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Reproductive tissues-specific meta-QTLs and candidate genes for development of heat-tolerant rice cultivars

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By integrating genetics and genomics data, reproductive tissues-specific and heat stress responsive 35 meta-QTLs and 45 candidate genes were identified, which could be exploited through marker-assisted breeding for fast-track development of heat-tolerant rice cultivars.

Abstract

Rice holds the key to future food security. In rice-growing areas, temperature has already reached an optimum level for growth, hence, any further increase due to global climate change could significantly reduce rice yield. Several mapping studies have identified a plethora of reproductive tissue-specific and heat stress associated inconsistent quantitative trait loci (QTL), which could be exploited for improvement of heat tolerance. In this study, we performed a meta-analysis on previously reported QTLs and identified 35 most consistent meta-QTLs (MQTLs) across diverse genetic backgrounds and environments. Genetic and physical intervals of nearly 66% MQTLs were narrower than 5 cM and 2 Mb respectively, indicating hotspot genomic regions for heat tolerance. Comparative analyses of MQTLs underlying genes with microarray and RNA-seq based transcriptomic data sets revealed a core set of 45 heat-responsive genes, among which 24 were reproductive tissue-specific and have not been studied in detail before. Remarkably, all these genes corresponded to various stress associated functions, ranging from abiotic stress sensing to regulating plant stress responses, and included heat-shock genes (OsBiP2, OsMed37_1), transcription factors (OsNAS3, OsTEF1, OsWRKY10, OsWRKY21), transmembrane transporters (OsAAP7A, OsAMT2;1), sugar metabolizing (OsSUS4, α-Gal III) and abiotic stress (OsRCI2-7, SRWD1) genes. Functional data evidences from Arabidopsis heat-shock genes also suggest that OsBIP2 may be associated with thermotolerance of pollen tubes under heat stress conditions. Furthermore, promoters of identified genes were enriched with heat, dehydration, pollen and sugar responsive cis-acting regulatory elements, proposing a common regulatory mechanism might exist in rice for mitigating reproductive stage heat stress. These findings strongly support our results and provide new candidate genes for fast-track development of heat-tolerant rice cultivars.

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References

  • Akaike H (1998) A bayesian analysis of the minimum AIC procedure. Selected Papers of Hirotugu Akaike. Springer, Berling, pp 275–280

    Google Scholar 

  • Bahuguna RN, Jha J, Pal M, Shah D, Lawas LM, Khetarpal S, Jagadish KS (2015) Physiological and biochemical characterization of NERICA-L-44: a novel source of heat tolerance at the vegetative and reproductive stages in rice. Physiol Plant 154:543–559

    CAS  PubMed  Google Scholar 

  • Baniwal SK et al (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    CAS  PubMed  Google Scholar 

  • Bargsten JW, Nap J-P, Sanchez-Perez GF, van Dijk AD (2014) Prioritization of candidate genes in QTL regions based on associations between traits and biological processes. BMC Plant Biol 14:330

    PubMed  PubMed Central  Google Scholar 

  • Bashir K, Matsui A, Rasheed S, Seki M (2019) Recent advances in the characterization of plant transcriptomes in response to drought, salinity, heat, and cold stress. F1000 Res. https://doi.org/10.12688/f1000research.18424.1

    Article  Google Scholar 

  • Bhuria M, Goel P, Kumar S, Singh AK (2016) The promoter of AtUSP is co-regulated by phytohormones and abiotic stresses in Arabidopsis thaliana. Front Plant Sci 7:1957

    PubMed  PubMed Central  Google Scholar 

  • Buu BC et al (2014) Quantitative trait loci associated with heat tolerance in rice (Oryza sativa L.). Plant Breed Biotechnol 2:14–24

    Google Scholar 

  • Cao L, Zhao J, Zhan X, Li D, He L, Cheng S (2003) Mapping QTLs for heat tolerance and correlation between heat tolerance and photosynthetic rate in rice. Chin J Rice Sci 17:223–227

    CAS  Google Scholar 

  • Cao Z et al (2020) Fine mapping of the qHTB1–1 QTL, which confers heat tolerance at the booting stage, using an Oryza rufipogon Griff. introgression line. Theor Appl Genet 133:1161–1175

    CAS  PubMed  Google Scholar 

  • Cheng L-R et al (2012) Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice (Oryza sativa L.). J Integr Agric 11:359–367

    Google Scholar 

  • Confalonieri R, Rosenmund AS, Baruth B (2009) An improved model to simulate rice yield. Agron Sustain Dev 29:463–474

    Google Scholar 

  • Darvasi A, Soller M (1997) A simple method to calculate resolving power and confidence interval of QTL map location. Behav Genet 27:125–132

