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Flooding tolerance in Rice: adaptive mechanism and marker-assisted selection breeding approaches

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Abstract

Natural and man-made ecosystems worldwide are subjected to flooding, which is a form of environmental stress. Genetic variability in the plant response to flooding involves variations in metabolism, architecture, and elongation development that are related with a low oxygen escape strategy and an opposing quiescence scheme that enables prolonged submergence endurance. Flooding is typically associated with a decrease in O2 in the cells, which is especially severe when photosynthesis is absent or limited, leading to significant annual yield losses globally. Over the past two decades, considerable advancements have been made in understanding of mechanisms of rice adaptation and tolerance to flooding/submergence. The mapping and identification of Sub1 QTL have led to the development of marker-assisted selection (MAS) breeding approach to improve flooding-tolerant rice varieties in submergence-prone ecosystems. The Sub1 incorporated in rice varieties showed tolerance during flash flood, but not during stagnant conditions. Hence, gene pyramiding techniques can be applied to combine/stack multiple resistant genes for developing flood-resilient rice varieties for different types of flooding stresses. This review contains an update on the latest advances in understanding the molecular mechanisms, metabolic adaptions, and genetic factors governing rice flooding tolerance. A better understanding of molecular genetics and adaptation mechanisms that enhance flood-tolerant varieties under different flooding regimes was also discussed.

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References

  1. Yu S, Lee H, Lo S, Ho TD (2021) How does rice cope with too little oxygen during its early life? New Phytol 229:36–41. https://doi.org/10.1111/nph.16395

    Article  PubMed  Google Scholar 

  2. Afrin W, Nafis MH, Hossain MA et al (2018) Responses of rice (Oryza sativa L.) genotypes to different levels of submergence. C R Biol 341:85–96. https://doi.org/10.1016/j.crvi.2018.01.001

    Article  PubMed  Google Scholar 

  3. Singh R, Singh Y, Xalaxo S et al (2016) From QTL to variety-harnessing the benefits of QTLs for drought, flood and salt tolerance in mega rice varieties of India through a multi-institutional network. Plant Sci 242:278–287. https://doi.org/10.1016/j.plantsci.2015.08.008

    Article  CAS  PubMed  Google Scholar 

  4. Leridon H, (2020) World population outlook. Explosion or implosion. Pop Soci 573:1–4.

  5. Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00067

  6. Barik J, Kumar V, Lenka SK, Panda D (2020) Assessment of variation in morpho-physiological traits and genetic diversity in relation to submergence tolerance of five indigenous lowland rice landraces. Rice Sci 27:32–43. https://doi.org/10.1016/j.rsci.2019.12.004

    Article  Google Scholar 

  7. Singh A, Septiningsih EM, Balyan HS et al (2017) Genetics, physiological mechanisms and breeding of flood-tolerant Rice (Oryza sativa L.). Plant Cell Physiol 158(2):185–197. https://doi.org/10.1093/pcp/pcw206.

  8. Septiningsih EM, Mackill DJ (2018) Genetics and breeding of flooding tolerance in rice. Rice genomics, genetics and breeding. Springer Singapore, Singapore, pp 275–295

    Chapter  Google Scholar 

  9. Kuroha T, Ashikari M (2020) Molecular mechanisms and future improvement of submergence tolerance in rice. Mol Breed 40:41. https://doi.org/10.1007/s11032-020-01122-y

    Article  CAS  Google Scholar 

  10. Vergara GV, Nugraha Y, Esguerra MQ et al (2014) Variation in tolerance of rice to long-term stagnant flooding that submerges most of the shoot will aid in breeding tolerant cultivars. AoB Plants 6:plu055–plu055. https://doi.org/10.1093/aobpla/plu055

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sarkar RK, Reddy JN, Sharma SG, Ismail AM (2006) Physiological basis of submergence tolerance in rice and implications for crop improvement.Curr Sci:899–906

  12. Oladosu Y, Rafii MY, Arolu F et al (2020) Submergence tolerance in rice: Review of mechanism, breeding and, future prospects. Sustainability 12:1632

    Article  Google Scholar 

  13. Mackill DJ, Ismail AM, Singh US et al (2012) Development and rapid adoption of submergence-tolerant (Sub1) rice Varieties. Elsevier, Amsterdam, Netherlands, pp 299–352

    Google Scholar 

  14. Yang S-Y, Wu Y-S, Chen C-T et al (2017) Physiological and molecular responses of seedlings of an upland rice (‘Tunglu 3’) to total submergence compared to those of a submergence-tolerant lowland rice (‘FR13A’). Rice 10:42. https://doi.org/10.1186/s12284-017-0180-3

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lee KW, Chen PW, Yu SM (2014) Metabolic adaptation to sugar/O2 deficiency for anaerobic germination and seedling growth in rice. Plant Cell Environ 37:2234–2244. https://doi.org/10.1111/pce.12311

    Article  CAS  PubMed  Google Scholar 

  16. Ismail AM, Johnson DE, Ella ES et al (2012) Adaptation to flooding during emergence and seedling growth in rice and weeds, and implications for crop establishment. AoB Plants 2012. https://doi.org/10.1093/aobpla/pls019.

