Advertisement

Genetics and Breeding of Flooding Tolerance in Rice

Chapter

Abstract

Flooding is a frequent natural calamity, affecting global food supply and financial security. The intensity of rainfall events is expected to increase under future climate change scenarios, which will greatly impact rice production. Different flooding patterns can cause damage or complete yield loss in rice plants at different stages of growth. This includes (a) complete submergence due to flash flood at vegetative or pre-flowering stages, (b) stagnant flooding of medium-deep water and deepwater or floating rice, and (c) submergence at germination or anaerobic germination. Different molecular and physiological mechanisms underly tolerance to each type of flooding. Several major QTLs have been mapped and several key genes underlying the QTLs have been cloned. Remarkable progress has been achieved through conventional and molecular breeding strategies in developing tolerant varieties to mitigate the impact of different flood events. This effort will be continued in the future by incorporating new QTLs/genes and tolerance to other abiotic and biotic stresses according to the needs of the target regions. Genetics, genomics, and other modern technologies will also be continuously explored to further our understanding of how rice plants cope with different types of flooding stress.

Keywords

Flooding tolerance Sub1 varieties Stagnant flooding Deepwater rice Anaerobic germination QTLs Genes Molecular breeding 

Notes

Acknowledgment

The work of the authors reported here was supported by the Bill and Melinda Gates Foundation (BMGF) through the Stress-Tolerant Rice for Africa and South Asia (STRASA) projects, grants from the German Federal Ministry of Economic Cooperation and Development (BMZ), and Global Rice Science Partnership (GRiSP). Additional support to E.M.S. was provided by the National Institute of Food and Agriculture, US Department of Agriculture under award number 2017-67013-26194 and Hatch project 1009300.

