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Overexpression of OsDT11, which encodes a novel cysteine-rich peptide, enhances drought tolerance and increases ABA concentration in rice

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Abstract

Short-chain peptides play important roles in plant development and responses to abiotic and biotic stresses. Here, we characterized a gene of unknown function termed OsDT11, which encodes an 88 amino acid short-chain peptide and belongs to the cysteine-rich peptide family. It was found that the expression of OsDT11 can be activated by polyethylene glycol (PEG) treatment. Compared with wild-type lines, the OsDT11-overexpression lines displayed dramatically enhanced tolerance to drought and had reduced water loss, reduced stomatal density, and an increased the concentration of abscisic acid (ABA). The suppression of OsDT11 expression resulted in an increased sensitivity to drought compared to wild-type expression. Several drought-related genes, including genes encoding abscisic acid (ABA) signaling markers, were also strongly induced in the OsDT11-overexpressing lines. Moreover, the expression of OsDT11 was repressed in ABA-insensitive mutant Osbzip23 and Os2H16 RNAi lines. These results suggest that OsDT11-mediated drought tolerance may be dependent on the ABA signaling pathway.

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References

  • Astafieva AA, Rogozhin EA, Andreev YA, Odintsova TI, Kozlov SA, Grishin EV, Egorov TA (2013) A novel cysteine-rich antifungal peptide ToAMP4 from Taraxacum officinale Wigg. flowers. Plant Physiol Biochem 70:93–99. doi:10.1016/j.plaphy.2013.05.022

    Article  CAS  PubMed  Google Scholar 

  • Baron KN, Schroeder DF, Stasolla C (2014) GEm-Related 5 (GER5), an ABA and stress-responsive GRAM domain protein regulating seed development and inflorescence architecture. Plant Sci 223:153–166. doi:10.1016/j.plantsci.2014.03.017

    Article  CAS  PubMed  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SiganlP 3.0. J Mol Biol 340(4):783–795. doi:10.1016/j.jmb.2004.05.028

    Article  PubMed  Google Scholar 

  • Campo S, Peris-Peris C, Montesinos L, Penas G, Messeguer J, San Segundo B (2012) Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection. J Exp Bot 63(2):983–999. doi:10.1093/jxb/err328

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55(3):604–619. doi:10.1093/pcp/pct204

    Article  CAS  PubMed  Google Scholar 

  • Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162(3):1566–1582. doi:10.1104/pp.113.221911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dresselhaus T, Franklin-Tong N (2013) Male–female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6(4):1018–1036. doi:10.1093/mp/sst061

    Article  CAS  PubMed  Google Scholar 

  • Ebrahimpour S, Tabari MA, Youssefi MR, Aghajanzadeh H, Behzadi MY (2013) Synergistic effect of aged garlic extract and naltrexone on improving immune responses to experimentally induced fibrosarcoma tumor in BALB/c mice. Pharmacogn Res 5(3):189–194. doi:10.4103/0974-8490.112426

    Article  Google Scholar 

  • Farkas A, Maróti G, DurgÓ§ H, Györgypál Z, Lima RM, Medzihradszky KF, Kereszt A, Mergaert P, Kondorosi É (2014) Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc Natl Acad Sci USA 111(14):5183–5188. doi:10.1073/pnas.1404169111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan D, Jiang H, Zhang J, Zhao Y, Zhu S, Cheng B (2011) Genome-wide analysis of BURP domain-containing genes in maize and sorghum. Mol Biol Rep 38(7):4553–4563. doi:10.1007/s11033-010-0587-z

    Article  CAS  PubMed  Google Scholar 

  • Ge X, Chang F, Ma H (2010) Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol 20(22):988–997. doi:10.1016/j.cub.2010.09.040

    Article  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175(4023):776–777. doi:10.1126/science.175.4023.776

    Article  CAS  PubMed  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6(2):271–282. doi:10.1046/j.1365-313X.1994.6020271.x

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52(12):2136–2146. doi:10.1093/pcp/pcr143

    Article  CAS  PubMed  Google Scholar 

  • Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, Mizuno S, Masuda Y, Irie K, Tanaka Y, Takada S, Kakimoto T, Sakagami Y (2010) Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol 51(1):1–8. doi:10.1093/pcp/pcp180

