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Differential Impact of Acclimation and Acute Water Deprivation in the Expression of Key Transcription Factors in Soybean Roots

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Abstract

Soybean (Glycine max) is one of the major world commodities. In order to increase the soybean yields, it has been searched drought-tolerant cultivars, once the drought is the major constraint to soybean grown. Therefore, it is crucial to elucidate the molecular mechanisms associated with drought tolerance. Here, the in silico approach allowed us to identify 12 genes belonging to six different transcription factor families in soybean that have been associated with key events on drought response. The expression pattern of each gene was investigated by qPCR in root samples of drought-sensitive and drought-tolerant cultivars undergoing drought stress in pot-based (PSys) and hydroponic (HSys) cultivation systems. GmaxMYC2-like 2 was induced under abrupt drought conditions in HSys in both cultivars, whereas GmaxAREB1-like 1 and GmaxDREB2A-like were highly induced only in the PSys. However, GmaxMYB2-like 1, GmaxMYB2-like 2, GmaxRD26/NAC-like 1, GmaxRD26/NAC-like 2, GmaxAREB1-like 2, and GmaxDREB1A-like were upregulated in both systems, while the GmaxHB6-like and GmaxHB13-like are repressed under all of the investigated conditions. Exogenous abscisic acid (ABA) treatment was used to identify those genes belonging to the ABA-dependent drought response. The genes identified in this work have potential application for the improvement of drought resistance in soybean and markers for breeding programs.

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Abbreviations

ABA:

abscisic acid

ABAD:

ABA dependent

ABAI:

ABA independent

ABF:

ABA-responsive transcriptional factors

ABRE/ABFs:

ABA-responsive element binding/ABRE-binding protein

BG:

background

BZIP:

basic leucine zipper

DREB:

dehydration-responsive element binding

HB:

homeobox domain HD-zip

HSys:

hydroponic system

MYB:

myeloblastosis oncogene

MYC:

myelocytomatosis oncogene

NAC:

nitrogene assimilation control protein

PSys:

pot-based system

BR 16:

sensitive cultivar

Embrapa 48:

tolerant cultivar

Ψw:

water potential

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in Abscisic acid signaling. Plant Cell Online 15:63–78

    Article  CAS  Google Scholar 

  • Andersen C, Jensen J, Orntoft T (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64(15):5245–5250

    Article  CAS  PubMed  Google Scholar 

  • Aubert Y, Leba L-J, Cheval C, Ranty B, Vavasseur A, Aldon D, Galaud J-P (2011) Involvement of RD20, a member of caleosin family, in ABA-mediated regulation of germination in Arabidopsis thaliana. Plant Signal Behav 6:538–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159

    Article  CAS  PubMed  Google Scholar 

  • Bu Q et al. (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18:756–767

    Article  CAS  PubMed  Google Scholar 

  • Busk PK, Pagès M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  CAS  PubMed  Google Scholar 

  • Casagrande EC, et al. (2001) Expressão gênica diferencial durante déficit hídrico em soja. Rev Bras Fisiol Veg 13:168–184

    Article  Google Scholar 

  • Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151:1030–1040. doi:10.1104/pp.109.146282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comlekcioglu N, Simsek M (2011) Effects of deficit irrigation on yield and yield components of vegetable soybean Glycine max L. (Merr.) in semi-arid conditions. Afr J Biotechnol 10:6227–6234

    Google Scholar 

  • Cowan IR (1965) Transport of water in the soil-plant-atmosphere system. J Appl Ecol 2:221–239

    Article  Google Scholar 

  • Crandall K, Lagergren J, Simonsen M, Mailund T, Pedersen C (2008) Rapid neighbour-joining. In: Algorithms in bioinformatics, vol 5251. Lecture notes in computer science. Springer Berlin/Heidelberg, pp 113–122. doi:10.1007/978-3-540-87361-7_10

  • de Paiva Rolla AA et al. (2014) Phenotyping soybean plants transformed with rd29A:AtDREB1A for drought tolerance in the greenhouse and field Transgenic. Research 23:75–87. doi:10.1007/s11248-013-9723-6

