The Arabidopsis GTL1 Transcription Factor Regulates Water Use Efficiency and Drought Tolerance by Modulating Stomatal Density via Transrepression of SDD1[W][OA]

This work provides evidence that Arabidopsis GTL1 functions as a focal regulator of water use efficiency and water stress tolerance. The results establish a potential paradigm for how the environment influences stomatal development to reduce transpiration under low water availability conditions. A goal of modern agriculture is to improve plant drought tolerance and production per amount of water used, referred to as water use efficiency (WUE). Although stomatal density has been linked to WUE, the causal molecular mechanisms have yet to be determined. Arabidopsis thaliana GT-2 LIKE 1 (GTL1) loss-of-function mutations result in increased water deficit tolerance and higher integrated WUE by reducing daytime transpiration without a demonstrable reduction in biomass accumulation. gtl1 plants had higher instantaneous WUE that was attributable to ~25% lower transpiration and stomatal conductance but equivalent CO2 assimilation. Lower transpiration was associated with higher STOMATAL DENSITY AND DISTRIBUTION1 (SDD1) expression and an ~25% reduction in abaxial stomatal density. GTL1 expression occurred in abaxial epidermal cells where the protein was localized to the nucleus, and its expression was downregulated by water stress. Chromatin immunoprecipitation analysis indicated that GTL1 interacts with a region of the SDD1 promoter that contains a GT3 box. An electrophoretic mobility shift assay was used to determine that the GT3 box is necessary for the interaction between GTL1 and the SDD1 promoter. These results establish that GTL1 negatively regulates WUE by modulating stomatal density via transrepression of SDD1.

[1]  K. Torii,et al.  Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases , 2005, Science.

[2]  D. Bergmann,et al.  Stomatal patterning and development. , 2010, Current topics in developmental biology.

[3]  T. Wada,et al.  The Trihelix Transcription Factor GTL1 Regulates Ploidy-Dependent Cell Growth in the Arabidopsis Trichome[W][OA] , 2009, The Plant Cell Online.

[4]  J. Schroeder,et al.  Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. , 2010, Annual review of plant biology.

[5]  M. Thattai,et al.  Intrinsic noise in gene regulatory networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Stuart A. Casson,et al.  Influence of environmental factors on stomatal development. , 2008, The New phytologist.

[7]  M. Thomashow,et al.  The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression , 1994, Plant Molecular Biology.

[8]  P. Quail,et al.  GT-2: in vivo transcriptional activation activity and definition of novel twin DNA binding domains with reciprocal target sequence selectivity. , 1996, The Plant cell.

[9]  K. Kaneko,et al.  Adaptive Response of a Gene Network to Environmental Changes by Fitness-Induced Attractor Selection , 2006, PloS one.

[10]  K. G. McNaughton,et al.  Stomatal Control of Transpiration: Scaling Up from Leaf to Region , 1986 .

[11]  Imara Y. Perera,et al.  Transgenic Arabidopsis Plants Expressing the Type 1 Inositol 5-Phosphatase Exhibit Increased Drought Tolerance and Altered Abscisic Acid Signaling[W] , 2008, The Plant Cell Online.

[12]  P. Brewer,et al.  PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower , 2004, Development.

[13]  K. Torii,et al.  SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation[W][OA] , 2008, The Plant Cell Online.

[14]  D. Bergmann,et al.  Arabidopsis Stomatal Initiation Is Controlled by MAPK-Mediated Regulation of the bHLH SPEECHLESS , 2008, Science.

[15]  Zhou,et al.  Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. , 1999, Trends in plant science.

[16]  Hans Lambers,et al.  Plant Physiological Ecology , 2000, Springer New York.

[17]  F. Woodward,et al.  The role of stomata in sensing and driving environmental change , 2003, Nature.

[18]  U. Alon Network motifs: theory and experimental approaches , 2007, Nature Reviews Genetics.

[19]  H. Bohnert,et al.  yucca6, a Dominant Mutation in Arabidopsis, Affects Auxin Accumulation and Auxin-Related Phenotypes1[W][OA] , 2007, Plant Physiology.

[20]  E. Richards,et al.  Preparation of Genomic DNA from Plant Tissue , 1994, Current protocols in molecular biology.

[21]  R. Albert,et al.  Predicting Essential Components of Signal Transduction Networks: A Dynamic Model of Guard Cell Abscisic Acid Signaling , 2006, PLoS biology.

[22]  D. Bergmann,et al.  Arabidopsis FAMA Controls the Final Proliferation/Differentiation Switch during Stomatal Development[W][OA] , 2006, The Plant Cell Online.

[23]  Stuart A Casson,et al.  Environmental regulation of stomatal development. , 2010, Current opinion in plant biology.

[24]  Rossana Henriques,et al.  Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method , 2006, Nature Protocols.

[25]  Guangsheng Zhou,et al.  Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass , 2008, Journal of experimental botany.

[26]  Ramón Serrano,et al.  Enhancement of Abscisic Acid Sensitivity and Reduction of Water Consumption in Arabidopsis by Combined Inactivation of the Protein Phosphatases Type 2C ABI1 and HAB11[W] , 2006, Plant Physiology.

[27]  Dominique C Bergmann,et al.  Integrating signals in stomatal development. , 2004, Current opinion in plant biology.

