Using chromosome introgression lines to map quantitative trait loci for photosynthesis parameters in rice (Oryza sativa L.) leaves under drought and well-watered field conditions

Photosynthesis is fundamental to biomass production, but sensitive to drought. To understand the genetics of leaf photosynthesis, especially under drought, upland rice cv. Haogelao, lowland rice cv. Shennong265, and 94 of their introgression lines (ILs) were studied at flowering and grain filling under drought and well-watered field conditions. Gas exchange and chlorophyll fluorescence measurements were conducted to evaluate eight photosynthetic traits. Since these traits are very sensitive to fluctuations in microclimate during measurements under field conditions, observations were adjusted for microclimatic differences through both a statistical covariant model and a physiological approach. Both approaches identified leaf-to-air vapour pressure difference as the variable influencing the traits most. Using the simple sequence repeat (SSR) linkage map for the IL population, 1–3 quantitative trait loci (QTLs) were detected per trait–stage–treatment combination, which explained between 7.0% and 30.4% of the phenotypic variance of each trait. The clustered QTLs near marker RM410 (the interval from 57.3 cM to 68.4 cM on chromosome 9) were consistent over both development stages and both drought and well-watered conditions. This QTL consistency was verified by a greenhouse experiment under a controlled environment. The alleles from the upland rice at this interval had positive effects on net photosynthetic rate, stomatal conductance, transpiration rate, quantum yield of photosystem II (PSII), and the maximum efficiency of light-adapted open PSII. However, the allele of another main QTL from upland rice was associated with increased drought sensitivity of photosynthesis. These results could potentially be used in breeding programmes through marker-assisted selection to improve drought tolerance and photosynthesis simultaneously.

[1]  O. Panaud,et al.  Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.) , 1996, Molecular and General Genetics MGG.

[2]  Z. W. Shappley,et al.  Quantitative Trait Loci Associated with Agronomic and Fiber Traitsof Upland Cotton , 1998 .

[3]  Xinyou Yin,et al.  A Model of the Generalized Stoichiometry of Electron Transport Limited C3 Photosynthesis: Development and Applications , 2009 .

[4]  S. Long,et al.  Can improvement in photosynthesis increase crop yields? , 2006, Plant, cell & environment.

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

[6]  Maria Manuela Chaves,et al.  Effects of Water Deficits on Carbon Assimilation , 1991 .

[7]  Xinyou Yin,et al.  Mathematical review of literature to assess alternative electron transports and interphotosystem excitation partitioning of steady-state C3 photosynthesis under limiting light. , 2006, Plant, cell & environment.

[8]  Gary Atlin,et al.  A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. , 2007 .

[9]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[10]  L. Xiong,et al.  Genetic analysis for drought resistance of rice at reproductive stage in field with different types of soil , 2005, Theoretical and Applied Genetics.

[11]  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.

[12]  Lei Wang,et al.  Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice , 2008, Nature Genetics.

[13]  Xin-Guang Zhu,et al.  Improving photosynthetic efficiency for greater yield. , 2010, Annual review of plant biology.

[14]  M. J. Kropff,et al.  AFLP mapping of quantitative trait loci for yield-determining physiological characters in spring barley , 1999, Theoretical and Applied Genetics.

[15]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[16]  Pierre Martre,et al.  Under what circumstances can process-based simulation models link genotype to phenotype for complex traits? Case-study of fruit and grain quality traits. , 2010, Journal of experimental botany.

[17]  S. V. Caemmerer,et al.  Biochemical models of leaf photosynthesis. , 2000 .

[18]  S. Long,et al.  Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. , 2003, Journal of experimental botany.

[19]  D. Lawlor,et al.  Effects of water deficit on photosynthesis , 1995 .

[20]  Lloyd W. Martin,et al.  Stomatal behavior and leaf water status of strawberry in different growth environments , 1982 .

[21]  A. Price,et al.  A combined RFLP and AFLP linkage map of upland rice (Oryza sativa L.) used to identify QTLs for root-penetration ability , 2000, Theoretical and Applied Genetics.

[22]  E. Lander,et al.  Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results , 1995, Nature Genetics.

[23]  R. Lyman Ott.,et al.  An introduction to statistical methods and data analysis , 1977 .

[24]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.

[25]  Arana,et al.  Progress in Photosynthesis Research , 1987, Springer Netherlands.

