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The rice OsDIL gene plays a role in drought tolerance at vegetative and reproductive stages

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Abstract

Drought is one of the critical factors limiting reproductive yields of rice and other crops globally. However, little is known about the molecular mechanism underlying reproductive development under drought stress in rice. To explore the potential gene function for improving rice reproductive development under drought, a drought induced gene, Oryza sativa Drought-Induced LTP (OsDIL) encoding a lipid transfer protein, was identified from our microarray data and selected for further study. OsDIL was primarily expressed in the anther and mainly responsive to abiotic stresses, including drought, cold, NaCl, and stress-related plant hormone abscisic acid (ABA). Compared with wild type, the OsDIL-overexpressing transgenic rice plants were more tolerant to drought stress during vegetative development and showed less severe tapetal defects and fewer defective anther sacs when treated with drought at the reproductive stage. The expression levels of the drought-responsive genes RD22, SODA1, bZIP46 and POD, as well as the ABA synthetic gene ZEP1 were up-regulated in the OsDIL-overexpression lines but the ABA degradation gene ABAOX3 was down-regulated. Moreover, overexpression of OsDIL lessened the down-regulation by drought of anther developmental genes (OsC4, CYP704B2 and OsCP1), providing a mechanism supporting pollen fertility under drought. Overexpression of OsDIL significantly enhanced drought resistance in transgenic rice during reproductive development, while showing no phenotypic changes or yield penalty under normal conditions. Therefore, OsDIL is an excellent candidate gene for genetic improvement of crop yield in adaption to unfavorable environments.

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References

  • Audran C, Liotenberg S, Gonneau M, North H, Frey A, Tap-Waksman K, Vartanian N, Marion-Poll A (2001) Localisation and expression of zeaxanthin epoxidase mRNA in Arabidopsis in response to drought stress and during seed development. Aust J Plant Physiol 28:1161–1173

    CAS  Google Scholar 

  • Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472. doi:10.1105/tpc.108.062935

    Article  PubMed  CAS  Google Scholar 

  • Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9:86. doi:10.1186/1471-2164-9-86

    Article  PubMed  Google Scholar 

  • Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183. doi:10.1104/pp.105.069724

    Article  PubMed  CAS  Google Scholar 

  • Canevascini S, Caderas D, Mandel T, Fleming AJ, Dupuis I, Kuhlemeier C (1996) Tissue-specific expression and promoter analysis of the tobacco LTP1 gene. Plant Physiol 112:513–524

    Article  PubMed  CAS  Google Scholar 

  • Carvalho AO, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology: a concise review. Peptides 28:1144–1153

    Article  CAS  Google Scholar 

  • Chae K, Zhang K, Zhang L, Morikis D, Kim ST, Mollet JC, de la Rosa N, Tan K, Lord EM (2007) Two SCA (stigma/style cysteine-rich adhesin) isoforms show structural differences that correlate with their levels of in vitro pollen tube adhesion activity. J Biol Chem 282:33845–33858. doi:10.1074/jbc.M703997200

    Google Scholar 

  • Debono A, Yeats TH, Rose JK, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21:1230–1238. doi:10.1105/tpc.108.064451

    Article  PubMed  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Firon N, Nepi M, Pacini E (2012) Water status and associated processes mark critical stages in pollen development and functioning. Ann Bot 109:1201–1214. doi:10.1093/aob/mcs070

    Article  PubMed  CAS  Google Scholar 

  • García-Olmedo F, Molina A, Segura A, Moreno M (1995) The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol 3:72–74

    Article  PubMed  Google Scholar 

  • Ge X, Chen J, Li N, Lin Y, Sun C, Cao K (2003) Resistance function of rice lipid transfer protein LTP110. J Biochem Mol Biol 36:603–607

    Article  PubMed  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases II purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318

    Article  PubMed  CAS  Google Scholar 

  • He H, Serraj R (2012) Involvement of peduncle elongation, anther dehiscence and spikelet sterility in upland rice response to reproductive-stage drought stress. Environ Exp Bot 75:120–127. doi:10.1016/j.envexpbot.2011.09.004

    Article  Google Scholar 

  • Hihara Y, Hara C, Uchimiya H (1996) Isolation and characterization of two cDNA clones for mRNAs that are abundantly expressed in immature anthers of rice (Oryza sativa L.). Plant Mol Biol 30:1181–1193

