Abstract
Background
The drought condition is responsible for considerable losses in soybean production, which in turn may result in billionaire losses. After drought perception, plants activate a cascade of protecting genes against water deficit (WD), many of which are responsive to abscisic acid, the most important phytohormone to plants’ adaptation. This work aimed to recover abscisic acid (ABA)-responsive differentially expressed genes (DEG) from an RNA-Seq, carried out from leaves and roots of drought-sensitive (BR16) and tolerant (Embrapa 48) soybean cultivars under mild (MiWD), moderate (MoWD), and severe (SWD) water-deficit treatments. Enriched ABA-responsive pathways important to drought tolerance in soybean were also identified.
Results
In drought-sensitive and tolerant soybean cultivars, approximately 75% of genes were identified as ABA-responsive by containing more than two ABRE (ABA-responsive elements) in the promoter region. Most of these genes were positively regulated. Roots were the tissue with more ABA-responsive genes and pathways triggered in response to WD in both cultivars, although, on the tolerant cultivar, these pathways were higher expressed. The most important enriched ABA pathways observed in the roots of both cultivars were involved in sugar and sulfur amino acid biosynthesis, osmoregulation, and crosstalk among ABA and ethylene, jasmonate, auxin, and cytokinin. Other pathways enriched were involved in phytoalexin production, ROS homeostasis, and membrane stability by glycerolipid and glycerophospholipid production. ABA-responsive genes were also ordered based on their expression profile in tissue and cultivar, and nine confidence groups could be observed. More than 80% of these clustered genes showed the same regulation profile under MiWd, MoWD, and SWD treatments. Activation of ABA biosynthesis under water deficit was validated by RT-qPCR by increasing the expression level of NCED3, an important enzyme in this pathway, and GOLS, a known ABA-responsive gene.
Conclusions
A robust catalog of ABA-responsive genes was made available in this work. Considering ABA’s role in drought-response mechanisms, the genes in the groups pointed out in this study would be reliable candidates to be used in strategies to develop soybean lines more tolerant to drought. This paper, presented for the first time, ABA-responsive genes and ABA-enriched pathways in contrasting soybean cultivars for drought tolerance.
Availability of Data and Material
The datasets generated and/or analyzed during this study are available in the NCBI Sequence Read Archive (SRA) database (BioProject accession: PRJNA615913), https://www.ncbi.nlm.nih.gov/sra?linkname=bioproject_sra_all&from_uid=615913
Abbreviations
- ABA:
-
Abscisic acid
- ABRE:
-
Abscisic acid-responsive element
- ACS:
-
1-Aminocyclopropane-1-carboxylate synthase
- AP2:
-
Apetala2
- ARFs:
-
Auxin response factors
- At:
-
Arabidopsis thaliana
- ATAF1-2:
-
Arabidopsis transcription activation factor 1–2
- cDNA:
-
Complementary deoxyribonucleic acid
- CKK:
-
Cytokinin dehydrogenase
- CUC2:
-
Cup-shaped cotyledon
- DEGs:
-
Differentially expressed genes
- DNA:
-
Deoxyribonucleic acid
- DNAse:
-
Deoxyribonuclease
- DREB:
-
Dehydration-responsive element-binding protein
- E48:
-
Embrapa 48
- EREBPs:
-
Ethylene-responsive element binding proteins
- ERF:
-
Responsive factors of ethylene
- ET:
-
Ethylene
- Gm:
-
Glycine max
- GOLS:
-
Galactinol synthase
- HSFs:
-
Heat shock factors
- JA:
-
Jasmonic acid
- JAI3/JAZ:
-
Jasmonate-insensitive/jasmonate-zim
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- LEA:
-
Late embryogenesis abundant
- Log2 FC:
-
Log2 fold-change
- MiWD:
-
Mild water-deficit treatment
- MoWD:
-
Moderate water-deficit treatment
- mRNA:
-
Messenger ribonucleic acid
- NAC:
-
No apical meristem
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
- NCED3:
-
9-Cis-epoxycarotenoid dioxygenase
- NO:
-
Nitric oxide
- OST1:
-
Open stomata 1
- RFO:
-
Raffinose family oligosaccharide
- RIN:
-
RNA integrity number
- RNA:
-
Ribonucleic acid
- RNA-Seq:
-
RNA sequencing
- ROS:
-
Reactive oxygen species
- rRNA:
-
Ribosomal ribonucleic acid
- RT-qPCR:
-
Reverse transcriptase quantitative polymerase chain reaction
- SA:
-
Salicylic acid
- SWD:
-
Severe water-deficit treatment
- TFs:
-
Transcription factors
- TSS:
-
Transcription start site
- WD:
-
Water deficit.