    Google Scholar 

  • Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Commun 3 doi:10.1038/ncomms1732

  • Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol 13:1–11. doi:10.1186/1471-2229-13-229

  • Doyle JJ, Egan AN (2010) Dating the origins of polyploidy events. New Phytol 186:73–85. doi:10.1111/j.1469-8137.2009.03118.x

    Article  PubMed  Google Scholar 

  • Fan CM, Wang X, Wang YW, Hu RB, Zhang XM, Chen JX, Fu YF (2013) Genome-wide expression analysis of soybean MADS genes showing potential function in the seed development. PLoS ONE 8:e62288. doi:10.1371/journal.pone.0062288

  • Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72(4):673–689

    Article  CAS  PubMed  Google Scholar 

  • Fehr W, Caviness C (1977) Stages of soybean development. Iowa State University, Ames, IA

    Google Scholar 

  • Ferreira Neto JRC, Pandolfi V, Guimaraes FCM, Benko-Iseppon AM, Romero C, Silva RLDO, Rodrigues FA, Abdelnoor RV, Nepomuceno AL, Kido EA (2013) Early transcriptional response of soybean contrasting accessions to root dehydration. PLoS One 8(12):e83466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujimoto R, Sasaki T, Ishikawa R, Osabe K, Kawanabe T, Dennis ES (2012) Molecular mechanisms of epigenetic variation in plants. Int J Mol Sci 13(8):9900–9922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita M et al. (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  CAS  PubMed  Google Scholar 

  • Guimarães-Dias F, Neves-Borges AC, Viana AAB, Mesquita RO, Romano E, Grossi-de-Sá MF, Nepomuceno AL, Loureiros ME, Alves-Ferreira M (2012) Expression analysis in response to drought stress in soybean: shedding light on the regulation of metabolic pathway genes. Genet Mol Biol 35(1):222–232

    Article  PubMed  PubMed Central  Google Scholar 

  • Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154(3):1254–1271. doi:10.1104/pp.110.161752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M (2016) Signalling roles of methylglyoxal and the involvement of the glyoxalase system in plant abiotic stress responses and tolerance. In: Plant-Environment Interaction. John Wiley & Sons, Ltd, pp 311–326

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinforma 2008

  • Hu R, Fan C, Li H, Zhang Q, Fu Y-F (2009) Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Mol Biol 10(1):93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain SS, Kayani MA, Amjad M (2011) Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol Prog 27(2):297–306. doi:10.1002/btpr.514

    Article  CAS  PubMed  Google Scholar 

  • Kankainen M, Holm L (2004) POBO, transcription factor binding site verification with bootstrapping. Nucleic Acids Res 32:W222–W229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6:686–703

    Article  CAS  PubMed  Google Scholar 

  • Kilian J, Peschke F, Berendzen KW, Harter K, Wanke D (2012) Prerequisites, performance and profits of transcriptional profiling the abiotic stress response. Biochim Biophys Acta Gene Regul Mech 1819(2):166–175. doi:10.1016/j.bbagrm.2011.09.005

    Article  CAS  Google Scholar 

  • Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114. doi:10.3389/fpls.2015.00114

    PubMed  PubMed Central  Google Scholar 

  • Kulcheski FR, Marcelino-Guimaraes FC, Nepomuceno AL, Abdelnoor RV, Margis R (2010) The use of microRNAs as reference genes for quantitative polymerase chain reaction in soybean. Anal Biochem 406(2):185–192

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res. doi:10.1093/dnares/dsr015

