, Santana O, Quinto C. The NodI and NodJ proteins from Rhizobium andBradyrhizobium strains are similar to capsular polysaccharide secretion proteins from gram-negative bacteria. Molecular Microbiology 1993;8: 369-377. - 41.
Carlson R, Price N, Stacey G. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Molecular Plant Microbe Interactions 1994;7: 684-95. - 42.
Schultze M, Kondorosi Á. The role of lipochitooligosaccharides in root nodule organogenesis and plant cell growth. Current Opinion in Genetics and Development 1996;6: 631-638. - 43.
Schultze M, Kondorosi Á. Regulation of symbiotic root nodule development. Annual Reviews in Genetics 1998;32: 33-57. - 44.
Bai Y, D’Aoust F, Smith DL, Driscoll BT. Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Canadian Journal of Microbiology 2002a;48: 230-238. - 45.
Prithiviraj B, Souleimanov A, Zhou X, Smith DL. Differential response of soybean ( Glycine max (L.) Merr.) genotypes to lipo-chito-ligosaccharide Nod Bj-V (C18:1 MeFuc). Journal of Experimental Botany 2000;51: 2045-2051. - 46.
López-Lara I, Drift K, Brussel A, Haverkamp J, Lugtenberg B, Thomas-Oates J, Spaink H. Induction of nodule primordia on Phaseolus andAcacia by lipo-chitin oligosaccharide nodulation signals from broad-host-range rhizobium strain GRH2. Plant Molecular Biology 1995;29: 465-477. - 47.
Denarie J, Cullimore J. Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell 1993;74: 951-954. - 48.
Schmidt J, Rohrig H, John M, Wieneke U, Stacey G, Koncz C, Schell J. Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant Journal 1993;4: 651-658. - 49.
Dyachok J, Tobin A, Price N, von Arnold S. Rhizobial Nod factors stimulate somatic embryo development in Picea abies . Plant Cell Reports 2000;19: 290-297. - 50.
Dyachok J, Wiweger M, Kenne L, von Arnold S. Endogenous nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiology 2002;128: 523-533. - 51.
Cook D, Dreyer D, Bonnet D, Howell M, Nony E, VandenBosch K. Transient induction of a peroxidase gene in Medicago truncatula precedes infection byRhizobium meliloti . The Plant Cell 1995;7: 43-55. - 52.
Inui H, Yamaguchi Y, Hirano S. Elicitor actions of N-acetylchitooligosaccharides and laminarioligosaccharides for chitinase and L-phenylalanine ammonia-lyase induction in rice suspension culture. Bioscience, Biotechnology and Biochemistry 1997;61: 975-978. - 53.
Zhang F, Smith DL. Interorganismal signaling in suboptimum environments: the legume–rhizobia symbiosis. Advances in Agronomy 2001;76: 125–161. - 54.
Souleimanov A, Prithiviraj B, Smith DL. The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. Journal of Experimental Botany 2002a;53: 1929-1934. - 55.
Souleimanov A, Prithiviraj B, Carlson RW, Jeyaretnam B, Smith DL. Isolation and characterization of the major nod factor of Bradyrhizobium japonicum strain 532C. Microbiological Research 2002b;157: 25-28. - 56.
Khan W (2003) Signal compounds involved with plant perception and response to microbes alter plant physiological activities and growth of crop plants. PhD Thesis, McGill University. - 57.
Chen C, McIver J, Yang Y, Bai Y, Schultz B, McIver A. Foliar application of lipo-chitooligosaccharides (Nod factors) to tomato ( Lycopersicon esculentum ) enhances flowering and fruit production. Canadian Journal of Plant Science 2007;87: 365-372. - 58.
Oláh B, Brière C, Bécard G, Dénarié J, Gough C. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant Journal 2005;44: 195-207. - 59.
Wang N, Khan W, Smith DL. Changes in soybean global gene expression after application of Lipo-chitooligosaccharide from Bradyrhizobium japonicum under sub-optimal temperature. PLoS ONE 2012;7(2): e31571. - 60.
Sha Valli Khan PS, Hoffmann L, Renaut J, Hausman JF Current initiatives in proteomics for the analysis of plant salt tolerance, Current Science 2007;93: 6-11. - 61.
Nanjo Y, Nouri M-Z, Komatsu S. Quantitative proteomic analyses of crop seedlings subjected to stress conditions; a commentary. Phytochemistry 2011;72: 1263-1272. - 62.
Paoletti AC, Zybailov B, Washburn MP. Principles and applications of multidimensional protein identification technology. Expert Review of Proteomics 2004;1: 275-282. - 63.
