High Resolution Mapping of QTLs for Heat Tolerance in Rice Using a 5K SNP Array

BackgroundHeat stress is one of the major abiotic threats to rice production, next to drought and salinity stress. Incidence of heat stress at reproductive phase of the crop results in abnormal pollination leading to floret sterility, low seed set and poor grain quality. Identification of QTLs and causal genes for heat stress tolerance at flowering will facilitate breeding for improved heat tolerance in rice. In the present study, we used 272 F8 recombinant inbred lines derived from a cross between Nagina22, a well-known heat tolerant Aus cultivar and IR64, a heat sensitive popular Indica rice variety to map the QTLs for heat tolerance.ResultsTo enable precise phenotyping for heat stress tolerance, we used a controlled phenotyping facility available at ICAR-Indian Institute of Wheat and Barley Research, Karnal, India. Based on ‘days to 50% flowering’ data of the RILs, we followed staggered sowing to synchronize flowering to impose heat stress at uniform stage. Using the Illumina infinium 5K SNP array for genotyping the parents and the RILs, and stress susceptibility and stress tolerance indices (SSI and STI) of percent spikelet sterility and yield per plant (g), we identified five QTLs on chromosomes 3, 5, 9 and 12. The identified QTLs explained phenotypic variation in the range of 6.27 to 21. 29%. Of these five QTLs, two high effect QTLs, one novel (qSTIPSS9.1) and one known (qSTIY5.1/qSSIY5.2), were mapped in less than 400 Kbp genomic regions, comprising of 65 and 54 genes, respectively.ConclusionsThe present study identified two major QTLs for heat tolerance in rice in narrow physical intervals, which can be employed for crop improvement by marker assisted selection (MAS) after development of suitable scorable markers for breeding of high yielding heat tolerant rice varieties. This is the first report of a major QTL for heat tolerance on chromosome 9 of rice. Further, a known QTL for heat tolerance on chromosome 5 was narrowed down from 23 Mb to 331 Kbp in this study.

[1]  Z. Tao,et al.  QTL mapping for heat tolerance of the tassel period of rice , 2008 .

[2]  C. Douglas,et al.  Role of Glycosyltransferases in Pollen Wall Primexine Formation and Exine Patterning1[OPEN] , 2016, Plant Physiology.

[3]  P. Craufurd,et al.  Genetic analysis of heat tolerance at anthesis in rice , 2010 .

[4]  L. H. Allen,et al.  Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress , 2006 .

[5]  T. G. Owens,et al.  Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Guoying Xiao,et al.  Bulked segregant analysis to detect QTL related to heat tolerance in rice (Oryza sativa L.) using SSR markers. , 2009 .

[7]  B. Williams,et al.  An Integrated Physical and Genetic Map of the Rice Genome , 2002, The Plant Cell Online.

[8]  D. Lobell,et al.  Climate Trends and Global Crop Production Since 1980 , 2011, Science.

[9]  Kenji Omasa,et al.  High Temperature-Induced Spikelet Sterility of Japonica Rice at Flowering in Relation to Air Temperature, Humidity and Wind Velocity Conditions , 1997 .

[10]  Lukas H. Meyer,et al.  Summary for Policymakers , 2022, The Ocean and Cryosphere in a Changing Climate.

[11]  Ashutosh Kumar Singh,et al.  Mapping QTLs for Salt Tolerance in Rice (Oryza sativa L.) by Bulked Segregant Analysis of Recombinant Inbred Lines Using 50K SNP Chip , 2016, PloS one.

[12]  Kanoe Sato,et al.  High Temperature Injury of Ripening in Rice Plant : V. On the barly decline of assimilate storing ability of grains at high temperature , 1976 .

[13]  S. R. Voleti,et al.  Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits , 2013, Rice.

[14]  M. Wolters-Arts,et al.  Ensuring Reproduction at High Temperatures: The Heat Stress Response during Anther and Pollen Development , 2013, Plants.

[15]  Dabing Zhang,et al.  PERSISTENT TAPETAL CELL1 Encodes a PHD-Finger Protein That Is Required for Tapetal Cell Death and Pollen Development in Rice1[C][W][OA] , 2011, Plant Physiology.

[16]  T. Mohapatra,et al.  EMS Induced Mutants of Upland Rice Variety Nagina22: Generation and Characterization , 2014 .

[17]  G. Gregorio,et al.  Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations , 2015, BMC Genetics.

[18]  Ling-hua Zhu,et al.  Genetic Analysis of Cold Tolerance at Seedling Stage and Heat Tolerance at Anthesis in Rice (Oryza sativa L.) , 2012 .

[19]  R. Fischer,et al.  Drought resistance in spring wheat cultivars, 1. Grain yield responses. , 1978 .

[20]  X. Qi,et al.  Characterization and Functional Analysis of the Potato Pollen-Specific Microtubule-Associated Protein SBgLR in Tobacco , 2013, PloS one.

[21]  P. Hussey,et al.  The Arabidopsis Microtubule-Associated Protein AtMAP65-1: Molecular Analysis of Its Microtubule Bundling Activity , 2004, The Plant Cell Online.

[22]  P. Craufurd,et al.  High temperature stress and spikelet fertility in rice (Oryza sativa L.). , 2007, Journal of experimental botany.

[23]  Yi Pan,et al.  Quantitative Trait Loci Associated with Pollen Fertility under High Temperature Stress at Flowering Stage in Rice (Oryza sativa) , 2011 .

[24]  K. Jung,et al.  Rice GLYCOSYLTRANSFERASE1 Encodes a Glycosyltransferase Essential for Pollen Wall Formation1[C][W][OA] , 2012, Plant Physiology.

