Skip to main navigation menu Skip to main content Skip to site footer

Review Articles

Vol. 12 No. 1 (2025)

Adaptive mechanism of submergence tolerance by Sub1 A

DOI
https://doi.org/10.14719/pst.4632
Submitted
12 August 2024
Published
21-12-2024 — Updated on 01-01-2025
Versions

Abstract

Among the various abiotic stresses affecting the growth, development, and yield of rice, submergence caused by continuous flooding without adequate drainage poses a significant threat. This stress is particularly detrimental in lowland areas with poor drainage, often near coastal regions, where excessive rainfall leads to prolonged waterlogging. Continuous waterlogging during germination severely impacts the germination of directly seeded rice crops, while seedling establishment suffers post-transplantation due to seedling decay and mortality. Submergence tolerance is an adaptive physiological and biochemical mechanism that has evolved in indica rice, enabling the plant to cope with the effects of anaerobic conditions caused by prolonged submergence. The putative progenitor Oryza rufipogon is well adapted to marshy environments. This study discusses the mechanisms of introgression of anaerobic germination and submergence tolerance from O. rufipogon through molecular analysis of genomic regions. It also explains the physiological and biochemical mechanisms that influence anaerobic germination and submergence tolerance. Lowland areas characterized by flooding due to excessive rainfall and inadequate drainage, particularly near coastal regions, require anaerobic germination and submergence tolerance for rice cultivation. Identifying new sources of submergence tolerance beyond the Sub1 gene, followed by genomic structural characterization for the development of pre-breeding genetic sources, is essential. Additionally, well-characterized quantitative trait loci (QTLs) and genes that confer submergence tolerance need to be transferred precisely.

References

  1. Pathak H, Tewari A, Sankhyan S, Dubey D, Mina U, Singh VK, et al. Direct-seeded rice: Potential, performance and problems-A review. Curr Adv Agric Sci Int J. 2011;3(2):77-88.
  2. Sarkar R, Reddy J, Sharma S, Ismail AM. Physiological basis of submergence tolerance in rice and implications for crop improvement. Curr Sci. 2006;899-906.
  3. Singh A, Septiningsih EM, Balyan HS, Singh NK, Rai V. Genetics, physiological mechanisms and breeding of flood-tolerant rice (Oryza sativa L.). Plant Cell Physiol. 2017;58(2):185-97. https://doi.org/10.1093/pcp/pcw206
  4. Yang SY, Wu YS, Chen CT, Lai MH, Yen HM, Yang CY. Physiological and molecular responses of seedlings of an upland rice (‘Tung Lu 3’) to total submergence compared to those of a submergence-tolerant lowland rice (‘FR13A’). Rice. 2017;10:1-10. https://doi.org/10.1186/s12284-017-0180-3
  5. Ismail AM, Johnson DE, Ella ES, Vergara GV, Baltazar AM. Adaptation to flooding during emergence and seedling growth in rice and weeds and implications for crop establishment. AoB Plants. 2012;2012:pls019. https://doi.org/10.1093/aobpla/pls019
  6. Ismail AM, Ella ES, Vergara GV, Mackill DJ. Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann Bot. 2009;103(2):197-209. https://doi.org/10.1093/aob/mcn211
  7. Vergara GV, Nugraha Y, Esguerra MQ, Mackill DJ, Ismail AM. Variation in tolerance of rice to long-term stagnant flooding that submerges most of the shoot will aid in breeding tolerant cultivars. AoB Plants. 2014;6:plu055. https://doi.org/10.1093/aobpla/plu055
  8. Catling D. Rice in deep water. Springer; 1993. https://doi.org/10.1007/978-1-349-12309-4
  9. Khush GS. Origin, dispersal, cultivation and variation of rice. Plant Mol Biol. 1997;35:25-34. https://doi.org/10.1023/A:1005810616885
  10. Wang X, Zhao Y, Jiang C, Wang L, Chen L, Li F, et al. Evolution of different rice ecotypes and genetic basis of flooding adaptability in deep water rice by GWAS. BMC Plant Biol. 2022;22(1):526. https://doi.org/10.1186/s12870-022-03924-y