  17. Angaji SA, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica 172:159–168. https://doi.org/10.1007/s10681-009-0014-5

    Article  Google Scholar 

  18. Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann Bot 103:197–209. https://doi.org/10.1093/aob/mcn211

    Article  CAS  PubMed  Google Scholar 

  19. Magneschi L, Perata P (2009) Rice germination and seedling growth in the absence of oxygen. Ann Bot 103:181–196. https://doi.org/10.1093/aob/mcn121

    Article  CAS  PubMed  Google Scholar 

  20. Catling, D. (1999) Rice in Deep Water. Palgrave Macmillan, London. https://doi.org/10.1007/978-1-349-12309-4

  21. Kuanar SR, Ray A, Sethi SK et al (2017) Physiological basis of stagnant flooding tolerance in rice. Rice Sci 24:73–84. https://doi.org/10.1016/j.rsci.2016.08.008

    Article  Google Scholar 

  22. Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot 91:227–241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bin Rahman ANMR, Zhang J (2016) Flood and drought tolerance in rice: opposite but may coexist. Food Energy Secur 5:76–88. https://doi.org/10.1002/fes3.79

    Article  Google Scholar 

  24. Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49. https://doi.org/10.1046/j.1469-8137.2003.00907.x

    Article  Google Scholar 

  25. Pedersen O, Rich SM, Colmer TD (2009) Surviving floods: leaf gas films improve O2 and CO2 exchange, root aeration, and growth of completely submerged rice. Plant J 58:147–156. https://doi.org/10.1111/j.1365-313X.2008.03769.x

    Article  CAS  PubMed  Google Scholar 

  26. Parlanti S, Kudahettige NP, Lombardi L et al (2011) Distinct mechanisms for aerenchyma formation in leaf sheaths of rice genotypes displaying a quiescence or escape strategy for flooding tolerance. Ann Bot 107:1335–1343. https://doi.org/10.1093/aob/mcr086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378. https://doi.org/10.1111/j.1469-8137.2010.03496.x

    Article  CAS  PubMed  Google Scholar 

  28. Yamauchi T, Colmer TD, Pedersen O, Nakazono M (2018) Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. Plant Physiol 176:1118–1130. https://doi.org/10.1104/pp.17.01157

    Article  CAS  PubMed  Google Scholar 

  29. Yamauchi T, Tanaka A, Inahashi H et al (2019) Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling. Proc Natl Acad Sci 116:20770–20775. https://doi.org/10.1073/pnas.1907181116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shiono K, Takahashi H, Colmer TD, Nakazono M (2008) Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Sci 175:52–58. https://doi.org/10.1016/j.plantsci.2008.03.002

    Article  CAS  Google Scholar 

  31. Yamauchi T, Shiono K, Nagano M et al (2015) Ethylene biosynthesis is promoted by very-long-chain fatty acids during lysigenous aerenchyma formation in rice roots. Plant Physiol 169:180–193. https://doi.org/10.1104/pp.15.00106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Yamauchi T, Yoshioka M, Fukazawa A et al (2017) An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29:775–790. https://doi.org/10.1105/tpc.16.00976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lorbiecke R, Sauter M (1999) Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol 119:21–30. https://doi.org/10.1104/pp.119.1.21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617. https://doi.org/10.1104/pp.15.01360

    Article  CAS  PubMed  Google Scholar 

  35. Meng F, Xiang D, Zhu J (2019) Molecular mechanisms of root development in rice. Rice 12:1. https://doi.org/10.1186/s12284-018-0262-x

    Article  PubMed  PubMed Central  Google Scholar 

  36. Steffens B, Kovalev A, Gorb SN, Sauter M (2012) Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling. Plant Cell 24:3296–3306. https://doi.org/10.1105/tpc.112.101790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lin CC, Chao YT, Chen WC et al (2019) Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. Proc Nat Acad Sci 116:3300–3309. https://doi.org/10.1073/pnas.1818507116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pramanik M, Shelley I, Adhikary D, Islam M (2016) Carbohydrate reserve and aerenchyma formation enhance submergence tolerance in rice. Progress Agric 27:256–264. https://doi.org/10.3329/pa.v27i3.30805

    Article  Google Scholar 

  39. Rachmawati D (2015) Growth and aerenchyma formation of rice (Oryza sativa L.) Cv. Ir64 and Inpara5 at different inundation conditions. KnE Life Sci 2:348. https://doi.org/10.18502/kls.v2i1.172

    Article  Google Scholar 

  40. Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot 60:2155–2167. https://doi.org/10.1093/jxb/erp089

