Abstract
Main conclusion
HDA704 enhances drought and salt tolerance via stomata-regulated mechanism. HDA704 negatively regulates stomatal aperture and density, repressing the transcription of DST and ABIL2 by histone deacetylation modification.
Abstract
Drought and salinity can damage crop growth and reduce yield. Stomata play an important role in abiotic stress tolerance. In this study on rice, we identified the RPD3/HDA1-type histone deacetylase HDA704 as a positive regulatory factor in drought and salt tolerance. HDA704 was induced by drought and salt stresses. Overexpression of HDA704 in transgenic rice promoted stomatal closure, decreased the number of stomata and slowed down the rate of water loss, consequently resulting in increased drought and salt tolerance. By contrast, knockdown of HDA704 in transgenic rice decreased stomatal closure and accelerated the rate of water loss, leading to decrease drought and salt tolerance. We detected the transcript expression of DST (Drought and Salt Tolerance) and ABIL2 (Abscisic Acid-insensitive Like2), which positively regulate stomatal aperture and density in rice. Our results showed that HDA704 directly binds to DST and ABIL2, repressing their expression via histone deacetylation modification. Collectively, these findings reveal that HDA704 positively regulates drought and salt tolerance by repressing the expression of DST and ABIL2. Our findings provide a new insight into the molecular mechanisms of stomata-regulated abiotic stress tolerance of plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABIL2:
-
Abscisic acid-insensitive like2
- CFP:
-
Cyan fluorescent protein
- DST:
-
Drought and salt tolerance
- EGFP:
-
Enhanced green fluorescent protein.
- HDAC:
-
Histone deacetylase
References
Alinsug MV, Yu CW, Wu KQ (2009) Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol 9:37. https://doi.org/10.1186/1471-2229-9-37
Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447(7143):407–412. https://doi.org/10.1038/nature05915
Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev 14(9):1119–1131. https://doi.org/10.1101/gad.14.9.1119
Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304(5676):1494–1497. https://doi.org/10.1126/science.1096014
Brock AK, Willmann R, Kolb D, Grefen L, Lajunen HM, Bethke G, Lee J, Nurnberger T, Gust AA (2010) The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol 153(3):1098–1111. https://doi.org/10.1104/pp.110.156109
Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13(1):90–95. https://doi.org/10.1016/j.pbi.2009.08.005
Chen LT, Luo M, Wang YY, Wu KQ (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61(12):3345–3353. https://doi.org/10.1093/jxb/erq154
Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2015) DCA1 acts as a transcriptional co-activator of DST and contributes to drought and salt tolerance in rice. PLoS Genet 11(10):e1005617. https://doi.org/10.1371/journal.pgen.1005617
Ding B, Bellizzi MD, Ning YS, Meyers BC, Wang GL (2012) HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24(9):3783–3794. https://doi.org/10.1105/tpc.112.101972
Fu WQ, Wu KQ, Duan J (2007) Sequence and expression analysis of histone deacetylases in rice. Biochem Biophys Res Comm 356(4):843–850. https://doi.org/10.1016/j.bbrc.2007.03.010
Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462(7273):660–664. https://doi.org/10.1038/nature08599
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106(50):21425–21430. https://doi.org/10.1073/pnas.0912021106
Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2(3):213–218. https://doi.org/10.1038/nmeth0305-213
Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11(10):1897–1909. https://doi.org/10.1105/tpc.11.10.1897
Gu DC, Chen CY, Zhao ML, Zhao LM, Duan XW, Duan J, Wu KQ, Liu XC (2017) Identification of HDA15-PIF1 as a key repression module directing the transcriptional network of seed germination in the dark. Nucleic Acids Res 45(12):7137–7150. https://doi.org/10.1093/nar/gkx283
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424(6951):901–908. https://doi.org/10.1038/nature01843
Huang LM, Sun QW, Qin FJ, Li C, Zhao Y, Zhou DX (2007) Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144(3):1508–1519. https://doi.org/10.1104/pp.107.099473
Huang XY, Chao DY, Gao JP, Shi MZ, Zhu M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23(15):1805–1817. https://doi.org/10.1101/gad.1812409
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions – beta-glucuronidase as a sensitive and versatile gene fusion marker in higher-plants. EMBO J 6(13):3901–3907. https://doi.org/10.1002/j.1460-2075.1987.tb02730.x
Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20(7):1775–1785. https://doi.org/10.1105/tpc.108.060848
Kim TH, Bohmer M, Hum H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network, advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591. https://doi.org/10.1146/annurev-arplant-042809-112226