[26]  L. Lipovich,et al.  Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.) , 2000, Theoretical and Applied Genetics.

[27]  M. Yano,et al.  Dro1, a major QTL involved in deep rooting of rice under upland field conditions. , 2011, Journal of experimental botany.

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

[29]  E H Murchie,et al.  Agriculture and the new challenges for photosynthesis research. , 2009, The New phytologist.

[30]  Ray Leuning,et al.  Modelling Stomatal Behaviour and and Photosynthesis of Eucalyptus grandis , 1990 .

[31]  R. Voorrips.  MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.

[32]  D. Lawlor,et al.  Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. , 2002, Plant, cell & environment.

[33]  Gary Atlin,et al.  Response to two cycles of divergent selection for grain yield under drought stress in four rice breeding populations , 2008 .

[34]  R. Torres,et al.  QTLs for drought escape and tolerance identified in a set of random introgression lines of rice , 2005, Theoretical and Applied Genetics.

[35]  H. Nguyen,et al.  Genetic analysis of drought resistance in rice by molecular markers: association between secondary traits and field performance , 2003 .

[36]  P. Horton,et al.  Studies on the induction of chlorophyll fluorescence in barley protoplasts. II. Resolution of fluorescence quenching by redox state and the transthylakoid pH gradient , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[37]  I. E. Woodrow,et al.  A Model Predicting Stomatal Conductance and its Contribution to the Control of Photosynthesis under Different Environmental Conditions , 1987 .

[38]  D. Lawlor,et al.  Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP , 1999, Nature.

[39]  L. Stein,et al.  Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[40]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[41]  G. Farquhar,et al.  Effects of temperature, oxygen concentration, leaf age and seasonal variations on the CO2 compensation point of Lolium perenne L. , 1981, Planta.

[42]  Jian Jin,et al.  Development of Genome-Wide DNA Polymorphism Database for Map-Based Cloning of Rice Genes1[w] , 2004, Plant Physiology.

[43]  H. Nguyen,et al.  Breeding for Drought Resistance in Rice: Physiology and Molecular Genetics Considerations , 1997 .

[44]  F. V. van Eeuwijk,et al.  QTL analysis and QTL-based prediction of flowering phenology in recombinant inbred lines of barley. , 2005, Journal of experimental botany.

[45]  M. Yano,et al.  Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines , 2000, Theoretical and Applied Genetics.

[46]  J. Kervella,et al.  QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana , 2004, Theoretical and Applied Genetics.

[47]  A. Paterson,et al.  Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum population. , 1995, Genetics.

[48]  J. Li,et al.  Identification of QTLs affecting traits of agronomic importance in a recombinant inbred population derived from a subspecific rice cross , 1996, Theoretical and Applied Genetics.

[49]  Mark G. M. Aarts,et al.  Natural genetic variation in plant photosynthesis. , 2011, Trends in plant science.

[50]  I. R. Cowan.  Stomatal Behaviour and Environment , 1978 .

[51]  S. Rogers,et al.  Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues , 1985, Plant Molecular Biology.

[52]  C. Borror.  An Introduction to Statistical Methods and Data Analysis, 5th Ed. , 2002 .

[53]  Q. Zhang,et al.  The genetic basis of stay-green in rice analyzed in a population of doubled haploid lines derived from an indica by japonica cross , 2004, Theoretical and Applied Genetics.

[54]  Jianhua Zhang,et al.  Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants , 1999 .

[55]  M. Havaux.  Stress Tolerance of Photosystem II in Vivo: Antagonistic Effects of Water, Heat, and Photoinhibition Stresses. , 1992, Plant physiology.

[56]  S. Adachi,et al.  Identification and characterization of genomic regions on chromosomes 4 and 8 that control the rate of photosynthesis in rice leaves , 2011, Journal of experimental botany.

[57]  Olivier Panaud,et al.  Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice ( , 1996 .

[58]  H. Lafitte,et al.  Response to Direct Selection for Grain Yield under Drought Stress in Rice , 2007 .

[59]  D. Ort,et al.  Agu Laisk, Ladislav Nedbal, and Govindjee (eds): Photosynthesis in silico. Understanding complexity from molecules to ecosystems , 2010, Photosynthesis Research.

