Abstract
The drought response is a genome-wide phenomenon that, due to its complexity, is hard to achieve a “universal” response requiring an analysis method that takes this characteristic into account. Here, the Transcriptogramer tool was used to (i) produce a Glycine max ordering list based on protein–protein associations and (ii) analyze transcriptome data from soybean roots submitted to dehydration for 1, 6, and 12 h in a genome-wide scale. Sixteen, five, and six gene ontology (GO) categories were differentially expressed at 1, 6, and 12 h of drought stress, respectively. The most enriched GO categories are cell division, cell cycle, cell wall organization, stress responses, hormone signaling pathways, phosphorelay signal transduction, and regulation of gene expression. In total, 274 genes were differentially expressed (DE). The list includes 15 calcium-binding proteins, 17 TIFY, 3 ABA receptors, 5 E2 ubiquitin-conjugatin enzymes, 2 E3 ligases, 4 proteasome regulatory subunits, 1 chloroplastic superoxide dismutase, 1 peroxidase, and 10 thioredoxin-encoding genes already known to be related to drought response. The Transcriptogramer has evinced a global reprogrammed transcriptome and revealed that the most observable effects of water deficit occur during the first hour.
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References
Ahanger MA, Morad‐Talab N, Abd-Allah EF, Ahmad P, Hajiboland R (2016) Plant growth under drought stress: significance of mineral nutrients. In: Ahmad (ed) Water Stress and Crop Plants: A Sustainable Approach, 1st edn. John Wiley & Sons, Ltd
Ambrosone A, Costa A, Leone A, Grillo S (2012) Beyond transcription: RNA-binding proteins as emerging regulators of plant response to environmental constraints. Plant Science 12–18
Arraes FBM, Beneventi A, de Sa MEL, Paixao FR, Albuquerque EVS, Marin SRR, Purgatto E, Nepomuceno AL, Grossi-de-Sa MF (2015) Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance. BMC Plant Biol 3:213
Arumingtyas EL, Widoretno W, Indriyani S (2012) Somaclonal variations of soybeans (Glycine max. L. Merr) stimulated by drought stress based on random amplified polymorphic DNAs (RAPDs), p 85–91
Bao Y, Song WM, Jin YL, Jiang CM, Yang Y, Li B, Huang WJ, Liu H, Zhang HX (2014) Characterization of Arabidopsis Tubby-like proteins and redundant function of AtTLP3 and AtTLP9 in plant response to ABA and osmotic stress. Plant Mol Biol 29:471–483
Batistic O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1283–1293
Bechtold U, Penfold CA, Jenkins DJ, Legaie R, Moore JD, Lawson T, Matthews JS, Vialet-Chabrand SR, Baxter L, Subramaniam S, Hickman R, Florance H, Sambles C, Salmon DL, Feil R, Bowden L, Hill C, Baker NR, Lunn JE, Finkenstädt B et al (2016) Time-series transcriptomics reveals that AGAMOUS-LIKE22 affects primary metabolism and developmental processes in drought-stressed Arabidopsis. Plant Cell 28:345–366
Belamkar V, Weeks NT, Bharti K, Farmer D, Graham MA, Cannon B (2014) Comprehensive characterization and RNA-Seq profiling of the HD-Zip transcription factor family in soybean (Glycine max) during dehydration and salt stress. BMC Genom 3:950
Bohnert HJ, Sheveleva E (1998) Plant stress adaptations—making metabolism move. Curr Opin Plant Biol 267–274
Buchanan BB, Gruissem W, Jones RL (2015) Biochemistry & molecular biology of plants, 2nd edn. Wiley Blackwell
Cadavid IC, Guzman F, Oliveira-Busatto LA, de Almeida RMC, Margis R (2020) Transcriptional analyses of two soybean cultivars under salt stress. Mol Biol Rep 47:2871–2888
Cha JY, Kim JY, Jung IJ, Kim MR, Melencion A, Alam SS, Yun DJ, Lee SY, Kim MG, Kim WY (2014) NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiol Biochem 184–191
Chakraborty U, Pradhan B (2012) Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Braz J Plant Physiol 117–130
Chaves MM, Maroco J, Pereira JS (2003) Unserstanding palnt responses to drought- from genes to whole plant. Funct Plant Biol 239–264
Chefdor F, Bénédetti H, Depierreux C, Delmotte M, Carpin S (2006) Osmotic stress sensing in Populus: components identification of a phosphorelay system. FEBS Lett 9 77–81