[25]  Chandra Prakash,et al.  Unraveling the molecular basis of oxidative stress management in a drought tolerant rice genotype Nagina 22 , 2016, BMC Genomics.

[26]  H. Piepho,et al.  Drought yield index to select high yielding rice lines under different drought stress severities , 2012, Rice.

[27]  Caiyun Yang,et al.  MALE STERILITY1 Is Required for Tapetal Development and Pollen Wall Biosynthesis[W][OA] , 2007, The Plant Cell Online.

[28]  K. Omasa,et al.  Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. , 2002, Annals of botany.

[29]  H. L. Miller,et al.  Climate Change 2007: The Physical Science Basis , 2007 .

[30]  T. Matsui,et al.  QTL analyses for anther length and dehiscence at flowering as traits for the tolerance of extreme temperatures in rice (Oryza sativa L.) , 2014, Euphytica.

[31]  Atmakuri R. Rao,et al.  Genome-wide association mapping of salinity tolerance in rice (Oryza sativa) , 2015, DNA research : an international journal for rapid publication of reports on genes and genomes.

[32]  L. M. Lagrimini,et al.  Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions , 2015, Nature Biotechnology.

[33]  Hong Ma,et al.  The Rice Tapetum Degeneration Retardation Gene Is Required for Tapetum Degradation and Anther Development[W] , 2006, The Plant Cell Online.

[34]  X. Deng,et al.  Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice , 2011, Planta.

[35]  Lei Zhao,et al.  Mapping quantitative trait loci for heat tolerance at anthesis in rice using chromosomal segment substitution lines , 2016, Breeding science.

[36]  L. An,et al.  Annexin5 Plays a Vital Role in Arabidopsis Pollen Development via Ca2+-Dependent Membrane Trafficking , 2014, PloS one.

[37]  Inna Dubchak,et al.  Rice SNP-seek database update: new SNPs, indels, and queries , 2016, Nucleic Acids Res..

[38]  Yonghua Wang,et al.  Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. , 2008, Journal of genetics and genomics = Yi chuan xue bao.

[39]  C. China QTL IciMapping:Integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations , 2015 .

[40]  Zichao Li,et al.  Genetic variation in the sensitivity of anther dehiscence to drought stress in rice , 2006 .

[41]  Zhai Huqu,et al.  Mapping QTL for Heat-Tolerance at Grain Filling Stage in Rice , 2005 .

[42]  Nguyen Trong Phuoc,et al.  Quantitative Trait Loci Associated with Heat Tolerance in Rice (Oryza sativa L.) , 2013 .

[43]  Xia Li,et al.  Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses , 2014, Plant Cell Reports.

[44]  F. Rijsberman,et al.  More Crop Per Drop , 2007 .

[45]  R. Reuter,et al.  Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis , 2013, Mechanisms of Development.

[46]  Takeshi Horie,et al.  Effects of climate change on rice production and adaptive technologies , 2003 .

[47]  P. Craufurd,et al.  Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.) , 2009, Journal of experimental botany.

[48]  Fine mapping and candidate gene analysis of the novel thermo-sensitive genic male sterility tms9-1 gene in rice , 2014, Theoretical and Applied Genetics.

[49]  Mou Tong-min Identification of QTLs for Heat Tolerance at Flowering Stage in Rice , 2008 .

[50]  A. K. Mishra,et al.  Structure and regulatory networks of WD40 protein in plants , 2012, Journal of Plant Biochemistry and Biotechnology.

[51]  Emma Marris,et al.  Water: More crop per drop , 2008, Nature.

[52]  Lei Li,et al.  Comprehensive analyses of the annexin gene family in wheat , 2016, BMC Genomics.

[53]  K. Omasa,et al.  Rapid Swelling of Pollen Grains in Response to Floret Opening Unfolds Anther Locules in Rice (Oryza sativa L.) , 1999 .

[54]  Ashutosh Kumar Singh,et al.  Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryzasativa L.) , 2010, Molecular Genetics and Genomics.

[55]  P. Craufurd,et al.  Phenotyping Parents of Mapping Populations of Rice for Heat Tolerance during Anthesis , 2008 .

[56]  J. Thevelein,et al.  A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis , 2007, Planta.

[57]  Kanoe Sato,et al.  High Temperature Injury of ripening in rice plant : I. The effects of high temperature Treatments as different stages of panicle development on the ripening , 1973 .

[58]  C. Qingquan,et al.  Identification of QTLs for heat tolerance at flowering stage in rice , 2008 .

[59]  M. Wunderlich,et al.  Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis , 2004, Molecular Genetics and Genomics.

[60]  M. Thomson,et al.  Mapping QTL for heat tolerance at flowering stage in rice using SNP markers , 2012 .

[61]  Cao Liyong Mapping QTLs for Heat Tolerance and Correlation between Heat Tolerance and Photosynthetic Rate in Rice , 2003 .

[62]  Charles L. Guy,et al.  Exploring the Temperature-Stress Metabolome of Arabidopsis1[w] , 2004, Plant Physiology.

[63]  G. Fernandez Effective selection criteria for assessing plant stress tolerance , 1992 .

[64]  Guo‐Liang Wang,et al.  Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice (Oryza sativa L.) , 2011, Euphytica.

[65]  Caiguo Zhang,et al.  The Multifunctions of WD40 Proteins in Genome Integrity and Cell Cycle Progression , 2015, Journal of genomics.

[66]  Kenny Paul,et al.  Potato Annexin STANN1 Promotes Drought Tolerance and Mitigates Light Stress in Transgenic Solanum tuberosum L. Plants , 2015, PloS one.

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

[68]  J. Doyle,et al.  Isolation of plant DNA from fresh tissue , 1990 .