Genetics of Drought Adaptation in Arabidopsis thaliana II. Qtl Analysis of a New Mapping Population, Kas-1 × Tsu-1

Abstract Despite compelling evidence that adaptation to local climate is common in plant populations, little is known about the evolutionary genetics of traits that contribute to climatic adaptation. A screen of natural accessions of Arabidopsis thaliana revealed Tsu-1 and Kas-1 to be opposite extremes for water-use efficiency and climate at collection sites for these accessions differs greatly. To provide a tool to understand the genetic basis of this putative adaptation, Kas-1 and Tsu-1 were reciprocally crossed to create a new mapping population. Analysis of F3 families showed segregating variation in both δ13C and transpiration rate, and as expected these traits had a negative genetic correlation (rg=− 0.3). 346 RILs, 148 with Kas-1 cytoplasm and 198 with Tsu-1 cytoplasm, were advanced to the F9 and genotyped using 48 microsatellites and 55 SNPs for a total of 103 markers. This mapping population was used for QTL analysis of δ13C using F9 RIL means. Analysis of this reciprocal cross showed a large effect of cytoplasmic background, as well as two QTL for δ13C. The Kas-1 × Tsu-1 mapping population provides a powerful new resource for mapping QTL underlying natural variation and for dissecting the genetic basis of water-use efficiency differences.

[1]  P. Jones,et al.  Representing Twentieth-Century Space-Time Climate Variability. Part II: Development of 1901-96 Monthly Grids of Terrestrial Surface Climate , 2000 .

[2]  T. Mitchell-Olds,et al.  Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits , 2003, Molecular ecology.

[3]  Thomas Girke,et al.  Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[4]  X. Sirault,et al.  QTLs for grain carbon isotope discrimination in field-grown barley , 2002, Theoretical and Applied Genetics.

[5]  G. Sills,et al.  Variance for water‐use efficiency among ecotypes and recombinant inbred lines of Arabidopsis thaliana (Brassicaceae) , 1994 .

[6]  Defining selection criteria to improve yield under drought , 1996 .

[7]  J. Chory,et al.  Coordination of gene expression between organellar and nuclear genomes , 2008, Nature Reviews Genetics.

[8]  I. Hiscock Communities and Ecosystems , 1970, The Yale Journal of Biology and Medicine.

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

[10]  A. Condon,et al.  Breeding for high water-use efficiency. , 2004, Journal of experimental botany.

[11]  R. C. Muchow,et al.  A critical evaluation of traits for improving crop yields in water-limited environments. , 1990 .

[12]  Alain Charcosset,et al.  Combining Quantitative Trait Loci Analysis and an Ecophysiological Model to Analyze the Genetic Variability of the Responses of Maize Leaf Growth to Temperature and Water Deficit1 , 2003, Plant Physiology.

[13]  T. Toojinda,et al.  Quantitative Trait Loci Associated with Drought Tolerance at Reproductive Stage in Rice1 , 2004, Plant Physiology.

[14]  M. Purugganan,et al.  Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  N. Barton,et al.  Evolutionary quantitative genetics: how little do we know? , 1989, Annual review of genetics.

[16]  R. Richards,et al.  Defining selection criteria to improve yield under drought , 1996, Plant Growth Regulation.

[17]  P. Scott Resurrection Plants and the Secrets of Eternal Leaf , 2000 .

[18]  Claude Lebreton,et al.  Identification of QTL for drought responses in maize and their use in testing causal relationships between traits , 1995 .

[19]  E. Bray Plant responses to water deficit , 1997 .

[20]  A. Condon,et al.  Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat , 2002 .

[21]  Kirk A. Stowe,et al.  Identification and characterization of QTL underlying whole‐plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency , 2005 .

[22]  H. A. Orr,et al.  The genetic theory of adaptation: a brief history , 2005, Nature Reviews Genetics.

[23]  E. Bray Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. , 2004, Journal of experimental botany.

[24]  S. A. Dudley DIFFERING SELECTION ON PLANT PHYSIOLOGICAL TRAITS IN RESPONSE TO ENVIRONMENTAL WATER AVAILABILITY: A TEST OF ADAPTIVE HYPOTHESES , 1996, Evolution; international journal of organic evolution.

[25]  H. Bohnert,et al.  Adaptations to Environmental Stresses. , 1995, The Plant cell.

[26]  G. Farquhar,et al.  Analysis of Restriction Fragment Length Polymorphisms Associated with Variation of Carbon Isotope Discrimination among Ecotypes of Arabidopsis thaliana , 1993 .

[27]  Drought and drought tolerance , 1996 .

[28]  P. Templer,et al.  Stable Isotopes in Plant Ecology , 2002 .

[29]  Robert W. Pearcy,et al.  Plant Physiological Ecology , 1989, Springer Netherlands.

[30]  K. Akiyama,et al.  Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. , 2002, The Plant journal : for cell and molecular biology.

[31]  G. Farquhar,et al.  Effect of salinity and humidity on δ13C value of halophytes—Evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions , 2004, Oecologia.

[32]  J. Passioura Drought and drought tolerance , 1996, Plant Growth Regulation.

[33]  J. Boyer Plant Productivity and Environment , 1982, Science.

[34]  D. Cameron,et al.  Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis. , 2001, Journal of experimental botany.

[35]  P. Stam,et al.  Construction of integrated genetic linkage maps by means of a new computer package: JOINMAP. , 1993 .

[36]  Mattias Jakobsson,et al.  The Pattern of Polymorphism in Arabidopsis thaliana , 2005, PLoS biology.