  11. Pucciariello C, Voesenek LA, Perata P, Sasidharan R. Plant responses to flooding. Front Plant Sci. 2014;5:226. https://doi.org/10.3389/fpls.2014.00226
  12. Colmer TD, Armstrong W, Greenway H, Ismail A, Kirk G, Atwell B. Physiological mechanisms of flooding tolerance in rice: Transient complete submergence and prolonged standing water. Prog Bot. 2014;75:255-307. https://doi.org/10.1007/978-3-642-38797-5_9
  13. Kurokawa Y, Nagai K, Huan PD, Shimazaki K, Qu H, Mori Y, et al. Rice leaf hydrophobicity and gas films are conferred by a wax synthesis gene (LGF 1) and contribute to flood tolerance. New Phytol. 2018;218(4):1558-69. https://doi.org/10.1111/nph.15070
  14. Winkel A, Colmer TD, Ismail AM, Pedersen O. Internal aeration of paddy field rice (Oryza sativa) during complete submergence–importance of light and floodwater O2. New Phytol. 2013;197(4):1193-203. https://doi.org/10.1111/nph.12048
  15. Greenway H, Gibbs J. Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol. 2003;30(10):999-1036. https://doi.org/10.1071/PP98096
  16. Edwards JM, Roberts TH, Atwell BJ. Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. J Exp Bot. 2012;63(12):4389-402. https://doi.org/10.1093/jxb/ers114
  17. Lee KW, Chen PW, Lu CA, Chen S, Ho THD, Yu SM. Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal. 2009;2(91):ra61–ra61. https://doi.org/10.1126/scisignal.2000333
  18. Vijayan J, Senapati S, Ray S, Chakraborty K, Molla KA, Basak N, et al. Transcriptomic and physiological studies identify cues for germination stage oxygen deficiency tolerance in rice. Environ Exp Bot. 2018;147:234-48. https://doi.org/10.1016/j.envexpbot.2017.12.013
  19. Ma M, Cen W, Li R, Wang S, Luo J. The molecular regulatory pathways and metabolic adaptation in the seed germination and early seedling growth of rice in response to low O2 stress. Plants. 2020;9(10):1363. https://doi.org/10.3390/plants9101363
  20. Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants. 2015;1(9):1-5. https://doi.org/10.1038/nplants.2015.124
  21. Senapati S, Kuanar SR, Sarkar RK. Anaerobic germination potential in rice (Oryza sativa L.): Role of amylases, alcohol deydrogenase and ethylene. J Stress Physiol Biochem. 2019;15(4):39-52.
  22. Pujadas G, Palau J. Evolution of alpha-amylases: Architectural features and key residues in the stabilization of the (beta/alpha) 8 scaffold. Mol Biol Evol. 2001;18(1):38-54. https://doi.org/10.1093/oxfordjournals.molbev.a003718
  23. Guglielminetti L, Yamaguchi J, Perata P, Alpi A. Amylolytic activities in cereal seeds under aerobic and anaerobic conditions. Plant Physiol. 1995;109(3):1069-76. https://doi.org/10.1104/pp.109.3.1069
  24. Hwang YS, Thomas B, Rodriguez R. Differential expression of rice alpha-amylase genes during seedling development under anoxia. Plant Mol Biol. 1999;40:911-20. https://doi.org/10.1023/A:1006241811136
  25. Singh S, Mackill DJ, Ismail AM. Physiological basis of tolerance to complete submergence in rice involves genetic factors in addition to the SUB1 gene. AoB Plants. 2014;6:plu060. https://doi.org/10.1093/aobpla/plu060
  26. Jackson MB, Ram PC. Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot. 2003;91(2):227-41. https://doi.org/10.1093/aob/mcf242
  27. Kuroha T, Ashikari M. Molecular mechanisms and future improvement of submergence tolerance in rice. Mol Breed. 2020;40(4):41. https://doi.org/10.1007/s11032-020-01122-y
  28. Evans DE. Aerenchyma formation. New Phytol. 2004;161(1):35-49. https://doi.org/10.1046/j.1469-8137.2003.00907.x
  29. Shiono K, Takahashi H, Colmer TD, Nakazono M. Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Sci. 2008;175(1–2):52-58. https://doi.org/10.1016/j.plantsci.2008.03.002
  30. Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, et al. An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell. 2017;29(4):775-90. https://doi.org/10.1105/tpc.16.00976
  31. Lorbiecke R, Sauter M. Adventitious root growth and cell-cycle induction in deep water rice. Plant Physiol. 1999;119(1):21-30. https://doi.org/10.1104/pp.119.1.21