Delahunty C, Yates JR. Protein identification using 2D-LC-MS/MS. Methods 2005;35(3): 248–255. - 64.
Herbert BR, Molloy MP, Gooley AA, Walsh BJ, Bryson WG, Williams KL. Improved protein solubility in two-dimensional electrophoresis using tributyl phosphine as reducing agent. Electrophoresis 1998;19(5):845-51. - 65.
Molloy MP, Herbert BR, Walsh BJ, Tyler MI, Traini M, Sanchez JC, Hochstrasser DF, Williams KL, Gooley AA. Extraction of membrane proteins by differential solubilization for separation using two-dimensional gel electrophoresis. Electrophoresis 1998;19(5):837-44. - 66.
Ferro M, Seigneurin-Berny D, Rolland N, Chapel A, Salvi D, Garin J, Joyard J. Organic solvent extraction as a versatile procedure to identify hydrophobic chloroplast membrane proteins. Electrophoresis 2000;21: 3517-3526. - 67.
Cilia M, Fish T, Yang X, McLaughlin M, Thannhauser TW, Gray S. A comparison of protein extraction methods suitable for gel-based proteomic studies of aphid proteins. Journal of Biomolecular Techniques 2009;20(4): 201-215. - 68.
Amalraj RS, Selvaraj N, Veluswamy GK, Ramanujan RP, Muthurajan R, Agrawal GK, Rakwal R, Viswanathan R. Sugarcane proteomics: establishment of a protein extraction method for 2-DE in stalk tissues and initiation of sugarcane proteome reference map. Electrophoresis 2010;31(12): 1959-1974. - 69.
Dawe AL, Mu R, Rivera G, Salamon JA. Molecular methods for studying the Cryphonectria parasitica - hypovirus experimental system. Methods in Molecular Biology 2011;722, 225-236. - 70.
Koay SY, Gam LH. Method development for analysis of proteins extracted from the leaves of Orthosiphon aristatus . Journal of Chromatography B. Analytical Technologies in The Biomedical and Life Sciences 2011;879: 2179-2183. - 71.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin phenol reagent. Journal of Biological Chemistry 1951;193: 265-275. - 72.
Washburn MP, Ulaszek R, Deciu C, Schieltz DM, Yates JR. III. Analysis of quantitative proteomic data generated via multidimensional protein identification technology. Analytical Chemistry 2002;74: 1650-1657. - 73.
Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 2003;422(6928): 198-207. - 74.
Lill J. Proteomic tools for quantitation by mass spectrometry. Mass Spectrometry Reviews 2003;22(3): 182-194. - 75.
Liu H, Sadygov RG, Yates JR. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Analytical Chemistry 2004;76: 4193-4201. - 76.
Ahsan N, Komatsu S. Comparative analyses of the proteomes of leaves and flowers at various stages of development reveal organ specific functional differentiation of proteins in soybean. Proteomics 2009;9: 4889-4907. - 77.
Arai Y, Hayashi M, Nishimura M. Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid b-oxidation in soybean and arabidopsis. The Plant Cell 2008;20: 3227-3240. - 78.
Djordjevic MA, Oakes M, Li DX, Hwang CH, Hocart CH, and Gresshoff PM. The glycine max xylem sap and apoplast proteome. Journal of Proteome Research 2007;6: 3771-3779. - 79.
Khan NA, Takahashi R, Abe J, Komatsu S. Identification of cleistogamy-associated proteins in flower buds of near-isogenic lines of soybean by differential proteomic analysis. Peptides 2009;30: 2095-2102. - 80.
Hajduch M, Ganapathy A, Stein JW, Thelen JJ. A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiology 2005;137: 1397-1419. - 81.
http://www.oilseedproteomics.missouri.edu/soybean.php - 82.
Mooney BP, Thelen JJ. High-throughput peptide mass fingerprinting of soybean seed proteins: automated workflow and utility of UniGene expressed sequence tag databases for protein identification. Phytochemistry 2004;65: 1733-1744. - 83.
Natarajan SS, Xu C, Caperna TJ, Garrett WM. Comparison of protein solubilization methods suitable for proteomic analysis of soybean seed proteins. Analytical Biochemistry 2005;342: 214-220. - 84.
Natarajan SS, Xu C, Bae H, Caperna TJ, Garrett WM. Characterization of storage proteins in wild ( Glycine soja ) and cultivated (Glycine max ) soybean seeds using proteomic analysis. Journal of Agriculture and Food Chemistry 2006;54: 3114-3120. - 85.
Kim HT, Choi U-K, Ryu HS, Lee SJ, Kwon O-S. Mobilization of storage proteins in soybean seed ( Glycine max L.) during germination and seedling growth. Biochimica et Biophysica Acta 2011;1814: 1178-1187. - 86.
