Multi-omics approaches for abiotic stress tolerance in rice (Oryza sativa L.)

Papanaboyina Archana; Pushpam Ramamoorthy; Manonmani Swaminathan; Raveendran Muthurajan; Senthil Alagarsamy; Pravin Kumar Kathiresan

doi:10.14719/pst.4843

Authors

Papanaboyina Archana Centre for Plant Breeding and Genetics, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0009-0002-5184-613X
Pushpam Ramamoorthy Centre for Plant Breeding and Genetics, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0000-0001-6991-6090
Manonmani Swaminathan Centre for Plant Breeding and Genetics, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0000-0003-3532-3363
Raveendran Muthurajan Directorate of Research, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0000-0002-8803-7662
Senthil Alagarsamy Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0000-0002-6438-8935
Pravin Kumar Kathiresan Centre for Plant Breeding and Genetics, Tamil Nadu Agricultural University, Coimbatore - 641003, Tamil Nadu, India https://orcid.org/0000-0003-2884-4291

DOI:

https://doi.org/10.14719/pst.4843

Keywords:

abiotic stress, genomics, proteomics, transcriptomics

Abstract

Rice, one of the world's staple crops, faces significant challenges due to abiotic stresses such as drought, salinity and extreme temperatures, which threaten global food security. Traditional breeding methods have limitations in developing stress-tolerant rice varieties within a short time frame. Thus, there is a growing interest in employing multi-omics approaches, integrating genomics, transcriptomics, proteomics, metabolomics and epigenomics, to unravel the complex molecular mechanisms underlying abiotic stress tolerance in rice. In contrast to a single-omics method, this combination of multi-dimensional approaches provides an extensive understanding of cellular dynamics under abiotic stress conditions. This review discusses recent advances in multi-omics technologies and their applications in dissecting the molecular responses of rice to abiotic stresses. It highlights the integration of multi-omics data to identify critical genes, pathways and regulatory networks involved in stress responses and tolerance mechanisms.
Furthermore, it explores the potential of multi-omics-assisted breeding strategies for developing stress-tolerant rice varieties with improved agronomic traits. The challenges and future perspectives in utilizing multi-omics approaches to enhance rice's abiotic stress tolerance are also discussed. Overall, multi-omics approaches offer a comprehensive platform to understand the molecular basis of stress tolerance in rice and accelerate the development of resilient varieties to ensure global food security.

Downloads

Download data is not yet available.

References

Pradhan SK, Pandit E, Pawar S, Baksh SY, Mukherjee AK, Mohanty SP. Development of flash-flood tolerant and durable bacterial blight resistant versions of mega rice variety 'Swarna ’ through marker-assisted backcross breeding. Scientific Reports. 2019 Sep 5;9(1):12810. https://doi.org/10.1038/s41598-019-49176-z

Gregorio GB, Islam MR, Vergara GV, Thirumeni S. Recent advances in rice science to design salinity and other abiotic stress-tolerant rice varieties. https://www.researchgate.net/profile/SaminadaneThirumeni2/publication/282365544_sabrao_2013_45-1_31-41/links/560eb4ee08ae4833751713e9/sabrao-2013-45-1-31-41.pdf

Zhang H, Li Y, Zhu JK. Developing naturally stress-resistant crops for a sustainable agriculture. Nature Plants. 2018 Dec;4(12):989-96. https://doi.org/10.1038/s41477-018-0309-4

Singh N, Choudhury DR, Tiwari G, Singh AK, Kumar S, Srinivasan K, Tyagi RK, Sharma AD, Singh NK, Singh R. Genetic diversity trend in Indian rice varieties: an analysis using SSR markers. BMC Genetics. 2016 Dec;17:1-3. https://doi.org/10.1186/s12863-016-0437-7

Farooq M, Hussain M, Wahid A, Siddique KH. Drought stress in plants: an overview. In: Plant responses to droughT stress: From morphological to molecular features. Aroca, R. (eds) Plant Responses to Drought Stress. Springer, Berlin, Heidelberg. 2012:1-33. https://doi.org/10.1007/978-3-642-32653-0_1

Hassan MA, Dahu N, Hongning T, Qian Z, Yueming Y, Yiru L, Shimei W. Drought stress in rice: morpho-physiological and molecular responses and marker-assisted breeding. Frontiers in Plant Science.2023 Jul 18;14:1215371. https://doi.org/10.3389/fpls.2023.1215371