Kollist H, Nuhkat M, Roelfsema MR (2014) Closing gaps: linking elements that control stomatal movement. New Phytol 203(1):44–62. https://doi.org/10.1111/nph.12832
Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic-acid insensitive mutants of Arabidopsis thaliana. Physiol Plant 61(3):377–383. https://doi.org/10.1111/j.1399-3054.1984.tb06343.x
Lampard GR, MacAlister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322(5904):1113–1116. https://doi.org/10.1126/science.1162263
Larue HC, Zhang SQ (2019) SCREAM in the making of stomata. Nature Plants 5(7):648–649. https://doi.org/10.1038/s41477-019-0460-6
Lee HG, Seo PJ (2019) MYB96 recruits the HDA15 protein to suppress negative regulators of ABA signaling in Arabidopsis. Nat Commun 10:1713. https://doi.org/10.1038/s41467-019-09417-1
Li CX, Shen HY, Wang T, Wang XL (2015) ABA regulates subcellular redistribution of OsABI-LIKE2, a negative regulator in ABA signaling, to control root architecture and drought resistance in Oryza sativa. Plant Cell Physiol 56(12):2396–2408. https://doi.org/10.1093/pcp/pcv154
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. https://doi.org/10.1042/bst0110591
Luo M, Wang YY, Liu XC, Yang SG, Lu Q, Cui YH, Wu KQ (2012) HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot 63(8):3297–3306. https://doi.org/10.1093/jxb/ers059
MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445(7127):537–540. https://doi.org/10.1038/nature05491
Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25(3):295–303. https://doi.org/10.1046/j.1365-313x.2001.00965.x
Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62(2):316–329. https://doi.org/10.1111/j.1365-313X.2010.04146.x
Saez A, Apostolova N, Gonzalez GM, Gonzalez GMP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signaling. Plant J 37(3):354–369. https://doi.org/10.1046/j.1365-313X.2003.01966.x
Schroeder JI, Allen GJ, Hugouvieux V (2001a) Guard cell signal transduction. Annu Rev Plant Biol 52:627–658. https://doi.org/10.1146/annurev.arplant.52.1.627
Schroeder JI, Kwak JM, Allen GJ (2001b) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410(6826):327–330. https://doi.org/10.1038/35066500
Sridha S, Wu KQ (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46(1):124–133. https://doi.org/10.1111/j.1365-313X.2006.02678.x
Tahtiharju S, Palva T (2001) Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J 26(4):461–470. https://doi.org/10.1046/j.1365-313X.2001.2641048.x
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi SK, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106(41):17588–17593. https://doi.org/10.1073/pnas.0907095106
Xie KB, Yang YN (2013) RNA-guided genome editing in plants using a CRISPR–Cas system. Mol Plant 6(6):1975–1983. https://doi.org/10.1093/mp/sst119
Xue WY, Xing YZ, Weng XY, Zhao Y, Tang WJ, Wang L, Zhou HJ, Yu SB, Xu CG, Li XH, Zhang QF (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40(6):761–767. https://doi.org/10.1038/ng.143
Zhang XQ, Wei PC, Xiong YM, Yang Y, Chen J, Wang XC (2011) Overexpression of the -expansin gene AtEXPA1 accelerates stomatal opening by decreasing the volumetric elastic modulus. Plant Cell Rep 30(1):27–36. https://doi.org/10.1007/s00299-010-0937-2
Zhao JH, Zhang JX, Zhang W, Wu KL, Zheng F, Tian LN, Liu XC, Duan J (2015) Expression and functional analysis of the plant-specific histone deacetylase HDT701 in rice. Front Plant Sci 5:764. https://doi.org/10.3389/fpls.2014.00764
Zhao JH, Li MZ, Gu DC, Liu XC, Zhang JX, Wu KL, Zhang XH, Teixeira SJA, Duan J (2016) Involvement of rice histone deacetylase HDA705 in seed germination and in response to ABA and abiotic stresses. Biochem Biophys Res Comm 470(2):439–444. https://doi.org/10.1016/j.bbrc.2016.01.016
Zhong XC, Zhang H, Zhao Y, Sun QW, Hu YF, Peng H, Zhou DX (2013) The rice NAD(+)-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS ONE 8(6):e66807. https://doi.org/10.1371/journal.pone.0066807
Zhu JH, Gong ZZ, Zhang CQ, 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 14(12):3009–3028. https://doi.org/10.1105/tpc.006981
Funding
This work was supported by the National Natural Science Foundation of China (Grant No. 31901521), the Natural Science Foundation of HuBei Province (Grant No. 2019CFB134), the China Postdoctoral Science Foundation Funded Project (Grant No. 216535) and the National Natural Science Foundation of China (U2004141).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data availability
All data generated or analysed during this study is included in this published article and its supplementary information files.
Additional information
Communicated by Dorothea Bartels.
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
Zhao, J., Zhang, W., da Silva, J.A.T. et al. Rice histone deacetylase HDA704 positively regulates drought and salt tolerance by controlling stomatal aperture and density. Planta 254, 79 (2021). https://doi.org/10.1007/s00425-021-03729-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03729-7