  32. Steffens B, Rasmussen A. The physiology of adventitious roots. Plant Physiol. 2016;170(2):603-17. https://doi.org/10.1104/pp.15.01360
  33. Lin CC, Chao YT, Chen WC, Ho HY, Chou MY, Li YR, et al. Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. Proc Natl Acad Sci. 2019;116(8):3300-09. https://doi.org/10.1073/pnas.1818507116
  34. Rachmawati D. Growth and aerenchyma formation of rice (Oryza sativa L.) Cv. Ir64 and in para 5 at different inundation conditions. KnE Life Sci. 2015;348-53. https://doi.org/10.18502/kls.v2i1.172
  35. Kotula L, Ranathunge K, Schreiber L, Steudle E. 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. 2009;60(7):2155-67. https://doi.org/10.1093/jxb/erp089
  36. Herzog M, Konnerup D, Pedersen O, Winkel A, Colmer TD. Leaf gas films contribute to rice (Oryza sativa) submergence tolerance during saline floods. Plant Cell Environ. 2018;41(5):885-97. https://doi.org/10.1111/pce.12873
  37. Pedersen O, Rich SM, Colmer TD. Surviving floods: Leaf gas films improve O2 and CO2 exchange, root aeration and growth of completely submerged rice. Plant J. 2009;58(1):147-56. https://doi.org/10.1111/j.1365-313X.2008.03769.x
  38. Bin Rahman AR, Zhang J. Flood and drought tolerance in rice: Opposite but may coexist. Food Energy Secur. 2016;5(2):76-88. https://doi.org/10.1002/fes3.79
  39. Kulichikhin K, Yamauchi T, Watanabe K, Nakazono M. Biochemical and molecular characterization of rice (Oryza sativa L.) roots forming a barrier to radial oxygen loss. Plant Cell Environ. 2014;37(10):2406-20. https://doi.org/10.1111/pce.12294
  40. Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, et al. Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot. 2011;107(1):89-99. https://doi.org/10.1093/aob/mcq221
  41. Bailey-Serres J, Voesenek L. Flooding stress: Acclimations and genetic diversity. Annu Rev Plant Biol. 2008;59:313-39. https://doi.org/10.1146/annurev.arplant.59.032607.092752
  42. Azarin KV, Usatov AV, Kostylev PI. Molecular breeding of submergence-tolerant rice. Annu Res Rev Biol. 2017;1-10. https://doi.org/10.9734/ARRB/2017/35616
  43. Ayano M, Kani T, Kojima M, Sakakibara H, Kitaoka T, Kuroha T, et al. Gibberellin biosynthesis and signal transduction is essential for internode elongation in deep water rice. Plant Cell Environ. 2014;37(10):2313-24. https://doi.org/10.1111/pce.12377
  44. Minami A, Yano K, Gamuyao R, Nagai K, Kuroha T, Ayano M, et al. Time-course transcriptomics analysis reveals key responses of submerged deep water rice to flooding. Plant Physiol. 2018;176(4):3081-102. https://doi.org/10.1104/pp.17.00858
  45. Kuroha T, Nagai K, Gamuyao R, Wang DR, Furuta T, Nakamori M, et al. Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science. 2018;361(6398):181-86. https://doi.org/10.1126/science.aat1577
  46. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature. 2006;442(7103):705-08. https://doi.org/10.1038/nature04920
  47. Fukao T, Xu K, Ronald PC, Bailey-Serres J. A variable cluster of ethylene response factor–like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell. 2006;18(8):2021-34. https://doi.org/10.1105/tpc.106.043000
  48. Schmitz AJ, Folsom JJ, Jikamaru Y, Ronald P, Walia H. SUB 1 A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. New Phytol. 2013;198(4):1060-70. https://doi.org/10.1111/nph.12202
  49. Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D. Submergence tolerant rice: SUB1’s journey from landrace to modern cultivar. Rice. 2010;3(2):138-47. https://doi.org/10.1007/s12284-010-9048-5
  50. Ahmed F, Rafii M, Ismail MR, Juraimi AS, Rahim H, Asfaliza R, et al. Waterlogging tolerance of crops: Breeding, mechanism of tolerance, molecular approaches and future prospects. BioMed Res Int. 2013;2013. https://doi.org/10.1155/2013/963525
  51. Vergara BS, Mazaredo A. Screening for resistance to submergence under greenhouse conditions. In Proceedings International Seminar on Deepwater Rice. Dhaka, Bangladesh: Bangladesh Rice Research Institute; 1975. p. 67–70.