Samarah NH. Understanding how plants respond to drought stress at the molecular and whole plant levels. Drought Stress Tolerance in Plants, Vol 2: Molecular and Genetic Perspectives. 2016:1-37. https://doi.org/10.1007/978-3-319-32423-4_1

Bui LT, Ella ES, Dionisio-Sese ML, Ismail AM. Morpho-physiological changes in roots of rice seedling upon submergence. Rice Science. 2019 May 1;26(3):167-77. https://doi.org/10.1016/j.rsci.2019.04.003

Yan T, Sun M, Su R, Wang X, Lu X, Xiao Y, Deng H, Liu X, Tang W, Zhang G. Transcriptomic profiling of cold stress-induced differentially expressed genes in seedling stage of Indica rice. Plants. 2023 Jul 17;12(14):2675. https://doi.org/10.3390/plants12142675

Agarwal PK, Agarwal P, Reddy MK, Sopory SK. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports. 2006 Dec;25:1263-74. https://doi.org/10.1007/s00299-006-0204-8

Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP. Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. Journal of Experimental Botany. 2014 Nov 1;65(21):6265-78. https://doi.org/10.1093/jxb/eru363

Gregoria GB, Senadhira D, Mendoza RD. Screening rice for salinity tolerance. https://ageconsearch.umn.edu/record/287589/files/Gregorio.pdf

Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics. 2005 Oct 1;37(10):1141-6. https://doi.org/10.1038/ng1643

Huang YN, Yang SY, Li JL, Wang SF, Wang JJ, Hao DL, Su YH. The rectification control and physiological relevance of potassium channel OsAKT2. Plant Physiology. 2021 Dec 1;187(4):2296-310. https://doi.org/10.1093/plphys/kiab462

Xu Y, Chu C, Yao S. The impact of high-temperature stress on rice: Challenges and solutions. The Crop Journal. 2021 Oct 1;9(5):963-76. https://doi.org/10.1016/j.cj.2021.02.011

Melo FV, Oliveira MM, Saibo NJ, Lourenço TF. Modulation of abiotic stress responses in rice by E3-ubiquitin ligases: a promising way to develop stress-tolerant crops. Frontiers in Plant Science. 2021 Mar 23;12:640193. https://doi.org/10.3389/fpls.2021.640193

Song Y, Ai C rui, Jing S juan, Yu D qiu. Research Progress on Functional Analysis of Rice WRKY Genes. Rice Sci. 2010 Mar;17(1):60–72. https://doi.org/10.1016/S1672-6308(08)60105-5

Liu H, Timko MP. Jasmonic acid signaling and molecular crosstalk with other phytohormones. International Journal of Molecular Sciences. 2021 Mar 13;22(6):2914. https://doi.org/10.3390/ijms22062914

Nuruzzaman M, Sharoni AM, Satoh K, Karim MR, Harikrishna JA, Shimizu T, Sasaya T, Omura T, Haque MA, Hasan SM, Ahmad A. NAC transcription factor family genes are differentially expressed in rice during infections with Rice dwarf virus, rice black-streaked dwarf virus, Rice grassy stunt virus, Rice ragged stunt virus, and Rice transitory yellowing virus. Frontiers in Plant Science. 2015 Sep 9;6:676. https://doi.org/10.3389/fpls.2015.00676

Liu P, Wu X, Gong B, Lü G, Li J, Gao H. Review of the mechanisms by which transcription factors and exogenous substances regulate ROS metabolism under abiotic stress. Antioxidants. 2022 Oct 25;11(11):2106. https://doi.org/10.3390/antiox11112106

Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi?Shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought?, high?salt?and cold?responsive gene expression. The Plant Journal. 2003 Feb;33(4):751-63. https://doi.org/10.1046/j.1365-313X.2003.01661.x

Wani SH, Kumar V, Shriram V, Sah SK. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. The Crop Journal. 2016 Jun 1;4(3):162-76. https://doi.org/10.1016/j.cj.2016.01.010

Feng LY, Lin PF, Xu RJ, Kang HQ, Gao LZ. Comparative Genomic Analysis of Asian Cultivated Rice and Its Wild Progenitor (Oryza rufipogon) Has Revealed Evolutionary Innovation of the Pentatricopeptide Repeat Gene Family through Gene Duplication. International Journal of Molecular Sciences. 2023 Nov 14;24(22):16313. https://doi.org/10.3390/ijms242216313

Chen G, Zou Y, Hu J, Ding Y. Genome-wide analysis of the rice PPR gene family and their expression profiles under different stress treatments. BMC genomics. 2018 Dec;19:1-4. https://doi.org/10.1186/s12864-018-5088-9

