PL EN


Preferences help
enabled [disable] Abstract
Number of results
2016 | 63 | 4 | 631-643
Article title

Deciphering the soybean molecular stress response via high-throughput approaches

Content
Title variants
Languages of publication
EN
Abstracts
EN
As a result of thousands of years of agriculture, humans had created many crop varieties that became the basis of our daily diet, animal feed and also carry industrial application. Soybean is one of the most important crops worldwide and because of its high economic value the demand for soybean products is constantly growing. In Europe, due to unfavorable climate conditions, soybean cultivation is restricted and we are forced to rely on imported plant material. The development of agriculture requires continuous improvements in quality and yield of crop varieties under changing or adverse conditions, namely stresses. To achieve this goal we need to recognize and understand the molecular dependencies underlying plant stress responses. With the advent of new technologies in studies of plant transcriptomes and proteomes, now we have the tools necessary for fast and precise elucidation of desirable crop traits. Here, we present an overview of high-throughput techniques used to analyze soybean responses to different abiotic (drought, flooding, cold stress, salinity, phosphate deficiency) and biotic (infections by F. oxysporum, cyst nematode, SMV) stress conditions at the level of the transcriptome (mRNAs and miRNAs) and the proteome.
Publisher

Year
Volume
63
Issue
4
Pages
631-643
Physical description
Dates
published
2016
received
2016-05-31
revised
2016-07-30
accepted
2016-08-05
(unknown)
2016-11-17
Contributors
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
author
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
References
  • Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15: 78-91. https://doi.org/10.1101/gr.2908205.
  • Akpinar BA, Lucas S, Budak H (2013) Genomics approaches for crop improvement against abiotic stress. ScientificWorldJournal 2013: id 361921, https://doi.org/10.1155/2013/361921.
  • Agarwal P, Parida SK, Mahto A, Das S, Mathew IE, Malik N, Tyagi AK (2014) Expanding frontiers in plant transcriptomics in aid of functional genomics and molecular breeding. Biotechnol J 9: 1480-1492. https://doi.org/10.1002/biot.201400063.
  • Arias MM, Leandro LF, Munkvold GP (2013) Aggressiveness of Fusarium species and impact of root infection on growth and yield of soybeans. Phytopathology 103: 822-832. https://doi.org/10.1094/PHYTO-08-12-0207-R.
  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7: 225-232.
  • Anderson L, Seilhamer J (1997) A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 18: 533-537.
  • Balestrasse KB, Tomaro ML, Batlle A, Noriega GO (2010) The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71: 2038-2045. https://doi.org/10.1016/j.phytochem.2010.07.012.
  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297. https://doi.org/10.1016/S0092-8674(04)00045-5.
  • Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, Bentwich Z (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 37: 766-770. https://doi.org/10.1038/ng1590.
  • Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49: 61-72.
  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190. https://doi.org/10.1126/science.1159151.
  • Chandramouli K, Qian PY (2009) Proteomics: Challenges, techniques and possibilities to overcome biological sample complexity. Hum Genomics Proteomics 2009: 239204. https://doi.org/10.4061/2009/239204.
  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103: 551-560. https://doi.org/10.1093/aob/mcn125.
  • Chen LM, Zhou XA, Li WB, Chang W, Zhou R, Wang C, Sha AH, Shan ZH, Zhang CJ, Qiu DZ, Yang ZL, Chen SL (2013) Genome-wide transcriptional analysis of two soybean genotypes under dehydration and rehydration conditions. BMC Genomics 14: 687. https://doi.org/10.1186/1471-2164-14-687.
  • Chen Z, Cui Q, Liang C, Sun L, Tian J (2011) Identification of differentially expressed proteins in soybean nodules under phosphorus deficiency through proteomic analysis. Proteomics 11: 4648-4659. https://doi.org/10.1002/pmic.201100231.
  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends in Plant Science 12: 444-451. https://doi.org/10.1016/j.tplants.2007.07.002.
  • Cozzone AJ (1988) Protein phosphorylation in prokaryotes. Annu Rev Microbiol 42: 97-125. https://doi.org/10.1146/annurev.mi.42.100188.000525.
  • Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A 103: 6765-6770. https://doi.org/10.1073/pnas.0600863103.