    CAS  PubMed  Google Scholar 

  • Darzi-Ramandi H, Shariati JV, Tavakol E, Najafi-Zarini H, Bilgrami SS, Razavi K (2017) Detection of consensus genomic regions associated with root architecture of bread wheat on groups 2 and 3 chromosomes using QTL meta-analysis. Aust J Crop Sci 11:777

    CAS  Google Scholar 

  • Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473

    CAS  PubMed  PubMed Central  Google Scholar 

  • González-Schain N et al (2016) Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties. Plant Cell Physiol 57:57–68

    PubMed  Google Scholar 

  • Hakata M, Wada H, Masumoto-Kubo C, Tanaka R, Sato H, Morita S (2017) Development of a new heat tolerance assay system for rice spikelet sterility. Plant Methods 13:34

    PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

    PubMed  PubMed Central  Google Scholar 

  • Hassani-Pak K, Castellote M, Esch M, Hindle M, Lysenko A, Taubert J, Rawlings C (2016) Developing integrated crop knowledge networks to advance candidate gene discovery. Appl Transl Genom 11:18–26

    PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    PubMed  PubMed Central  Google Scholar 

  • Hwang Y-S, Karrer E, Thomas B, Chen L, Rodriguez R (1998) Three cis-elements required for rice α-amylase Amy3D expression during sugar starvation. Plant Mol Biol 36:331–341

    CAS  PubMed  Google Scholar 

  • Jagadish S, Craufurd P, Wheeler T (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot 58:1627–1635

    CAS  PubMed  Google Scholar 

  • Jagadish S, Cairns J, Lafitte R, Wheeler TR, Price A, Craufurd PQ (2010a) Genetic analysis of heat tolerance at anthesis in rice. Crop Sci 50:1633–1641

    CAS  Google Scholar 

  • Jagadish S, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J, Craufurd PQ (2010b) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61:143–156

    CAS  PubMed  Google Scholar 

  • Jain M (2012) Next-generation sequencing technologies for gene expression profiling in plants. Brief Funct Genom 11:63–70

    CAS  Google Scholar 

  • Khahani B, Tavakol E, Shariati V (2019) Genome-wide meta-analysis on yield and yield-related QTLs in barley (Hordeum vulgare L.). Mol breed 39:56

    Google Scholar 

  • Kilasi NL, Singh J, Vallejos CE, Ye C, Jagadish S, Kusolwa P, Rathinasabapathi B (2018) Heat stress tolerance in rice (Oryza sativa L.): identification of quantitative trait loci and candidate genes for seedling growth under heat stress. Front Plant Sci 9:1578

    PubMed  PubMed Central  Google Scholar 

  • Krishnan P, Ramakrishnan B, Reddy KR, Reddy V (2011) High-temperature effects on rice growth, yield, and grain quality. Advances in agronomy, vol 111. Elsevier, Amsterdam, pp 87–206

    Google Scholar 

  • Lafarge T, Bueno C, Frouin J, Jacquin L, Courtois B, Ahmadi N (2017) Genome-wide association analysis for heat tolerance at flowering detected a large set of genes involved in adaptation to thermal and other stresses. PLoS ONE 12:e0171254

    PubMed  PubMed Central  Google Scholar 

  • Liu L, Mei Q, Yu Z, Sun T, Zhang Z, Chen M (2013) An integrative bioinformatics framework for genome-scale multiple level network reconstruction of rice. J Integr Bioinform 10:94–102

    Google Scholar 

  • Liu G et al (2020) Dynamic transcriptome analysis of anther response to heat stress during anthesis in thermotolerant rice (Oryza sativa L.). Int J Mol Sci 21:1155

    PubMed Central  Google Scholar 

  • Ma Z-X, Leng Y-J, Chen G-X, Zhou P-M, Ye D, Chen L-Q (2015) The thermosensitive male sterile 1 interacts with the BiPs via DnaJ domain and stimulates their ATPase enzyme activities in Arabidopsis. PloS one 10

  • Martinez AK, Soriano JM, Tuberosa R, Koumproglou R, Jahrmann T, Salvi S (2016) Yield QTLome distribution correlates with gene density in maize. Plant Sci 242:300–309

    CAS  PubMed  Google Scholar 

  • Maruyama A, Weerakoon W, Wakiyama Y, Ohba K (2013) Effects of increasing temperatures on spikelet fertility in different rice cultivars based on temperature gradient chamber experiments. J Agron Crop Sci 199:416–423

    Google Scholar 

  • Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7:e40899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Narusaka Y et al (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    CAS  PubMed  Google Scholar 

  • Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf K-D (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177

    CAS  PubMed  PubMed Central  Google Scholar 

  • O'Neill SD, Kumagai MH, Majumdar A, Huang N, Sutliff TD, Rodriguez RL (1990) The α-amylase genes in Oryza sativa: characterization of cDNA clones and mRNA expression during seed germination. Mol General Genet MGG 221:235–244

    CAS  Google Scholar 

  • Peraudeau S et al (2015) Effect of carbohydrates and night temperature on night respiration in rice. J Exp Bot 66:3931–3944

    CAS  PubMed  Google Scholar 

  • Poli Y et al (2013) Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits. Rice 6:36

    PubMed  PubMed Central  Google Scholar 

  • Prasad PV, Bheemanahalli R, Jagadish SK (2017) Field crops and the fear of heat stress—opportunities, challenges and future directions. Field Crops Res 200:114–121

    Google Scholar 

  • Qingquan C, Sibin Y, Chunhai L (2008) Identification of QTLs for heat tolerance at flowering stage in rice. Sci Agric Sin

  • Raza Q, Riaz A, Sabar M, Atif RM, Bashir K (2019) Meta-analysis of grain iron and zinc associated QTLs identified hotspot chromosomal regions and positional candidate genes for breeding biofortified rice. Plant Sci 288:110214

    CAS  PubMed  Google Scholar 

  • Rieping M, Schöffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco. Mol General Genet MGG 231:226–232

    CAS  Google Scholar 

  • Sakai H et al (2013) Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6–e6

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakurai H, Enoki Y (2010) Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression. FEBS J 277:4140–4149

    CAS  PubMed  Google Scholar 

  • Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Jpn J Crop Sci 47:6–17

    Google Scholar 

  • Sato Y et al (2011a) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:D1141–D1148

    CAS  PubMed  Google Scholar 

  • Sato Y et al (2011b) Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol 11:10

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scafaro AP, Atwell BJ, Muylaert S, Reusel BV, Ruiz GA, Rie JV, Gallé A (2018) A thermotolerant variant of Rubisco activase from a wild relative improves growth and seed yield in rice under heat stress. Front Plant Sci 9:1663

    PubMed  PubMed Central  Google Scholar 

  • Shah F, Huang J, Cui K, Nie L, Shah T, Chen C, Wang K (2011) Impact of high-temperature stress on rice plant and its traits related to tolerance. J Agric Sci 149:545–556

    CAS  Google Scholar 

  • Shanmugavadivel P, Sv AM, Prakash C, Ramkumar M, Tiwari R, Mohapatra T, Singh NK (2017) High resolution mapping of QTLs for heat tolerance in rice using a 5K SNP array. Rice 10:28

    Google Scholar 

  • Shanmugavadivel P, Prakash C, Mithra SA (2019) Molecular approaches for dissecting and improving drought and heat tolerance in rice. Advances in rice research for abiotic stress tolerance. Elsevier, Amsterdam, pp 839–867

    Google Scholar 

  • Sharma N, Russell SD, Bhalla PL, Singh MB (2011) Putative cis-regulatory elements in genes highly expressed in rice sperm cells. BMC Res Notes 4:319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh UM, Yadav S, Dixit S, Ramayya PJ, Devi MN, Raman KA, Kumar A (2017) QTL hotspots for early vigor and related traits under dry direct-seeded system in rice (Oryza sativa L.). Front Plant Sci 8:286

    PubMed  PubMed Central  Google Scholar 

  • Sosnowski O, Charcosset A, Joets J (2012) BioMercator V3: an upgrade of genetic map compilation and quantitative trait loci meta-analysis algorithms. Bioinformatics 28:2082–2083

    CAS  PubMed  PubMed Central  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Udawela U, Ananda G, Karunarathne S, Sooriyapathirana S, Li F, Liu Z (2018) Development of heat tolerant introgression lines and preliminary quantitative trait loci (QTL) analysis at flowering stage in Oryza sativa L. J Nat Sci Found Sri Lanka 46:253–270

    CAS  Google Scholar 

  • von Gromoff ED, Schroda M, Oster U, Beck CF (2006) Identification of a plastid response element that acts as an enhancer within the Chlamydomonas HSP70A promoter. Nucleic Acids Res 34:4767–4779

    Google Scholar 

  • Wilkins O et al (2016) EGRINs (environmental gene regulatory influence networks) in rice that function in the response to water deficit, high temperature, and agricultural environments. Plant Cell 28:2365–2384

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Y-H, Yi P, Luo L-H, Deng H-B, Zhang G-L, Tang W-B, Chen L-Y (2011a) Quantitative trait loci associated with pollen fertility under high temperature stress at flowering stage in rice (Oryza sativa). Rice Sci 18:204–209