Barkan A, Small I. Pentatricopeptide repeat proteins in plants. Annual review of Plant Biology. 2014 Apr 29;65(1):415-42. https://doi.org/10.1146/annurev-arplant-050213-040159

Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends in Plant Science. 2008 Dec 1;13(12):663-70. https://doi.org/10.1016/j.tplants.2008.10.001

Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T. Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. The Plant Cell. 2009 Jan 1;21(1):146-56. https://doi.org/10.1105/tpc.108.064667

Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A. RNA editing in plants and its evolution. Annual Review of Genetics. 2013 Nov 23;47(1):335-52. https://doi.org/10.1146/annurev-genet-111212-133519

Chateigner?Boutin AL, Ramos?Vega M, Guevara?García A, Andrés C, De La Luz Gutiérrez?Nava M, Cantero A, Delannoy E, Jiménez LF, Lurin C, Small I, León P. CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. The Plant Journal. 2008 Nov;56(4):590-602. https://doi.org/10.1111/j.1365-313X.2008.03634.x

Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. The Plant Cell. 2003 Jun 1;15(6):1480-95. https://doi.org/10.1105/tpc.010397

Singh DK, Mehra S, Chatterjee S, Purty RS. In silico identification and validation of miRNA and their DIR specific targets in Oryza sativa Indica under abiotic stress. Non-coding RNA Research. 2020 Dec 1;5(4):167-77. https://doi.org/10.1016/j.ncrna.2020.09.002

Liao Y, Liu S, Jiang Y, Hu C, Zhang X, Cao X, Xu Z, Gao X, Li L, Zhu J, Chen R. Genome-wide analysis and environmental response profiling of dirigent family genes in rice (Oryza sativa). Genes & Genomics. 2017 Jan;39:47-62. https://doi.org/10.1007/s13258-016-0474-7

Davin LB, Lewis NG. Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiology. 2000 Jun 1;123(2):453-62. https://doi.org/10.1104/pp.123.2.453

Moura JC, Bonine CA, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P. Abiotic and biotic stresses and changes in the lignin content and composition in plants. Journal of integrative Plant Biology. 2010 Apr;52(4):360-76. https://doi.org/10.1111/j.1744-7909.2010.00892.x

Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S. Salinity induced physiological and biochemical changes in plants: An omic approach towards salt stress tolerance. Plant Physiology and Biochemistry. 2020 Nov 1;156:64-77. https://doi.org/10.1016/j.plaphy.2020.08.042

Kovacs D, Kalmar E, Torok Z, Tompa P. Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiology. 2008 May 1;147(1):381-90. https://doi.org/10.1104/pp.108.118208

Hara M. The multifunctionality of dehydrins: an overview. Plant Signaling & Behavior. 2010 May 1;5(5):503-8. https://doi.org/10.4161/psb.11085

Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR. Characterization of an abiotic stress-inducible dehydrin gene, OsDhn1, in rice (Oryza sativa L.). Molecules and cells. 2005 Apr 1;19(2):212-8. https://doi.org/10.1016/S1016-8478(23)13158-X

Verma G, Dhar YV, Srivastava D, Kidwai M, Chauhan PS, Bag SK, Asif MH, Chakrabarty D. Genome-wide analysis of rice dehydrin gene family: Its evolutionary conservedness and expression pattern in response to PEG induced dehydration stress. PLoS One. 2017 May 1;12(5):e0176399. https://doi.org/10.1371/journal.pone.0176399

Du Z, Su Q, Wu Z, Huang Z, Bao J, Li J, Tu H, Zeng C, Fu J, He H. Genome-wide characterization of MATE gene family and expression profiles in response to abiotic stresses in rice (Oryza sativa). BMC Ecology and Evolution. 2021 Dec;21:1-4. https://doi.org/10.1186/s12862-021-01873-y

Yokosho K, Yamaji N, Ma JF. An Al?inducible MATE gene is involved in external detoxification of Al in rice. The Plant Journal. 2011 Dec;68(6):1061-9. https://doi.org/10.1111/j.1365-313X.2011.04757.x

Ding X, Hou X, Xie K, Xiong L. Genome-wide identification of BURP domain-containing genes in rice reveals a gene family with diverse structures and responses to abiotic stresses. Planta. 2009 Jun;230:149-63. https://doi.org/10.1007/s00425-009-0929-z