    Article  CAS  PubMed  Google Scholar 

  41. Herzog M, Konnerup D, Pedersen O et al (2018) Leaf gas films contribute to rice (Oryza sativa) submergence tolerance during saline floods. Plant Cell Environ 41:885–897. https://doi.org/10.1111/pce.12873

    Article  CAS  PubMed  Google Scholar 

  42. Kurokawa Y, Nagai K, Huan PD et al (2018) Rice leaf hydrophobicity and gas films are conferred by a wax synthesis gene (LGF1) and contribute to flood tolerance. New Phytol 218:1558–1569. https://doi.org/10.1111/nph.15070

    Article  CAS  PubMed  Google Scholar 

  43. Nishiuchi S, Yamauchi T, Takahashi H et al (2012) Mechanisms for coping with submergence and waterlogging in rice. Rice 5:2. https://doi.org/10.1186/1939-8433-5-2

    Article  PubMed  PubMed Central  Google Scholar 

  44. Shiono K, Ogawa S, Yamazaki S et al (2011) Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot 107:89–99. https://doi.org/10.1093/aob/mcq221

    Article  CAS  PubMed  Google Scholar 

  45. Kulichikhin K, Yamauchi T, Watanabe K, Nakazono M (2014) Biochemical and molecular characterization of rice (Oryza sativa L.) roots forming a barrier to radial oxygen loss. Plant Cell Environ 37(10):2406–2420. https://doi.org/10.1111/pce.12294

    Article  CAS  PubMed  Google Scholar 

  46. Shiono K, Ando M, Nishiuchi S et al (2014) RCN1/OsABCG5, an ATP-binding cassette (ABC) transporter, is required for hypodermal suberization of roots in rice (Oryza sativa). Plant J 80:40–51. https://doi.org/10.1111/tpj.12614

    Article  CAS  PubMed  Google Scholar 

  47. Bailey-Serres J, Fukao T, Ronald P et al (2010) Submergence tolerant rice: SUB1’s journey from landrace to modern cultivar. Rice 3:138–147. https://doi.org/10.1007/s12284-010-9048-5

    Article  Google Scholar 

  48. Tamang B, Fukao T (2015) Plant adaptation to multiple stresses during submergence and following desubmergence. Int J Mol Sci 16:30164–30180. https://doi.org/10.3390/ijms161226226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Azarin K, Usatov A, Kostylev P (2017) Molecular breeding of submergence-tolerant rice. Annu Res Rev Biol 18:1–10. https://doi.org/10.9734/ARRB/2017/35616

    Article  Google Scholar 

  50. Ayano M, Kani T, Kojima M et al (2014) Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ 37:2313–2324. https://doi.org/10.1111/pce.12377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Minami A, Yano K, Gamuyao R et al (2018) Time-course transcriptomics analysis reveals key responses of submerged deepwater rice to flooding. Plant Physiol 176:3081–3102. https://doi.org/10.1104/pp.17.00858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Fukao T, Bailey-Serres J (2008) Ethylene—A key regulator of submergence responses in rice. Plant Sci 175:43–51. https://doi.org/10.1016/j.plantsci.2007.12.002

    Article  CAS  Google Scholar 

  53. Kuroha T, Nagai K, Gamuyao R et al (2018) Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Sci (80-) 361:181–186. https://doi.org/10.1126/science.aat1577

    Article  CAS  Google Scholar 

  54. Ram P, Singh B, Singh A et al (2002) Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker-aided breeding. F Crop Res 76:131–152. https://doi.org/10.1016/S0378-4290(02)00035-7

    Article  Google Scholar 

  55. Xu K, Xu X, Fukao T et al (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708. https://doi.org/10.1038/nature04920

    Article  CAS  PubMed  Google Scholar 

  56. Xu K, Deb R, Mackill DJ (2004) A microsatellite marker and a codominant PCR-based marker for marker‐assisted selection of submergence tolerance in rice. Crop Sci 44:248–253. https://doi.org/10.2135/cropsci2004.2480

    Article  CAS  Google Scholar 

  57. Septiningsih EM, Sanchez DL, Singh N et al (2012) Identifying novel QTLs for submergence tolerance in rice cultivars IR72 and Madabaru. Theor Appl Genet 124:867–874. https://doi.org/10.1007/s00122-011-1751-0

    Article  PubMed  Google Scholar 

  58. Pucciariello C, Perata P (2013) Quiescence in rice submergence tolerance: an evolutionary hypothesis. Trends Plant Sci 18:377–381. https://doi.org/10.1016/j.tplants.2013.04.007

    Article  CAS  PubMed  Google Scholar 

  59. Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects. Front Plant Sci 10:340. https://doi.org/10.3389/fpls.2019.00340