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 Genom 6:687
Chen W, Yao Q, Patil GB, Agarwal G, Deshmukh RK, Lin L, Wang B, Wang Y, Prince SJ, Song L, Xu D, An YC, Valliyodan B, Varshney RK, Nguyen HT (2016) Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and flooding stress revealed by RNA-Seq. Front Plant Sci 7:1044. https://doi.org/10.3389/fpls.2016.01044
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 9:666–671
Chung E, Cho CW, So HA, Kang JS, Chung YS, Lee JH (2013) Overexpression of VrUBC1, a mung bean E2 Ubiquitin-conjugating enzyme, enhances osmotic stress tolerance in Arabidopsis. Plos One e66056
Cominelli E, Galbiati M, Tonelli C (2010) Transcription factors controlling stomatal movements and drought tolerance. Transcription 41–45
Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szczesniak M, Gaffney DJ, Elo LL, Zhang X, Mortazavi A (2016) A survey of best practices for RNA-seq data analysis Genom Biol 1–19
Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q (2012) Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 233–244
da Silva SRM, Perrone GC, Dinis JM, de Almeida MC (2014) Reproducibility enhancement and differential expression of non predefined functional gene sets in human genome. BMC Genomics 1181
Darmanti S, Santosa, Kumala D, Nugroho LH (2016) Antioxidative defenses of soybean [Glycine max (L.) Merr. cv. Grobogan] against purple nutsedge (Cyperus rotundus L.) interference during drought stress. J Anim Plant Sci 225–232
de Almeida RMC, Clendenon SG, Richards WG, Boedigheimer M, Damore M, Rossetti S, Harris PC, Herbert BS, Xu WM, Wandiger-Ness A, Ward H, Glazier JA, Bacallao RL (2016) Transcriptome analysis reveals manifold mechanisms of cyst development in ADPKD. Hum Genomics 37
de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev 3:833–845
Ding F, Cui W, Zhang A, Xiong (2014) Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genomics 4:431
Divi K, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol 131–136
Faize M, Nicolás E, Faize L, Díaz-Vivancos P, Burgos L, Hernández JA (2015) Cytosolic ascorbate peroxidase and Cu, Zn-superoxide dismutase improve seed germination, plant growth, nutrient uptake and drought tolerance in tobacco. Theor Exp Plant Physiol 215–226
Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 673–689
Fan W, Zhao M, Li S, Bai X, Li J, Meng H, Mu Z (2016) Contrasting transcriptional responses of PYR1/PYL/RCAR ABA receptors to ABA or dehydration stress between maize seedling leaves and roots. BMC Plant Biol 21:99
Fercha A, Gherroucha H (2014) The role of osmoprotectants and antioxidant enzymes in the differential response of durum wheat genotypes to salinity. J Appl Bot Food Qual 74–79
Ferrareze PAG, Streit RSA, dos Santos PR, dos Santos FM, de Almeida RMC, Schrank A, Kmetzsch L, Vainstein MH, Staats CC (2017) Transcriptional analysis allows genome reannotation and reveals that Cryptococcus gatii CGII undergoes nutrient restriction during infection. Microorganisms 49
Geigenberger P, Thormahlen I, Daloso DM, Fernie AR (2017) The unprecedented versatility of the plant thioredoxin system. Trends Plant Sci 249–262
Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 256–267
Gong P, Zhang J, Li H, Yang C, Zhang C, Zhang X, Khurram Z, Zhang Y, Wang T, Fei Z, Ye Z (2010) Transcriptional profiles of drought-responsive genes in modulating transcription signal transduction, and biochemical pathways in tomato. J Exp Bot 3563–3575
Gupta D, Tuteja N (2011) Chaperones and foldases in endoplasmic reticulum stress signaling in plants. Plant Signal Behav 1:232–236
Gutle DD, Roret T, Hecker A, Reski R, Jacquot JP (2017) Dithiol disulphide exchange in redox regulation of chloroplast enzymes in response to evolutionary and structural constraints. Plant Sci 1–11
Haider MS, Zhang C, Kurjogi M, Pervaiz T, Zheng T, Zhang Cb, Lide C, Shangguan L, Fang J (2016) Insights into grapevine defense response against drought as revealed by biochemical, physiological and RNA-Seq analysis. bioRxiv 21
Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 28:3735–3740