Ganie SA, Molla KA, Henry RJ, Bhat KV, Mondal TK. Advances in understanding salt tolerance in rice. Theoretical and Applied Genetics. 2019 Apr 1;132:851-70. https://doi.org/10.1007/s00122-019-03301-8

Moin M, Bakshi A, Madhav MS, Kirti PB. Expression profiling of ribosomal protein gene family in dehydration stress responses and characterization of transgenic rice plants overexpressing RPL23A for water-use efficiency and tolerance to drought and salt stresses. Frontiers in Chemistry. 2017 Nov 14;5:97. https://doi.org/10.3389/fchem.2017.00097

Moin M, Saha A, Bakshi A, Madhav MS, Kirti PB. Ribosomal Protein Large subunit RPL6 modulates salt tolerance in rice. bioRxiv. 2020 May 31:2020-05. https://doi.org/10.1101/2020.05.31.126102

Zanetti ME, Chang IF, Gong F, Galbraith DW, Bailey-Serres J. Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiology. 2005 Jun 1;138(2):624-35. https://doi.org/10.1104/pp.105.059477

Singh RK, Sood P, Prasad A, Prasad M. Advances in omics technology for improving crop yield and stress resilience. Plant Breeding. 2021 Oct;140(5):719-31. https://doi.org/10.1111/pbr.12963

Zhou X, Bai X, Xing Y. A rice genetic improvement boom by next-generation sequencing. Current Issues in Molecular Biology. 2018 Jul;27(1):109-26. https://doi.org/10.21775/cimb.027.109

Yang Y, Saand MA, Huang L, Abdelaal WB, Zhang J, Wu Y, Li J, Sirohi MH, Wang F. Applications of multi-omics technologies for crop improvement. Frontiers in Plant Science. 2021 Sep 3;12:563953. https://doi.org/10.3389/fpls.2021.563953

Sinclair TR. Challenges in breeding for yield increase for drought. Trends in plant science. 2011 Jun 1;16(6):289-93. https://doi.org/10.1016/j.tplants.2011.02.008

Collard BC, Mackill DJ. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences. 2008 Feb 12;363(1491):557-72. https://doi.org/10.1098/rstb.2007.2170

Wang SC. Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. 2012.

Jiang C, Wang Y, Zhou J, Rashid MA, Li Y, Peng Y, Xie L, Zhou G, He Y, Sun W, Zheng C. Genome-Wide Scan for Genetic Signatures Based on the Whole-Genome Resequencing of Salt-and Drought-Tolerant Rice Varieties. Agronomy. 2023 Jul 22;13(7):1936. https://doi.org/10.3390/agronomy13071936

Wang N, Gao Z, Zhang W, Qian Y, Bai D, Zhao X, Bao Y, Zheng Z, Wang X, Li J, Wang W. Genome-Wide association analysis reveals the gene loci of yield traits under drought stress at the rice reproductive stage. Agronomy. 2023 Aug 10;13(8):2096. https://doi.org/10.3390/agronomy13082096

Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, et al. Genetic Basis of Drought Resistance at Reproductive Stage in Rice: Separation of Drought Tolerance From Drought Avoidance. Genetics. 2006 Feb 1;172(2):1213–28. https://doi.org/10.1534/genetics.105.045062

Jiang Y, Wang X, Yu X, Zhao X, Luo N, Pei Z, et al. Quantitative Trait Loci Associated with Drought Tolerance in Brachypodium distachyon. Front Plant Sci. 2017 May 17;8:811. https://doi.org/10.3389/fpls.2017.00811

Zhao XQ, Xu JL, Zhao M, Lafitte R, Zhu LH, Fu BY, Gao YM, Li ZK. QTLs affecting morph-physiological traits related to drought tolerance detected in overlapping introgression lines of rice (Oryza sativa L.). Plant Science. 2008 Jun 1;174(6):618-25. https://doi.org/10.1016/j.plantsci.2008.03.009

Subudhi PK, Shankar R, Jain M. Whole genome sequence analysis of rice genotypes with contrasting response to salinity stress. Scientific Reports. 2020 Dec 4;10(1):21259. https://doi.org/10.1038/s41598-020-78256-8

Nagai K, Mori Y, Ishikawa S, Furuta T, Gamuyao R, Niimi Y, Hobo T, Fukuda M, Kojima M, Takebayashi Y, Fukushima A. Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature. 2020 Aug 6;584(7819):109-14. https://doi.org/10.1038/s41586-020-2501-8

