Abstract
Sweet sorghum is an annual C4 crop that has high salt tolerance. However, the role of hormones in salt tolerance of sweet sorghum remains unelucidated. In the present study, growth parameters, endogenous hormone concentrations, and transcriptomes of leaves and roots of two inbred lines of sweet sorghum (salt-tolerant M-81E and salt-sensitive Roma) were analyzed under 0 or 150 mM NaCl in order to elucidate hormonal regulation for salt tolerance in sweet sorghum. We found that salt stress inhibited the growth of both genotypes. The concentration of abscisic acid (ABA) changed more significantly in M-81E leaves, and concentration of jasmonate (JA) changed more significantly in Roma roots. While, the concentration of indole-3-acetic acid (IAA) increased in both genotypes, particularly in the leaves. We identified 17 and 15 differentially expressed genes in M-81E between control plants and those subjected to salt stress annotated into pathways of hormone biosynthesis and hormone signal transduction, respectively. In Roma, 16 and 34 differentially expressed genes annotated into pathways of hormone biosynthesis and hormone signal transduction were identified, respectively. Hormone biosynthesis, and signal transduction, may play an important role in regulating the growth and development of sweet sorghum under salt stress. In salt-tolerant inbred line M-81E, ABA may play a key role in salt stress response. In salt-sensitive inbred line Roma, JA may act as the key hormone in response to salt stress. These revealed that hormones are involved in the response of sweet sorghum to salt stress. Furthermore, in different inbred lines, different hormones might play significant roles in regulating the growth and development of sweet sorghum through different regulation pathways.
Similar content being viewed by others
References
Almodares A, Hadi M (2009) Production of bioethanol from sweet sorghum: a review. Afr J Agric Res 4:772–780
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106
Casaretto J, Ho THD (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15(1):271–284
Castillo MC, León J (2004) Gene-specific involvement of β-oxidation in wound-activated responses in Arabidopsis. Plant Physiol 135(1):85–94
Chai YY, Jiang CD, Shi L, Shi TS, Gu WB (2010) Effects of exogenous spermine on sweet sorghum during germination under salinity. Biol Plant 54(1):145–148
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):343–353
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448(7154):666–671
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217(Pt 1):67–75
Dai LY, Zhang LJ, Jiang SJ, Yin KD (2014) Saline and alkaline stress genotypic tolerance in sweet sorghum is linked to sodium distribution. Acta Agric Scand Sect B Soil Plant Sci 64(6):471–481
Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4(397):397
Fonseca S, Chico JM, Solano R, Lohmann JU, Nemhauser J (2009) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12(5):539–547
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62(8):2431–2452
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N et al (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50(50):2123–2132
Gamalero, E., and Glick, B.R. (2012). Ethylene and abiotic stress tolerance in plants
Guóth A, Tari I, Gallé Á, Csiszár J, Pécsváradi A, Cseuz L et al (2009) Comparison of the drought stress responses of tolerant and sensitive wheat cultivars during grain filling: changes in flag leaf photosynthetic activity, ABA levels, and grain yield. J Plant Growth Regul 28(2):167–176
Ha S, Vankova R, Yamaguchishinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17(3):172–179
He T, Cramer GR (1996) Abscisic acid concentrations are correlated with leaf area reductions in two salt-stressed rapid-cycling Brassica species. Plant Soil 179(1):25–33
Hua W, Ye H, Yao R, Tao Z, Xiong L (2015) OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Sci 232:1
Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37(3):422–429
Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T et al (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J Cell Mol Biol 27(4):325–333
Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011a) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 32(5):557–564
Javid MG, Sorooshzadeh A, Allahdadi I, Moradi F (2011b) Effects of the exogenous application of auxin and cytokinin on carbohydrate accumulation in grains of rice under salt stress. Plant Growth Regul 65(2):305–313
Jiyoung Y, Hamayun M, Sukyung L, Injung L (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12(2):63–68
Jung JH, Park CM (2011) Auxin modulation of salt stress signaling in Arabidopsis seed germination. Plant Signal Behav 6(8):1198–1200
Küpper FC, Gaquerel E, Cosse A, Adas F, Peters AF, Müller DG et al (2009) Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant Cell Physiol 50(4):789–800