He J, Du YL, Wang T, Turner NC, Xi Y, Li FM (2015) Old and new cultivars of soya bean (Glycine max L.) subjected to soil drying differ in abscisic acid accumulation, water relations characteristics and yield. J Agron Crop Sci 21:1–12
Herrero S, González E, Gillikin JW, Vélëz H, Daub ME (2011) Identification and characterization of a pyridoxal reductase involved in the vitamin B6 salvage pathway in Arabidopsis. Plant Mol Biol 157–169
Hong Y, Zheng S, Wang X (2008) Dual functions of phospholipase Dα1 in plant response to drought. Mol Plant 262–269
Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 969–987
Hua Z, Vierstra RD (2011) The cullin-ring ubiquitin-protein ligases, Ann Rev Plant Biol 299–334
Hu X, Page T, Sumida A, Tanaka A, Terry MJ, Tanaka R (2017) The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. Plant J 1184–1194
Huseynova IM, Aliyeva DR, Aliyev JA (2014) Subcellular localization and responses of superoxide dismutase isoforms in local wheat varieties subjected to continuous soil drought. Plant Physiol Biochem 54–60
Jain M, Tyagi AK, Khurana JP (2008) Constitutive expression of a meiotic recombination protein gene homolog, OsTOP6A1, from rice confers abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Rep 767–778
Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochim Biophys Acta (BBA) - Gene Structure and Expression 330–345
Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA. J Exp Bot 37–43
Johnson ES (2002) Ubiquitin branches out. Nat Cell Biol E295–E298
Johnson JM, Reichelt M, Vadassery J, Gershenzon J, Oelmüller R (2014) An Arabidopsis mutant impaired in intracellular calcium elevation is sensitive to biotic and abiotic stress. BMC Plant Biol 11:162
Ju HW, Min JH, Chung MS, Kim CS (2013) The atrzf1 mutation of the novel RING-type E3 ubiquitin ligase increases proline contents and enhances drought tolerance in Arabidopsis. Plant Sci 1–7
Jung HJ, Park SJ, Kang H (2013) Regulation of RNA metabolism in plant development and stress. J Plant Biol 123–129
Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in arabidopsis. Plant Cell 18:2733–2748
Kim MR, Khaleda L, Jung IJ, Kim JY, Lee SY, Cha JY, Kim WY (2017) Overexpression of chloroplast-localized NADPH-dependent thioredoxin reductase C (NTRC) enhances tolerance to photo-oxidative and drought stresses in Arabidopsis thaliana. J Plant Biol 175–180
Komatsu S, Nanjo Y, Nishimura M (2013) Proteomic analysis of the flooding tolerance mechanism in mutant soybean. J Proteomics 21:231–250
Kong D, Li M, Dong Z, Ji H, Li X (2015) Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses. Plant Cell Rep 395–410
Kuchelski FR, de Oliveira LF, Molina G, Almerão MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimarães FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Pereira GA, Margis R (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307–324
Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 112–166
Lee JH, Kim WT (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31:201–208
Liang X, Qin L, Liu P, Wang M, Ye H (2014) Genes for iron–sulphur cluster assembly are targets of abiotic stress in rice, Oryza sativa. Plant Cell Environ 780–794
Liu ZB, Wang JM, Yang FX, Yang L, Yue YF, Xiang JB, Gao M, Xiong FJ, Lv D, Wu XJ, Liu N, Zhang X, Li XF, Yang Y (2014) A novel membrane-bound E3 ubiquitin ligase enhances the thermal resistance in plants. Plant Biotechnol J 93–104
Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 28:3730–3734
Liu J, Xi, Z, Wang M, Zhang X, Yang T, Wu J (2013) Overexpression of a maize E3 ubiquitin ligase gene enhances drought tolerance through regulating stomatal aperture and antioxidant system in transgenic tobacco. Plant Physiol Biochem 114–120
Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 19:1943–1945
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Li X, Zhang Y, Yin L, Lu J (2017) Overexpression of pathogen-induced grapevine TIR-NB-LRR gene VaRGA1 enhances disease resistance and drought and salt tolerance in Nicotiana benthamiana. Protoplasma 957–969