Xu S, Cui J, Cao H, Liang S, Ma T, Liu H, et al. Identification of candidate genes for salinity tolerance in Japon Xu S, Cui J, Cao H, Liang S, Ma T, Liu H, Wang J, Yang L, Xin W, Jia Y, Zou D. Identification of candidate genes for salinity tolerance in Japonica rice at the seedling stage based on genome-wide association study and linkage mapping. Frontiers in Plant Science. 2023 May 10;14:1184416. https://doi.org/10.3389/fpls.2023.1184416

Chen T, Shabala S, Niu Y, Chen ZH, Shabala L, Meinke H, Venkataraman G, Pareek A, Xu J, Zhou M. Molecular mechanisms of salinity tolerance in rice. The Crop Journal. 2021 Jun 1;9(3):506-20. https://doi.org/10.1016/j.cj.2021.03.005

Morimoto RI. The heat shock response: systems biology of proteotoxic stress in aging and disease. InCold Spring Harbor symposia on quantitative biology 2011 Jan 1 (Vol. 76, pp. 91-99). Cold Spring Harbor Laboratory Press. https://doi.org/10.1101/sqb.2012.76.010637

Barna J, Csermely P, Vellai T. Roles of heat shock factor 1 beyond the heat shock response. Cellular and Molecular Life Sciences. 2018 Aug;75:2897-916. https://doi.org/10.1007/s00018-018-2836-6

Wu C. Heat shock transcription factors: structure and regulation. Annual Review of Cell and Developmental Biology. 1995 Nov;11(1):441-69. https://doi.org/10.1146/annurev.cellbio.11.1.441

Chauhan H, Khurana N, Agarwal P, Khurana P. Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Molecular Genetics and Genomics. 2011 Aug;286:171-87. https://doi.org/10.1007/s00438-011-0638-8

Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature. 2006 Aug 10;442(7103):705-8. https://doi.org/10.1038/nature04920

Pervaiz T, Amjid MW, El-Kereamy A, Niu SH, Wu HX. MicroRNA and cDNA-microarray as potential targets against abiotic stress response in plants: Advances and prospects. Agronomy. 2021 Dec 22;12(1):11. https://doi.org/10.3390/agronomy12010011

Ismail AM, Singh US, Singh S, Dar MH, Mackill DJ. The contribution of submergence-tolerant (Sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. Field Crops Research. 2013 Oct 1;152:83-93. https://doi.org/10.1016/j.fcr.2013.01.007

Mackill DJ, Ismail AM, Singh US, Labios RV, Paris TR. Development and rapid adoption of submergence-tolerant (Sub1) rice varieties. Advances in Agronomy. 2012 Jan 1;115:299-352. https://doi.org/10.1016/B978-0-12-394276-0.00006-8

Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics. 2009 Jan;10(1):57-63. https://doi.org/10.1038/nrg2484

Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szcze?niak MW, Gaffney DJ, Elo LL, Zhang X, Mortazavi A. A survey of best practices for RNA-seq data analysis. Genome biology. 2016 Dec;17:1-9. https://doi.org/10.1186/s13059-016-0881-8

Mochida K, Shinozaki K. Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant and Cell Physiology. 2011 Dec 1;52(12):2017-38. https://doi.org/10.1093/pcp/pcr153

Wei H, Wang X, Zhang Z, Yang L, Zhang Q, Li Y, He H, Chen D, Zhang B, Zheng C, Leng Y. Uncovering key salt-tolerant regulators through a combined eQTL and GWAS analysis using the super pan-genome in rice. National Science Review. 2024 Apr;11(4):nwae043. https://doi.org/10.1093/nsr/nwae043

Kong W, Zhang C, Zhang S, Qiang Y, Zhang Y, Zhong H, Li Y. Uncovering the novel QTLs and candidate genes of salt tolerance in rice with linkage mapping, RTM-GWAS, and RNA-seq. Rice. 2021 Dec;14:1-2. https://doi.org/10.1186/s12284-021-00535-3

Kazemitabar SK, Tomsett AB, Collin HA, Wilkinson MC, Jones MG. Effect of short term cold stress on rice seedlings. Euphytica. 2003 Jan;129:193-200. https://doi.org/10.1023/A:1021975118340

Arshad MS, Farooq M, Asch F, Krishna JS, Prasad PV, Siddique KH. Thermal stress impacts reproductive development and grain yield in rice. Plant Physiology and Biochemistry. 2017 Jun 1;115:57-72. https://doi.org/10.1016/j.plaphy.2017.03.011

