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Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice

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Abstract

Plant responses to abiotic stresses are coordinated by arrays of growth and developmental programs. Phytohormones such as abscisic acid (ABA) and indole-3-acetic acid (IAA) play critical roles in developmental progresses and environmental responses through complex signalling networks. However, crosstalk between the two hormones at the biosynthesis level remains largely unknown. Here, we report that carotenoid-deficient mutants (phs1, phs2, phs3-1, phs4, and PDS-RNAi transgenic rice) were impaired in the biosynthesis of ABA and IAA. Under drought conditions, phs3-1 and PDS-RNAi transgenic rice showed larger stomata aperture and earlier wilting compared to the wild type at both seedling and panicle developmental stage. Interestingly, these carotenoid-deficient lines showed increased cold resistance, which was likely due to the combined effects of reduced IAA content, alleviated oxidative damage and decreased membrane penetrability. Furthermore, we found that IAA content was significantly declined in rice treated with fluridone (a carotenoid and ABA biosynthesis inhibitor), and expression of auxin synthesis and metabolism-related genes were altered in the fluridone-treated rice similar to that in the carotenoid-deficient mutants. In addition, exogenous IAA, but not ABA, could restore the dwarf phenotype of phs3-1 and PDS-RNAi transgenic rice. These results support a crosstalk between ABA and IAA at the biosynthesis level, and this crosstalk is involved in development and differentially affects drought and cold tolerance in rice.

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References

  • Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34:67–75

    Article  PubMed  CAS  Google Scholar 

  • Cao H, Zhang J, Xu J, Ye J, Yun Z, Xu Q, Xu J, Deng X (2012) Comprehending crystalline beta-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus. J Exp Bot 63:4403–4417

    Article  PubMed  CAS  Google Scholar 

  • Cheng Q (2006) Structural diversity and functional novelty of new carotenoid biosynthesis genes. J Ind Microbiol Biotechnol 33:552–559

    Article  PubMed  CAS  Google Scholar 

  • Cheng NH, Liu JZ, Liu X, Wu Q, Thompson SM, Lin J, Chang J, Whitham SA, Park S, Cohen JD, Hirschi KD (2011) Arabidopsis monothiol glutaredoxin, AtGRXS17, is critical for temperature-dependent postembryonic growth and development via modulating auxin response. J Biol Chem 286:20398–20406

    Article  PubMed  CAS  Google Scholar 

  • Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (2008) Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240

    Article  PubMed  CAS  Google Scholar 

  • Domingo C, Andres F, Tharreau D, Iglesias DJ, Talon M (2009) Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant Microbe Interact 22:201–210

    Article  PubMed  CAS  Google Scholar 

  • Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318

    Article  PubMed  CAS  Google Scholar 

  • Du H, Wu N, Fu J, Wang S, Li X, Xiao J, Xiong L (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J Exp Bot 63:6467–6480

    Article  PubMed  CAS  Google Scholar 

  • Fang J, Chai C, Qian Q, Li C, Tang J, Sun L, Huang Z, Guo X, Sun C, Liu M, Zhang Y, Lu Q, Wang Y, Lu C, Han B, Chen F, Cheng Z, Chu C (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J 54:177–189

    Article  PubMed  CAS  Google Scholar 

  • Finch Savage WE, Leubner Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  PubMed  CAS  Google Scholar 

  • Fu J, Liu H, Li Y, Yu H, Li X, Xiao J, Wang S (2010) Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155:589–602

    Article  PubMed  Google Scholar 

  • Fukaki H, Fujisawa H, Tasaka M (1996) Gravitropic response of inflorescence stems in Arabidopsis thaliana. Plant Physiol 110:933–943

    Article  PubMed  CAS  Google Scholar 

  • Garbers C, DeLong A, Deruere J, Bernasconi P, Soll D (1996) A mutation in protein phosphatase 2A regulatory subunit a affects auxin transport in Arabidopsis. EMBO J 15:2115–2124

    PubMed  CAS  Google Scholar 

  • Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Tyagi AK, Khurana JP (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genomics 6:36–46