Lodish H (2000) Translocation of Secretory Proteins across the ER Membrane. In Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J (eds) Molecular Cell Biol, 4th edn. New York: W. H. Freeman and Company
Loudet O, Michael TP, Burger BT, Le M, Mockle TC, Weigel D, Chory (2008) A zinc knuckle protein that negatively controls morning-specific growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 4:17193–17198
Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 75–87
Luo X, Bai X, Zhu D, Li Y, Ji W, Cai H, Wu J, Liu B, Zhu Y (2011) GsZFP1, a new Cys2/His2-type zinc-finger protein, is a positive regulator of plant tolerance to cold and drought stress. Planta 9:1141–115
Marrocco K, Bergdoll M, Achard P, Criqui MC, Genschik P (2010) Selective proteolysis sets the tempo of the cell cycle. Curr Opin Plant Biol 631–639
Mascher T, Helmann JD, Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 910–938
Miotto YE, Tesser da Costa C, de Oliveira BH, Guzman F, Margis R, de Almeida RMC, Offringa R, Dos Santos Maraschin F (2019) Identification of root transcriptional responses to shoot illumination in Arabidopsis thaliana. Plant Mol Biol. Nov;101(4-5):487-498. https://doi.org/10.1007/s11103-019-00918-7. Epub 2019 Sep 27. PMID: 31560104. https://pubmed.ncbi.nlm.nih.gov/31560104/
Mishra AK, Puranik S, Prasad M (2012) Structure and regulatory networks of WD40 protein in plants. J Plant Biochem Biotechnol 32–39
Morais DAA, de Almeida RMC, Dalmolin RJS (2018) Transcriptogramer: an R/bioconductor package for transcriptional analysis based on canonical protein-protein interaction data. Bioinformatics - Submitted
Nagahatenna DSK, Langridge P, Whitford R (2015) Tetrapyrrole-based drought stress signalling. Plant Biotechnol J 447–459
Nakata M, Mitsuda N, Herde M, Koo AJK, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M (2013) A bHLH-Type transcription factor, ABA-inducible BHLH-type transcription factor/JA-associated MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis. Plant Cell 1641–1656
Nguyen HT, Neelakadan AK, Quach TN, Valliyodan B, Kumar R, Zhang Z, Nguyen HT (2013) Molecular characterization of Glycine max squalene synthase genes in seed phytosterol biosynthesis. Plant Physiol Biochem 23–32
Pan L, Zhang X, Wang J, Ma X, Zhou M, Huang L, Nie G, Wang P, Yang Z, Li J (2016) Transcriptional profiles of drought-related genes in modulating metabolic processes and antioxidant defenses in Lolium multiflorum. Front Plant Sci 25:519
Pang YLJ, Poruri K, Martinis SA (2014) tRNA synthetase: tRNA aminoacylation and beyond. Wiley Interdiscip Rev RNA 461–480
Park SY, Fung P, Nishimura N, Jensen DR, Fujii HZ, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009a) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 22
Park SK, Jung YJ, Lee JR, Lee YM, Jang HH, Lee SS, Park JH, Kim SY, Moon JC, Lee SY, Chae HB, Shin MR, Jung JH, Kim MG, Kim WY, Yun DJ, Lee KO, Lee SY (2009b) Heat-shock and redox-dependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone. Plant Physiol 552–561
Peng X, Zhao Y, Cao J, Zhang, W, Jiang H, Li X, Ma Q, Zhu S, Cheng B (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 6:e40120
Raghavendra AS, Gonugunta VK, Christamnn A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 395–401
Reis RR, Mertz-Henning LM, Marcolino-Gomes J, Rodrigues FA, Rockenbach-Marin S, Fuganti-Pagliarini R, Koltun A, Gonçalves LSA, Nepomuceno AL (2020) Differential gene expression in response to water deficit in leaf and root tissues of soybean genotypes with contrasting tolerance profiles. Genet Mol Biol 43(2)
Reitz MU, Pai S, Imani J, Schäfer P (2013) New insights into the subcellular localization of Tubby-like proteins and their participation in the Arabidopsis-Piriformospora indica interaction. Plant Signal Behav 1:e25198
Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 01:1077
Rodrigo-Moreno A, Andrés-Colás N, Poschenrieder C, Gunsé B, Peñarrubia L, Shabala S (2012) Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant Cell Environ 844–855
Rodrigues A, Fuganti-Pagliarini R, Marcolino-Gomes Nakayama J, Molinari HBC, Lobo Harmon G, Nepomuceno L (2015) Daytime soybean transcriptome fluctuations during water deficit stress. BMC Genomics 505