Guan S, Xu Q, Ma D, Zhang W, Xu Z, Zhao M, Guo Z. Transcriptomics profiling in response to cold stress in cultivated rice and weedy rice. Gene. 2019 Feb 15;685:96-105. https://doi.org/10.1016/j.gene.2018.10.066

Jagadish SV, Murty MV, Quick WP. Rice responses to rising temperatures–challenges, perspectives and future directions. Plant, Cell & Environment. 2015 Sep;38(9):1686-98. https://doi.org/10.1111/pce.12430

Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand JL. Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of sciences. 2017 Aug 29;114(35):9326-31. https://doi.org/10.1073/pnas.1701762114

Wei Z, Yuan Q, Lin H, Li X, Zhang C, Gao H, Zhang B, He H, Liu T, Jie Z, Gao X. Linkage analysis, GWAS, transcriptome analysis to identify candidate genes for rice seedlings in response to high temperature stress. BMC Plant Biology. 2021 Dec;21:1-3. https://doi.org/10.1186/s12870-021-02857-2

Yang Y, Zhang C, Zhu D, He H, Wei Z, Yuan Q, Li X, Gao X, Zhang B, Gao H, Wang B. Identifying candidate genes and patterns of heat-stress response in rice using a genome-wide association study and transcriptome analyses. The Crop Journal. 2022 Dec 1;10(6):1633-43. https://doi.org/10.1016/j.cj.2022.02.011

Yoo YH, Nalini Chandran AK, Park JC, Gho YS, Lee SW, An G, Jung KH. OsPhyB-mediating novel regulatory pathway for drought tolerance in rice root identified by a global RNA-Seq transcriptome analysis of rice genes in response to water deficiencies. Frontiers in Plant Science. 2017 Apr 26;8:580. https://doi.org/10.3389/fpls.2017.00580

Kong W, Zhong H, Gong Z, Fang X, Sun T, Deng X, Li Y. Meta-analysis of salt stress transcriptome responses in different rice genotypes at the seedling stage. Plants. 2019 Mar 12;8(3):64. https://doi.org/10.3390/plants8030064

Smita S, Katiyar A, Lenka SK, Dalal M, Kumar A, Mahtha SK, Yadav G, Chinnusamy V, Pandey DM, Bansal KC. Gene network modules associated with abiotic stress response in tolerant rice genotypes identified by transcriptome meta-analysis. Functional & integrative genomics. 2020 Jan;20:29-49. https://doi.org/10.1007/s10142-019-00697-w

Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J. Proteomic analysis of rice leaves during drought stress and recovery. Proteomics: International Edition. 2002 Sep;2(9):1131-45. https://doi.org/10.1002/1615-9861(200209)2:9%3C1131::AID-PROT1131%3E3.0.CO;2-1

Muthurajan R, Shobbar ZS, Jagadish SV, Bruskiewich R, Ismail A, Leung H, Bennett J. Physiological and proteomic responses of rice peduncles to drought stress. Molecular biotechnology. 2011 Jun;48:173-82. https://doi.org/10.1007/s12033-010-9358-2

Raorane ML, Pabuayon IM, Varadarajan AR, Mutte SK, Kumar A, Treumann A, Kohli A. Proteomic insights into the role of the large-effect QTL qDTY 12.1 for rice yield under drought. Molecular Breeding. 2015 Jun;35:1-4. https://doi.org/10.1007/s11032-015-0321-6

Lakra N, Kaur C, Singla-Pareek SL, Pareek A. Mapping the ‘early salinity response’triggered proteome adaptation in contrasting rice genotypes using iTRAQ approach. Rice. 2019 Dec;12:1-22. https://doi.org/10.1186/s12284-018-0259-5

López-Cristoffanini, C., Bundó, M., Serrat, X., San Segundo, B., López-Carbonell, M. and Nogués, S., 2021. A comprehensive study of the proteins involved in salinity stress response in roots and shoots of the FL478 genotype of rice (Oryza sativa L. ssp. indica). The Crop Journal, 9(5), pp.1154-1168. https://doi.org/10.1016/j.cj.2020.10.009

Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ. Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC plant biology. 2011 Dec;11:1-5. https://doi.org/10.1186/1471-2229-11-34

Kumar N, Suyal DC, Sharma IP, Verma A, Singh H. Elucidating stress proteins in rice (Oryza sativa L.) genotype under elevated temperature: a proteomic approach to understand heat stress response. 3 Biotech. 2017 Jul;7(3):205. https://doi.org/10.1007/s13205-017-0856-9