[37]  Graham D. Farquhar,et al.  On the Relationship Between Carbon Isotope Discrimination and the Intercellular Carbon Dioxide Concentration in Leaves , 1982 .

[38]  Alcalde Rovira Roure Plant Breeding and Drought in C 3 Cereals: What Should We Breed For? , 2002 .

[39]  Die Vegetation der Erde , 1977 .

[40]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .

[41]  M. Purugganan,et al.  A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  H. A. Orr,et al.  THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION , 1998, Evolution; international journal of organic evolution.

[43]  Hao Wu,et al.  R/qtl: QTL Mapping in Experimental Crosses , 2003, Bioinform..

[44]  T. Juenger,et al.  Natural genetic variation in whole‐genome expression in Arabidopsis thaliana: the impact of physiological QTL introgression , 2006, Molecular ecology.

[45]  S. Chapman,et al.  Genetic variation for carbon isotope discrimination in sunflower: Association with transpiration efficiency and evidence for cytoplasmic inheritance , 2004 .

[46]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[47]  J. Chory,et al.  A tale of two genomes: role of a chloroplast signal in coordinating nuclear and plastid genome expression , 1992 .

[48]  J. Comstock,et al.  Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. , 2002, Journal of experimental botany.

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

[50]  T. Juenger,et al.  QUANTITATIVE TRAIT LOCI AFFECTING δ13C AND RESPONSE TO DIFFERENTIAL WATER AVAILIBILITY IN ARABIDOPSIS THALLANA , 2005, Evolution; international journal of organic evolution.

[51]  M. M. Chaves,et al.  Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. , 2004, Journal of experimental botany.

[52]  J. Schmitt,et al.  Population Differentiation and Natural Selection for Water‐Use Efficiency in Impatiens capensis (Balsaminaceae) , 2002, International Journal of Plant Sciences.

[53]  Thomas Mitchell-Olds,et al.  Evolutionary and ecological functional genomics , 2003, Nature Reviews Genetics.

[54]  T. Dawson,et al.  Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum , 1997, Oecologia.

[55]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[56]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  G. Farquhar,et al.  Correlation Between Water-Use Efficiency and Carbon Isotope Discrimination in Diverse Peanut (Arachis) Germplasm , 1986 .

[58]  J. Ehleringer,et al.  Correlating genetic variation in carbon isotopic composition with complex climatic gradients. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[59]  C. Dawson The World’s Water 1998-1999. The Biennial Report on Freshwater Resources. , 2000 .

[60]  W. Ewens Genetics and analysis of quantitative traits , 1999 .

[61]  Kazuo Shinozaki,et al.  AREB1 Is a Transcription Activator of Novel ABRE-Dependent ABA Signaling That Enhances Drought Stress Tolerance in Arabidopsis[W][OA] , 2005, The Plant Cell Online.

[62]  Richard M. Clark,et al.  Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana , 2007, Science.

[63]  C. Riginos,et al.  Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminaceae). , 2005, American journal of botany.

[64]  J. Araus,et al.  Plant breeding and drought in C3 cereals: what should we breed for? , 2002, Annals of botany.

[65]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[66]  K. Shinozaki,et al.  Regulatory network of gene expression in the drought and cold stress responses. , 2003, Current opinion in plant biology.

[67]  V. V. Symonds,et al.  A simple and inexpensive method for producing fluorescently labelled size standard , 2004 .

[68]  G. D. FarquharA,et al.  On the Relationship between Carbon Isotope Discrimination and the Intercellular Carbon Dioxide Concentration in Leaves , 2005 .

[69]  G. Edmeades,et al.  Drought tolerance improvement in tropical maize source populations: evidence of progress , 2006 .

[70]  R. A. Fischer,et al.  Wheat Yield Progress Associated with Higher Stomatal Conductance and Photosynthetic Rate, and Cooler Canopies , 1998 .

[71]  R. Doerge,et al.  Permutation tests for multiple loci affecting a quantitative character. , 1996, Genetics.

[72]  T. Mitchell-Olds,et al.  Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  H. A. Orr,et al.  The Genetics of Adaptation: A Reassessment , 1992, The American Naturalist.

[74]  Ernst-Detlef Schulze,et al.  Carbon Dioxide and Water Vapor Exchange in Response to Drought in the Atmosphere and in the Soil , 1986 .

[75]  L. Xiong,et al.  Genetic Basis of Drought Resistance at Reproductive Stage in Rice: Separation of Drought Tolerance From Drought Avoidance , 2006, Genetics.

[76]  J. Ecker,et al.  Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. , 1994, Genomics.

[77]  H. Griffiths,et al.  Linking drought-resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. , 2002, Journal of experimental botany.

[78]  T. Vision,et al.  The effects of resource availability and environmental conditions on genetic rankings for carbon isotope discrimination during growth in tomato and rice. , 2005, Functional plant biology : FPB.

[79]  R. Monson,et al.  Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation , 1993 .

[80]  G. Stebbins Aridity as a Stimulus to Plant Evolution , 1952, The American Naturalist.

[81]  A. Condon,et al.  Improving Intrinsic Water-Use Efficiency and Crop Yield. , 2002, Crop science.

[82]  Stomatal Water Relations and the Control of Hydraulic Supply and Demand , 2002 .

[83]  V. V. Symonds,et al.  An analysis of microsatellite loci in Arabidopsis thaliana: mutational dynamics and application. , 2003, Genetics.

[84]  E. Stahl,et al.  Genetic variation in Arabidopsis thaliana for night-time leaf conductance. , 2008, Plant, cell & environment.

[85]  R. Amasino,et al.  Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. , 2000, Science.

[86]  Die Vegetation der Erde , 1912, Nature.