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Hwang IS, Choi HW, Hwang BK (2008) Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol 148(2):1004–1020. doi:10.1104/pp.108.123836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Kong L, Zhou W, Zhang X, Wei S, Ding X, Chu Z (2013a) Overexpression of Os2H16 enhances resistance to phytopathogens and tolerance to drought stress in rice. Plant Cell Tissue Org 115(3):429–441. doi:10.1007/s11240-013-0374-3

  • Li XM, Sang YL, Zhao XY, Zhang XS (2013b) High-throughput sequencing of small RNAs from pollen and silk and characterization of miRNAs as candidate factors involved in pollen-silk interactions in maize. PLoS One 8(8):e0072852. doi:10.1371/journal.pone.0072852

  • Liu C, Wu Y, Wang X (2012) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235(6):1157–1169. doi:10.1007/s00425-011-1564-z

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9(9):e1003790. doi:10.1371/journal.pgen.1003790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TD, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187(2):343–354. doi:10.1111/j.1469-8137.2010.03291.x

    Article  PubMed  Google Scholar 

  • Maróti G, Kondorosi E (2014) Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? Front Microbiol 5:326. doi:10.3389/fmicb.2014.00326

    PubMed  PubMed Central  Google Scholar 

  • Maróti G, Downie JA, Kondorosi É (2015) Plant cysteine-rich peptides that inhibit pathogen growth and control rhizobial differentiation in legume nodules. Curr Opin Plant Biol 26:57–63. doi:10.1016/j.pbi.2015.05.031

    Article  PubMed  Google Scholar 

  • Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell–cell communication in plant reproduction and development. J Exp Bot 62(5):1677–1686. doi:10.1093/jxb/err002

    Article  CAS  PubMed  Google Scholar 

  • Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, Matsukura S, Takasaki H, Sakurai T, Yamamoto YY, Yoshiwara K, Kojima M, Sakakibara H, Shinozaki K, Yamaguchi-Shinozaki K (2012) Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19(1):37–49. doi:10.1093/dnares/dsr040

    Article  CAS  PubMed  Google Scholar 

  • Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S (2014) Abscisic acid and abiotic stress tolerance - different tiers of regulation. J Plant Physiol 171(7):486–496. doi:10.1016/j.jplph.2013.12.007

    Article  CAS  PubMed  Google Scholar 

  • Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R (2011) Nitric oxide in legume-rhizobium symbiosis. Plant Sci 181(5):573–581. doi:10.1016/j.plantsci.2011.04.007

    Article  CAS  PubMed  Google Scholar 

  • Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18(5):259–266. doi:10.1016/j.tplants.2012.11.002

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32(7):959–970. doi:10.1007/s00299-013-1418-1

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1):88–95. doi:10.1104/pp.108.129791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):97–103. doi:10.1016/j.bbagrm.2011.10.005

    Article  CAS  PubMed  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, 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. doi:10.1046/j.1365-313X.2003.01708.x

    Article  CAS  PubMed  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253(5022):895–897. doi:10.1126/science.253.5022.895

    Article  CAS  PubMed  Google Scholar 

  • Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate- dependent signaling. Mol Plant Microbe Interact 20(5):492–499. doi:10.1094/MPMI-20-5-0492

    Article  CAS  PubMed  Google Scholar 

  • Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4):1755–1767. doi:10.1104/pp.103.025742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rombauts S, Dehais P, Montagu MV, Rouze P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27(1):295–296. doi:10.1093/nar/27.1.295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330. doi:10.1038/35066500

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Chen C-N, Brands A, Pan S-M, Ho T-HD (2001) The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Mol Biol 45(3):327–340. doi:10.1023/A:1006460231978

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3(3):217–223. doi:10.1016/S1369-5266(00)80068-0

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Silverstein KA, Moskal WA, Wu HC, Underwood BA, Graham MA, Town CD, VandenBosch KA (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been underpredicted in plants. Plant J 51(2):262–280. doi:10.1111/j.1365-313X.2007.03136.x