Zhou H, Wang X, Huo C, Wang H, An Z, Sun D, Liu J, Tang W, Zhang B. A Quantitative Proteomics Study of Early Heat?Regulated Proteins by Two?Dimensional Difference Gel Electrophoresis Identified OsUBP21 as a Negative Regulator of Heat Stress Responses in Rice. Proteomics. 2019 Oct;19(20):1900153. https://doi.org/10.1002/pmic.201900153

Timabud T, Yin X, Pongdontri P, Komatsu S. Gel-free/label-free proteomic analysis of developing rice grains under heat stress. Journal of proteomics. 2016 Feb 5;133:1-9. https://doi.org/10.1016/j.jprot.2015.12.003

Ji L, Zhou P, Zhu Y, Liu F, Li R, Qiu Y. Proteomic analysis of rice seedlings under cold stress. The protein journal. 2017 Aug;36:299-307. https://doi.org/10.1007/s10930-017-9721-2

Wang J, Wang J, Wang X, Li R, Chen B. Proteomic response of hybrid wild rice to cold stress at the seedling stage. PLoS One. 2018 Jun 7;13(6):e0198675. https://doi.org/10.1371/journal.pone.0198675

Zhang Z, Xiao W, Qiu J, Xin Y, Liu Q, Chen H, Fu Y, Ma H, Chen W, Huang Y, Ruan S. Nystose regulates the response of rice roots to cold stress via multiple signaling pathways: A comparative proteomics analysis. Plos one. 2020 Sep 3;15(9):e0238381. https://doi.org/10.1371/journal.pone.0238381

Wang X, Zhang H, Shao LY, Yan X, Peng H, Ouyang JX, Li SB. Expression and function analysis of a rice OsHSP40 gene under salt stress. Genes & genomics. 2019 Feb 8;41:175-82. https://doi.org/10.1007/s13258-018-0749-2

Hwang SG, Lee SC, Lee J, Lee JW, Kim JH, Choi SY, Kim JB, Choi HI, Jang CS. Resequencing of a core rice mutant population induced by gamma-ray irradiation and its application in a genome-wide association study. Journal of Plant Biology. 2020 Dec;63:463-72. https://doi.org/10.1007/s12374-020-09266-2

Yoon DH, Lee SS, Park HJ, Lyu JI, Chong WS, Liu JR, Kim BG, Ahn JC, Cho HS. Overexpression of OsCYP19-4 increases tolerance to cold stress and enhances grain yield in rice (Oryza sativa). Journal of Experimental Botany. 2016 Jan 1;67(1):69-82. https://doi.org/10.1093/jxb/erv421

Hwang JE, Jang DS, Lee KJ, Ahn JW, Kim SH, Kang SY, Kim DS, Kim JB. Identification of gamma ray irradiation-induced mutations in membrane transport genes in a rice population by TILLING. Genes & Genetic Systems. 2016 Oct 1;91(5):245-56. https://doi.org/10.1266/ggs.15-00052

Li C, Lu C, Yang M, Wu G, Nyasulu M, He H, He X, Bian J. Uncovering Novel QTLs and Candidate Genes for Salt Tolerance at the Bud Burst Stage in Rice through Genome-Wide Association Study. Plants. 2024 Jan 8;13(2):174. https://doi.org/10.3390/plants13020174

Santosh Kumar VV, Verma RK, Yadav SK, Yadav P, Watts A, Rao MV, Chinnusamy V. CRISPR-Cas9 mediated genome editing of drought and salt tolerance (OsDST) gene in indica mega rice cultivar MTU1010. Physiology and Molecular Biology of Plants. 2020 Jun;26:1099-110. https://doi.org/10.1007/s12298-020-00819-w

Zhou L, Liu Z, Liu Y, Kong D, Li T, Yu S, Mei H, Xu X, Liu H, Chen L, Luo L. A novel gene OsAHL1 improves both drought avoidance and drought tolerance in rice. Scientific reports. 2016 Jul 25;6(1):30264. https://doi.org/10.1038/srep30264

Duan J, Cai W. OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. https://doi.org/10.1371/journal.pone.0045117

Kim SJ, Jeong DH, An G, Kim SR. Characterization of a drought-responsive gene, OsTPS1, identified by the T-DNA gene-trap system in rice. Journal of Plant Biology. 2005 Dec;48:371-9. https://doi.org/10.1007/BF03030578

Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y. CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Frontiers in Plant Science. 2017 Sep 13;8:1598. https://doi.org/10.3389/fpls.2017.01598