Kakimoto T (2003) Biosynthesis of cytokinins. J Plant Res 116(3):233–239
Kang DJ, Seo YJ, Lee JD, Ishii R, Kim U, Shin DH et al (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars. J Agron Crop Sci 191(4):273–282
Kannangara T, Seetharama N, Durley RC, Simpson GM (1983) Drought resistance of Sorghum bicolor. 6. Changes in endogenous growth regulators of plants grown across an irrigation gradient. Can J Plant Sci 63(1):147–155
Kefu Z, Munns R, King R (1991) Abscisic acid levels in NaCl-treated barley, cotton and saltbush. Funct Plant Biol 18(1):17–24
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T et al (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J Cell Mol Biol 44(6):939–949
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T et al (2006) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(6):939–949
Koo AJ, Chung HS, Kobayashi Y, Howe GA (2006) Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. J Biol Chem 281(44):33511–33520
Koo AJK, Gao X, Daniel Jones A, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J Cell Mol Biol 59(6):974–986
Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22(4):289–297
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T et al (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23(7):1647–1656
Lackman P, Gonzálezguzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T et al (2011) Jasmonate signaling involves the abscisic acid receptor pyl4 to regulate metabolic reprogramming in arabidopsis and tobacco. Proc Natl Acad Sci 108(14):5891
Lee M, Jung JH, Han DY, Seo PJ, Park WJ, Park CM (2012) Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis. Planta 235(5):923–938
Li C, Liu G, Lee GI, Vrebalov J, Giovannoni JJ, Howe GA (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17(3):971–986
Luo M, Liu JH, Mohapatra S, Hill RD, Mohapatra SS (1992) Characterization of a gene family encoding abscisic acid- and environmental stress-inducible proteins of alfalfa. J Biol Chem 267(22):15367–15374
Ma Y, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068
Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259
Nakashima K (2013) ABA signaling in stress. Plant Cell Rep 32(7):959–970
Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S et al (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50(7):1345–1363
Ng LM, Melcher K, Teh BT, Xu HE (2014) Abscisic acid perception and signaling: structural mechanisms and applications. Acta Pharmacol Sin 35(5):567–584
Nguyen KH, Ha CV, Nishiyama R, Watanabe Y, Leyva-González MA, Fujita Y, et al (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci 113(11):3090–3095
Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC et al (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61(2):290–299
Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, Seki M et al (2012) Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS One 7(2):e32124–e32124
Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T et al (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(6):2169–2183
Oliveira ABD, Alencar NLM, Prisco JT, Gomes-Filho E (2011) Accumulation of organic and inorganic solutes in NaCl-stressed sorghum seedlings from aged and primed seeds. Sci Agric 68(6):632–637
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324(5930):1068–1071
Pedranzani H, Racagni G, Alemano S, Miersch O (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41(2):149–158
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14(3):290
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(2):544–551
Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104(1):202–208
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15(7):395
Ruan C-J, da Silva JAT, Mopper S, Qin P, Lutts S (2010) Halophyte improvement for a salinized world. Crit Rev Plant Sci 29(6):329–359. doi:https://doi.org/10.1080/07352689.2010.524517
Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. J Plant Biol 58(3):147–155
Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7(571)
Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Plant Biol 57(57):431–449
Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M et al (2009a) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462(7273):665–668
Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F et al (2009b) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J Cell Mol Biol 60(4):575–588
Schneider K, Kienow L, Schmelzer E, Colby T, Bartsch M, Miersch O et al (2005) A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J Biol Chem 280(14):13962–13972
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7(1):41–48
Song J, Shi W, Liu R, Xu Y, Sui N, Zhou J et al (2016) The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biol
Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506(2):265–273
Sui N, Yang Z, Liu M, Wang B (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16(1):534