  • Dong Z, Shi L, Wang Y, Chen L, Cai Z, Wang Y, Jin J, Li X (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int J Mol Sci 14: 2717-2738. https://doi.org/10.3390/ijms14022717.
  • Fu H, Tie Y, Xu C, Zhang Z, Zhu J, Shi Y, Jiang H, Sun Z, Zheng X (2005) Identification of human fetal liver miRNAs by a novel method. FEBS Lett 579: 3849-3854. https://doi.org/10.1016/j.febslet.2005.05.064.
  • Garrett RD, Rueda X, Lambin EF (2014) Globalization's unexpected impact on soybean production in South America: linkages between preferences for non-genetically modified crops, eco-certifications, and land use. Environ Res Lett 8: 1-11. https://doi.org/10. 1088/1748-9326/8/4/044055
  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30: 353. https://doi.org/10. 1071/PP98095
  • Gietz RD (2006) Yeast two-hybrid system screening. Methods Mol Biol 313: 345-371.
  • Githiri SM, Watanabe S, Harada K, Takahashi R (2006) QTL analysis of flooding tolerance in soybean at an early vegetative growth stage. Plant Breed 125: 613-618. https://doi.org/10.1111/j.1439-0523.2006.01291. x
  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40: D1178-D1186. https://doi.org/10.1093/nar/gkr944.
  • Gracz J (2016) Alternative splicing in plant stress response. BioTechnologia 97: 9-17 https://doi.org/10.5114/bta.2016. 57719
  • Guimaraes FVA, de Lacerda CF, Marques EC, de Miranda MRA, de Abreu EB, Prisco JT, Gomes-Filho E (2011) Calcium can moderate changes on membrane structure and lipid composition in cowpea plants under salt stress. Plant Growth Regul 65: 55-63. https://doi.org/10. 1007/s10725-011-9574-1
  • Gupta S, Manubhai KP, Kulkarni V, Srivastava S (2016) An overview of innovations and industrial solutions in Protein Microarray Technology. Proteomics 16: 1297-1308. https://doi.org/10.1002/pmic.201500429.
  • Han X, Aslanian A, Yates JR 3rd (2008) Mass spectrometry for proteomics. Curr Opin Chem Biol 12: 483-490. https://doi.org/10.1016/j.cbpa.2008.07.024.
  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51: 463-499. https://doi.org/10.1146/annurev.arplant.51.1.463.
  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61: 1041-1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x.
  • Hu Z, Jiang Q, Ni Z, Chen R, Xu S, Zhang H (2013) Analyses of a Glycine max degradome library identify microRNA targets and microRNAs that trigger secondary siRNA biogenesis. J Integr Plant Biol 55: 160-176. https://doi.org/10.1111/jipb.12002.
  • Ingolia NT (2014) Ribosome profiling: new views of translation, from single codons to genome scale. Nature Reviews Genetics 15: 205-213. https://doi.org/10.1038/nrg3645.
  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 377-403. https://doi.org/10.1146/annurev.arplant.47.1.377.
  • Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96: 501-505. https://doi.org/10.1093/aob/mci205.
  • Kavar T, Maras M, Kidric M, Sustar-Vozlic J, Meglic V (2007) Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 21: 159-172. https://doi.org/10. 1007/s11032-007-9116-8
  • Khan AR, James MN (1998) Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Protein Sci 7: 815-836. https://doi.org/10.1002/pro.5560070401.
  • Khan MN, Sakata K, Komatsu S (2015) Proteomic analysis of soybean hypocotyl during recovery after flooding stress. J Proteomics 121: 15-27. https://doi.org/10.1016/j.jprot.2015.03.020.
  • Komatsu S, Kobayashi Y, Nishizawa K, Nanjo Y, Furukawa K (2010) Comparative proteomics analysis of differentially expressed proteins in soybean cell wall during flooding stress. Amino Acids 39: 1435-1449. https://doi.org/10.1007/s00726-010-0608-1.
  • Komatsu S, Shirasaka N, Sakata KJ (2013) 'Omics' techniques for identifying flooding-response mechanisms in soybean. Proteomics 93: 169-178. https://doi.org/10.1016/j.jprot.2012.12.016.