    Article  PubMed  PubMed Central  Google Scholar 

  60. Septiningsih EM, Pamplona AM, Sanchez DL et al (2009) Genetic mechanisms conferring adaptation to submergence and drought in rice: Simple or complex? Ann Bot 103:151–160. https://doi.org/10.1016/j.pbi.2013.02.003

    Article  CAS  PubMed  Google Scholar 

  61. Panda D, Barik J (2021) Flooding tolerance in rice: focus on mechanisms and approaches. Rice Sci 28:43–57. https://doi.org/10.1016/j.rsci.2020.11.006

    Article  Google Scholar 

  62. de Sousa CAF, Sodek L (2002) The metabolic response of plants to oxygen deficiency. Brazilian J Plant Physiol 14:83–94. https://doi.org/10.1590/S1677-04202002000200002

    Article  Google Scholar 

  63. Hsu SK, Tung CW (2017) RNA-seq analysis of diverse rice genotypes to identify the genes controlling coleoptile growth during submerged germination. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00762

  64. Greenway H, Gibbs J (2003) Mechanisms of anoxia tolerance in plants.  I. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol 30:999. https://doi.org/10.1071/PP98096

    Article  CAS  PubMed  Google Scholar 

  65. Edwards JM, Roberts TH, Atwell BJ (2012) Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. J Exp Bot 63:4389–4402. https://doi.org/10.1093/jxb/ers114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Miro B, Longkumer T, Entila FD et al (2017) Rice seed germination underwater: morpho-physiological responses and the bases of differential expression of alcoholic fermentation enzymes. Front Plant Sci 8:1857. https://doi.org/10.3389/fpls.2017.01857

    Article  PubMed  PubMed Central  Google Scholar 

  67. Lee KW, Chen PW, Lu CA et al (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61–ra61. https://doi.org/10.1126/scisignal.2000333

    Article  PubMed  Google Scholar 

  68. Senapati S, Kuanar SR (2019) Anaerobic germination potential in rice (Oryza sativa L.): role of amylases, alcohol deydrogenase and ethylene. J Stress Physiol Biochem 15:39–52

    CAS  Google Scholar 

  69. Pujadas G, Palau J (2001) Evolution of α-amylases: architectural features and key residues in the stabilization of the (β/α)8 scaffold. Mol Biol Evol 18:38–54. https://doi.org/10.1093/oxfordjournals.molbev.a003718

    Article  CAS  PubMed  Google Scholar 

  70. Hwang YS, Thomas BR, Rodriguez RL (1999) Differential expression of rice alpha-amylase genes during seedling development under anoxia. Plant Mol Biol 40:911–920. https://doi.org/10.1023/a:1006241811136

    Article  CAS  PubMed  Google Scholar 

  71. Huang N, Stebbins GL, Rodriguez RL (1992) Classification and evolution of alpha-amylase genes in plants. Proc Nat Acad Sci 89:7526–7530. https://doi.org/10.1073/pnas.89.16.7526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Guglielminetti L, Yamaguchi J, Perata P, Alpi A (1995) Amylolytic activities in cereal seeds under aerobic and anaerobic conditions. Plant Physiol 109:1069–1076. https://doi.org/10.1104/pp.109.3.1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Vijayan J, Senapati S, Ray S et al (2018) Transcriptomic and physiological studies identify cues for germination stage oxygen deficiency tolerance in rice. Environ Exp Bot 147:234–248. https://doi.org/10.1016/j.envexpbot.2017.12.013

    Article  CAS  Google Scholar 

  74. Saika H, Matsumura H, Takano T et al (2006) A Point mutation of Adh1 gene is involved in the repression of coleoptile elongation under submergence in rice. Breed Sci 56:69–74. https://doi.org/10.1270/jsbbs.56.69

    Article  CAS  Google Scholar 

  75. Miro B, Ismail AM (2013) Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.). Front Plant Sci 4:269. https://doi.org/10.3389/fpls.2013.00269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lasanthi-KR, Magneschi L, Loreti E et al (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231. https://doi.org/10.1104/pp.106.093997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ma M, Cen W, Li R et al (2020) The molecular regulatory pathways and metabolic adaptation in the seed germination and early seedling growth of rice in response to low O2 Stress. Plants 9:1363. https://doi.org/10.3390/plants9101363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Baltazar MD, Ignacio JCI, Thomson MJ et al (2019) QTL mapping for tolerance to anaerobic germination in rice from IR64 and the aus landrace Kharsu 80A. Breed Sci 69:227–233. https://doi.org/10.1270/jsbbs.18159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Jiang L, Hou M, Wang C, Wan J (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa). Rice Sci 11:238–244

    Google Scholar 

  80. Nishimura T, Sasaki K, Yamaguchi T et al (2020) Detection and characterization of quantitative trait loci for coleoptile elongation under anaerobic conditions in rice. Plant Prod Sci 23:374–383. https://doi.org/10.1080/1343943X.2020.1740600