[28]  J. Gray,et al.  The Signaling Peptide EPF2 Controls Asymmetric Cell Divisions during Stomatal Development , 2009, Current Biology.

[29]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[30]  A. Blum Crop responses to drought and the interpretation of adaptation , 1996, Plant Growth Regulation.

[31]  Alan M. Jones,et al.  Abscisic acid regulation of guard-cell K+ and anion channels in Gβ- and RGS-deficient Arabidopsis lines , 2008, Proceedings of the National Academy of Sciences.

[32]  D. Bergmann,et al.  Transcription factor control of asymmetric cell divisions that establish the stomatal lineage , 2007, Nature.

[33]  D. Bergmann,et al.  Stomatal development. , 2007, Annual review of plant biology.

[34]  G. Farquhar,et al.  The ERECTA gene regulates plant transpiration efficiency in Arabidopsis , 2005, Nature.

[35]  F. Woodward,et al.  Plant development: Signals from mature to new leaves , 2001, Nature.

[36]  M. Sheshshayee,et al.  Carbon Isotope Discrimination Accurately Reflects Variability in WUE Measured at a Whole Plant Level in Rice , 2005 .

[37]  A. Hall Water Use Efficiency in Plant Biology , 2005 .

[38]  S. Assmann,et al.  The Control of Transpiration. Insights from Arabidopsis1 , 2006, Plant Physiology.

[39]  J. Fisahn,et al.  Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. , 2006, Functional plant biology : FPB.

[40]  S. Kay,et al.  Sequence‐specific interactions of a pea nuclear factor with light‐responsive elements upstream of the rbcS‐3A gene. , 1987, The EMBO journal.

[41]  J. Schroeder,et al.  Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells , 2010, Nature Cell Biology.

[42]  John C. Walker,et al.  Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis[W] , 2007, The Plant Cell Online.

[43]  T. Altmann,et al.  A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. , 2000, Genes & development.

[44]  T. Altmann,et al.  The Subtilisin-Like Serine Protease SDD1 Mediates Cell-to-Cell Signaling during Arabidopsis Stomatal Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001016. , 2002, The Plant Cell Online.

[45]  M. Sheshshayee,et al.  Why has breeding for water use efficiency not been successful? An analysis and alternate approach to exploit this trait for crop improvement , 1998 .

[46]  T. Sharkey,et al.  Stomatal conductance and photosynthesis , 1982 .

[47]  K. Shinozaki,et al.  Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis , 1998, Plant Cell.

[48]  C. B. Tanner,et al.  Water-Use Efficiency in Crop Production , 1984 .

[49]  D. Bergmann,et al.  BASL Controls Asymmetric Cell Division in Arabidopsis , 2009, Cell.

[50]  D. Chao,et al.  A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. , 2009, Genes & development.

[51]  X. Chen,et al.  Activated Expression of an Arabidopsis HD-START Protein Confers Drought Tolerance with Improved Root System and Reduced Stomatal Density[W][OA] , 2008, The Plant Cell Online.

[52]  P. Mullineaux,et al.  Improving water use in crop production , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  J. Gray,et al.  The signalling peptide EPFL9 is a positive regulator of stomatal development. , 2010, The New phytologist.

[54]  K. Torii,et al.  The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. , 2007, Genes & development.

[55]  Dominique C Bergmann,et al.  Stomatal Development and Pattern Controlled by a MAPKK Kinase , 2004, Science.

[56]  D. Straeten,et al.  Tuning the pores: towards engineering plants for improved water use efficiency. , 2005, Trends in biotechnology.

[57]  H. Lambers,et al.  Growth and water‐use efficiency of 10 Triticum aestivum cultivars at different water availability in relation to allocation of biomass , 1997 .

[58]  S. Assmann,et al.  The α-Subunit of the Arabidopsis Heterotrimeric G Protein, GPA1, Is a Regulator of Transpiration Efficiency1[C][W][OA] , 2010, Plant Physiology.

[59]  K. Okawa,et al.  Stomagen positively regulates stomatal density in Arabidopsis , 2010, Nature.

[60]  D. E. Somers,et al.  The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure , 2007, The Plant journal : for cell and molecular biology.

[61]  F. Ahmed,et al.  The Bases of Blepharis sp. Adaptation to Water-Limited Environment , 2010 .

[62]  P. Quail,et al.  A trans-acting factor that binds to a GT-motif in a phytochrome gene promoter. , 1990, Science.

[63]  P. Nobel Physicochemical & environmental plant physiology , 1999 .

[64]  P. Hasegawa,et al.  Regulation of Transpiration to Improve Crop Water Use , 2009 .

[65]  Daniel B. Sloan,et al.  Termination of asymmetric cell division and differentiation of stomata , 2007, Nature.

[66]  S. Chen,et al.  Soybean Trihelix Transcription Factors GmGT-2A and GmGT-2B Improve Plant Tolerance to Abiotic Stresses in Transgenic Arabidopsis , 2009, PloS one.

[67]  R. Kuhn,et al.  DNA binding factor GT-2 from Arabidopsis , 1993, Plant Molecular Biology.

[68]  Xian-Jun Song,et al.  Bar the windows: an optimized strategy to survive drought and salt adversities. , 2009, Genes & development.

[69]  J. Pereira,et al.  Understanding plant responses to drought - from genes to the whole plant. , 2003, Functional plant biology : FPB.