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 579:1243–1248

    Article  PubMed  CAS  Google Scholar 

  • Joshi-Saha A, Valon C, Leung J (2011) Abscisic acid signal off the STARTing Block. Mol Plant 4:562–580

    Article  PubMed  CAS  Google Scholar 

  • Kim JI, Baek D, Park HC, Chun HJ, Oh DH, Lee MK, Cha JY, Kim WY, Kim MC, Chung WS, Bohnert HJ, Lee SY, Bressan RA, Lee SW, Yun DJ (2013) Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol Plant 6:337–349

    Google Scholar 

  • Kwak JM, Moon JH, Murata Y, Kuchitsu K, Leonhardt N, DeLong A, Schroeder JI (2002) Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 14:2849–2861

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Mano Y, Nemoto K, Suzuki M, Seki H, Fujii I, Muranaka T (2010) The AMI1 gene family: indole-3-acetamide hydrolase functions in auxin biosynthesis in plants. J Exp Bot 61:25–32

    Article  PubMed  CAS  Google Scholar 

  • Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi K, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci U S A 108:18512–18517

    Article  PubMed  CAS  Google Scholar 

  • Nadella V, Shipp MJ, Muday GK, Wyatt SE (2006) Evidence for altered polar and lateral auxin transport in the gravity persistent signal (gps) mutants of Arabidopsis. Plant, Cell Environ 29:682–690

    Article  CAS  Google Scholar 

  • Nambara E, Marion Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  PubMed  CAS  Google Scholar 

  • Park WJ, Kriechbaumer V, Moller A, Piotrowski M, Meeley RB, Gierl A, Glawischnig E (2003) The Nitrilase ZmNIT2 converts indole-3-acetonitrile to indole-3-acetic acid. Plant Physiol 133:794–802

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  PubMed  CAS  Google Scholar 

  • Schaub P, Al Babili S, Drake R, Beyer P (2005) Why is golden rice golden (yellow) instead of red? Plant Physiol 138:441–450

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151:275–289

    Article  PubMed  CAS  Google Scholar 

  • Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21:3823–3838

    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

    Article  PubMed  CAS  Google Scholar 

  • Shobbar ZS, Oane R, Gamuyao R, De Palma J, Malboobi MA, Karimzadeh G, Javaran MJ, Bennett J (2008) Abscisic acid regulates gene expression in cortical fiber cells and silica cells of rice shoots. New Phytol 178:68–79

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Kao CY, Cocciolone S, McCarty DR (2001) Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J 28:409–418

    Google Scholar 

  • 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 166:1637–1645

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Hua D, He J, Duan Y, Chen Z, Hong X, Gong Z (2011) Auxin Response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7:e1002172

    Article  PubMed  CAS  Google Scholar 

  • Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A 108:18518–18523

    Article  PubMed  CAS  Google Scholar 

  • Wyatt SE, Rashotte AM, Shipp MJ, Robertson D, Muday GK (2002) Mutations in the gravity persistence signal loci in Arabidopsis disrupt the perception and/or signal transduction of gravitropic stimuli. Plant Physiol 130:1426–1435

    Article  PubMed  CAS  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 148:1938–1952

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Google Scholar 

  • Yang X, Yang YN, Xue LJ, Zou MJ, Liu JY, Chen F, Xue HW (2011) Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol 156:1397–1409

    Article  PubMed  CAS  Google Scholar 

  • Yuan B, Shen X, Li X, Xu C, Wang S (2007) Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226:953–960

    Article  PubMed  CAS  Google Scholar 

  • Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D, Xing Y, Zhang Q (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228

    Article  PubMed  Google Scholar 

  • Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–1901

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Program for Basic Research of China (2012CB114305), the National Program on High Technology Development (2012AA10A303), the National Natural Science Foundation of China (30921091, 31271316 and J1103510 to Wu N and Chang Y), and the National Program of China for Transgenic Research (2011ZX08009-003-002, 2011ZX08001-003).

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Correspondence to Lizhong Xiong.

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Du, H., Wu, N., Chang, Y. et al. Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83, 475–488 (2013). https://doi.org/10.1007/s11103-013-0103-7

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