Schmidt MA, Barbazuk WB, Sandford M, May G, Song Z, Zhou W, Nikolau BJ, Herman EM. Silencing of soybean seed storage proteins results in a rebalanced protein composition preserving seed protein content without major collateral changes in the metabolome and transcriptome. Plant Physiology 2011; 156: 330-345. - 87.
Brandao AR, Barbosa HS, Arruda MAZ. Image analysis of two-dimensional gel electrophoresis for comparative proteomics of transgenic and non-transgenic soybean seeds. Journal of proteomics 2010;73: 1433-1440. - 88.
Barbosa HS, Arruda SCC, Azevedo RA, Arruda MAZ. New insights on proteomics of transgenic soybean seeds: evaluation of differential expressions of enzymes and proteins. Analytical and Bioanalytical Chemistry 2012;402: 299-314. - 89.
Krishnan HB. Evidence for accumulation of the β-subunit of β-conglycinin in soybean [ Glycine max (L) Merr.] embryonic axes. Plant Cell report 2002;20: 869-875. - 90.
Krishnan HB, Nelson RL. Proteomic analysis of high protein soybean ( Glycine max ) accessions demonstrates the contribution of novel glycinin subunits. Journal of Agriculture and Food Chemistry 2011;59: 2432-2439. - 91.
Mathesius U, Djordjevic MA, Oakes M, Goffard N, Haerizadeh F, Weiller GF, Singh MB, Bhalla PL. Comparative proteomic profiles of the soybean ( Glycine max ) root apex and differentiated root zone. Proteomics 2011;11: 1707-1719. - 92.
Brechenmacher L, Lee J, Sachdev S, Song Z, Nguyen THN, Joshi T, Oehrle N, Libault M, Mooney B, Xu D, Cooper B, Stacey G. Establishment of a protein reference map for soybean root hair cells. Plant Physiology 2009;149: 670-682. - 93.
Toorchi M, Yukawa K, Nouri M-Z, Komatsu S. Proteomics approach for identifying osmotic-stress-related proteins in soybean roots. Peptides 2009;30: 2108-2117. - 94.
Wan J, Torres M, Ganapathy A, Thelen J, DaGue BB, Mooney B, Xu D, Gary Stacey. Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum. Molecular Plant Microbe Interactions 2005;18: 458–467. - 95.
Oerhle NW, Sarma AD, Waters JK, Emerich DW. Proteomic analysis of soybean nodule cytosol. Phytochemistry 2008;69: 2426-2438. - 96.
Panter S, Thomson R, de Bruxelles G, Laver D, Trevaskis B, Udvardi M. Identification with proteomics of novel proteins associated with the peribacteroid membrane of soybean root nodules. Molecular Plant Microbe Interactions 2000;13: 325-333. - 97.
Komatsu S, Wada T, Abale´a Y, Nouri M-Z, Nanjo Y, Nakayama N, Shimamura S, Yamamoto R, Nakamura T, Furukawa K. Analysis of plasma membrane proteome in soybean and application to flooding stress response. Journal of Proteome Research 2009a;8: 4487-4499. - 98.
Nanjo Y, Skultety L, Uváčková L, Klubicová K, Hajduch M, Komatsu S. Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. Journal of Proteome Research 2012;11: 372-385. - 99.
Komatsu S, Yamamoto R, Nanjo Y, Mikami Y, Yunokawa H, Sakata K. A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. Journal of Proteome Research 2009b;8: 4766-4778. - 100.
Nanjo Y, Skultety L, Ashraf Y, Komatsu S. Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. Journal of Proteome Research 2010;9: 3989-4002. - 101.
Alam I, Lee D-G, Kim K-H, Park C-H, Sharmin S A, Lee H, Oh K-W, Yun B-W, Lee B-H. Proteome analysis of soybean roots under water logging stress at an early vegetative stage. Journal of Biosciences 2010;35: 49-62. - 102.
Komatsu S, Yamamoto A, Nakamura T, Nouri M-Z, Nanjo Y, Nishizawa K, Furukawa K. Comprehensive analysis of mitochondria in roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. Journal of Proteome Research 2011;10: 3993-4004. - 103.
Hashiguchi A, Sakata K, Komatsu S. Proteome analysis of early-stage soybean seedlings under flooding stress. Journal of Proteome Research 2009;8: 2058-2069. - 104.
Yamaguchi M, Valliyodan B, Zhang J, Lenoble ME, Yu O, Rogers EE, Nguyen HT, Sharp RE. Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant, Cell and Environment 2010;33: 223-243. - 105.