    Article  CAS  Google Scholar 

  81. Septiningsih EM, Ignacio JCI, Sendon PMD et al (2013) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet 126:1357–1366. https://doi.org/10.1007/s00122-013-2057-1

    Article  PubMed  Google Scholar 

  82. Jeong J, Cho Y, Jeong J et al (2020) QTL mapping and effect confirmation for anaerobic germination tolerance derived from the japonica weedy rice landrace PBR. Plant Breed 139:83–92. https://doi.org/10.1111/pbr.12753

    Article  CAS  Google Scholar 

  83. Kretzschmar T, Pelayo MAF, Trijatmiko KR et al (2015) A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants 1:15124. https://doi.org/10.1038/nplants.2015.124

    Article  CAS  PubMed  Google Scholar 

  84. Hsu SK, Tung CW (2015) Genetic mapping of anaerobic germination-associated QTLs controlling coleoptile elongation in rice. Rice 8:38. https://doi.org/10.1186/s12284-015-0072-3

    Article  PubMed  PubMed Central  Google Scholar 

  85. Nghi KN, Tondelli A, Valè G et al (2019) Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses. Plant Cell Environ 42:1832–1846. https://doi.org/10.1111/pce.13540

    Article  CAS  PubMed  Google Scholar 

  86. Rohilla M, Singh N, Mazumder A et al (2020) Genome-wide association studies using 50 K rice genic SNP chip unveil genetic architecture for anaerobic germination of deep-water rice population of Assam, India. Mol Genet Genomics 295:1211–1226. https://doi.org/10.1007/s00438-020-01690-w

    Article  CAS  PubMed  Google Scholar 

  87. Zhang M, Lu Q, Wu W et al (2017) Association mapping reveals novel genetic loci contributing to flooding tolerance during germination in Indica rice. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00678

  88. Xu K, Mackill DJ (1996) A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed 2:219–224. https://doi.org/10.1007/BF00564199

    Article  CAS  Google Scholar 

  89. Gonzaga ZJC, Carandang J, Sanchez DL et al (2016) Mapping additional QTLs from FR13A to increase submergence tolerance in rice beyond SUB1. Euphytica 209:627–636. https://doi.org/10.1007/s10681-016-1636-z

    Article  CAS  Google Scholar 

  90. Nagai K, Mori Y, Ishikawa S et al (2020) Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature 584:109–114. https://doi.org/10.1038/s41586-020-2501-8

    Article  CAS  PubMed  Google Scholar 

  91. Hattori Y, Nagai K, Furukawa S et al (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030. https://doi.org/10.1038/nature08258

    Article  CAS  PubMed  Google Scholar 

  92. Mühlenbock P, Plaszczyca M, Plaszczyca M et al (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell 19:3819–3830. https://doi.org/10.1105/tpc.106.048843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Loreti E, Valeri MC, Novi G, Perata P (2018) Gene regulation and survival under hypoxia requires starch availability and metabolism. Plant Physiol 176:1286–1298. https://doi.org/10.1104/pp.17.01002

    Article  CAS  PubMed  Google Scholar 

  94. Toledo AMU, Ignacio JCI, Casal C et al (2015) Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breed Biotechnol 3:77–87. https://doi.org/10.9787/PBB.2015.3.2.077

    Article  Google Scholar 

  95. Baltazar MD, Ignacio JCI, Thomson MJ et al (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197:251–260. https://doi.org/10.1007/s10681-014-1064-x

    Article  CAS  Google Scholar 

  96. Jiang L, Liu S, Hou M et al (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). F Crop Res 98:68–75. https://doi.org/10.1016/j.fcr.2005.12.015

    Article  Google Scholar 

  97. Yang J, Sun K, Li D et al (2019) Identification of stable QTLs and candidate genes involved in anaerobic germination tolerance in rice via high-density genetic mapping and RNA-Seq. BMC Genomics 20:355. https://doi.org/10.1186/s12864-019-5741-y

    Article  PubMed  PubMed Central  Google Scholar 

  98. Kuya N, Sun J, Iijima K et al (2019) Novel method for evaluation of anaerobic germination in rice and its application to diverse genetic collections. Breed Sci 69:633–639. https://doi.org/10.1270/jsbbs.19003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Septiningsih EM, Pamplona AM, Sanchez DL et al (2009) Development of submergence-tolerant rice cultivars: The Sub1 locus and beyond. Ann Bot 103:151–160. https://doi.org/10.1093/aob/mcn206

    Article  CAS  PubMed  Google Scholar 

  100. Dixit S, Singh A, Sandhu N et al (2017) Combining drought and submergence tolerance in rice: marker-assisted breeding and QTL combination effects. Mol Breed 37:143. https://doi.org/10.1007/s11032-017-0737-2