Rohwer CL, Erwin JE (2008) Horticultural applications of jasmonates: a review. J Horticult Sci Biotechnol 283–304
Roy S (2014) Maintenance of genome stability in plants: repairing DNA double strand breaks and chromatin structure stability. Front Plant Sci
Rybarczyk-Filho L, Castro MAA, Dalmolin RJS, Moreira JCF, Brunnet LG de Almeida RMC (2011) Towards a genome-wide transcriptogram: the Saccharomyces cerevisiae case. Nucleic Acids Res 3005–3016
Santiago J, Dupeux F, Betz K, Antoni R, Gonzalez-Gusman M, Rodriguez L, Márquez JA, Rodriguez PL (2012) Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci 3–11
Savchenko T, Dehesh K (2014) Drought stress modulates oxylipin signature by eliciting 12-OPDA as a potent regulator of stomatal aperture. Plant Signal Behav e28304
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 327–330
Sharma B, Joshi D, Yadav PK, Gupta AK, Bhatt TK (2016) Role of ubiquitin-mediated degradation system in plant biology. Front Plant Sci 806
Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 209–217
Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 6
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 26
Shivakumara TN, Sreevathsa R, Dash PK, Sheshshayee MS, Papolu PK, Rao U, Tuteja N, UdayaKumar M (2017) Overexpression of Pea DNA Helicase 45 (PDH45) imparts tolerance to multiple abiotic stresses in chili (Capsicum annuum L.). Sci Rep 2760
Singh AP, Pandey BK, Deveshwar P, Narnoliya L, Parida SK, Giri J (2015) JAZ Repressors: potential involvement in nutrients deficiency response in rice and chickpea. Front Plant Sci 975
Spratt DE, Wu K, Kovacev J, Pan ZQ, Shaw GS (2012) Selective recruitment of an E2∼ubiquitin complex by an E3 ubiquitin ligase. J Biol Chem 17374–17385
Sung P, Prakash S, Prakash L (1990) Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions. Proc Natl Acad Sci USA 2695–2699
Suzuki T, Imamura A, Ueguchi C, Mizuno T (1998) Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol 1258–1268
Taiz L, Zeiger E, Moller IM, Murphy A (2014) Plant Physiology and Development, 6th edn. Sinauer Associates Incorporated Publishers
Thatcher SR, Danilevskaya ON, Meng X, Beatty M, Zastrow-Hayes G, Harris C, Van Allen B, Habben J, Li B (2016) Genome-wide analysis of alternative splicing during development and drought stress in maize. Plant Physiol 586–599
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 102
Trivedi I, Rai KM, Singh SK, Kumar V, Singh M, Ranjan A, Lodhi N, Sawant SV (2011) Analysis of histones and histone variants in plants. In: Methods in Molecular Biology. Springer
Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 134–149
Tuteja N, Singh S, Tuteja R (2012) Helicases in improving abiotic stress tolerance in crop plants, in Tuteja N, Gill SS, Tiburcio AF, and Tuteja, R, Improving Crop Resistance to Abiotic Stress, 1st edn. Wiley-VCH Verlag GmbH & Co. KGaA
Urao T, Miyata S, Yamaguchi-Shinozaki K, Shinozaki K (2000) Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett 227–232
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(research0034):1
Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 385–397
Voet DJ, Voet JG, Pratt CW (2008) Mitochondrial ATP synthesis. In: Principles of Biochemistry. Wiley
Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 842–857
Wan X, Mo A, Liu S, Yang L, Li L (2011) Constitutive expression of a peanut ubiquitin-conjugating enzyme gene in Arabidopsis confers improved water-stress tolerance through regulation of stress-responsive gene expression. J Biosci Bioeng 478–484
Wang G, Cai G, Kong F, Deng Y, Ma N, Me Q (2014a) Overexpression of tomato chloroplast-targeted DnaJ protein enhances tolerance to drought stress and resistance to Pseudomonas solanacearum in transgenic tobacco. Plant Physiol Biochem 95–104
Wang X, Cai X, Xu C, Wang Q, Dai S (2016) Drought-responsive mechanisms in plant leaves revealed by proteomics. Int J Mol Sci 2–30
Wang B, Du Q, Yang X, Zhang D (2014b) Identification and characterization of nuclear genes involved in photosynthesis in Populus. BMC Plant Biol 81
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 244–252