  52. Angaji SA, Septiningsih EM, Mackill D, Ismail AM. QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica. 2010;172:159-68. https://doi.org/10.1007/s10681-009-0014-5
  53. Puckridge DW, Kupkanchanul T, Palaklang W, Kupkanchanakul K. Production of rice and associated crops in deeply flooded areas of the Chao Phraya delta. In Proceedings of the International Conference: The Chao Phraya Delta: Historical Development, Dynamics and Challenges of Thailand’s Rice Bowl, Bangkok, Thailand, 12–15 December 2000; p. 12–15.
  54. Nakamura M, Noguchi K. Tolerant mechanisms to O2 deficiency under submergence conditions in plants. J Plant Res. 2020;133:343-71. https://doi.org/10.1007/s10265-020-01176-1
  55. Dos Santos RS, Farias D da R, Pegoraro C, Rombaldi CV, Fukao T, Wing RA, et al. Evolutionary analysis of the SUB1 locus across the Oryza genomes. Rice. 2017;10:1-5. https://doi.org/10.1186/s12284-016-0140-3
  56. Perata P, Voesenek LA. Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci. 2007;12(2):43-46. https://doi.org/10.1016/j.tplants.2006.12.005
  57. Fukao T, Yeung E, Bailey-Serres J. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell. 2011;23(1):412-27. https://doi.org/10.1105/tpc.110.080325
  58. Fukao T, Bailey-Serres J. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci. 2008;105(43):16814-19. https://doi.org/10.1073/pnas.0807821105
  59. De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, et al. Brassinosteroids antagonize gibberellin-and salicylate-mediated root immunity in rice. Plant Physiol. 2012;158(4):1833-46. https://doi.org/10.1104/pp.112.193672
  60. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, et al. Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1 and gibberellin. Plant Cell. 2007;19(7):2140-55. https://doi.org/10.1105/tpc.106.043729
  61. Singh S, Mackill DJ, Ismail AM. Responses of SUB1 rice introgression lines to submergence in the field: Yield and grain quality. Field Crops Res. 2009;113(1):12-23. https://doi.org/10.1016/j.fcr.2009.04.003
  62. Nagai K, Hattori Y, Ashikari M. Stunt or elongate? Two opposite strategies by which rice adapts to floods. J Plant Res. 2010;123:303-09. https://doi.org/10.1007/s10265-010-0332-7
  63. Niroula RK, Pucciariello C, Ho VT, Novi G, Fukao T, Perata P. SUB1A-dependent and independent mechanisms are involved in the flooding tolerance of wild rice species. Plant J. 2012;72(2):282-93. https://doi.org/10.1111/j.1365-313X.2012.05078.x
  64. HilleRisLambers D, Vergara BS. Summary results of an international collaboration on screening methods for flood tolerance. In: Proceedings of the 1981 international deepwater rice workshop. International Rice Research Institute, Los Baños, Philippines, 1982. p. 347–53.
  65. Mohanty H, Chaudhary R. Breeding for submergence tolerance in rice in India. Prog Rainfed Low land Rice. 1986;191-200.
  66. Mackill D, Amante M, Vergara B, Sarkarung S. Improved semidwarf rice lines with tolerance to submergence of seedlings. Crop Sci. 1993;33(4):749-53. https://doi.org/10.2135/cropsci1993.0011183X003300040023x
  67. Loreti E, Valeri MC, Novi G, Perata P. Gene regulation and survival under hypoxia requires starch availability and metabolism. Plant Physiol. 2018;176(2):1286-98. https://doi.org/10.1104/pp.17.01002
  68. Toledo AMU, Ignacio JCI, Casal Jr C, Gonzaga ZJ, Mendioro MS, Septiningsih EM. Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breed Biotech. 2015;3:77–87.
