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Phytochrome B control of total leaf area and stomatal density affects drought tolerance in rice

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Abstract

We report that phytochrome B (phyB) mutants exhibit improved drought tolerance compared to wild type (WT) rice (Oryza sativa L. cv. Nipponbare). To understand the underlying mechanism by which phyB regulates drought tolerance, we analyzed root growth and water loss from the leaves of phyB mutants. The root system showed no significant difference between the phyB mutants and WT, suggesting that improved drought tolerance has little relation to root growth. However, phyB mutants exhibited reduced total leaf area per plant, which was probably due to a reduction in the total number of cells per leaf caused by enhanced expression of Orysa;KRP1 and Orysa;KRP4 (encoding inhibitors of cyclin-dependent kinase complex activity) in the phyB mutants. In addition, the developed leaves of phyB mutants displayed larger epidermal cells than WT leaves, resulting in reduced stomatal density. phyB deficiency promoted the expression of both putative ERECTA family genes and EXPANSIN family genes involved in cell expansion in leaves, thus causing greater epidermal cell expansion in the phyB mutants. Reduced stomatal density resulted in reduced transpiration per unit leaf area in the phyB mutants. Considering all these findings, we propose that phyB deficiency causes both reduced total leaf area and reduced transpiration per unit leaf area, which explains the reduced water loss and improved drought tolerance of phyB mutants.

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References

  • Barrôco RM, Peres A, Droual AM, De Veylder L, Nguyen LSL, De Wolf J, Mironov V, Peerbolte R, Beemster GTS, Inzé D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa; KRP1 plays an important role in seed development of rice. Plant Physiol 142:1053–1064

    Article  PubMed  Google Scholar 

  • Basu D, Dehesh K, Schneider-Poetsch HJ, Harrington SE, McCouch SR, Quail PH (2000) Rice PHYC gene: structure, expression, map position and evolution. Plant Mol Biol 44:27–42

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Boccalandro HE, Ploschuk EL, Yanovsky MJ, Sánchez RA, Gatz C, Casal JJ (2003) Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol 133:1539–1546

    Article  PubMed  CAS  Google Scholar 

  • Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. Plant Physiol 150:1083–1092

    Article  PubMed  CAS  Google Scholar 

  • Bradford KJ, Sharkey TD, Farquhar GD (1983) Gas exchange, stomatal behavior, and δ13C values of the flacca tomato mutant in relation to abscisic acid. Plant Physiol 72:245–250

    Article  PubMed  CAS  Google Scholar 

  • Casal JJ, Aphalo PJ, Sánchez RA (1987) Phytochrome effects on leaf growth and chlorophyll content in Petunia axillaris. Plant Cell Environ 10:509–514

    Article  CAS  Google Scholar 

  • Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95

    Article  PubMed  CAS  Google Scholar 

  • Casson SA, Franklin KA, Gray JE, Grierson CS, Whitelam GC, Hetherington AM (2009) Phytochrome B and PIF4 regulate stomatal development in response to light quantity. Curr Biol 19:229–234

    Article  PubMed  CAS  Google Scholar 

  • Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788

    Article  PubMed  CAS  Google Scholar 

  • Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of Expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398

    Article  PubMed  CAS  Google Scholar 

  • Choi D, Cho HT, Lee Y (2006) Expansins: expanding importance in plant growth and development. Physiol Plant 126:511–518

    CAS  Google Scholar 

  • Dehesh K, Tepperman J, Christensen AH, Quail PH (1991) PhyB is evolutionarily conserved and constitutively expressed in rice seedling shoots. Mol Gen Genet 225:305–313

    Article  PubMed  CAS  Google Scholar 

  • Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC (1999) Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol 119:909–915

    Article  PubMed  CAS  Google Scholar 

  • Frankland B, Letendre RJ (1978) Phytochrome and effects of shading on growth of woodland plants. Photochem Photobiol 27:223–230

    Article  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24

    Article  PubMed  CAS  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  PubMed  CAS  Google Scholar 

  • Holmes M, Smith H (1977) The function of phytochrome in the natural environment. III. Measurement and calculation of phytochrome photoequilibria. Photochem Photobiol 25:547–550

    Article  Google Scholar 

  • Kasperbauer MJ (1971) Spectral distribution of light in a tobacco canopy and effects of end-of-day light quality on growth and development. Plant Physiol 47:775–778

    Article  PubMed  CAS  Google Scholar 

  • Kay SA, Keith B, Shinozaki K, Chua NH (1989) The sequence of the rice phytochrome gene. Nucleic Acids Res 17:2865–2866

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Kende H (2002) Expression of α-Expansin and Expansin-like genes in deepwater rice. Plant Physiol 130:1396–1405

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4:527–532

    Article  PubMed  CAS  Google Scholar 

  • Liu T, Ohashi-Ito K, Bergmann DC (2009) Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136:2265–2276

    Article  PubMed  CAS  Google Scholar 

  • López Juez E, Buurmeijer WF, Heeringa GH, Kendrick RE, Wesselius JC (1990) Response of light-grown wild type and long hypocotyl mutant cucumber plants to end-of-day far-red light. Photochem Photobiol 52:143–149

    Article  Google Scholar 

  • Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102:12270–12275

    Article  PubMed  CAS  Google Scholar 

  • Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870

    Article  PubMed  CAS  Google Scholar 

  • Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Neff MM, Fankhauser C, Chory J (2000) Light: an indicator of time and place. Genes Dev 14:257–271

    PubMed  CAS  Google Scholar 

  • Ouedraogo M, Hubac C (1982) Effect of far red light on drought resistance of cotton. Plant Cell Physiol 23:1297–1303

