Differential regulation of aquaporins, small GTPases and V‐ATPases proteins in rice leaves subjected to drought stress and recovery

Mechanisms of drought tolerance are complex, interacting, and polygenic. This paper describes patterns of gene expression at precise physiological stages of drought in 35‐day‐old seedlings of Oryza sativa cv. Nipponbare. Drought was imposed gradually for up to 15 days, causing abscisic acid levels to rise and growth to cease, and plants were then re‐watered. Proteins were identified from leaf samples after moderate drought, extreme drought, and 3 and 6 days of re‐watering. Label‐free quantitative shotgun proteomics resulted in identification of 1548 non‐redundant proteins. More proteins were down‐regulated in early stages of drought but more were up‐regulated as severe drought developed. After re‐watering, there was notable down regulation, suggesting that stress‐related proteins were being degraded. Proteins involved in signalling and transport became dominant as severe drought took hold but decreased again on re‐watering. Most of the nine aquaporins identified were responsive to drought, with six decreasing rapidly in abundance as plants were re‐watered. Nine G‐proteins appeared in large amounts during severe drought and dramatically degraded once plants were re‐watered. We speculate that water transport and drought signalling are critical elements of the overall response to drought in rice and might be the key to biotechnological approaches to drought tolerance.

[1]  Dana Pascovici,et al.  Shotgun proteomic profiling of five species of New Zealand Pachycladon , 2011, Proteomics.

[2]  Yong Zheng,et al.  A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. , 2009, Gene.

[3]  P. Streb,et al.  Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. , 1992, Plant physiology.

[4]  L. Breci,et al.  Proteomic analysis of shade-avoidance response in tomato leaves. , 2007, Journal of agricultural and food chemistry.

[5]  R. Beavis,et al.  A method for reducing the time required to match protein sequences with tandem mass spectra. , 2003, Rapid communications in mass spectrometry : RCM.

[6]  Paul A Haynes,et al.  Quantitative proteomic analysis of cold‐responsive proteins in rice , 2011, Proteomics.

[7]  Robertson Craig,et al.  TANDEM: matching proteins with tandem mass spectra. , 2004, Bioinformatics.

[8]  A. Yamauchi,et al.  Genotypic Variation in Response of Rainfed Lowland Rice to Drought and Rewatering , 2000 .

[9]  T C Hsiao,et al.  Influence of Osmotic Adjustment on Leaf Rolling and Tissue Death in Rice (Oryza sativa L.). , 1984, Plant physiology.

[10]  M. Mirzaei,et al.  Proteomic analysis of temperature stress in plants , 2010, Proteomics.

[11]  G. Spangenberg,et al.  Identification of plant defence genes in canola using Arabidopsis cDNA microarrays. , 2008, Plant biology.

[12]  Dana Pascovici,et al.  Transcript and protein profiling identify candidate gene sets of potential adaptive significance in New Zealand Pachycladon , 2010, BMC Evolutionary Biology.

[13]  Ying Zhang,et al.  Effect of dynamic exclusion duration on spectral count based quantitative proteomics. , 2009, Analytical chemistry.

[14]  Xin-Yao Yu,et al.  Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment , 2006, Cell Research.

[15]  Hyungwon Choi,et al.  Significance Analysis of Spectral Count Data in Label-free Shotgun Proteomics*S , 2008, Molecular & Cellular Proteomics.

[16]  Konstantinos Thalassinos,et al.  A comparison of labeling and label-free mass spectrometry-based proteomics approaches. , 2009, Journal of proteome research.

[17]  Xin-Yao Yu,et al.  The role of aquaporin RWC3 in drought avoidance in rice. , 2004, Plant & cell physiology.

[18]  Felipe Rodrigues da Silva,et al.  Identification of drought-responsive genes in roots of upland rice (Oryza sativa L) , 2008, BMC Genomics.

[19]  Michael K. Coleman,et al.  Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. , 2006, Journal of proteome research.

[20]  Paul A Haynes,et al.  Subcellular shotgun proteomics in plants: Looking beyond the usual suspects , 2007, Proteomics.

[21]  U. Lüttge,et al.  Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. , 2001, Journal of experimental botany.

[22]  Jay J. Thelen,et al.  Quantitative Proteomics in Plants: Choices in Abundance , 2007, The Plant Cell Online.

[23]  R. T. Cruz,et al.  Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. , 1980, Plant physiology.