    Article  PubMed  PubMed Central  Google Scholar 

  101. Toojinda T (2003) Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot 91:243–253. https://doi.org/10.1093/aob/mcf072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Xu K, Xu X, Ronald PC, Mackill DJ (2000) A high-resolution linkage map of the vicinity of the rice submergence tolerance locus Sub1. Mol Gen Genet MGG 263:681–689. https://doi.org/10.1007/s004380051217

    Article  CAS  PubMed  Google Scholar 

  103. Tiwari DN (2018) A critical review of submergence tolerance breeding beyond Sub1 gene to mega varieties in the context of climate change. Int J Adv Sci Res Eng. https://doi.org/10.7324/IJASRE.2018.32647

    Article  Google Scholar 

  104. Septiningsih EM, Pamplona AM, Sanchez DL et al (2009) Mechanisms for coping with submergence andwaterlogging in rice. Ann Bot 103:151–160. https://doi.org/10.1186/1939-8433-5-2

    Article  CAS  PubMed  Google Scholar 

  105. Winkel A, Pedersen O, Ella E et al (2014) Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. J Exp Bot 65:3225–3233. https://doi.org/10.1093/jxb/eru166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ramiah K (1940) Floating habit in rice.Indian J Agric Sci p1–8

  107. Hamamura K, Kupkanchanakul T (1979) Inheritance of floating ability in rice. Japanese J Breed 29:211–216. https://doi.org/10.1270/jsbbs1951.29.211

    Article  Google Scholar 

  108. Inouye J (1983) Relation between elongation ability and internode elongation of floating rice under rising water conditions. Japanese J Trop Agric 27:181–186

    Google Scholar 

  109. Tripathi RS, Balakrishna Rao MJ (1985) Inheritance studies of characters associated with floating habit and their linkage relationship in rice. Euphytica 34:875–881. https://doi.org/10.1007/BF00035427

    Article  Google Scholar 

  110. Suge H (1987) Physiological genetics of internodal elongation under submergence in floating rice. Japanese J Genet 62:69–80. https://doi.org/10.1266/jjg.62.69

    Article  Google Scholar 

  111. Eiguchi M, Hirano H-Y, Sano Y, Morishima H (1993) Effects of water depth on internodal elongation and floral induction in a deepwater-tolerant rice line carrying the dw3 gene. Japanese J Breed 43:135–139. https://doi.org/10.1270/jsbbs1951.43.135

    Article  Google Scholar 

  112. Sripongpangkul K, Posa GBT, Senadhira DW et al (2000) Genes/QTLs affecting flood tolerance in rice. Theor Appl Genet 101:1074–1081. https://doi.org/10.1007/s001220051582

    Article  CAS  Google Scholar 

  113. Nemoto K, Ukai Y, Tang D-Q et al (2004) Inheritance of early elongation ability in floating rice revealed by diallel and QTL analyses. Theor Appl Genet 109:42–47. https://doi.org/10.1007/s00122-004-1600-5

    Article  CAS  PubMed  Google Scholar 

  114. Kawano R, Doi K, Yasui H et al (2008) Mapping of QTLs for floating ability in rice. Breed Sci 58:47–53. https://doi.org/10.1270/jsbbs.58.47

    Article  CAS  Google Scholar 

  115. Hattori Y, Miura K, Asano K et al (2007) A major QTL confers rapid internode elongation in response to water rise in deepwater rice. Breed Sci 57:305–314. https://doi.org/10.1270/jsbbs.57.305

    Article  Google Scholar 

  116. Hattori Y, Nagai K, Mori H et al (2008) Mapping of three QTLs that regulate internode elongation in deepwater rice. Breed Sci 58:39–46. https://doi.org/10.1270/jsbbs.58.39

    Article  CAS  Google Scholar 

  117. Cho HT, Kende H (1997) Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9:1661–1671. https://doi.org/10.1105/tpc.9.9.1661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Sauter M, Seagull R, Kende H (1993) Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 190. https://doi.org/10.1007/BF00196964

  119. Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378. https://doi.org/10.1111/j.1469-8137.2010.03496.x

    Article  CAS  PubMed  Google Scholar 

  120. Nagai K, Kuroha T, Ayano M et al (2012) Two novel QTLs regulate internode elongation in deepwater rice during the early vegetative stage. Breed Sci 62:178–185. https://doi.org/10.1270/jsbbs.62.178

    Article  PubMed  PubMed Central  Google Scholar 

  121. Kuroha T, Nagai K, Kurokawa Y et al (2017) eQTLs regulating transcript variations associated with rapid internode elongation in deepwater rice. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01753

  122. Singh A, Carandang J, Gonzaga ZJC et al (2017) Identification of QTLs for yield and agronomic traits in rice under stagnant flooding conditions. Rice 10:15. https://doi.org/10.1186/s12284-017-0154-5

    Article  PubMed  PubMed Central  Google Scholar 

  123. Haque MA, Rafii MY, Yusoff MM et al (2021) Recent advances in rice varietal development for durable resistance to biotic and abiotic stresses through marker-assisted gene pyramiding. Sustainability 13:10806. https://doi.org/10.3390/su131910806