  • Kurien BT, Scofield RH (2015) Western blotting: an introduction. Methods Mol Biol 1312: 17-30. https://doi.org/10.1007/978-1-4939-2694-7_5.
  • Lanubile A, Muppirala UK, Severin AJ, Marocco A, Munkvold GP (2015) Transcriptome profiling of soybean (Glycine max) roots challenged with pathogenic and non-pathogenic isolates of Fusarium oxysporum. BMC Genomics 16: 1089. https://doi.org/10.1186/s12864-015-2318-2.
  • Le DT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Ham le H, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS One 7: e49522. https://doi.org/10.1371/journal.pone.0049522.
  • Le Roux MR, Ward CL, Botha FC, Valentine AJ (2006) The route of pyruvate synthesis under Pi starvation in legume root systems. New Phytol 169: 399-408. https://doi.org/10.1111/j.1469-8137.2005.01594. x
  • Levitt J (1980) Responses of plants to environmental stresses. Vol 2. Water, radiation, salt and other stresses. pp 93-128. New York: Academic Press
  • Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biology 11: 170. https://doi.org/10.1186/1471-2229-11-170.
  • Li Q, Cao J, Yu L, Li M, Liao J, Lu G (2012a) Effects on physiological characteristics of honeysuckle (Lonicera japonica Thunb) and the role of exogenous calcium under drought stress. Plant Omics 5: 1-5.
  • Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012b) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS One 7: e39650. https://doi.org/10.1371.
  • Li Y, Li W, Jin YX (2005) Computational identification of novel family members of microRNA genes in Arabidopsis thaliana and Oryza sativa. Acta Biochim Biophys Sin 37: 75-87. https://doi.org/10.1093/abbs/37.2.75.
  • Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP (2003) The microRNAs of Caenorhabditis elegans. Genes Dev 17: 991-1008. https://doi.org/10.1101/gad.1074403.
  • Ma G, Chen P, Buss GR, Tolin SA (2004) Genetics of resistance to two strains of Soybean mosaic virus in differential soybean genotypes. Journal of Heredity 95: 322-326. https://doi.org/10.1093/jhered/esh059.
  • Ma H, Song L, Shu Y, Wang S, Niu J, Wang Z, Yu T, Gu W, Ma H (2012) Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J Proteomics 75: 1529-1546. https://doi.org/10.1016/j.jprot.2011.11.026.
  • Mańkowski D, Laudański Z, Flaszka M (2012) Proposal of a method for assessment of biological and technological progress in crops cultivation on the example of winter wheat. Biuletyn IHAR 263: 91-104 (in Polish).
  • Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: When post-transcriptional and post-translational regulations control transcription. Plant Sci 174: 420-431. https://doi.org/10.1016/j.plantsci.2008.02. 005
  • McDonough AA, Veiras LC, Minas JN, Ralph DL (2015) Considerations when quantitating protein abundance by immunoblot. Am J Physiol Cell Physiol 308: C426-C433. https://doi.org/10.1152/ajpcell.00400.2014.
  • Mitulović G, Mechtler K (2006) HPLC techniques for proteomics analysis-a short overview of latest developments. Brief Funct Genomic Proteomic 5: 249-260. https://doi.org/10.1093/bfgp/ell034.
  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.
  • Nanjo Y, Skultety L, Ashraf Y, Komatsu S (2010) Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. J Proteome Res 9: 3989-4002. https://doi.org/10.1021/pr100179f.
  • Nanjo Y, Maruyama K, Yasue H, Yamaguchi-Shinozaki K, Shinozaki K (2011a) Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol Biol 77: 129-144. https://doi.org/10.1007/s11103-011-9799-4.
  • Nanjo Y, Skultety L, Uváčková LU, Klubicová K, Hajduch M, Komatsu S (2011b) Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. J Proteome Res 11: 372-385. https://doi.org/10.1021/pr100179f.
  • Olivera M, Tejera N, Iribarne C, Ocaná A, Lluch C (2004) Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): effect of phosphorus. Physiol Plantarum 121: 498-505. https://doi.org/10.1111/j.0031-9317.2004.00355. x
  • Oliveira BM, Coorssen JR, Martins-de-Souza D (2014) 2DE: the phoenix of proteomics. J Proteomics 104: 140-150. https://doi.org/10.1016/j.jprot.2014.03.035.