Tani T, Sobajima H, Okada K, Chujo T, Arimura S, Tsutsumi N et al (2008) Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227:517–526
Thines B (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448(7154):661–665
Thompson AJ, Mulholland BJ, Jackson AC, Mckee JMT, Hilton HW, Symonds RC et al (2007) Regulation and manipulation of ABA biosynthesis in roots. Plant Cell Environ 30(1):67–78
To, J.P, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13(2):85–92
Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K (2010) Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal Behav 5(2):148–150
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30(4):410
Wang C, Yang A, Yin H, Zhang J, Wang C, Yin H (2008) Influence of water stress on endogenous hormone contents and cell damage of maize seedlings. J Integr Plant Biol 50(4):427–434
Wang F, Xu YG, Wang S, Shi W, Liu R, Feng G et al (2015a) Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol Biochem 95:41–48
Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166(15):1637–1645
Wang Y, Mopper S, Hasenstein KH (2001) Effects of salinity on endogenous Aba, Iaa, Ja, and Sa in Iris hexagona. J Chem Ecol 27(2):327–342
Wang Y, Shen W, Chan Z, Wu Y (2015b) Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis thaliana. Front Plant Sci 6(8)
Wang Y, Tao X, Tang XM, Xiao L, Sun J, Yan XF et al (2013) Comparative transcriptome analysis of tomato (Solanum lycopersicum) in response to exogenous abscisic acid. BMC Genomics 14(1):841
Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697
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 111(6):1021–1058
Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33(4):510–525
Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20(4):1101–1117
Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37(3):326–339
Yang YM, Xu CN, Wang BM, Jia JZ (2001) Effects of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regul 35(3):233–237
Ye H, Hao D, Ning T, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71(3):291–305
Zörb C, Geilfus CM, Mühling KH, Ludwigmüller J (2013) The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 170(2):220–224
Zahir ZA, Asghar HN, Arshad M (2001) Cytokinin and its precursors for improving growth and yield of rice. Soil Biol Biochem 33(3):405–408
Zeevaart JA (1999) Abscisic acid metabolism and its regulation. New Compr Biochem
Zeevaart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Plant Biol 39(39):439–473
Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y et al (2011) High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc 2011(8):940–949
Zhu D, Cai H, Luo X, Bai X, Deyholos MK, Chen Q et al (2012) Over-expression of a novel JAZ family gene from Glycine soja, increases salt and alkali stress tolerance. Biochem Biophys Res Commun 426(2):273
Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot 66(16):4863
Acknowledgements
We are grateful for the financial support from the NSFC (National Natural Science Research Foundation of China, project no. 31570251), the independent innovation and achievement transformation of special major key technical plans of Shandong Province (2015ZDJS03002) and Natural Science Research Foundation of Shandong Province (ZR2016JL028ZR, 2014CZ002, ZR2013CQ009), the Science and Technology Development Projects of Shandong Province (2014GNC113005), the Opening Foundation of the State Key Laboratory of Crop Biology, China (2015KF01), the Opening Foundation of Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology, and Physiology, and the Program for Scientific research innovation team in colleges and universities of Shandong Province.
Author information
Authors and Affiliations
Contributions
ZY and NS wrote this manuscript; ZY, YW, and XZ performed experiments; ZY and XW collected data and carried out all analyses; BW and NS conceptualized the idea and revised the manuscript.
Corresponding authors
Additional information
Availability of Supporting Data
The reads produced in this study have been deposited in the National Center for Biotechnology Information (NCBI) SRA database with accession number of SRP059052 for leaves and SRX1090369 for roots. Access to the data is available upon http://www.ncbi.nlm.nih.gov/sra/.
Electronic supplementary material
Figure S1
Leaf length and root length of M-81E and Roma treated with different concentrations of NaCl (0 and 150 mM) for 48 h. Values are means ±SD of five replicates. (GIF 19 kb)
Figure S2
KEGG map of the plant hormone signal transduction pathway. (GIF 38 kb)
Table S1
(XLSX 10 kb)
Table S2
(XLSX 14 kb)
Table S3
(XLSX 15 kb)
Rights and permissions
About this article
Cite this article
Yang, Z., Wang, Y., Wei, X. et al. Transcription Profiles of Genes Related to Hormonal Regulations Under Salt Stress in Sweet Sorghum. Plant Mol Biol Rep 35, 586–599 (2017). https://doi.org/10.1007/s11105-017-1047-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-017-1047-x