    Article  CAS  Google Scholar 

  124. Ullah MA, Abdullah-Zawawi MR, Zainal-Abidin RA et al (2022) A review of integrative omic approaches for understanding rice salt response mechanisms. Plants 11:1430. https://doi.org/10.3390/plants11111430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Septiningsih EM, Hidayatun N, Sanchez DL et al (2015) Accelerating the development of new submergence tolerant rice varieties: the case of Ciherang-Sub1 and PSB Rc18-Sub1. Euphytica 202:259–268. https://doi.org/10.1007/s10681-014-1287-x

    Article  Google Scholar 

  126. Haque MA, Rafii MY, Yusoff MM et al (2021) Advanced breeding strategies and future perspectives of salinity tolerance in rice. Agronomy 11:1631. https://doi.org/10.3390/agronomy11081631

    Article  CAS  Google Scholar 

  127. Iftekharuddaula KM, Ahmed HU, Ghosal S et al (2016) Development of early maturing submergence-tolerant rice varieties for Bangladesh. F Crop Res 190:44–53. https://doi.org/10.1016/j.fcr.2015.12.001

    Article  Google Scholar 

  128. Dar MH, Chakravorty R, Waza SA et al (2017) Transforming rice cultivation in flood prone coastal Odisha to ensure food and economic security. Food Secur 9:711–722. https://doi.org/10.1007/s12571-017-0696-9

    Article  Google Scholar 

  129. Ahmed AU, Hernandez R, Naher F (2016) Adoption of stress-tolerant rice varieties in Bangladesh: technological and institutional innovations for marginalized smallholders in agricultural development. Springer international publishing, Cham, pp 241–255

    Chapter  Google Scholar 

  130. Rafael AB, Barroga WV, Marcelo PNM, Septiningsih EM et al (2015) Introgression of Sub1 and AG1 tolerance genes to NSIC Rc222 through marker-assisted backcrossing. Philippine Journal of Crop Science, Philippines

    Google Scholar 

  131. Mondal S, Khan MIR, Dixit S et al (2020) Growth, productivity and grain quality of AG1 and AG2 QTLs introgression lines under flooding in direct-seeded rice system. F Crop Res 248:107713. https://doi.org/10.1016/j.fcr.2019.107713

    Article  Google Scholar 

  132. Nair MM, Shylaraj KS (2021) Introgression of dual abiotic stress tolerance QTLs (Saltol QTL and Sub1 gene) into rice (Oryza sativa L.) variety Aiswarya through marker- assisted backcross breeding. Physiol Mol Biol Plants 27:497–514. https://doi.org/10.1007/s12298-020-00893-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Hifzur R, Vijayalakshmi D, Sasikala R et al (2018) Introgression of submergence tolerance into CO 43, a popular rice variety of India, through marker-assisted backcross breeding. Czech J Genet Plant Breed 54:101–108. https://doi.org/10.17221/149/2017-CJGPB

    Article  Google Scholar 

  134. Mojulat WC, Yusop R, Ismail R et al (2017) Analysis of simple sequence repeat markers linked to submergence tolerance on newly developed rice lines derived from MR263 × Swarna-Sub1. Sains Mal 46:521–528. https://doi.org/10.17576/jsm-2017-4604-02

    Article  CAS  Google Scholar 

  135. Ahmed F, Rafii MY, Ismail MR et al (2016) Recurrent parent genome recovery in different populations with the introgression of Sub1 gene from a cross between MR219 and Swarna-Sub1. Euphytica 207:605–618. https://doi.org/10.1007/s10681-015-1554-5

    Article  Google Scholar 

  136. Iftekharuddaula KM, Ahmed HU, Ghosal S et al (2015) Development of new submergence tolerant rice variety for Bangladesh using marker-assisted backcrossing. Rice Sci 22:16–26. https://doi.org/10.1016/j.rsci.2015.05.003

    Article  Google Scholar 

  137. Arya KV, Shylaraj KS (2018) Introgression of Sub1 QTL (Submergence tolerant QTL) into the elite rice variety Jaya by marker-assisted backcross breeding. J Trop Agric 56:114–128

    CAS  Google Scholar 

  138. John D, Shylaraj KS (2017) Introgression of sub1 QTL into an elite rice (Oryza sativa L.) variety Jyothi through marker-assisted backcross breeding. J Trop Agric 55:1–11

    CAS  Google Scholar 

  139. Huyen LTN, Cuc LM, Ismail AM, Ham LH (2012) Introgression of the salinity tolerance QTLs into AS996, the elite rice variety of Vietnam. Am J Plant Sci 03:981–987. https://doi.org/10.4236/ajps.2012.37116

  140. Neeraja CN, Maghirang-Rodriguez R, Pamplona A et al (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767–776. https://doi.org/10.1007/s00122-007-0607-0