    Google Scholar 

  • Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different Jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109(1):7–13. doi:10.1104/pp.109.1.7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcolino-Gomes J, Rodrigues FA, Neves Oliveira MC, Boucas Farias JR, Neumaier N, Abdelnoor RV, Marcelino-Guimaraes FC, Nepomuceno AL (2013) Expression patterns of GmAP2/EREB-like transcription factors involved in soybean responses to water deficit. PLoS One 8(5):e62294. doi:10.1371/journal.pone.0062294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martins PK, Jordao BQ, Yamanaka N, Farias JRB, Beneventi MA, Binneck E, Fuganti R, Stolf R, Nepomuceno AL (2008) Differential gene expression and mitotic cell analysis of the drought tolerant soybean (Glycine max L. Merrill Fabales, Fabaceae) cultivar MG/BR46 (Conquista) under two water deficit induction systems. Genet Mol Biol 31(2):512–521

    Article  CAS  Google Scholar 

  • Mayer Weber RL, Wiebke-Strohm B, Bredemeier C, Margis-Pinheiro M, de Brito GG, Rechenmacher C, Bertagnolli PF, Lisei de Sa ME, Campos MdA, Santos de Amorim RM, Beneventi MA, Margis R, Grossi-de-Sa MF, Bodanese-Zanettini MH (2014) Expression of an osmotin-like protein from Solanum nigrum confers drought tolerance in transgenic soybean. Bmc Plant Biol 14. doi:10.1186/s12870–014-0343-y

  • Miyamoto K, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2015) Overexpression of the bZIP transcription factor OsbZIP79 suppresses the production of diterpenoid phytoalexin in rice cells. J Plant Physiol 173:19–27. doi:10.1016/j.jplph.2014.09.001

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James RA, Sirault XRR, Furbank RT, Jones HG (2010) New phenotyping methods for screening wheat and barley for beneficial responses to water deficit. J Exp Bot 61(13):3499–3507

    Article  CAS  PubMed  Google Scholar 

  • Mutava RN, Prince SJK, Syed NH, Song L, Valliyodan B, Chen W, Nguyen HT (2015) Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol Biochem 86:109–120. doi:10.1016/j.plaphy.2014.11.010

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60(1):51–68

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170. doi:10.3389/fpls.2014.00170

    Article  PubMed  PubMed Central  Google Scholar 

  • Narusaka Y et al. (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses the. Plant J 34:137–148

    Article  CAS  PubMed  Google Scholar 

  • Neves-Borges AC et al. (2012) Expression pattern of drought stress marker genes in soybean roots under two water deficit systems. Genet Mol Biol 35:212–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86. doi:10.3389/fpls.2014.00086

    Article  PubMed  PubMed Central  Google Scholar 

  • Oya T, Nepomuceno AL, Neumaier N, Farias JRB, Tobita S, Ito O (2004) Drought tolerance characteristics of Brazilian soybean cultivars—evaluation and characterization of drought tolerance of various Brazilian soybean cultivars in the field. Plant Prot Sci 7(2):129–137. doi:10.1626/pps.7.129

    Article  Google Scholar 

  • Pandey A, Misra P, Bhambhani S, Bhatia C, Trivedi PK (2014) Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content. Sci Report 4:5018. doi:10.1038/srep05018

    Article  CAS  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36. doi:10.1093/nar/30.9.e36

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao Z, Li C-L, Zhang W (2016) WRKY1 regulates stomatal movement in drought-stressed Arabidopsis thaliana Plant Mol Biol:1–13

  • Sahu P, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32(8):1151–1159. doi:10.1007/s00299-013-1462-x

    Article  CAS  PubMed  Google Scholar 

  • Savitri E, Basuki N, Aini N, Arumingtyas E (2013) Identification and characterization drought tolerance of gene LEA-D11 soybean (Glycine max L. Merr) based on PCR-sequencing. Am J Mol Biol 3:32–37. doi:10.4236/ajmb.2013.31004

    Article  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng JL, 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 SQ, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du JC, Tian ZX, Zhu LC, 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(7278):178–183

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227. doi:10.1093/jxb/erl164

    Article  CAS  PubMed  Google Scholar 

  • Sitnikova T, Rzhetsky A, Nei M (1995) Interior-branched and bootstrap tests of phylogenetic trees. Mol Biol Evol 12(2):319–333