  • Prabakaran S, Lippens G, Steen H, Gunawardena J (2012) Post-translational modification: nature's escape from genetic imprisonment and the basis for dynamic information encoding. Wiley Interdiscip Rev Syst Biol Med 4: 565-583. https://doi.org/10.1002/wsbm.1185.
  • Price AH, Cairns JE, Horton P, Jones HG, Griffiths H (2002) Linking drought-resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. J Exp Bot 53: 989-1004.
  • Qiu Y, Xi J, Du L, Suttle JC, Poovaiah BW (2012) Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol Biol 79: 89-99. https://doi.org/10.1007/s11103-012-9896-z.
  • Ranjeva R, Boudet AM (1987) Phosphorylation of proteins in plants: regulatory effects and potential involvement in stimulus/response coupling. Annu Rev Plant Biol 38: 73-94. https://doi.org/10.1146/annurev.pp.38.060187. 000445
  • Roe MR, Griffin TJ (2006) Gel-free mass spectrometry-based high throughput proteomics: tools for studying biological response of proteins and proteomes. Proteomics 6: 4678-4687.
  • Sa TM, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97: 928-935.
  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183. https://doi.org/10.1038/nature08670.
  • Shao HB, Chu LY, Jaleel CA, Zhao CX (2008) Water-deficit stress-induced anatomical changes in higher plants. C R Biol 331: 215-225. https://doi.org/10.1016/j.crvi.2008.01.002.
  • Shen J, Zhang W, Fang H, Perkins R, Tong W, Hong H (2013) Homology modeling, molecular docking, and molecular dynamics simulations elucidated α-fetoprotein binding modes. BMC Bioinformatics 14 (Suppl 14): S6. https://doi.org/10.1186/1471-2105-14-S14-S6.
  • Shin JH, Vaughn JN, Abdel-Haleem H, Chavarro C, Abernathy B, Kim KD, Jackson SA, Li Z (2015) Transcriptomic changes due to water deficit define a general soybean response and accession-specific pathways for drought avoidance. BMC Plant Biol 15: 26. https://doi.org/10.1186/s12870-015-0422-8.
  • Sun Z, Wang Y, Mou F, Tian Y, Chen L, Zhang S, Jiang Q, Li X (2016) Genome-wide small RNA analysis of soybean reveals auxin-responsive microRNAs that are differentially expressed in response to salt stress in root. Apex Front Plant Sci 6: 1273. https://doi.org/10.3389/fpls.2015.01273.
  • Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol 21: 805-811. https://doi.org/10.1016/j.semcdb.2010.04.001.
  • Sunkar R, Girke T, Zhu JK (2005) Identification and characterization of endogenous small interfering RNAs from rice. Nucleic Acids Res 33: 4443-4454. https://doi.org/10.1093/nar/gki758.
  • Tang C, Hinsinger P, Drevon JJ, Jaillard B (2001) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula. L Ann Bot 88: 131-138. https://doi.org/10.1006/anbo.2001. 1440
  • Tian X, Liu Y, Huang Z, Duan H, Tong J (2015) Comparative proteomic analysis of seedling leaves of cold-tolerant and -sensitive spring soybean cultivars. Mol Biol Rep 42: 581-601. https://doi.org/10.1007/s11033-014-3803-4.
  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J Proteomics 71: 391-411. https://doi.org/10.1016/j.jprot.2008.07.005.
  • Thao NP, Tran LS (2011) Potentials toward genetic engineering of drought tolerant soybean. Crit Rev Biotechnol 32: 349-362 https://doi.org/10.3109/07388551.2011.643463.
  • Trindade I, Santos D, Dalmay T, Fevereiro P (2011) Facing the environment: small RNAs and the regulation of gene expression under abiotic stress in plants. In Abiotic Stress Response in Plants - Physiological, Biochemical and Genetic Perspectives. Shanker A, Venkateswarlu B eds, pp 113-136. InTech. https://doi.org/10. 5772/22250
  • Tripathi P, Rabara RC, Reese RN, Miller MA, Rohila JS, Subramanian S, Shen QJ, Morandi D, Bücking H, Shulaev V, Rushton PJ (2016) A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics 17: 102. https://doi.org/10.1186/s12864-016-2420-0.