References
Abdelgawad ZA, Khalafaallah AA, Abdallah MM (2014) Impact of methyl jasmonate on antioxidant activity and some biochemical aspects of maize plant grown under water stress condition. Agric Sci 5(12):1077–1088. https://doi.org/10.4236/as.2014.512117
Agurla S, Gahir S, Munemasa S, Murata Y, Raghavendra AS (2018) Mechanism of stomatal closure in plants exposed to drought and cold stress. In: Iwaya-Inoue M, Sakurai M, Uemura M (eds) Survival strategies in extreme cold and desiccation. Advances in experimental medicine and biology, vol 1081. Springer, Singapore, pp 215–232
Ahrazem O, Rubio-Moraga A, Trapero A, Gómez-Gómez L (2012) Developmental and stress regulation of gene expression for a 9-cis-epoxycarotenoid dioxygenase, CstNCED, isolated from Crocus sativus stigmas. J Exp Bot 63(2):681–694. https://doi.org/10.1093/jxb/err293
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 28 Mar 2022
Aslam MM, Waseem M, Jakada BH, Okal EJ, Lei Z, Saqib HSA, Yuan W, Xu W, Zhang Q (2022) Mechanisms of abscisic acid-mediated drought stress responses in plants. Int J Mol Sci 23(3):1084. https://doi.org/10.3390/ijms23031084
Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15(1):1–7. https://doi.org/10.1186/1471-2105-15-293
Behnam B, Iuchi S, Fujita M, Fujita Y, Takasaki H, Osakabe Y, Shinozaki K (2013) Characterization of the promoter region of an Arabidopsis gene for 9-cis-epoxycarotenoid dioxygenase involved in dehydration-inducible transcription. DNA Res 20(4):315–324. https://doi.org/10.1093/dnares/dst012
Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Front Plant Sci 12:615114. https://doi.org/10.3389/fpls.2021.615114
Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the highly ABA-responsive clade A protein phosphatase 2Cs. Plant Physiol 160(1):379–395. https://doi.org/10.1104/pp.112.202408
Bijalwan P, Sharma M, Kaushik P (2022) Review of the effects of drought stress on plants: a systematic approach. Preprints 2022020014:1–21. https://doi.org/10.20944/preprints202202.0014.v1
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine M (2018) Auxin response factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLoS ONE 13(2):e0193517. https://doi.org/10.1371/journal.pone.0193517
Bulgakov VP, Wu HC, Jinn TL (2019) Coordination of ABA and chaperone signaling in plant stress responses. Trends Plant Sci 24(7):636–651. https://doi.org/10.1016/j.tplants.2019.04.004
Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17(4):427–431. https://doi.org/10.1046/j.1365-313X.1999.00386.x
Chaichi M, Sanjarian F, Razavi K, Gonzalez-Hernandez JL (2019) Analysis of transcriptional responses in root tissue of bread wheat landrace (Triticum aestivum L.) reveals drought avoidance mechanisms under water scarcity. PloS ONE 14(3): e0212671. https://doi.org/10.1371/journal.pone.0212671
Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281. https://doi.org/10.1186/1471-2229-10-281
Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124(1):343–354. https://doi.org/10.1104/pp.124.1.343
Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao L, Guo X (2015) The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana. PLoS ONE 10(11):e0143022. https://doi.org/10.1371/journal.pone.0143022
Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette M-L, Lelandais G, Ningre N, Renou JP, Tamby JP, Thiec DL, Hummel I (2010) Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics 11:630. https://doi.org/10.1186/1471-2164-11-630
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75. https://doi.org/10.1242/jeb.089938
Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szcześniak MW, Wojciech M, Gaffney DJ, Elo LL, Zhang X, Mortazavi A (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17(1):1–19. https://doi.org/10.1186/s13059-016-0881-8
Contreras-Moreira B, Castro-Mondragon JA, Rioualen C, Cantalapiedra CP, Van Helden J (2016) RSAT:Plants: Motif discovery within clusters of upstream sequences in plant genomes. In: Hehl R (ed) Plant Synthetic Promoters, vol 1482. Humana Press, New York, pp 279–295
Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703. https://doi.org/10.1126/science.223.4637.701
De Ollas C, Dodd IC (2016) Physiological impacts of ABA-JA interactions under water-limitation. Plant Mol Biol 91:641–650. https://doi.org/10.1007/s11103-016-0503-6
Ding ZJ, Yan JY, Li CX, Li GX, Wu YR, Zheng SJ (2015) Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J 84(1):56–69. https://doi.org/10.1111/tpj.12958
dos Santos TB, Budzinski IGF, Marura CJ, Petkowicz CLO, Pereira LFP, Vieira LGE (2011) Expression of three galactinol synthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant Physiol Biochem 49:441–448. https://doi.org/10.1016/j.plaphy.2011.01.023
dos Santos TB, Lima RB, Nagashima GT, Petkowicz CLO, Carpentieri-Pípolo V, Pereira LFP, Domingues DS, Vieira LGE (2015) Galactinol synthase transcriptional profile in two genotypes of Coffea canephora with contrasting tolerance to drought. Genet Mol Biol 38(2):182–190. https://doi.org/10.1590/S1415-475738220140171
Downie B, Gurusinghe S, Dahal P, Thacker RR, Snyder JC, Nonogaki H, Yim K, Fukanaga K, Alvarado V, Bradford KJ (2003) Expression of a galactinol synthase gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131:1347–1359. https://doi.org/10.1104/pp.016386
Duarte KE, de Souza WR, Santiago TR, Sampaio BL, Ribeiro AP, Cotta MG, Molinari HBC (2019) Identification and characterization of core abscisic acid (ABA) signaling components and their gene expression profile in response to abiotic stresses in Setaria viridis. Sci Rep 9(1):4028. https://doi.org/10.1038/s41598-019-40623-5
Estrada-Melo AC, Chao C, Reid MS, Jiang CZ (2015) Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Hortic Res 2:1–9. https://doi.org/10.1038/hortres.2015.13
Fehr WR, Caviness CE, Burmood DT, Pernnigton JS (1971) Stage of development description for soybeans [Glycine max (L.) Merrill]. Crop Sci 11(6):929–931. https://doi.org/10.2135/cropsci1971.0011183X001100060051x
Feng J, Meyer CA, Wang Q, Liu JS, Liu X, Zhang Y (2012) GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics 28(21):2782–2788. https://doi.org/10.1093/bioinformatics/bts515
Ferreira RC (2016) Quantification of drought losses in soybean crop in Brazil. State University of Londrina, Thesis
Finatto T, Viana VE, Woyann LG, Busanello C, da Maia LC, de Oliveira AC (2018) Can WRKY transcription factors help plants to overcome environmental challenges? Genet Mol Biol 41(3):533–544. https://doi.org/10.1590/1678-4685-GMB-2017-0232
Fuganti-Pagliarini R, Ferreira LC, Rodrigues FA, Molinari HBC, Marin SRR, Molinari MDC, Marcolino-Gomes J, Mertz-Henning LM, Farias JRB, de Oliveira MCN, Neumaier N, Kanamori N, Fujita Y, Mizoi J, Nakashima K, Yamaguchi-Shinozaki K, Nepomuceno AL (2017) Characterization of soybean genetically modified for drought tolerance in field conditions. Front Plant Sci 8:448. https://doi.org/10.3389/fpls.2017.00448
Ge SX, Jung D, Yao R (2020) ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics 36(8):2628–2629. https://doi.org/10.1093/bioinformatics/btz931
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(D1):D1178–D1186. https://doi.org/10.1093/nar/gkr944
Gu L, Zhang Y, Zhang M, Li T, Dirk LMA, Downie B, Zhao T (2016) ZmGOLS2, a target of transcription factor ZmDREB2A, offers similar protection against abiotic stress as ZmDREB2A. Plant Mol Biol 90:157–170. https://doi.org/10.1007/s11103-015-0403-1
Haworth M, Marino G, Cosentino SL, Brunetti C, De Carlo A, Avola G, Riggia E, Loreto F, Centritto M (2018) Increased free abscisic acid during drought enhances stomatal sensitivity and modifies stomatal behaviour in fast growing giant reed (Arundo donax L.). Environ Exp Bot 147:116–124. https://doi.org/10.1016/j.envexpbot.2017.11.002
Himuro Y, Ishiyama K, Mori F, Gondo T, Takahashi F, Shinozaki K, Kobayashi M, Akashi R (2014) Arabidopsis galactinol synthase AtGolS2 improves drought tolerance in the monocot model Brachypodium distachyon. J Plant Physiol 171(13):1127–1131. https://doi.org/10.1016/j.jplph.2014.04.007
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Second ed. Circular. Cal Agric Exp Sta Cir 347(2):1–32.
Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19(6):679–689. https://doi.org/10.1046/j.1365-313x.1999.00565.x
Honna PT, Fuganti-Pagliarini R, Ferreira LC, Molinari MDC, Marin SRR, Oliveira MCN, Farias JRB, Neumaier N, Mertz-Henning LM, Kanamori N, Nakashima K, Takasaki H, Urano K, Shinozaki K, Yamaguchi-Shinozaki K, Desidério JA, Nepomuceno AL (2016a) Molecular, physiological, and agronomical characterization, in greenhouse and in field conditions, of soybean plants genetically modified with AtGolS2 gene for drought tolerance. Mol Breeding 36:157. https://doi.org/10.1007/s11032-016-0570-z
Honna PT, Fuganti-Pagliarini R, Ferreira LC, Molinari MD, Marin SR, de Oliveira MC, Nepomuceno AL (2016b) Molecular, physiological, and agronomical characterization, in greenhouse and in field conditions, of soybean plants genetically modified with AtGolS2 gene for drought tolerance. Mol Breeding 36(11):1–17. https://doi.org/10.1007/s11032-016-0570-z
Huang YC, Niu CY, Yang CR, Jinn TL (2016) The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol 172:1182–1199. https://doi.org/10.1104/pp.16.00860
Huang Y, Guo Y, Liu Y, Zhang F, Wang Z, Wang H, Wang F, Li D, Mao D, Luan S, Liang M, Chen L (2018) 9-Cis-epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Front Plant Sci 9:162. https://doi.org/10.3389/fpls.2018.00162
Huang S, Waadt R, Nuhkat M, Kollist H, Hedrich R, Roelfsema MRG (2019) Calcium signals in guard cells enhance the efficiency by which abscisic acid triggers stomatal closure. New Phytol 224(1):177–187. https://doi.org/10.1111/nph.15985
Iqbal S, Wang X, Mubeen I, Kamran M, Kanwal I, Díaz GA, Abbas A, Parveen A, Atiq MN, Alshaya H, Zin El-Abedin TK, Fahad S (2022) Phytohormones trigger drought tolerance in crop plants: outlook and future perspectives. Front Plant Sci 12:799318. https://doi.org/10.3389/fpls.2021.799318
Iquebal MA, Sharma P, Jasrotia RS, Jaiswal S, Kaur A, Saroha M, Rai A (2019) RNA-Seq analysis reveals drought-responsive molecular pathways with candidate genes and putative molecular markers in root tissue of wheat. Sci Rep 9:1–18. https://doi.org/10.1038/s41598-019-49915-2
Intergovernmental Panel on Climate Change (2022) Climate change 2022: impacts, adaptation and vulnerability https://www.ipcc.ch/report/ar6/wg2/ Accessed 05 Jun 2022
Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123(2):553–562. https://doi.org/10.1104/pp.123.2.553
Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333. https://doi.org/10.1046/j.1365-313x.2001.01096.x
Janiak A, Kwaśniewski M, Szarejko I (2016) Gene expression regulation in roots under drought. J Exp Bot 67(4):1003–1014. https://doi.org/10.1093/jxb/erv512
Jung H, Lee D-K, Do Choi Y, Kim J-K (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312. https://doi.org/10.1016/j.plantsci.2015.04.018
Kaur H, Manna M, Thakur T, Gautam V, Salvi P (2021) Imperative role of sugar signaling and transport during drought stress responses in plants. Physiol Plant 171(4):833–848. https://doi.org/10.1111/ppl.13364
Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665. https://doi.org/10.1093/aob/mct229
Ke M, Zheng Y, Zhu Z (2015) Rethinking the origin of auxin biosynthesis in plants. Front Plant Sci 6:1093. https://doi.org/10.3389/fpls.2015.01093
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast-spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276. https://doi.org/10.1093/dnares/dsr015
León J, Castillo MC, Coego A, Lozano-Juste J, Mir R (2014) Diverse functional interactions between nitric oxide and abscisic acid in plant development and responses to stress. J Exp Bot 65(4):907–921. https://doi.org/10.1093/jxb/ert454
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li HC, Zhang HN, Li GL, Liu ZH, Zhang YM, Zhang HM, Guo XL (2015) Expression of maize heat shock transcription factor gene ZmHsf06 enhances the thermotolerance and drought-stress tolerance of transgenic Arabidopsis. Funct Plant Biol 42:1080–1091. https://doi.org/10.1071/FP15080
Li W, Herrera-Estrella L, Tran LP (2016) The Yin-Yang of cytokinin homeostasis and drought acclimation/adaptation. Trends Plant Sci 21:548–550. https://doi.org/10.1016/j.tplants.2016.05.006
Liu C, Zhang T (2017) Expansion and stress responses of the AP2/EREBP superfamily in cotton. BMC Genomics 18:118. https://doi.org/10.1186/s12864-017-3517-9
Liu W, Zhang Y, Li W, Lin Y, Wang C, Xu R, Zhang L (2020) Genome-wide characterization and expression analysis of soybean trihelix gene family. PeerJ 8:e8753. https://doi.org/10.7717/peerj.8753