  69. Baltazar MD, Ignacio JCI, Thomson MJ, Ismail AM, Mendioro MS, Septiningsih EM. QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica. 2014;197:251-60. https://doi.org/10.1007/s10681-014-1064-x
  70. Jiang L, Liu S, Hou M, Tang J, Chen L, Zhai H, et al. Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field Crops Res. 2006;98(1):68-75. https://doi.org/10.1016/j.fcr.2005.12.015
  71. Zhang M, Lu Q, Wu W, Niu X, Wang C, Feng Y, et al. Association mapping reveals novel genetic loci contributing to flooding tolerance during germination in Indica rice. 2017; https://doi.org/10.3389/fpls.2017.00678
  72. Nishimura T, Sasaki K, Yamaguchi T, Takahashi H, Yamagishi J, Kato Y. Detection and characterization of quantitative trait loci for coleoptile elongation under anaerobic conditions in rice. Plant Prod Sci. 2020;23(3):374-83. https://doi.org/10.1080/1343943X.2020.1740600
  73. Jeong J, Cho Y, Jeong J, Mo Y, Kim C, Kim W, et al. QTL mapping and effect confirmation for anaerobic germination tolerance derived from the japonica weedy rice landrace PBR. Plant Breed. 2020;139(1):83-92. https://doi.org/10.1111/pbr.12753
  74. Kuya N, Sun J, Iijima K, Venuprasad R, Yamamoto T. Novel method for evaluation of anaerobic germination in rice and its application to diverse genetic collections. Breed Sci. 2019;69(4):633-39. https://doi.org/10.1270/jsbbs.19003
  75. Xu K, Mackill DJ. A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed. 1996;2:219-24. https://doi.org/10.1007/BF00564199
  76. Toojinda T, Siangliw M, Tragoonrung S, Vanavichit A. Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot. 2003;91(2):243-53. https://doi.org/10.1093/aob/mcf072
  77. Tiwari DN. A critical review of submergence tolerance breeding beyond Sub 1 gene to mega varieties in the context of climate change. Int J Adv Sci Res Eng. 2018;4:140-48.
  78. Winkel A, Pedersen O, Ella E, Ismail AM, Colmer TD. Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. J Exp Bot. 2014;65(12):3225-33. https://doi.org/10.1093/jxb/eru166
  79. Hamamura K, Kupkanchanakul T. Inheritance of floating ability in rice. Jpn J Breed. 1979;29(3):211-16. https://doi.org/10.1270/jsbbs1951.29.211
  80. Sripongpangkul K, Posa G, Senadhira D, Brar D, Huang N, Khush G, et al. Genes/QTLs affecting flood tolerance in rice. Theor Appl Genet. 2000;101:1074-81. https://doi.org/10.1007/s001220051582
  81. Nemoto K, Ukai Y, Tang DQ, Kasai Y, Morita M. Inheritance of early elongation ability in floating rice revealed by diallel and QTL analyses. Theor Appl Genet. 2004;109:42-47. https://doi.org/10.1007/s00122-004-1600-5
  82. Kawano R, Doi K, Yasui H, Mochizuki T, Yoshimura A. Mapping of QTLs for floating ability in rice. Breed Sci. 2008;58(1):47-53. https://doi.org/10.1270/jsbbs.58.47
  83. Chakraborty K, Guru A, Jena P, Ray S, Guhey A, Chattopadhyay K, et al. Rice with SUB1 QTL possesses greater initial leaf gas film thickness leading to delayed perception of submergence stress. Ann Bot. 2021;127(2):251-65. https://doi.org/10.1093/aob/mcaa171
  84. Liang Y, Biswas S, Kim B, Bailey-Serres J, Septiningsih EM. Improved transformation and regeneration of indica rice: disruption of SUB1A as a test case via CRISPR-Cas9. Int J Mol Sci. 2021;22(13):6989. https://doi.org/10.3390/ijms22136989
  85. Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, et al. Development of submergence-tolerant rice cultivars: The Sub1 locus and beyond. Ann Bot. 2009;103(2):151-60. https://doi.org/10.1093/aob/mcn206
  86. Sarkar RK, Panda D. Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics. Funct Plant Biol. 2009;36(3):222-33. https://doi.org/10.1071/FP08218
  87. Xu K, Deb R, Mackill DJ. A microsatellite marker and a codominant PCR-based marker for marker-assisted selection of submergence tolerance in rice. Crop Sci. 2004;44(1):248-53. https://doi.org/10.2135/cropsci2004.2480
  88. Collard B, Mackill D. Marker-assisted selection: An approach for precision plant breeding in the 21st century. Philos Trans R Soc B Rev Doi. 2006;10.
  89. Sarkar R, Panda D, Reddy J, Patnaik S, Mackill DJ, Ismail AM. Performance of submergence tolerant rice (Oryza sativa) genotypes carrying the Sub1 quantitative trait locus under stressed and nonstressed natural field conditions. 2009; Indian J Agric Sci. 79;876–83.