    Article  PubMed  CAS  Google Scholar 

  • Hou X, Xie K, Yao J, Qi Z, Xiong L (2009) A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA 106:6410–6415. doi:10.1073/pnas.0901940106

    Article  PubMed  CAS  Google Scholar 

  • Hu L, Tan H, Liang W, Zhang D (2010) The post-meiotic deficicent anther 1 (PDA1) gene is required for post-meiotic anther development in rice. J Genet Genomics 37:37–46. doi:10.1016/s1673-8527(09)60023-0

    Article  PubMed  CAS  Google Scholar 

  • Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515–533. doi:10.1105/tpc.110.074369

    Article  PubMed  CAS  Google Scholar 

  • Iraki NM, Singh N, Bressan RA, Carpita NC (1989) Cell walls of tobacco cells and changes in composition associated with reduced growth upon adaptation to water and saline stress. Plant Physiol 91:48–53

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  PubMed  CAS  Google Scholar 

  • Jung HW, Kim W, Hwang BK (2003) Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ 26:915–928

    Article  PubMed  CAS  Google Scholar 

  • Kader JC (1997) Lipid-transfer proteins: a puzzling family of plant proteins. Trends Plant Sci 2:66–70

    Article  Google Scholar 

  • Koonjul PK, Minhas JS, Nunes C, Sheoran IS, Saini HS (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J Exp Bot 56:179–190. doi:10.1093/jxb/eri018

    PubMed  CAS  Google Scholar 

  • Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656

    Article  PubMed  CAS  Google Scholar 

  • Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121–1123. doi:10.4161/psb.5.9.12562

    Article  PubMed  CAS  Google Scholar 

  • Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014. doi:10.1105/tpc.106.044107

    Article  PubMed  CAS  Google Scholar 

  • Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190. doi:10.1105/tpc.109.070326

    Article  PubMed  CAS  Google Scholar 

  • Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630. doi:10.1104/pp.111.175760

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Suen DF, Huang CY, Kung SY, Huang AH (2012a) The maize tapetum employs diverse mechanisms to synthesize and store proteins and flavonoids and transfer them to the pollen surface. Plant Physiol 158:1548–1561. doi:10.1104/pp.111.189241

    Article  PubMed  CAS  Google Scholar 

  • Li YS, Sun H, Wang ZF, Duan M, Huang SD, Yang J, Huang J, Zhang HS (2012b) A novel nuclear protein phosphatase 2C negatively regulated by ABL1 is involved in abiotic stress and panicle development in rice. Mol Biotechnol. doi:10.1007/s12033-012-9614-8

    Google Scholar 

  • Lokko Y, Anderson JV, Rudd S, Raji A, Horvath D, Mikel MA, Kim R, Liu L, Hernandez A, Dixon AG, Ingelbrecht IL (2007) Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Rep 26:1605–1618. doi:10.1007/s00299-007-0378-8

    Article  PubMed  CAS  Google Scholar 

  • Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403

    Article  PubMed  CAS  Google Scholar 

  • Maldonado-Calderon MT, Sepulveda-Garcia E, Rocha-Sosa M (2012) Characterization of novel F-box proteins in plants induced by biotic and abiotic stress. Plant Sci 185–186:208–217. doi:10.1016/j.plantsci.2011.10.013

    Article  PubMed  Google Scholar 

  • Manavalan LP, Chen X, Clarke J, Salmeron J, Nguyen HT (2012) RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J Exp Bot 63:163–175. doi:10.1093/jxb/err258

    Article  PubMed  CAS  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379. doi:10.1104/pp.109.137554

    Article  PubMed  CAS  Google Scholar 

  • Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48:1319–1330. doi:10.1093/pcp/pcm100

    Article  PubMed  CAS  Google Scholar 

  • Ozawa K (2009) Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). Plant Sci 176:522–527

    Article  CAS  Google Scholar 

  • Qin BX, Tang D, Huang J, Li M, Wu XR, Lu LL, Wang KJ, Yu HX, Chen JM, Gu MH, Cheng ZK (2011) Rice OsGL1-1 is involved in leaf cuticular wax and cuticle membrane. Mol Plant 4:985–995. doi:10.1093/mp/ssr028

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues F, Da Graça J, De Laia M, Nhani-Jr A, Galbiati J, Ferro MIT, Ferro J, Zingaretti S (2011) Sugarcane genes differentially expressed during water deficit. Biol Plant 55:43–53