    Google Scholar 

  • Xiao Y et al (2011b) Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice (Oryza sativa L.). Euphytica 178:331–338

    Google Scholar 

  • Yadav A et al (2020) Heat shock proteins: master players for heat-stress tolerance in plants during climate change. Heat stress tolerance in plants: physiological, molecular and genetic perspectives, 1st edn. Wiley, Hoboken, pp 189–211

    Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    CAS  PubMed  Google Scholar 

  • Yang KZ et al (2009) A mutation in Thermosensitive Male Sterile 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophytic male sterility in Arabidopsis. Plant J 57:870–882

    CAS  PubMed  Google Scholar 

  • Ye C et al (2012) Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breed 131:33–41

    CAS  Google Scholar 

  • Ye C et al (2015a) Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations. BMC Genet 16:41

    PubMed  PubMed Central  Google Scholar 

  • Ye C, Tenorio FA, Redoña ED, Morales-Cortezano PS, Cabrega GA, Jagadish KS, Gregorio GB (2015b) Fine-mapping and validating qHTSF4. 1 to increase spikelet fertility under heat stress at flowering in rice. Theor Appl Genet 128:1507–1517

    CAS  PubMed  Google Scholar 

  • Yin X, Kropff MJ, Goudriaan J (1996) Differential effects of day and night temperature on development to flowering in rice. Ann Bot 77:203–213

    Google Scholar 

  • Zhang T, Yang L, Jiang K, Huang M, Sun Q, Chen W, Zheng J (2008) QTL mapping for heat tolerance of the tassel period of rice. Mol Plant Breed 6:867–873

    CAS  Google Scholar 

  • Zhang G-L, Chen L-Y, Xiao G-Y, Xiao Y-H, Chen X-B, Zhang S-T (2009) Bulked segregant analysis to detect QTL related to heat tolerance in rice (Oryza sativa L.) using SSR markers. Agric Sci China 8:482–487

    CAS  Google Scholar 

  • Zhang X et al (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS ONE 7:e49652

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C et al (2018) Heat stress induces spikelet sterility in rice at anthesis through inhibition of pollen tube elongation interfering with auxin homeostasis in pollinated pistils. Rice 11:1–12

    Google Scholar 

  • Zhao Z, Jiang L, Xiao Y, Zhang W, Zhai H, Wan J (2006) Identification of QTLs for heat tolerance at the booting stage in rice (Oryza saliva L.). Zuo Wu Xue Bao 32:640–644

    CAS  Google Scholar 

  • Zhao L et al (2016) Mapping quantitative trait loci for heat tolerance at anthesis in rice using chromosomal segment substitution lines. Breed Sci. https://doi.org/10.1270/jsbbs.15084

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou H-W et al (2019) Discovery of unique single nucleotide polymorphisms in rice in response to high nighttime temperature stress using a hybrid sequencing strategy. Environ Exp Bot 162:48–57

    CAS  Google Scholar 

  • Zhu S, Huang R, Wai HP, Xiong H, Shen X, He H, Yan S (2017) Mapping quantitative trait loci for heat tolerance at the booting stage using chromosomal segment substitution lines in rice. Physiol Mol Biol Plants 23:817–825

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The authors wish to acknowledge financial support from Punjab Agricultural Research Board, Pakistan under competitive research project grant nos. PARB 770 & PARB 904.

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Authors and Affiliations

  1. Molecular Breeding Laboratory, Division of Plant Breeding and Genetics, Rice Research Institute, Kala Shah Kaku, Lahore, Punjab, Pakistan

    Qasim Raza, Awais Riaz & Muhammad Sabar

  2. Plant Genomic Network Research Team, Center for Sustainable Resource Science, RIKEN, Yokohama Campus, Yokohama, Japan

    Khurram Bashir

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  1. Qasim Raza
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  2. Awais Riaz
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  4. Muhammad Sabar
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Contributions

QR and AR conceived the idea. AR retrieved QTL data, genes information & expression data. QR conducted meta-analysis, drew figures and drafted the manuscript. KB and MS reviewed and edited the manuscript. MS planned the projects, acquired funding and coordinated the collaboration between project partners. All authors listed have made direct and substantial efforts for improving the manuscript and approved the final version.

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Correspondence to Qasim Raza.

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Raza, Q., Riaz, A., Bashir, K. et al. Reproductive tissues-specific meta-QTLs and candidate genes for development of heat-tolerant rice cultivars. Plant Mol Biol 104, 97–112 (2020). https://doi.org/10.1007/s11103-020-01027-6

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