  • Turner NC, Wright GC, Siddique KHM (2001) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71: 123-231. https://doi.org/10. 1016/S0065-2113(01)71015-2
  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2: 79-85.
  • Tyczewska A, Gracz J, Twardowski T, Malyska A (2014) Time for soybean? Nauka 4/2014: 121-138 (in Polish).
  • Urano K, Kurihara Y, Seki M, Shinozaki K (2010) 'Omics' analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13: 132-138. https://doi.org/10.1016/j.pbi.2009.12.006.
  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157: 423-447. https://doi.org/10.1046/j.1469-8137.2003.00695. x
  • Varadi M, Tompa P (2015) The Protein Ensemble Database. Adv Exp Med Biol 870: 335-349. https://doi.org/10.1007/978-3-319-20164-1_11.
  • Waadt R, Schlücking K, Schroeder JI, Kudla J (2014) Protein fragment bimolecular fluorescence complementation analyses for the in vivo study of protein-protein interactions and cellular protein complex localizations. Methods Mol Biol 1062: 629-658. https://doi.org/10.1007/978-1-62703-580-4_33.
  • Wang Q, Wang J, Yang Y, Du W, Zhang D, Yu D, Cheng H (2016) A genome-wide expression profile analysis reveals active genes and pathways coping with phosphate starvation in soybean. BMC Genomics 17: 192. https://doi.org/10.1186/s12864-016-2558-9.
  • Wang WX, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1-14.
  • Weiss RB, Atkins JF (2011) Molecular biology. Translation Goes Global. Science 334(6062): 1509-1510. https://doi.org/10.1126/science.1216974. ISSN 0036-8075.
  • Wrather JA, Koenning SR (2009) Effects of diseases on soybean yields in the United States 1996 to 2007. Online Plant Health Progress https://doi.org/10. 1094/PHP-2009-0401-01-RS
  • Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14: 66. https://doi.org/10.1186/1471-2164-14-66.
  • Yin X, Komatsu S (2015) Quantitative proteomics of nuclear phosphoproteins in the root tip of soybean during the initial stages of flooding stress. J Proteomics 119: 183-195. https://doi.org/10.1016/j.jprot.2015.02.004.
  • Yin X, Wang J, Cheng H, Wang X, Yu D (2013) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta 237: 1213-1225. https://doi.org/10.1007/s00425-012-1835-3.
  • Yin X, Sakata K, Nanjo Y, Komatsu S (2014a) Analysis of initial changes in the proteins of soybean root tip under flooding stress using gel-free and gel-based proteomic techniques. J Proteomics 106: 1-16. https://doi.org/10.1016/j.jprot.2014.04.004.
  • Yin Y, Yang R, Guo Q, Gu Z (2014b) NaCl stress and supplemental CaCl2 regulating GABA metabolism pathways in germinating soybean. Eur Food Res Technol 238: 781-788. https://doi.org/10. 1007/s00217-014-2156-5
  • Yin Y, Yang R, Han Y, Gu Z (2015) Comparative proteomic and physiological analyses reveal the protective effect of exogenous calcium on the germinating soybean response to salt stress. J Proteomics 113: 110-126. https://doi.org/10.1016/j.jprot.2014.09.023.
  • Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50: 849-859. https://doi.org/10.1111/j.1744-7909.2008.00709.x.
  • Zeng H, Wang G, Zhang Y, Hu X, Pi E, Zhu Y, Wang H, Du L (2015) Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil 398: 207-227. https://doi.org/10. 1007/s11104-015-2657-4
  • Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167: 1289-1297. https://doi.org/10.1016/j.jplph.2010.04.017.
  • Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: A small regulatory molecule with big impact. Develop Biol 289: 3-16. https://doi.org/10.1016/j.ydbio.2005.10.036.
  • Zhu JK (2007) Plant Salt Stress. eLS https://doi.org/10.1002/9780470015902.a0001300. pub2
  • http://wwf.panda.org/what_we_do/footprint/agriculture/soy/facts/
  • http://faostat3.fao.org/browse/rankings/commodities_by_regions/E
  • https://www.broadinstitute.org/scientific-community/science/platforms/proteomics/lcms-overview
Document Type
Publication order reference
Identifiers
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv63p631kz
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.