  • Safařík IVO, Šantrůčková H (1992) Direct determination of total soil carbohydrate content. Plant Soil 143:109–114

    Article  Google Scholar 

  • Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28:419–427. doi:10.1007/s00299-008-0653-3

    Article  PubMed  CAS  Google Scholar 

  • Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, Scholz U, Wobus U, Sreenivasulu N (2011) ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. J Exp Bot 62:2615–2632. doi:10.1093/jxb/erq446

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417. doi:10.1016/s1369-5266(03)00092-x

    Article  PubMed  CAS  Google Scholar 

  • Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3:907–921

    PubMed  CAS  Google Scholar 

  • Talame V, Ozturk NZ, Bohnert HJ, Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot 58:229–240. doi:10.1093/jxb/erl163

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768. doi:10.1104/pp.111.190389

    Article  PubMed  CAS  Google Scholar 

  • Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660

    PubMed  CAS  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    Article  PubMed  CAS  Google Scholar 

  • Walbot V (1988) Preparation of DNA from single rice seedlings. Rice Genet Newsl 5:149–151

    Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  PubMed  CAS  Google Scholar 

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46. doi:10.1007/s00122-007-0538-9

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Zhang L, Fu G, Yang Y, Zhu C, Tao L (2012) Drought-induced proline accumulation is uninvolved with increased nitric oxide, which alleviates drought stress by decreasing transpiration in rice. J Plant Res 125:155–164. doi:10.1007/s10265-011-0417-y

    Article  PubMed  CAS  Google Scholar 

  • Ye N, Zhu G, Liu Y, Li Y, Zhang J (2011) ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant Cell Physiol 52:689–698. doi:10.1093/pcp/pcr028

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, 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. doi:10.1111/j.1365-313X.2009.04092.x

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q (2007) Strategies for developing green super rice. Proc Natl Acad Sci USA 104:16402–16409. doi:10.1073/pnas.0708013104

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Liang W, Yin C, Zong J, Gu F (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379–390. doi:10.1016/j.jgg.2011.08.001

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Li Y, Zhao BC, Ge RC, Shen YZ, Wang G, Huang ZJ (2009) Overexpression of TaSTRG gene improves salt and drought tolerance in rice. J Plant Physiol 166:1660–1671. doi:10.1016/j.jplph.2009.04.015

    Article  PubMed  CAS  Google Scholar 

  • Zhou Z, Dun X, Xia S, Shi D, Qin M, Yi B, Wen J, Shen J, Ma C, Tu J, Fu T (2012) BnMs3 is required for tapetal differentiation and degradation, microspore separation, and pollen-wall biosynthesis in Brassica napus. J Exp Bot 63:2041–2058. doi:10.1093/jxb/err405

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Chen H, Li H, Gao J, Jiang H, Wang C, Guan Y, Yang Z (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277. doi:10.1111/j.1365-313X.2008.03500.x

    Article  PubMed  CAS  Google Scholar 

  • Zhu L, Shi J, Zhao G, Zhang D, Liang W (2013) Post-meiotic deficient anther1 (PDA1) encodes an ABC transporter required for the development of anther cuticle and pollen exine in rice. J Plant Biol 56:59–68. doi:10.1007/s12374-013-0902-z

    Article  CAS  Google Scholar 

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Acknowledgments

This research work was supported by Grants from the Chinese National Transgenics Program (2009ZX08009-071B), the Chinese Ministry of Science and Technology 973 program (2012CB114300), and the Shanghai Key Basic Research Program (12JC1400500) and funds from Fudan University (211 and 985 programs). We sincerely thank Yingxiang Wang for comments on our manuscript. We thank Lingya Yao for providing transgenic seeds of pCAMBIA1301U empty vector and Aiwu Dong for providing the pGEM-RNAi vector.

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  1. State Key Laboratory of Genetic Engineering, Institute of Plant Biology, Center for Evolutionary Biology, School of Life Sciences, Fudan University, 220 Handan Road, Shanghai, 200433, China

    Changkui Guo, Xiaochun Ge & Hong Ma

  2. Institutes of Biomedical Sciences, 138 Yixueyuan Road, Shanghai, 200032, China

    Hong Ma

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  1. Changkui Guo
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Guo, C., Ge, X. & Ma, H. The rice OsDIL gene plays a role in drought tolerance at vegetative and reproductive stages. Plant Mol Biol 82, 239–253 (2013). https://doi.org/10.1007/s11103-013-0057-9

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