    Article  CAS  PubMed  Google Scholar 

  141. Pandit E, Pawar S, Barik SR et al (2021) Marker-assisted backcross breeding for improvement of submergence tolerance and grain yield in the popular rice variety. ‘Maudamani’ Agronomy 11:1263. https://doi.org/10.3390/agronomy11071263

    Article  CAS  Google Scholar 

  142. Kim S, Kim C, Jeong J et al (2019) Marker-assisted breeding for improvement of anaerobic germination in japonica rice (Oryza sativa). Plant Breed 138:810–819. https://doi.org/10.1111/pbr.12719

    Article  CAS  Google Scholar 

  143. Sarkar RK, Panda D, Reddy JN et al (2009) Performance of submergence tolerant rice (Oryza sativa) genotypes carrying the Sub1 quantitative trait locus under stressed and non-stressed natural field conditions. Indian J Agric Sci 79:876–883

    Google Scholar 

  144. Singh N, Jayaswal PK, Panda K et al (2015) Single-copy gene-based 50K SNP chip for genetic studies and molecular breeding in rice. Sci Rep 5:11600. https://doi.org/10.1038/srep11600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Lang NT, Van Tao N, Buu BC (2011) Marker-assisted backcrossing (MAB) for rice submergence tolerance in Mekong delta. Omonrice 18:11–21

    Google Scholar 

  146. Khanh D (2013) Rapid and high-precision marker-assisted backcrossing to introgress the SUB1 QTL into the Vietnamese elite rice variety. J Plant Breed Crop Sci 5:26–33. https://doi.org/10.5897/JPBCS12.052

    Article  Google Scholar 

  147. Das KK, Sarkar RK, Ismail AM (2005) Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice. Plant Sci 168:131–136. https://doi.org/10.1016/j.plantsci.2004.07.023

    Article  CAS  Google Scholar 

  148. Manzanilla DO, Paris TR, Vergara GV et al (2011) Submergence risks and farmer’s preferences: implications for breeding Sub1 rice in Southeast Asia. Agric Syst 104:335–347. https://doi.org/10.1016/j.agsy.2010.12.005

    Article  Google Scholar 

  149. Kato Y, Collard BCY, Septiningsih EM, Ismail AM (2019) Increasing flooding tolerance in rice: combining tolerance of submergence and of stagnant flooding. Ann Bot 124:1199–1209. https://doi.org/10.1093/aob/mcz118

    Article  CAS  PubMed Central  Google Scholar 

  150. Singh S, Mackill DJ, Ismail AM (2011) Tolerance of longer-term partial stagnant flooding is independent of the SUB1 locus in rice. F Crop Res 121:311–323. https://doi.org/10.1016/j.fcr.2010.12.021

    Article  Google Scholar 

  151. Kuanar SR, Molla KA, Chattopadhyay K et al (2019) Introgression of Sub1 (SUB1) QTL in mega rice cultivars increases ethylene production to the detriment of grain-filling under stagnant flooding. Sci Rep 9:18567. https://doi.org/10.1038/s41598-019-54908-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We gratefully acknowledge the financial support from the Higher Institution Centres of Excellence (HICoE) Research Grant, the Ministry of Higher Education, Malaysia. The first author also acknowledges the Bangabandhu Science and Technology Fellowship Trust (BBSTFT) under the Ministry of Science and Technology, The People’s Republic of Bangladesh, for PhD scholarship.

Funding

The Higher Institution Centres of Excellence (HICoE), Research Grant (Vot number 6369105), Ministry of Higher Education, Malaysia and Univisiti Putra Malaysia with Vot number 9724600.

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Authors and Affiliations

  1. Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia

    Md Azadul Haque, Mohd Y. Rafii, Oladosu Yusuff, Fatai Arolu & Mohammad Anisuzzaman

  2. Bangladesh Institute of Nuclear Agriculture, BAU Campus, 2202, Mymensingh, Bangladesh

    Md Azadul Haque

  3. Department of Crop Science, Faculty of Agriculture, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia

    Mohd Y. Rafii & Martini Mohammad Yusoff

  4. Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia

    Nusaibah Syd Ali

  5. Bangladesh Rice Research Institute, 1701, Joydebpur, Gazipur, Bangladesh

    Mohammad Anisuzzaman

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M.A.H., M.Y.R. and M.M.Y. drafted the manuscript, while the proofreading, editing and finishing were carried out by N.S.A., O.Y., M.A. and F. A. All authors offered suggestions on various drafts of the manuscript. All authors have read and agreed to the published version of the manuscript.

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Haque, M.A., Rafii, M.Y., Yusoff, M.M. et al. Flooding tolerance in Rice: adaptive mechanism and marker-assisted selection breeding approaches. Mol Biol Rep 50, 2795–2812 (2023). https://doi.org/10.1007/s11033-022-07853-9

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