  90. Manzanilla D, Paris T, Vergara G, Ismail A, Pandey S, Labios R, et al. Submergence risks and farmers’ preferences: Implications for breeding Sub1 rice in Southeast Asia. Agric Syst. 2011;104(4):335-47. https://doi.org/10.1016/j.agsy.2010.12.005
  91. Kim S, Kim C, Jeong J, Reinke RF, Jeong J. Marker-assisted breeding for improvement of anaerobic germination in japonica rice (Oryza sativa). Plant Breed. 2019;138(6):810-19. https://doi.org/10.1111/pbr.12719
  92. Septiningsih EM, Hidayatun N, Sanchez DL, Nugraha Y, Carandang J, Pamplona AM, et al. Accelerating the development of new submergence tolerant rice varieties: The case of Ciherang-Sub1 and PSB Rc18-Sub1. Euphytica. 2015;202:259-68. https://doi.org/10.1007/s10681-014-1287 x
  93. Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM. Submergence and waterlogging stress in plants: A review highlighting research opportunities and understudied aspects. Front Plant Sci. 2019;10:340. https://doi.org/10.3389/fpls.2019.00340
  94. Kuanar SR, Ray A, Sethi SK, Chattopadhyay K, Sarkar RK. Physiological basis of stagnant flooding tolerance in rice. Rice Sci. 2017;24(2):73-84. https://doi.org/10.1016/j.rsci.2016.08.008
  95. Shanmugam A, Manivelan K, Deepika K, Nithishkumar G, Blessy V, Monihasri RB, et al. Unraveling the genetic potential of native rice (Oryza sativa L.) landraces for tolerance to early-stage submergence.Front Plant Sci. 2023;14:1083177. https://doi.org/10.3389/fpls.2023.1083177
  96. Sarkar R, Reddy J, Patnaik S, Gautam P, Lal B. Submergence tolerance. In: ICAR-NRRI; 2017.
  97. Gonzaga ZJC, Carandang J, Sanchez DL, Mackill DJ, Septiningsih EM. Mapping additional QTLs from FR13A to increase submergence tolerance in rice beyond SUB1. Euphytica. 2016;209:627-36. https://doi.org/10.1007/s10681-016-1636-z
  98. Dixit S, Singh A, Sandhu N, Bhandari A, Vikram P, Kumar A. Combining drought and submergence tolerance in rice: Marker-assisted breeding and QTL combination effects. Mol Breed. 2017;37:1-12. https://doi.org/10.1007/s11032-017-0737-2
  99. Singh A, Carandang J, Gonzaga ZJC, Collard BC, Ismail AM, Septiningsih EM. Identification of QTLs for yield and agronomic traits in rice under stagnant flooding conditions. Rice. 2017;10:1-18. https://doi.org/10.1186/s12284-017-0154-5
  100. Arya K, Shylaraj K. Physiological and antioxidant responses associated with Sub1 gene introgressed rice (Oryza sativa L.) lines under complete submergence. Physiol Mol Biol Plants. 2023;29(11):1763-76. https://doi.org/10.1007/s12298-023-01400-x
  101. John D, Shylaraj K. Introgression of Sub1 QTL into an elite rice (Oryza sativa L.) variety Jyothi through marker assisted backcross breeding. J Trop Agric. 2017;55(1):1-11.
  102. Septiningsih EM, Ignacio JCI, Sendon PM, Sanchez DL, Ismail AM, Mackill DJ. QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet. 2013;126:1357-66. https://doi.org/10.1007/s00122-013-2057-1
  103. Ghosal S, Casal C, Quilloy FA, Septiningsih EM, Mendioro MS, Dixit S. Deciphering genetics underlying stable anaerobic germination in rice: Phenotyping, QTL identification and interaction analysis. Rice. 2019;12:1-15. https://doi.org/10.1186/s12284-019-0305-y
  104. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature. 2009;460(7258):1026-30. https://doi.org/10.1038/nature08258
  105. ICAR, KRISHI publication and data inventory repository. Rice ecosystems in India [Internet]. India: ICAR, Rice Knowledge Management Portal; 2013[2024 Aug 12]. Available from: http://krishi.icar.gov.in/jspui/handle/123456789/33998
  106. Bhattacharyya P, Chakraborty K, Molla K, Poonam A, Bhaduri D, Sah R, et al. Climate resilient technologies for rice based production systems in Eastern India. ICAR-Natl Rice Res Inst Cuttack Odisha. 2022;408.
  107. Mackill DJ, Ismail A, Singh US, Labios RV, Paris T. Development and rapid adoption of submergence-tolerant (Sub1) rice varieties. Adv Agron. 2012;115:299-352. https://doi.org/10.1016/B978-0-12-394276-0.00006-8

Downloads

Download data is not yet available.