Wang L, Liu L, Ma Y, Li S, Dong S, Zu W (2018) Transcriptome profilling analysis characterized the gene expression patterns responded to combined drought and heat stresses in soybean. Comput Biol Chem 77:413–429
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 1021–1058
Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell S165-S183
Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett 1037–1043
Xu C, Xia C, Xia Z, Zhou X, Huang J, Huang Z, Liu Y, Jiang Y, Casteel S, Zhang C (2018) Physiological and transcriptomic responses of reproductive stage soybean to drought stress. Plant Cell Rep 37(12):1611–1624
Yang H, Shi G, Du H, Wang H, Zhang Z, Hu D, Wang J, Huang F, Yu D (2017) Genome-wide analysis of soybean lateral organ boundaries domain-containing genes: a functional investigation of GmLBD12. Plant Genome 1–19
Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012) Genome-wide identification and analysis of the TIFY gene family in grape. PLoS One
Zhang CJ, Hou XM, Tan LM, Shao CR, Huang HW, Li YQ, Li L, Cai T, Chen S, He XJ (2016) (2016) The Arabidopsis acetylated histone-binding protein BRAT1 forms a complex with BRP1 and prevents transcriptional silencing. Nat Commun 7:11715
Zhao XC, Schaller GE (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 189–192
Zhao G, Song Y, Wang C, Butt H, Wang Q, Zhang C, Yang Z, Liu Z, Chen E, Zhang X, Li F (2016) Genome-wide identification and functional analysis of the TIFY gene family in response to drought in cotton. Mol Genet Genom 2173–2187
Zhou GA, Chang RZ, Qiu L (2010) Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Mol Biol 357–367
Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 247–273
Zhu D, Bai X, Luo X, Chen Q, Cai H, Ji W, Zhu Y (2013) Identification of wild soybean (Glycine soja) TIFY family genes. Plant Cell Rep 263–272
Zhu J, Gong Z, Zhang C, Song CP, Damsz B, Inan G, Koiwa H, Zhu JK, Hasegawa PM, Bressan RA (2002) OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid–mediated and non-abscisic acid–mediated responses to abiotic stress. Plant Cell 3009–3028
Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 4945–4950
Zoz T, Steiner F, Guimarães VF, Castagnara DD, Meinerz CC, Fey R (2013) Peroxidase activity as an indicator of water deficit tolerance in soybean cultivars. Biosci J 1664–1671
Acknowledgements
We would like to thank Dr. Steven B. Cannon (US Department of Agriculture-Agricultural Research Service, Corn Insects and Crop Genetics Research Unit) for granting permission to use the RNA-Seq data published by his group.
Funding
This work was supported by MCTI/CNPq/CAPES/FAPs no. 16/2014-National Institute of Science and Technology (INCT) in Biotech Assets Applied to Drought and Pests of Relevant Crops to Agrobusiness [88887.136360/2017–00-465480/2014-4]
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LAOB, RMCA, and MHBZ conceived the study; LAOB, RMCA, RLMW, and CPSG conducted the experiments; LAOB and RMCA analyzed the data, and LAOB, DF, RMCA, CB, and MHBZ wrote the manuscript. All authors read and approved the final version.
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Key Message
• The soybean root transcriptome undertakes an important reprogramming specially during the first hour of drought stress. The Transcriptogramer has evinced a global reprogramed transcriptome and biological processes not detected by conventional tools
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11105_2021_1297_MOESM6_ESM.tiff
Supplementary file6 Figure S1 – geNorm expression stability plot. Expression stability of four different tested primers. (TIFF 1521 KB)
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de Oliveira-Busatto, L.A., de Almeida, R.M.C., Weber, R.L.M. et al. The Soybean Transcriptogram Allows a Wide Genome-to-Single-Gene Analysis That Evinces Time-Dependent Drought Response. Plant Mol Biol Rep 40, 1–27 (2022). https://doi.org/10.1007/s11105-021-01297-4
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DOI: https://doi.org/10.1007/s11105-021-01297-4
Keywords
- Water stress
- RNA-Seq
- Gene expression
- Transcriptogramer
- Transcriptome