Koh S, Lee SC, Kim MK, Koh JH, Lee S, An G, Choe S, Kim SR. T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant molecular biology. 2007 Nov;65:453-66. https://doi.org/10.1007/s11103-007-9213-4

Wang Hh, Naredo ME, Wu JL, Till BJ, Greene EA, Henikoff S, Comai L, Leung H, Mcnally KL. EcoTILLING candidate genes for drought tolerance in rice. Resilient Crops for Water Limited Environments. 2004:75. https://books.google.co.in/books?id=APR1jfhrhfkC&lpg=PA75&ots=ldagc8GR4p&dq=Wang%20HH%2C%20Naredo%20ME%2C%20Wu%20JL%2C%20Till%20BJ%2C%20Greene%20EA%2C%20HENIKOFF%20S%2C%20COMAI%20L%2C%20LEUNG%20H%2C%20MCNALLY%20KL.%20EcoTILLING%20candidate%20genes%20for%20drought%20tolerance%20in%20rice.%20Resilient%20Crops%20for%20Water%20Limited%20Environments.%202004%3A75.&lr&pg=PA69#v=onepage&q&f=false

Casella L, Greco R, Bruschi G, Wozniak B, Dreni L, Kater M, Cavigiolo S, Lupotto E, Piffanelli P. TILLING in European rice: hunting mutations for crop improvement. Crop Science. 2013 Nov;53(6):2550-62. https://doi.org/10.2135/cropsci2012.12.0693

Paul P, Awasthi A, Rai AK, Gupta SK, Prasad R, Sharma TR, Dhaliwal HS. Reduced tillering in Basmati rice T-DNA insertional mutant OsTEF1 associates with differential expression of stress related genes and transcription factors. Functional & integrative genomics. 2012 Jun;12:291-304. https://doi.org/10.1007/s10142-012-0264-5

Giri J, Vij S, Dansana PK, Tyagi AK. Rice A20/AN1 zinc?finger containing stress?associated proteins (SAP1/11) and a receptor?like cytoplasmic kinase (OsRLCK253) interact via A20 zinc?finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytologist. 2011 Aug;191(3):721-32. https://doi.org/10.1111/j.1469-8137.2011.03740.x

Pandit A, Rai V, Bal S, Sinha S, Kumar V, Chauhan M, Gautam RK, Singh R, Sharma PC, Singh AK, Gaikwad K. Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryza sativa L.). Molecular Genetics and Genomics. 2010 Aug;284:121-36. https://doi.org/10.1007/s00438-010-0551-6

Chen L, Wang Q, Tang M, Zhang X, Pan Y, Yang X, Gao G, Lv R, Tao W, Jiang L, Liang T. QTL mapping and identification of candidate genes for heat tolerance at the flowering stage in rice. Frontiers in Genetics. 2021 Jan 22;11:621871. https://doi.org/10.3389/fgene.2020.621871

Dixit S, Huang BE, Sta Cruz MT, Maturan PT, Ontoy JC, Kumar A. QTLs for tolerance of drought and breeding for tolerance of abiotic and biotic stress: an integrated approach. PLoS One. 2014 Oct 14;9(10):e109574. https://doi.org/10.1371/journal.pone.0109574

Fengfeng F, Meng C, Xiong L, Manman L, Huanran Y, Mingxing C, Ahmad A, Nengwu L, Shaoqing L. Novel QTLs from wild rice Oryza longistaminata confer strong tolerance to high temperature at seedling stage. Rice Science. 2023 Nov 1;30(6):577-86. https://doi.org/10.1016/j.rsci.2023.07.004

Ps S, Sv AM, Prakash C, Mk R, Tiwari R, Mohapatra T, Singh NK. High resolution mapping of QTLs for heat tolerance in rice using a 5K SNP array. Rice. 2017 Dec;10:1-1. https://doi.org/10.1186/s12284-017-0167-0

Ye C, Tenorio FA, Argayoso MA, Laza MA, Koh HJ, Redoña ED, Jagadish KS, Gregorio GB. Identifying and confirming quantitative trait loci associated with heat tolerance at flowering stage in different rice populations. BMC genetics. 2015 Dec;16:1-0. https://doi.org/10.1186/s12863-015-0199-7

Das G, Rao GJ. Molecular marker assisted gene stacking for biotic and abiotic stress resistance genes in an elite rice cultivar. Frontiers in plant science. 2015 Sep 30;6:698. https://doi.org/10.3389/fpls.2015.00698