    Google Scholar 

  • Ouedraogo M, Hubac C, Monard JF (1986) Effect of far red light on root growth and on xylem sap in cotton (Gossypium hirsutum L.). Plant Cell Physiol 27:17–24

    CAS  Google Scholar 

  • Peterson KM, Rychel AL, Torii KU (2010) Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22:296–306

    Article  PubMed  CAS  Google Scholar 

  • Pillitteri LJ, Bogenschutz NL, Torii KU (2008) The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. Plant Cell Physiol 49:934–943

    Article  PubMed  CAS  Google Scholar 

  • Quail PH (2002a) Photosensory perception and signalling in plant cells: new paradigms? Curr Opin Cell Biol 14:180–188

    Article  PubMed  CAS  Google Scholar 

  • Quail PH (2002b) Phytochrome photosensory signalling networks. Natl Rev Mol Cell Biol 3:85–93

    Article  CAS  Google Scholar 

  • Robson PRH, Whitelam GC, Smith H (1993) Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants of Arabidopsis thaliana and Brassica rapa deficient in phytochrome B. Plant Physiol 102:1179–1184

    PubMed  CAS  Google Scholar 

  • Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421

    CAS  Google Scholar 

  • Schittenhelm S, Menge-Hartmann U, Oldenburg E (2004) Photosynthesis, carbohydrate metabolism, and yield of phytochrome-B-overexpressing potatoes under different light regimes. Crop Sci 44:131–143

    Article  CAS  Google Scholar 

  • Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, North H, Marion-Poll A, Sun TP, Koshiba T, Kamiya Y, Yamaguchi S, Nambara E (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48:354–366

    Article  PubMed  CAS  Google Scholar 

  • Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293

    Article  PubMed  CAS  Google Scholar 

  • Tahir M, Kanegae H, Takano M (1998) Phytochrome C (PHYC) gene in rice: isolation and characterization of a complete coding sequence. Plant Physiol 118:1535

    Google Scholar 

  • Takano M, Kanegae H, Shinomura T, Miyao A, Hirochika H, Furuya M (2001) Isolation and characterization of rice phytochrome A mutants. Plant Cell 13:521–534

    Article  PubMed  CAS  Google Scholar 

  • Takano M, Inagaki N, Xie X, Yuzurihara N, Hihara F, Ishizuka T, Yano M, Nishimura M, Miyao A, Hirochika H, Shinomura T (2005) Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17:3311–3325

    Article  PubMed  CAS  Google Scholar 

  • Takano M, Inagaki N, Xie X, Kiyota S, Baba-Kasai A, Tanabata T, Shinomura T (2009) Phytochromes are the sole photoreceptors for perceiving red/far-red light in rice. Proc Natl Acad Sci USA 106:14705–14710

    Article  PubMed  CAS  Google Scholar 

  • Tank JG, Thaker VS (2011) Cyclin dependent kinases and their role in regulation of plant cell cycle. Biol Plant 55:201–212

    Article  CAS  Google Scholar 

  • Thiele A, Herold M, Lenk I, Quail PH, Gatz C (1999) Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development. Plant Physiol 120:73–81

    Article  PubMed  CAS  Google Scholar 

  • Tisné S, Barbier F, Granier C (2011) The ERECTA gene controls spatial and temporal patterns of epidermal cell number and size in successive developing leaves of Arabidopsis thaliana. Ann Bot 108:159–168

    Article  PubMed  Google Scholar 

  • van Zanten M, Snoek LB, Proveniers MC, Peeters AJ (2009) The many functions of ERECTA. Trends Plant Sci 14:214–218

    Article  PubMed  Google Scholar 

  • van Zanten M, Basten Snoek L, van Eck-Stouten E, Proveniers MC, Torii KU, Voesenek LA, Peeters AJ, Millenaar FF (2010) Ethylene-induced hyponastic growth in Arabidopsis thaliana is controlled by ERECTA. Plant J 61:83–95

    Article  PubMed  Google Scholar 

  • Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212

    Article  PubMed  CAS  Google Scholar 

  • Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E, Theobald J, Knight MR, Davies WJ, Leyser HM, Hetherington AM (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol 16:882–887

    Article  PubMed  CAS  Google Scholar 

  • Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15

    Article  PubMed  Google Scholar 

  • Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. X. Liu for measuring the photosynthesis and transpiration rate. We also appreciate the native English-speaking experts of BioMed Proofreading for their proofreading this manuscript. This work was partly supported by grants from the Chinese National Natural Science Foundation (30971744), the Shandong Natural Science Funds for Distinguished Young Scholar (JQ200911), the Chinese Ministry of Agriculture (2009ZX08001-029B) and the Key Laboratory of Crop Biology (2009KF04).

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Authors and Affiliations

  1. College of Life Sciences, Shandong Normal University, 250014, Jinan, People’s Republic of China

    Jing Liu & Baoshan Wang

  2. High-Tech Research Center, Shandong Academy of Agricultural Sciences, 250100, Jinan, People’s Republic of China

    Jing Liu, Jinjun Zhou & Xianzhi Xie

  3. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 100190, Beijing, People’s Republic of China

    Fang Zhang & Fan Chen

  4. Laboratory of Crop Genetic Improvement and Biotechnology, Huanghuaihai, Ministry of Agriculture, 250100, Jinan, People’s Republic of China

    Jinjun Zhou & Xianzhi Xie

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  1. Jing Liu
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Correspondence to Baoshan Wang or Xianzhi Xie.

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Liu, J., Zhang, F., Zhou, J. et al. Phytochrome B control of total leaf area and stomatal density affects drought tolerance in rice. Plant Mol Biol 78, 289–300 (2012). https://doi.org/10.1007/s11103-011-9860-3

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