    CAS  PubMed  Google Scholar 

  • Stolf-Moreira R, Medri M, Neumaier N, Lemos N, Pimenta J, Tobita S, Brogin R, Marcelino-Guimarães F, Oliveira M, Farias J, Abdelnoor R, Nepomuceno A (2010b) Soybean physiology and gene expression during drought. Genet Mol Res 5:1946–1956

    Article  CAS  Google Scholar 

  • Stolf-Moreira R, Lemos E, Carareto-Alves L, Marcondes J, Pereira S, Rolla A, Pereira R, Neumaier N, Binneck E, Abdelnoor R, de Oliveira M, Marcelino F, Farias J, Nepomuceno A (2011) Transcriptional profiles of roots of different soybean genotypes subjected to drought stress. Plant Mol Biol Report 29(1):19–34. doi:10.1007/s11105-010-0203-3

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Texeira LR, de Lucca E, Braccini A, Sperandio D, Scapim CA, Schuster I, Vigano J (2008) Evaluation of soybean cultivars regarding tolerance to water stress in substrat containing polyethylene glycol. Acta Sci Agron 30(2):217–223

    Article  Google Scholar 

  • Thao NP, Tran L-SP (2012) Potentials toward genetic engineering of drought-tolerant soybean. Crit Rev Biotechnol 32(4):349–362. doi:10.3109/07388551.2011.643463

    Article  CAS  PubMed  Google Scholar 

  • Tran L-S, Mochida K (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10(4):447–462. doi:10.1007/s10142-010-0178-z

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51(11):1821–1839. doi:10.1093/pcp/pcq156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74

    Article  PubMed  PubMed Central  Google Scholar 

  • Vadez V (2014) Root hydraulics: the forgotten side of roots in drought adaptation. Field Crop Res 165:15–24. doi:10.1016/j.fcr.2014.03.017

    Article  Google Scholar 

  • Vidal RO, do Nascimento LC, Mondego JMC, Pereira GAG, Carazzolle MF (2012) Identification of SNPs in RNA-seq data of two cultivars of Glycine max (soybean) differing in drought resistance. Genet Mol Biol 35(1 Suppl):331–334. doi:10.1590/s1415-47572012000200014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H et al. (2012) Expression of an apoplast-localized BURP-domain protein from soybean (GmRD22) enhances tolerance towards abiotic stress plant. Cell Environ 35:1932–1947

    Article  CAS  Google Scholar 

  • Xu Z-S, Chen M, Li L-C, Ma Y-Z (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53(7):570–585. doi:10.1111/j.1744-7909.2011.01062.x

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet MGG 238:17–25. doi:10.1007/bf00279525

    CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139. doi:10.1016/j.pbi.2014.07.009

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12(8):1047–1064. doi:10.1089/cmb.2005.12.1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Durvalina Felix for the technical support. This work was part of Guimarães-Dias’s PhD research in Genetics, at the Department of Genetics of the Universidade Federal do Rio de Janeiro (UFRJ), and was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; M. Alves-Ferreira) and the Fundação de Amparo à Pesquisa do Rio de Janeiro (FAPERJ; M. Alves-Ferreira). The graduate PhD scholarship of F. Guimarães-Dias was granted by CNPq.

Authors’ Contributions

MA-F, ACNB, and FGD planned and supervised the study. MA-F, ACNB, and FGD contributed to the design and execution of the experiments and drafted the manuscript. LGK and AJC performed the expression analysis in the ABA samples. RMSA, MELS, AVJF, FGD, MAB, and ER contributed to the RNA extraction and expression analysis in the drought stress samples. ROM and MEL contributed to the development of the PSys experiment. FAR and AN contributed to the development of the HSys experiment. MAF, ACNB, and FGD contributed to the interpretation of the data and provided intellectual input. AN and MFGDS revised the manuscript and financial support. All of the authors have read and approved the final manuscript.

