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Expression of a gene encoding a rice RING zinc-finger protein, OsRZFP34, enhances stomata opening

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Abstract

By oligo microarray expression profiling, we identified a rice RING zinc-finger protein (RZFP), OsRZFP34, whose gene expression increased with high temperature or abscisic acid (ABA) treatment. As compared with the wild type, rice and Arabidopsis with OsRZFP34 overexpression showed increased relative stomata opening even with ABA treatment. Furthermore, loss-of-function mutation of OsRZFP34 and AtRZFP34 (At5g22920), an OsRZFP34 homolog in Arabidopsis, decreased relative stomata aperture under nonstress control conditions. Expressing OsRZFP34 in atrzfp34 reverted the mutant phenotype to normal, which indicates a conserved molecular function between OsRZFP34 and AtRZFP34. Analysis of water loss and leaf temperature under stress conditions revealed a higher evaporation rate and cooling effect in OsRZFP34-overexpressing Arabidopsis and rice than the wild type, atrzfp34 and osrzfp34. Thus, stomata opening, enhanced leaf cooling, and ABA insensitivity was conserved with OsRZFP34 expression. Transcription profiling of transgenic rice overexpressing OsRZFP34 revealed many genes involved in OsRZFP34-mediated stomatal movement. Several genes upregulated or downregulated in OsRZFP34-overexpressing plants were previously implicated in Ca2+ sensing, K+ regulator, and ABA response. We suggest that OsRZFP34 may modulate these genes to control stomata opening.

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Abbreviations

ABA:

Abscisic acid

Col:

Arabidopsis thaliana ecotype Columbia

HS:

Heat shock

HSPs:

Heat shock proteins

OS:

Opening solution

ROS:

Reactive oxygen species

RZFP:

RING zinc-finger protein

sHSPs:

Small heat shock proteins

TRIM:

Taiwan rice insertion mutant

WT:

Wild type

References

  • Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916

    Article  CAS  PubMed  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Nat Acad Sci 103:8281–8286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64:483–484

    Article  CAS  PubMed  Google Scholar 

  • Guan JC, Yeh CH, Lin YP, Ke YT, Chen MT, You JW, Liu YH, Lu CA, Wu SJ, Lin CY (2010) A 9 bp cis-element in the promoters of class I small heat shock protein genes on chromosome 3 in rice mediates L-azetidine-2-carboxylic acid and heat shock responses. J Exp Bot 61:4249–4261

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo WJ, Ho THD (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol 147:1710–1722

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    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 6:271–282

    Article  CAS  PubMed  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    Article  CAS  PubMed  Google Scholar 

  • Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:2546–2561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hurng WP, Lin TL, Ren SS, Chen JC, Chen YR, Kao CH (1988) Senescence of rice leaves XVIII. Changes of stomatal aperture during senescence. Plant Cell Physiol 29:27–31

    Google Scholar 

  • Hüve K, Bichele I, Rasulov B, Niinemets Ü (2011) When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant Cell Environ 34:113–126

    Article  PubMed  Google Scholar 

  • Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61:143–156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67:885–894

    Article  CAS  PubMed  Google Scholar 

  • Lebaudy A, Anne-Alie’nor Véry A-A, Sentenac A (2007) K+ channel activity in plants: genes, regulations and functions. FEBS Lett 581:2357–2366

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev 15:912–924

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris P-C, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448–1452

    Article  CAS  PubMed  Google Scholar 

  • Lewis DA, Nobel PS (1977) Thermal energy exchange model and water loss of a barrel cactus, Ferocactus acanthodes. Plant Physiol 60:609–616

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu FL, Jensen CR, Shahanzari A, Andersen MN, Jacobsen SE (2005) ABA regulated stomatal control and photosynthetic water use efficiency of potato (Solanum tuberosum L.) during progressive soil drying. Plant Sci 168:831–836

    Article  CAS  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nagy R, Grob H, Weder B, Green P, Klein M, Frelet-Barrand A, Schjoerring JK, Brearley C, Martinoia E (2009) The Arabidopsis ATP-binding cassette protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J Biol Chem 284:33614–33622

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Nat Acad Sci 101:9971–9975

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ricachenevsky FK, Sperotto RA, Menguer PK, Fett JP (2010) Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence. Mol Biol Rep 37:3735–3745

    Article  CAS  PubMed  Google Scholar 

  • Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842

    Article  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Siegel RS, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder JI (2009) Calcium elevation-and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and Kin channels in Arabidopsis guard cells. Plant J 59:207–220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J Exp Bot 60:1439–1463

    Article  CAS  PubMed  Google Scholar 

  • Suh SJ, Wang YF, Frelet A, Leonhardt N, Klein M, Forestier C, Mueller-Roeber B, Cho MH, Martinoia E, Schroeder JI (2007) The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J Biol Chem 282:1916–1924

    Article  CAS  PubMed  Google Scholar 

  • Sun W, van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochem Biophys Acta 1577:1–9

    CAS  PubMed  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283:9269–9275

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci 106:17588–17593

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weigel D, Glazebrook J (2002) Arabidopsis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Welch JR, Vincent JR, Auffhammer M, Moya PF, Dobermann A, Dawe D (2010) Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures. Proc Natl Acad Sci 107:14562–14567

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yeh CH, Chang PFL, Yeh KW, Lin WC, Chen YM, Lin CY (1997) Expression of a gene encoding a 16.9-kDa heat shock protein, Oshsp16.9, in Escherichia coli enhances thermotolerance. Proc Natl Acad Sci 94:10967–10972

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun DJ, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Lu YT (2003) Calmodulin-binding protein kinases in plants. Trends Plant Sci 8:123–127

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xiea Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou S, Zhao W, Li H, Guo Z, Peng YL (2008) Characterization of a novel RING finger gene OsRFP1, which is induced by ethylene, salicylic acid and blast fungus infection in rice. J Phytopathol 156:396–402

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Drs. Tong-Seung Tseng, Tzung-Meng Wu, and Kuo-Chen Yeh for comments and suggestions on the manuscript; and Dr. Yee-Yung Charng for technical assistance with thermal imaging. We thank the electron microscopy laboratory of Tzu Chi University. We also thank ABRC and TRIM for providing seeds. This work was supported by the National Science Council, Taiwan, ROC (NSC96-2317-B-008-003 and NSC98-2324-B-008-002 to C.H. Yeh).

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Correspondence to Ching-Hui Yeh.

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Hsu, KH., Liu, CC., Wu, SJ. et al. Expression of a gene encoding a rice RING zinc-finger protein, OsRZFP34, enhances stomata opening. Plant Mol Biol 86, 125–137 (2014). https://doi.org/10.1007/s11103-014-0217-6

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  • DOI: https://doi.org/10.1007/s11103-014-0217-6

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