[24]  R. Feron,et al.  PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. , 2004, Journal of experimental botany.

[25]  Jiaxu Li,et al.  Differential regulation of proteins and phosphoproteins in rice under drought stress. , 2009, Biochemical and biophysical research communications.

[26]  B. Ghareyazie,et al.  A proteomic approach to analyzing drought- and salt-responsiveness in rice , 2002 .

[27]  M. Carvajal,et al.  Are Root Hydraulic Conductivity Responses to Salinity Controlled by Aquaporins in Broccoli Plants? , 2005, Plant and Soil.

[28]  I. Henson Abscisic Acid and Water Relations of Rice (Oryza sativa L.): Effects of Drought Conditioning on Abscisic Acid Accumulation in the Leaf and Stomatal Response , 1983 .

[29]  K. Dietz,et al.  Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. , 2001, Plant physiology.

[30]  R. R. Ariza,et al.  Repair and tolerance of oxidative DNA damage in plants. , 2009, Mutation research.

[31]  Ying Xu,et al.  Aquaporin JcPIP2 is involved in drought responses in Jatropha curcas. , 2007, Acta biochimica et biophysica Sinica.

[32]  I. Moore,et al.  The Arabidopsis Rab GTPase family: another enigma variation. , 2002, Current opinion in plant biology.

[33]  J. Bennett,et al.  Abiotic stress tolerance in rice for Asia: progress and the future , 2004 .

[34]  W. Majeran,et al.  Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomicsw⃞ , 2005, The Plant Cell Online.

[35]  T. Rabilloud Membrane proteins ride shotgun , 2003, Nature Biotechnology.

[36]  Magnus Palmblad,et al.  Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. , 2008, Journal of proteome research.

[37]  Akira Yamauchi,et al.  Root biology and genetic improvement for drought avoidance in rice , 2011 .

[38]  B. Ghareyazie,et al.  Proteomic analysis of rice leaves during drought stress and recovery , 2002, Proteomics.

[39]  G. Galili,et al.  Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009225. , 2003, The Plant Cell Online.

[40]  Matthias Mann,et al.  Innovations: Functional and quantitative proteomics using SILAC , 2006, Nature Reviews Molecular Cell Biology.

[41]  K. Kang,et al.  A proteomic approach in analyzing heat‐responsive proteins in rice leaves , 2007, Proteomics.

[42]  Mehdi Mirzaei,et al.  Less label, more free: Approaches in label‐free quantitative mass spectrometry , 2011, Proteomics.

[43]  Dana Pascovici,et al.  Differential proteomic response of rice (Oryza sativa) leaves exposed to high‐ and low‐temperature stress , 2011, Proteomics.

[44]  P. Haynes,et al.  Phosphoglycosylation: a new structural class of glycosylation? , 1998, Glycobiology.

[45]  Q. Ma Small GTP-binding Proteins and their Functions in Plants , 2007, Journal of Plant Growth Regulation.

[46]  Jeroen Krijgsveld,et al.  In-gel isoelectric focusing of peptides as a tool for improved protein identification. , 2006, Journal of proteome research.

[47]  D. Luu,et al.  The cellular dynamics of plant aquaporin expression and functions. , 2009, Current opinion in plant biology.

[48]  P. Agarwal,et al.  Constitutive overexpression of a stress-inducible small GTP-binding protein PgRab7 from Pennisetum glaucum enhances abiotic stress tolerance in transgenic tobacco , 2007, Plant Cell Reports.

[49]  J. Renaut,et al.  Proteomics and low-temperature studies : bridging the gap between gene expression and metabolism , 2006 .

[50]  L. Zolla,et al.  Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). , 2008, Journal of proteomics.

[51]  Dana Pascovici,et al.  Differential metabolic response of cultured rice (Oryza sativa) cells exposed to high‐ and low‐temperature stress , 2010, Proteomics.

[52]  Erik Alexandersson,et al.  Whole Gene Family Expression and Drought Stress Regulation of Aquaporins , 2005, Plant Molecular Biology.

[53]  A. Wahid,et al.  Advances in Drought Resistance of Rice , 2009 .

[54]  G. Salekdeh,et al.  Proteomics uncovers a role for redox in drought tolerance in wheat. , 2007, Journal of proteome research.

[55]  S. Komatsu,et al.  Proteomic analysis of rice leaf sheath during drought stress. , 2006, Journal of proteome research.