Nouri M-Z, Komatsu S. Comparative analysis of soybean plasma membrane proteins under osmotic stress using gel-based and LC MS/MS-based proteomics approaches. Proteomics 2010;10: 1930-1945. - 106.
Mohammadi PP, Moieni A, Hiraga S, Komatsu S. Organ specific proteomic analysis of drought-stressed soybean seedlings. Journal of proteomics 2012;75: 1906-1923. - 107.
Ahsan N, Donnart T, Nouri M-Z, Komatsu S. Tissue-specific defense and thermo-adaptive mechanisms of soybean seedlings under heat stress revealed by proteomic approach. Journal of Proteome Research 2010;9: 4189-4204. - 108.
Yan L. Effect of salt stress on seed germination and seedling growth of three salinity plants. Pakistan Journal of Biological Sciences 2008;11: 1268-1272. - 109.
Parida AK, Das AB. Salt tolerance and salinity effects on plants: a review. Exotoxicology and Environmental Safety 2005;60:324-49. - 110.
Sobhanian H, Aghaei K, Komatsu S. Changes in the plant proteome resulting from salt stress: Towards the creation of salt tolerant crops? Journal of proteomics 2011;74: 1323-1337. - 111.
Agri-Facts: Salt tolerance of Plants: http://www1.agric.gov.ab.ca Nov 2001(last accessed 12th July 2012). - 112.
Dabuxilatu MI, Ikeda M. Distribution of K, Na and Cl in root and leaf cells of soybean and cucumber plants grown under salinity conditions. Soil Science Plant Nutrition 2005;51:1053-7. - 113.
Aghaei K, Ehsanpour AA, Shah AH, Komatsu S. Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 2009;36: 91-98. - 114.
Sobhanian H, Razavizadeh R, nanjo Y, Ehsanpour AA, Rastgar Jazii F, Motamed N, Komatsu S. Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Science 2010; 8: 1-15. - 115.
Xu X-Y, Fan R, Zheng R, Li C-M, Yu D-Y. Proteomic analysis of seed germination under salt stress in soybeans. Journal Zhejiang Univ-Sci B (Biomedicine and Biotechnology) 2011;12: 507-517. - 116.
Zhang YM, Zhao JM, Xiang Y, Bian XC, Zuo QM, Shen Q, Gai JY, Xing H. Proteomics study of changes in soybean lines resistant and sensitive to Phytophthora sojae . Proteome Science 2011;9: 52 – doi:10.1186/1477-5956-9-52 - 117.
Yang H, Huang Y, Zhi H, Yu D. Proteomics-based analysis of novel genes involved in response toward soybean mosaic virus infection. Molecular Biology Reports 2011;38:511-521. - 118.
Zhena Y, Qia J-L, Wanga S-S, Sua J, Xua G-H, Zhanga M-S, Miaoa L, Pengb X-X, Tiana D and Yanga Y-H. Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Physiologia Plantarum 2007;131: 542-554. - 119.
Vance CP. Symbiotic nitrogen fixation and phosphorus acquisition: plant nutrition in a world of declining renewable resources. Plant Physiology 2001;127: 390-397. - 120.
Chen Z, Cui Q, Liang C, Sun L, Tian J, Liao H. Identification of differentially expressed proteins in soybean nodules under phosphorus deficiency through proteomic analysis. Proteomics 2011;11: 4648-4659. - 121.
Houston NL, Lee D-G, Stevenson SE, Ladics GS, Bannon GA, McClain S, Privalle L, Stagg N, Herouet-Guicheney C, MacIntosh SC, Thelen JJ. Quantitation of soybean allergens using tandem mass spectrometry. Journal of Proteome Research 2011;10: 763-773. - 122.
Galant A, Koester RP, Ainsworth EA, Hicks LM, Jez JM. From climate change to molecular response: redox proteomics of ozone-induced responses in soybean. New Phytologist 2012;194: 220-229. - 123.
Joshi T, Patil K, Fitzpatrick MR, Franklin LD, Yao Q, Jeffrey R Cook JR, Wang Z, Libault M, Brechenmacher L, Valliyodan B, Wu X, Cheng J, Stacey G, Nguyen HT, Xu D. Soybean Knowledge Base (SoyKB): a web resource for soybean translational genomics. BMC Genomics 2012; 13 (Suppl 1):S15. - 124.
Sarma AD, Emerich DW. A comparative proteomic evaluation of culture grown vs nodule isolated Bradyrhizobium japonicum . Proteomics 2006;6(10):3008-28. - 125.
http://www.kazusa.or.jp/index.html (last accessed 12th July 2012). - 126.