[60]  Yunbi Xu,et al.  Leaf-level water use efficiency determined by carbon isotope discrimination in rice seedlings: genetic variation associated with population structure and QTL mapping , 2009, Theoretical and Applied Genetics.

[61]  P. Sharma,et al.  Rainwater Utilization Efficiency in Rain-Fed Lowland Rice , 1994 .

[62]  J. Pereira,et al.  How plants cope with water stress in the field. Photosynthesis and growth. , 2002, Annals of botany.

[63]  R. Leuning.  A critical appraisal of a combined stomatal‐photosynthesis model for C3 plants , 1995 .

[64]  Zhikang Li,et al.  Mapping osmotic adjustment in an advanced back-cross inbred population of rice , 2003, Theoretical and Applied Genetics.

[65]  A. Reddy.  Fructose 2,6-bisphosphate-modulated photosynthesis in sorghum leaves grown under low water regimes , 1996 .

[66]  Yuan-Ming Zhang,et al.  Mapping quantitative trait loci for seed size traits in soybean (Glycine max L. Merr.) , 2011, Theoretical and Applied Genetics.

[67]  Ladislav Nedbal,et al.  Photosynthesis in silico : understanding complexity from molecules to ecosystems , 2009 .

[68]  R. A. Fischer,et al.  Breeding and Cereal Yield Progress , 2010 .

[69]  Kenneth L. McNally,et al.  Genetic Variation in Biomass Traits among 20 Diverse Rice Varieties1[W][OA] , 2010, Plant Physiology.

[70]  Arvind Kumar,et al.  Breeding for drought tolerance: Direct selection for yield, response to selection and use of drought-tolerant donors in upland and lowland-adapted populations , 2008 .

[71]  R. Jansen.  Genetic mapping of quantitative trait loci in plants : a novel statistical approach , 1995 .

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

[73]  Makoto Matsuoka,et al.  The role of QTLs in the breeding of high-yielding rice. , 2011, Trends in plant science.

[74]  T. Sharkey.  Advances in photosynthesis and respiration , 2012, Photosynthesis Research.

[75]  Yinghua Huang,et al.  An SSR genetic map of Sorghum bicolor (L.) Moench and its comparison to a published genetic map. , 2007, Genome.

[76]  M. Yano,et al.  Detection of a quantitative trait locus controlling carbon isotope discrimination and its contribution to stomatal conductance in japonica rice , 2009, Theoretical and Applied Genetics.

[77]  Peter Horton,et al.  Studies on the induction of chlorophyll fluorescence in barley protoplasts. I. Factors affecting the observation of oscillations in the yield of chlorophyll fluorescence and the rate of oxygen evolution , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[78]  Qian Qian,et al.  QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.) , 2004, Euphytica.

[79]  S. Tanksley,et al.  Fine mapping of a quantitative trait locus (QTL) from Lycopersicon hirsutum chromosome 1 affecting fruit characteristics and agronomic traits: breaking linkage among QTLs affecting different traits and dissection of heterosis for yield , 2000, Theoretical and Applied Genetics.

[80]  Xinyou Yin,et al.  The role of ecophysiological models in QTL analysis: the example of specific leaf area in barley , 1999, Heredity.

[81]  G. May,et al.  Similarity of QTLs detected for in vitro and greenhouse development of potato plants , 1999, Molecular Breeding.

[82]  L. Stein,et al.  Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.) (supplement). , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[83]  D. Zamir,et al.  Introgressions fromLycopersicon pennellii can improve the soluble-solids yield of tomato hybrids , 1994, Theoretical and Applied Genetics.

[84]  A. Kamińska,et al.  Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes. , 2006, Journal of experimental botany.

[85]  Hervé Cochard,et al.  Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. , 2002, Plant physiology.

[86]  N. Baker,et al.  Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components – calculation of qP and Fv-/Fm-; without measuring Fo-; , 1997, Photosynthesis Research.

[87]  B. Courtois,et al.  Yield response to water deficit in an upland rice mapping population: associations among traits and genetic markers , 2004, Theoretical and Applied Genetics.

[88]  Zhikang Li,et al.  QTLs affecting morph-physiological traits related to drought tolerance detected in overlapping introgression lines of rice (Oryza sativa L.) , 2008 .

[89]  N. Baker,et al.  A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves , 1984 .

[90]  N. Smirnoff,et al.  Environment and plant metabolism: flexibility and acclimation. , 1995 .