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Authors and Affiliations

  1. Department of Genetics, Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Av. Prof. Rodolpho Paulo Rocco, s/n, 2° andar-sala A2-93, CSS, Rio de Janeiro, RJ, 21941-901, Brazil

    Fábia Guimarães-Dias, Alessandra J. Conforte, Leonardo Giovanella-Kampmann & Márcio Alves-Ferreira

  2. Department of Botany, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, 22290-240, Brazil

    Anna C. Neves-Borges

  3. Plant Biology Department, Universidade Federal de Viçosa (UFV), Viçosa, MG, 36570-900, Brazil

    Marcelo E. Loureiro

  4. Genetic Resources and Biotechnology (CENARGEN), Brasília, DF, 70770-901, Brazil

    André V. J. Ferreira, Regina M. S. Amorim, Magda A. Benevent, Maria Eugênia Lisei de Sá, Eduardo Romano & Maria Fátima Grossi-de-Sá

  5. Embrapa Soybean, Distrito de Warta, Londrina, PR, 86001-970, Brazil

    Fabiana A. Rodrigues & Alexandre L. Nepomuceno

  6. Department of Fitotecnia, Universidade Federal do Ceará (UFC), Ceará, CE, 60020-181, Brazil

    Rosilene O. Mesquita

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  1. Fábia Guimarães-Dias
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  2. Anna C. Neves-Borges
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  3. Alessandra J. Conforte
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  5. André V. J. Ferreira
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  6. Regina M. S. Amorim
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  7. Magda A. Benevent
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  8. Maria Eugênia Lisei de Sá
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  9. Rosilene O. Mesquita
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  10. Fabiana A. Rodrigues
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  11. Alexandre L. Nepomuceno
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  13. Marcelo E. Loureiro
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  14. Maria Fátima Grossi-de-Sá
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  15. Márcio Alves-Ferreira
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Corresponding author

Correspondence to Márcio Alves-Ferreira.

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Competing Interests

The authors declare that they have no competing interests.

Additional information

Fábia Guimarães-Dias and Anna C. Neves-Borges contributed equally to this work.

Electronic supplementary materials

Fig. S1

Digital expression profiles of the DTFGs that were submitted to treatment with ABA and drought stress in Arabidopsis. This analysis used available data from a microarray of the model plant A. thaliana and ATH1:22 K; the intensity of the red color is equivalent to increases in gene expression in response to drought stress. The increase in the intensity of the green color is equivalent to the increase in the gene repression in response to drought stress. The solid black color indicates no induction or repression under drought stress conditions in Genevestigator program: https://www.genevestigator.com/gv. (JPEG 799 kb)

Fig. S2

Strategy to search for TFRDs that are involved in the soybean response to water deficit. (JPEG 1041 kb)

Table S1

Primer sequences that were used in the RT-qPCR and the amplicon lengths. (DOC 54 kb)

Table S2

Description of the Cis-regulatory elements that were responsive to drought stress and ABA present in the transcription factors that were responsive to drought. Note: The symbol W was used in addition to A or T; the symbol R was used in addition to A or G; the symbol Y was used in addition to C or T; the symbol K was used in addition to G or T; and the symbol N was used in additional to A, C, G or T. (DOC 37 kb)

Table S3

Frequency of the Cis-regulatory elements present in promoters of the transcription factors responsive to drought. Note: All of the analyzed promoter sequences were 1000 bp, and POBO was run with the following parameters: Number of pseudo-clusters 1000 length of the background promoter 1000 bp, and number of bootstraps 1000. Calculated t-test using the link online at the GraphPad website: http://www.graphpad.com/quickcalcs/DistMenu.cfm). P < 0.0001. The symbol W was used in addition to A or T, and the symbol N was used in additional to A, C, G or T. (DOCX 842 kb)

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Guimarães-Dias, F., Neves-Borges, A.C., Conforte, A.J. et al. Differential Impact of Acclimation and Acute Water Deprivation in the Expression of Key Transcription Factors in Soybean Roots. Plant Mol Biol Rep 34, 1167–1180 (2016). https://doi.org/10.1007/s11105-016-0993-z

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