Sarma AD, Emerich DW. Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 2005;5(16):4170-84. - 127.
Jun L, Wen-Li X, Ming-chao MA, Da-wei G, Xin J, Feng-ming C, Delong S, Hui-jun C, Li L. Proteomic study on two Bradyrhizobium japonicum strains with different competitivenesses for nodulation. Journal of Integrative Agriculture 2011;10(7):1072-1079. - 128.
da Silva Batista JS, Hungria M. Proteomics reveals differential expression of proteins related to a variety of metabolic pathways by genistein-induced Bradyrhizobium japonicum strains. Journal of Proteomics. 2012;75(4):1211-9. Epub 2011 Nov 16. - 129.
Süss C, Hempel J, Zehner S, Krause A, Patschkowski T, Göttfert M. Identification of genistein-inducible and type III-secreted proteins of Bradyrhizobium japonicum . Journal of Biotechnology 2006;126(1):69-77. - 130.
Hempel J, Zehner S, Göttfert M, Patschkowski T. Analysis of the secretome of the soybean symbiont Bradyrhizobium japonicum . Journal of Biotechnology 2009;10:140(1-2):51-8. - 131.
Barcellos FG, Batista JS, Menna P, Hungria M. Genetic differences between Bradyrhizobium japonicum variant strains contrasting in N(2)-fixation efficiency revealed by representational difference analysis. Archives in Microbiology 2009;191(2):113-22. - 132.
Godoy, L. P., Vasconcelos, A. T. R., Chueire, L. M. O., Souza, R. C. et al. , Genomic panorama ofBradyrhizobium japonicum CPAC 15, a commercial inoculant strain largely established in Brazilian soils and belonging to the same serogroup as USDA 123. Soil Biol. Biochem. 2008; 40: 2743–2753. - 133.
Batista JS, Torres AR, Hungria M. Towards a two-dimensional proteomic reference map of Bradyrhizobium japonicum CPAC 15: spotlighting "hypothetical proteins". Proteomics 2010;10(17):3176-89. - 134.
Delmotte N, Ahrens CH, Knief C, Qeli E, Koch M, Fischer HM, Vorholt JA, Hennecke H, Pessi G. An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 2010;10(7):1391-400. - 135.
Gray EJ, Smith DL. Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biology and Biochemistry 2005;37: 395-412. - 136.
Kinross JM, von Roon AC, Holmes E, Darzi A and Nicholson JK 2008. The human gut microbiome: Implications for future health care. Current Gastroenterology Reports 10:396-403. - 137.
Tagg J, Daiani A, Wannamaker L. Bacteriocins of gram-positive bacteria. Bacteriological Reviews 1976;40: 722-756. - 138.
Pugsley AP. The ins and outs of colicins. II. Lethal action, immunity and ecological implications. Microbiological Sciences 1984;1: 203-205. - 139.
Jack RW, Tagg J, Ray B. Bacteriocins of gram positive bacteria. Microbiological Reviews 1995;59: 171-200. - 140.
Klaenhammer T. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiology Letters 1993;12: 39-86. - 141.
Bai Y, Souleimanov A, Smith DL. An inducible activator produced by a Serratia proteamaculans strain and its soybean growth-promoting activity under greenhouse conditions. Journal of Experimental Botany 2002b;373:1495-1502. - 142.
Bai Y, Zhou X, Smith DL Enhanced soybean plant growth resulting from co-inoculation of Bacillus strains withBradyrhizobium japonicum . Crop Science 2003;43: 1774-1781. - 143.
Gray EJ, Lee K, Di Falco M, Souleimanov A, Zhou X, Smith DL. A novel bacteriocin, thuricin 17, produced by PGPR strain Bacillus thuringiensis NEB17: isolation and classification. Journal of Applied Microbiology 2006b;100: 545-554. - 144.
Gray EJ, Di Falco M, Souleimanov A, Smith DL. Proteomic analysis of the bacteriocin, thuricin-17 produced by Bacillus thuringiensis NEB17. FEMS Microbiology Letters 2006a;255: 27-32. - 145.
Lee K, Gray EJ, Mabood F, Jung W, Charles T, Clark SRD, Ly A, Souleimanov A, Zhou X, Smith DL. The class IId bacteriocin thuricin-17 increases plant growth. Planta 2009;229: 747-755. - 146.
Jung W, Mabood F, Souleimanov A, Zhou X, Jaoua S, Kamoun F, Smith DL. Stability and antibacterial activity of bacteriocins produced by Bacillus thuringiensis andBacillus thuringiensis ssp.Kurstaki . Journal of Microbiology and Biotechnology 2008;18: 1836-1840.