Liu L, Long X, Wua W, Xiang S, Yu X, Demura T, Lia D, Zhuge Q (2021a) Galactinol synthase confers salt-stress tolerance by regulating the synthesis of galactinol and raffinose family oligosaccharides in poplar. Industrial Crops Prod 165:113432. https://doi.org/10.1016/j.indcrop.2021.113432
Liu L, Wu X, Sun W, Yu X, Demura T, Li D, Zhuge Q (2021b) Galactinol synthase confers salt-stress tolerance by regulating the synthesis of galactinol and raffinose family oligosaccharides in poplar. Ind Crops Prod 165:1–16. https://doi.org/10.1016/j.indcrop.2021.113432
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950. https://doi.org/10.1242/dev.086363
Lorenz WW, Alba R, Yu YS, Bordeaux JM, Simões M, Dean JF (2011) Microarray analysis and scale-free gene networks identify candidate regulators in drought-stressed roots of loblolly pine (P. taeda L.). BMC Genomics 12:264. https://doi.org/10.1186/1471-2164-12-264
Ma H, Wang C, Yang B, Cheng H, Wang Z, Mijiti A, Ren C, Qu G, Zhang H, Ma L (2016) CarHSFB2, a class B heat shock transcription factor, is involved in different developmental processes and various stress responses in chickpea (Cicer Arietinum L.). Plant Mol Biol Report 34:1–14. https://doi.org/10.1007/s11105-015-0892-8
Manna M, Thakur T, Chirom O, Mandlik R, Deshmukh R, Salvi P (2020) Transcription factors as key molecular target to strengthen the drought stress tolerance in plants. Physiol Plant 172(2):847–868. https://doi.org/10.1111/ppl.13268
Marcolino-Gomes J, Rodrigues FA, Fuganti-Pagliarini R, Bendix C, Nakayama TJ, Celaya B, Hugo Molinari BC, Oliveira MCN, Harmon FG, Nepomuceno AL (2014) Diurnal oscillations of soybean circadian clock and drought responsive genes. PLoS ONE 9(1):e86402. https://doi.org/10.1371/journal.pone.0086402
Marcolino-Gomes J, Rodrigues FA, Fuganti-Pagliarini R, Nakayama TJ, Reis RR, Farias JRB, Harmon F, Molinari HBC, Molinari MDC, Nepomuceno A (2015) Transcriptome-wide identification of reference genes for expression analysis of soybean responses to drought stress along the day. PLoS ONE 10(9):e0139051. https://doi.org/10.1371/journal.pone.0139051
Martins PK, Jordão BQ, Yamanaka N, Farias JR, Beneventi MA, Binneck E, 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
Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, Matsukura S, Kojima M (2012) Identification of cis-acting promoter elements in cold-and dehydration-responsive transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19(1):37–49. https://doi.org/10.1093/dnares/dsr040
Mashaki KM, Garg V, Ghomi AAN, Kudapa H, Chitikineni A, Nezhad KZ, Thudi M (2018) RNA-Seq analysis revealed genes associated with drought stress response in kabuli chickpea (Cicer arietinum L.). PloS ONE 13(6): e0199774. https://doi.org/10.1371/journal.pone.0199774
Mewis I, Khan MA, Glawischnig E, Schreiner M, Ulrichs C (2012) Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PloS ONE 7(11):e48661. https://doi.org/10.1371/journal.pone.0048661
Molinari MDC, Fuganti-Pagliarini R, Marin SRR, Ferreira LC, Barbosa DA, Marcolino-Gomes J, Oliveira MCN, Mertz-Henning LM, Kanamori N, Nakashima K, Takasaki H, Urano K, Shinozaki K, Yamaguchi-Shinozaki K, Nepomuceno AL (2020) Overexpression of AtNCED3 gene improved drought tolerance in soybean in greenhouse and field. Genet Mol Biol 43(3):e20190292. https://doi.org/10.1590/1678-4685-GMB-2019-0292
Molinari MDC, Fuganti-Pagliarini R, Marcolino-Gomes J, de Amorim BD, Rockenbach Marin SR, Mertz-Henning LM, Rech Filho EL (2021a) Flower and pod genes involved in soybean sensitivity to drought. J Plant Interact 16:187–200. https://doi.org/10.1080/17429145.2021.1921293
Molinari MDC, Fuganti-Pagliarini R, Mendonça JA, de Amorim BD, Marin DR, Mertz-Henning L, Nepomuceno AL (2021b) Transcriptome analysis using RNA-Seq from experiments with and without biological replicates: a review. Rev Ciênc Agrar 64:1–13
Moumeni A, Satoh K, Kondoh H, Asano T, Hosaka A, Venuprasad R, Serraj R, Kumar A, Leung H, Kikuchi S (2011) Comparative analysis of root transcriptome profiles of two pairs of drought-tolerant and susceptible rice near-isogenic lines under different drought stress. BMC Plant Biol 11:174. https://doi.org/10.1186/1471-2229-11-174
Multiple Primer Analyze software. https://www.thermofisher.com/br/pt/home/brands/thermo-scientific/molecular-biology/molecular-biology-learning-center/molecular-biology-resource-library/thermo-scientific-web-tools/multiple-primer-analyzer.html Accessed 06 Jun 2022
Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder JI (2015) Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol 28:154–162. https://doi.org/10.1016/j.pbi.2015.10.010
Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, 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. https://doi.org/10.1007/s11103-005-2418-5
Nakashima K, Jan A, Todaka D, Maruyama K, Goto S, Shinozaki K, Yamaguchi-Shinozaki K (2014) Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239(1):47–60. https://doi.org/10.1007/s00425-013-1960-7
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Yamaguchi-Shinozaki K (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. Plant J 34(2):137–148. https://doi.org/10.1046/j.1365-313x.2003.01708.x
Neves DM, Coelho Filho MA, Bellete BS, Silva MFGF, Souza DT, Soares Filho WDS, Gesteira AS (2013) Comparative study of putative 9-cis-epoxycarotenoid dioxygenase and abscisic acid accumulation in the responses of Sunki mandarin and Rangpur lime to water deficit. Mol Biol Rep 40:5339–5349. https://doi.org/10.1007/s11033-013-2634-z
Nishiyama R, Watanabe Y, Fujita Y, Dung TL, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran L-SP (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183. https://doi.org/10.1105/tpc.111.087395
Ortiz R (2019). Role of plant breeding to sustain food security under climate change. In: Yadav SS, Redden RJ, Hatfield JL, Ebert AW, Hunter D (eds) Food security and climate change, first ed. John Wiley & Sons Ltd, Hoboken, pp 145–158
Oya T, Nepomuceno AL, Neumaier N, Farias JRB, Tobita S, Ito O (2004) Drought tolerance characteristics of Brazilian soybean cultivars. Plant Prod Sci 7(2):129–137. https://doi.org/10.1626/pps.7.129
Pedrosa AM, Cidade LC, Martins CPS, Macedo AF, Neves DM, Gomes FP, Floh EIS, Costa MGC (2017) Effect of overexpression of citrus 9-cis-epoxycarotenoid dioxygenase 3 (CsNCED3) on the physiological response to drought stress in transgenic tobacco. Genet Mol Res 16(1):1–10. https://doi.org/10.4238/gmr16019292
Pedrosa AM, Martins CDPS, Goncalves LP, Costa MGC (2015) Late embryogenesis abundant (LEA) constitutes a large and diverse family of proteins involved in development and abiotic stress responses in sweet orange (Citrus sinensis L. Osb.). PloS ONE 10(12):e0145785. https://doi.org/10.1371/journal.pone.0145785
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Pillet J, Egert A, Pieri P, Lecourieux F, Kappel C, Charon J, Gomes E, Keller F, Delrot S, Lecourieux D (2012) VvGOLS1 and VvHsfA2 are involved in the heat stress responses in grapevine berries. Plant Cell Physiol 53:1776–1792. https://doi.org/10.1093/pcp/pcs121
Pizzio GA (2022) Abscisic acid machinery is under circadian clock regulation at multiple levels. Stresses 2(1):65–78. https://doi.org/10.3390/stresses2010006
Primer3Plus software. https://primer3plus.com/cgi-bin/dev/primer3plus.cgi Accessed 06 Jun 2022.
Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci 96:15354–15361. https://doi.org/10.1073/pnas.96.26.15354
Qin X, Zeevaart JA (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551. https://doi.org/10.1104/pp.010663
Ranjan A, Sawant S (2014) Genome-wide transcriptomic comparison of cotton (Gossypium herbaceum) leaf and root under drought stress. 3 Biotech 5:585–596. https://doi.org/10.1007/s13205-014-0257-2
Recchia GH, Gomes Caldas DG, Ahern Beraldo AL, da Silva MJ, Tsai SM (2013) Transcriptional analysis of drought-induced genes in the roots of a tolerant genotype of the common bean (Phaseolus vulgaris L.). Int J Mol Sci 14(4):7155–7179. https://doi.org/10.3390/ijms14047155
Rodrigo MJ, Alquezar B, Zacarías L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643. https://doi.org/10.1093/jxb/erj048
Rodrigues FA, Marcolino-Gomes J, Carvalho JDFC, Nascimento LCD, Neumaier N, Farias JRB, Nepomuceno AL (2012) Subtractive libraries for prospecting differentially expressed genes in the soybean under water deficit. Genet Mol Biol 35:304–314. https://doi.org/10.1590/S1415-47572012000200011
Rodrigues FA, Fuganti-Pagliarini R, Marcolino-Gomes J, Nakayama TJ, Molinari HBC, Lobo FP, Harmon FG, Nepomuceno AL (2015) Daytime soybean transcriptome fluctuations during water deficit stress. BMC Genomics 16:505. https://doi.org/10.1186/s12864-015-1731-x
Ruijter J, Van Der Velden S, Ilgun A (2019) LinRegPCR: analysis of quantitative RT-PCR data. https://www.gene-quantification.de/LinRegPCR_help_manual_v11.0.pdf. Accessed 28 Mar 2022