    Article  CAS  PubMed  Google Scholar 

  • Srivastava R, Liu JX, Guo H, Yin Y, Howell SH (2009) Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J 59(6):930–939. doi:10.1111/j.1365-313X.2009.03926.x

    Article  CAS  PubMed  Google Scholar 

  • Swamy BP, Kumar A (2013) Genomics-based precision breeding approaches to improve drought tolerance in rice. Biotechnol Adv 31(8):1308–1318. doi:10.1016/j.biotechadv.2013.05.004

    Article  CAS  PubMed  Google Scholar 

  • Tabata R, Sawa S (2014) Maturation processes and structures of small secreted peptides in plants. Front. Plant Sci 5:311. doi:10.3389/fpls.2014.00311

    Google Scholar 

  • Tiricz H, Szucs A, Farkas A, Pap B, Lima RM, Maróti G, Kondorosi É, Kereszt A (2013) Antimicrobial nodule-specific cysteine-rich peptides induce membrane depolarization-associated changes in the transcriptome of Sinorhizobium meliloti. Appl Environ Microbiol 79 (21):6737–6746. doi:10.1128/AEM.01791-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma SS, Yajima WR, Rahman MH, Shah S, Liu JJ, Ekramoddoullah AK, Kav NN (2012) A cysteine-rich antimicrobial peptide from Pinus monticola (PmAMP1) confers resistance to multiple fungal pathogens in canola (Brassica napus). Plant Mol Biol 79(1–2):61–74. doi:10.1007/s11103-012-9895-0

    Article  CAS  PubMed  Google Scholar 

  • Wei Q, Hu P, Kuai BK (2012) Ectopic expression of an Ammopiptanthus mongolicus H+-pyrophosphatase gene enhances drought and salt tolerance in Arabidopsis. Plant Cell Tissue Org 110(3):359–369. doi:10.1007/s11240-012-0157-2

    Article  CAS  Google Scholar 

  • Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenfuhrer J, von Mering C, Grossniklaus U (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20(6):506–512. doi:10.1016/j.cub.2010.01.051

    Article  CAS  PubMed  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148(4):1938–1952. doi:10.1104/pp.108.128199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu ZY, Kim SY, Hyeon do Y, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC, Hwang D, Hwang I (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25(11):4708–4724. doi:10.1105/tpc.113.119099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi N, Kim YS, Jeong MH, Oh SJ, Jeong JS, Park SH, Jung H, Choi YD, Kim JK (2010) Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232(3):743–754. doi:10.1007/s00425-010-1212-z

    Article  CAS  PubMed  Google Scholar 

  • Zhou P, Silverstein KA, Gao L, Walton JD, Nallu S, Guhlin J, Young ND (2013) Detecting small plant peptides using SPADA (small peptide alignment discovery application). BMC Bioinfo 14:335–350. doi:10.1186/1471-2105-14-335

    Article  Google Scholar 

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Acknowledgments

We are grateful to Prof. Lizhong Xiong (Huazhong Agricultural University, Wuhan, China) for providing the rice seeds of the osbzip23 T-DNA insertion line and to Dr. Yang Li (Key Laboratory of Plant Stress Biology, Henan University, Kaifeng, China) for helping with the ESEM assay. This work was funded by the Shandong Modern Agricultural Technology & Industry System (SDAIT-17-06), the National Program of Transgenic Variety Development of China (2013ZX08009-004, 2014ZX08001-002), the Shandong Provincial Natural Science Foundation of PR China (ZR2014CQ044), and the Taishan Scholar Program of Shandong Province.

Author contributions

Z.C., X.D. and X.L. designed the experiments. H.H., M.C., W.Y. and N.L. performed the experiments. X.L., X.D. and L.L. analyzed data. X.L. and Z.C. wrote the article.

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Correspondence to Zhaohui Chu.

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Xiaoming Li and Huipei Han have contributed equally to this work.

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Li, X., Han, H., Chen, M. et al. Overexpression of OsDT11, which encodes a novel cysteine-rich peptide, enhances drought tolerance and increases ABA concentration in rice. Plant Mol Biol 93, 21–34 (2017). https://doi.org/10.1007/s11103-016-0544-x

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