Scarpeci TE, Frea VS, Zanor MI, Valle EM (2017) Overexpression of AtERF019 delays plant growth and senescence and improves drought tolerance in Arabidopsis. J Exp Bot 68:673–685. https://doi.org/10.1093/jxb/erw429
Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405. https://doi.org/10.1007/s00709-015-0756-y
Shen QJ, Casaretto JA, Zhang P, Ho THD (2004) Functional definition of ABA-response complexes: the promoter units necessary and sufficient for ABA induction of gene expression in barley (Hordeum vulgare L.). Plant Mol Biol 54(1):111–124. https://doi.org/10.1023/B:PLAN.0000028773.94595.e8
Shimosaka E, Ozawa K (2015) Overexpression of cold-inducible wheat galactinol synthase confers tolerance to chilling stress in transgenic rice. Breeding Sci 65:363–371. https://doi.org/10.1270/jsbbs.65.363
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227. https://doi.org/10.1093/jxb/erl164
Singh PK, Indoliya Y, Agrawal L, Awasthi S, Deeba F, Dwivedi S, Chakrabarty D, Shirke PA, Pandey V, Singh N, Dhankher OP, Barik SK, Tripathi RD (2022) Genomic and proteomic responses to drought stress and biotechnological interventions for enhanced drought tolerance in plants. Curr Plant Biol 29:100239. https://doi.org/10.1016/j.cpb.2022.100239
Soar CJ, Speirs J, Maffei SM, Loveys BR (2004) Gradients in stomatal conductance, xylem sap ABA and bulk leaf ABA along canes of Vitis vinifera cv. Shiraz: molecular and physiological studies investigating their source. Funct Plant Biol 31:659–669. https://doi.org/10.1071/FP03238
Souza A, Batista VG, Pinheiro MP, Suassuna JF, Lima LMD, Fernandes PD (2016) Expression of NCED gene in colored cotton genotypes subjected to water stress. Rev Bras Eng Agríc Ambient 20:692–696. https://doi.org/10.1590/1807-1929/agriambi.v20n8p692-696
Suhartina, Purwantoro, Nugrahaeni N, Taufiq A, Mejaya MJ (2022) Yield stability performance of soybean (Glycine max [L.] Merrill) lines tolerant to drought. In: AIP Conference Proceedings, AIP Publishing LLC, 2462(1):020004 Jan 2022
Sultana S, Turečková V, Ho CL, Napis S, Namasivayam P (2014) Molecular cloning of a putative Acanthus ebracteatus-9-cis-epoxycarotenoid deoxygenase (AeNCED) and its overexpression in rice. J Crop Sci Biotechnol 17(4):239–246. https://doi.org/10.1007/s12892-014-0006-4
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426. https://doi.org/10.1046/j.0960-7412.2001.01227.x
Takahashi R, Joshee N, Kitagawa Y (1994) Induction of chilling resistance by water stress, and cDNA sequence analysis and expression of water stress regulated genes in rice. Plant Mol Biol 26:339–352. https://doi.org/10.1007/BF00039544
Tashi G, Zhan H, Xing G, Chang X, Zhang H, Nie X, Ji W (2018) Genome-wide identification and expression analysis of heat shock transcription factor family in Chenopodium quinoa Willd. Agronomy 8(7):103. https://doi.org/10.3390/agronomy8070103
Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23:363–374. https://doi.org/10.1046/j.1365-313x.2000.00789.x
Tong SM, Xi HX, Ai KJ, Hou HS (2017) Overexpression of wheat TaNCED gene in Arabidopsis enhances tolerance to drought stress and delays seed germination. Biol Plant 61:64–72. https://doi.org/10.1007/s10535-016-0692-5
Ullah A, Manghwar H, Shaban M, Khan AH, Akbar A, Ali U, Fahad S (2018) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25(33):33103–33118. https://doi.org/10.1007/s11356-018-3364-5
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci 97(21):11632–11637. https://doi.org/10.1073/pnas.190309197
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:1–10. https://doi.org/10.1186/s12870-016-0771-y
Wan XR, Li L (2006) Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochem Biophys Res Commun 347:1030–1038. https://doi.org/10.1016/j.bbrc.2006.07.026
Wang S, Wan C, Wang Y, Chen H, Zhou Z, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56:525–539. https://doi.org/10.1016/S0140-1963(03)00063-6
Wang D, Yao W, Song Y, Liu W, Wang Z (2012) Molecular characterization and expression of three galactinol synthase genes that confer stress tolerance in Salvia miltiorrhiza. J Plant Physiol 169:1838–1848. https://doi.org/10.1016/j.jplph.2012.07.015
Wang C, Zhao Y, Gu P, Zou F, Meng L, Song W, Yang Y, Wang S, Zhang Y (2018) Auxin is involved in lateral root formation induced by drought stress in tobacco seedlings. J Plant Growth Regul 37:539–549. https://doi.org/10.1007/s00344-017-9752-0
Wang X, Guo C, Peng J, Li C, Wan F, Zhang S, Yang S (2019) ABRE-binding factors play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol 221:341–355. https://doi.org/10.1111/nph.15345
Wang M, Vannozzi A, Wang G, Liang YH, Tornielli GB, Zenoni S, Cavallini E, Pezzotti M, Cheng ZM (2014) Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Horticult Res 1:14106. https://doi.org/10.1038/hortres.2014.16
Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30. https://doi.org/10.1007/s00299-008-0614-x
Yan Y, Jia H, Wang F, Wang C, Shuchang L, Xingqi G (2015) Overexpression of GhWRKY27a reduces tolerance to drought stress and resistance to Rhizoctonia solani infection in transgenic Nicotiana benthamiana. Front Physiol 6:265. https://doi.org/10.3389/fphys.2015.00265
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685. https://doi.org/10.1111/j.1365-313X.2009.04092.x
Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim J-M, Seki M, Todaka D (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286:321–332. https://doi.org/10.1007/s00438-011-0647-7
Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Biotechnol 21:133–139. https://doi.org/10.1016/j.pbi.2014.07.009
Zegada-Lizarazu W, Monti A (2019) Deep root growth, ABA adjustments and root water uptake response to soil water deficit in giant reed. Ann Bot 124:605–616. https://doi.org/10.1093/aob/mcz001
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60(13):3781–3796. https://doi.org/10.1093/jxb/erp214
Zhang N, Lariviere A, Tonsor SJ, Traw MB (2014) Constitutive camalexin production and environmental stress response variation in Arabidopsis populations from the Iberian Peninsula. Plant Sci 225:77–85. https://doi.org/10.1016/j.plantsci.2014.05.020
Zhang F, Zhou Y, Zhang M, Luo X, Xie J (2017) Effects of drought stress on global gene expression profile in leaf and root samples of Dongxiang wild rice (Oryza rufipogon). Biosci Rep 37(3):1–11. https://doi.org/10.1042/BSR20160509
Zhang DF, Zeng TR, Liu XY, Gao CX, Li YX, Li CH, Song YC, Shi YS, Wang TY, Yu LI (2019) Transcriptomic profiling of sorghum leaves and roots responsive to drought stress at the seedling stage. J Integr Agri 18(9):1980–1995. https://doi.org/10.1016/S2095-3119(18)62119-7
Zhang Y, Li Y, Hassan MJ, Li Z, Peng Y (2020b) Indole-3-acetic acid improves drought tolerance of white clover via activating auxin, abscisic acid and jasmonic acid related genes and inhibiting senescence genes. BMC Plant Biol 20:1–12. https://doi.org/10.1186/s12870-020-02354-y
Zhang Y, Li Y, Hassan MJ, Li Z, Peng Y (2020a) Indole-3-acetic acid improves drought tolerance of white clover via activating auxin, abscisic acid and jasmonic acid related genes and inhibiting senescence genes. BMC Plant Biol 20(1):1–12. https://doi.org/10.1186/s12870-020-02354-y
Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot 66:4863–4871. https://doi.org/10.1093/jxb/erv172
Acknowledgements
The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for granting a master’s scholarship to DRM and a doctoral scholarship to JMK and DAB, and the Embrapa Soybean and Arthur Bernardes Foundation for granting a postdoctoral fellowship to MDCM.
Funding
This research was funded by Embrapa (Brazilian Agricultural Research Corporation), CNPq (National Council for Scientific and Technological Development), and CAPES (Coordination for the Improvement of Higher Education Personnel).
Author information
Authors and Affiliations
Contributions
MDCM conceived and designed the study, performed data analysis and interpretation, and wrote the manuscript. RFP also conceived and designed the study, performed data analysis and results compilation, reviewed the manuscript, and provided scientific editing and language proofreading. EGB reviewed the manuscript and provided scientific editing and language proofreading. DAB, DRM, and SRRM were involved in the experiments and collecting of biological material in a greenhouse. LMMH and ALN are the principal researchers in the project and reviewed the final version of the manuscript. All authors have read and approved the final version of the article.
Corresponding author
Ethics declarations
Ethical Approval and Consent to Participate
Not applicable.
Consent for Publication
All authors gave their consent for the publication of the research results.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Molinari, M.D.C., Fuganti-Pagliarini, R., de Amorim Barbosa, D. et al. Comparative ABA-Responsive Transcriptome in Soybean Cultivars Submitted to Different Levels of Drought. Plant Mol Biol Rep 41, 260–276 (2023). https://doi.org/10.1007/s11105-022-01364-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-022-01364-4