References

  1. Ahmed F, Rafii MY, Ismail MR, Juraimi AS, Rahim HA, Latif MA, Hasan MM, Tanweer FA (2016) The addition of submergence-tolerant Sub1 gene into high yielding MR219 rice variety and analysis of its BC2F3 population in terms of yield and yield contributing characters to select advance lines as a variety. Biotechnol Biotechnol Equip 30:853–863CrossRefGoogle Scholar
  2. Angaji SA, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.) Euphytica 172:159–168CrossRefGoogle Scholar
  3. Auffhammer M, Ramanathan V, Vincent JR (2012) Climate change, the monsoon, and rice yield in India. Clim Chang 111:411–424CrossRefGoogle Scholar
  4. Ayano M, Kani T, Kojima M, Sakakibara H, Kitaoka T, Kuroha T, Angeles-Shim RB, Kitano H, Nagai K, Ashikari M (2014) Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ 37:2313–2324PubMedPubMedCentralGoogle Scholar
  5. Baltazar M, Ignacio J, Thomson M, Ismail A, Mendioro M, Septiningsih E (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197:251–260CrossRefGoogle Scholar
  6. Cai W, Santoso A, Wang G, Weller E, Wu L, Ashok K, Masumoto Y, Yamagata T (2014) Increased frequency of extreme Indian Ocean dipole events due to greenhouse warming. Nature 510:254–258CrossRefPubMedGoogle Scholar
  7. Catling D (1992) Rice in deep water. International Rice Research Institute, ManilaCrossRefGoogle Scholar
  8. Collard BCY, Kato Y, Septiningsih EM, Ismail AM, Mackill DJ (2013a) Defining IRRI’s role in the EIRLSBN: current status and future directions. In: Collard BCY, Ismail AM, Hardy B (eds) EIRLSBN: twenty years of achievements in rice breeding. International Rice Research Institute, Manila, pp 135–144Google Scholar
  9. Collard BCY, Septiningsih EM, Das SR, Carandang JJ, Pamplona AM, Sanchez DL, Kato Y, Ye G, Reddy JN, Singh US, Iftekharuddaula KM, Venuprasad R, Vera-Cruz CN, Mackill DJ, Ismail AM (2013b) Developing new flood-tolerant varieties at the International Rice Research Institute (IRRI). SABRAO J Breed Genet 45:42–56Google Scholar
  10. Dar MH, de Janvry A, Emerick K, Raitzer D, Sadoulet E (2013) Flood-tolerant rice reduces yield variability and raises expected yield, differentially benefitting socially disadvantaged groups. Sci Rep 3:3315CrossRefPubMedPubMedCentralGoogle Scholar
  11. dos Santos RS, Farias DD, Pegoraro C, Rombaldi CV, Fukao T, Wing RA, de Oliveira AC (2017) Evolutionary analysis of the SUB1 locus across the Oryza genomes. Rice 10:4CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fukao T, Bailey-Serres J (2008) Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci USA 105:16814–16819Google Scholar
  13. Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gonzaga ZJC, Carandang J, Sanchez DL, Mackill DJ, Septiningsih EM (2016) Mapping additional QTLs from FR13A to increase submergence tolerance in rice beyond SUB1. Euphytica 209:627–636CrossRefGoogle Scholar
  15. Gonzaga ZJC, Carandang J, Singh A, Collard BCY, Thomson MJ, Septiningsih EM (2017) Mapping QTLs for submergence tolerance in rice using a population fixed for SUB1A tolerant allele. Mol Breed 37:47CrossRefGoogle Scholar
  16. Graham RJD (1913) Preliminary note on the classification of rice in the Central Provinces. Published for the Imperial department of agriculture in India, by Thacker W. Thacker & co., Calcutta, LondonGoogle Scholar
  17. Guo F, Han N, Xie YK, Fang K, Yang YN, Zhu MY, Wang JH, Bian HW (2016) The miR393a/target module regulates seed germination and seedling establishment under submergence in rice (Oryza sativa L.) Plant Cell Environ 39:2288–2302CrossRefPubMedGoogle Scholar
  18. Hattori Y, Miura K, Asano K, Yamamoto E, Mori H, Kitano H, Matsuoka M, Ashikari M (2007) A major QTL confers rapid internode elongation in response to water rise in deepwater rice. Breed Sci 57:305–314CrossRefGoogle Scholar
  19. Hattori Y, Nagai K, Mori H, Kitano H, Matsuoka M, Ashikari M (2008) Mapping of three QTLs that regulate internode elongation in deepwater rice. Breed Sci 58:39–46CrossRefGoogle Scholar
  20. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu JZ, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1031CrossRefPubMedGoogle Scholar
  21. HilleRisLambers D, Vergara BS (1982) Summary results of an international collaboration on screening methods for flood tolerance, Proceedings of the 1981 International Deepwater Rice Workshop. International Rice Research Institute, Los Baños, pp 347–353Google Scholar
  22. Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nat Clim Chang 3:816–821CrossRefGoogle Scholar
  23. Hsu SK, Tung CW (2015) Genetic mapping of anaerobic germination-associated QTLs controlling coleoptile elongation in rice. Rice 8:38CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hwang ST, Choi D (2016) A novel rice protein family of OsHIGDs may be involved in early signalling of hypoxia-promoted stem growth in deepwater rice. Plant Cell Rep 35:2021–2031CrossRefPubMedGoogle Scholar
  25. Iftekharuddaula K, Newaz M, Salam M, Ahmed H, Mahbub M, Septiningsih E, Collard B, Sanchez D, Pamplona A, Mackill D (2011) Rapid and high-precision marker assisted backcrossing to introgress the SUB1 QTL into BR11, the rainfed lowland rice mega variety of Bangladesh. Euphytica 178:83–97CrossRefGoogle Scholar
  26. Iftekharuddaula KM, Ghosal S, Gonzaga ZJ, Amin A, Barman HN, Yasmeen R, Haque MM, Carandang J, Collard BCY, Septiningsih EM (2015) Allelic diversity of newly characterized submergence-tolerant rice (Oryza sativa L.) germplasm from Bangladesh. Genet Resour Crop Evol 63:859–867CrossRefGoogle Scholar
  27. Iftekharuddaula KM, Ahmed HU, Ghosal S, Amin A, Moni ZR, Ray BP, Barman HN, Siddique MA, Collard BCY, Septiningsih EM (2016) Development of early maturing submergence-tolerant rice varieties for Bangladesh. Field Crop Res 190:44–53CrossRefGoogle Scholar
  28. IRRI (1986) Progress in rainfed lowland rice. International Rice Research Institute, Los BañosGoogle Scholar
  29. 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 103:197–209CrossRefPubMedGoogle Scholar
  30. Ismail AM, Singh US, Singh S, Dar MH, Mackill DJ (2013) The contribution of submergence-tolerant (Sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. Field Crop Res 152:83–93CrossRefGoogle Scholar
  31. Jackson BR, HilleRisLambers D, Prechachat C (1982) Development of deepwater rice varieties and breeding materials for South and Southeast Asian countries, Proceedings of the 1981 International Deepwater Rice Workshop. International Rice Research Institute, Los Baños, pp 19–28Google Scholar
  32. Jena PP, Bharathkumar S, Reddy JN, Mohapatra T (2015) Introgression of Sub1 locus into highly preferred rice cultivars (Pooja and Pratikshya) in eastern region of India for submergence tolerance through marker assisted backcrossing. Adv Biores 6:45–53Google Scholar
  33. Jiang L, Liu SJ, Hou MY, Tang JY, Chen LM, Zhai HQ, Wan JM (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.) Field Crop Res 98:68–75CrossRefGoogle Scholar
  34. Kang N-Y, Elsner JB (2015) Trade-off between intensity and frequency of global tropical cyclones. Nat Clim Chang 5:661–664CrossRefGoogle Scholar
  35. Kato Y, Collard BCY, Septiningsih EM, Ismail AM (2014) Physiological analyses of traits associated with tolerance of long-term partial submergence in rice. AoB Plants 6:plu058CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kawano R, Doi K, Yasui H, Mochizuki T, Yoshimura A (2008) Mapping of QTLs for floating ability in rice. Breed Sci 58:47–53CrossRefGoogle Scholar
  37. Khush GS (1984) Terminology for rice-growing environments. International Rice Research Institute, ManilaGoogle Scholar
  38. Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, Mendioro MS, Slamet-Loedin IH, Sreenivasulu N, Bailey-Serres J, Ismail AM, Mackill DJ, Septiningsih EM (2015) A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants 1:15124CrossRefPubMedGoogle Scholar
  39. Kumar V, Ladha JK (2011) Direct seeding of rice. Adv Agron 111:297–413CrossRefGoogle Scholar
  40. Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61PubMedGoogle Scholar
  41. Lehmann J, Coumou D, Frieler K (2015) Increased record-breaking precipitation events under global warming. Clim Chang 132:501–515CrossRefGoogle Scholar
  42. Li Z-X, Septiningsih E, Quilloy-Mercado S, McNally K, Mackill D (2011) Identification of SUB1A alleles from wild rice Oryza rufipogon Griff. Genet Resour Crop Evol 58:1237–1242CrossRefGoogle Scholar
  43. Mackill DJ, Amante MM, Vergara BS, Sarkarung S (1993) Improved semidwarf rice lines with tolerance to submergence of seedlings. Crop Sci 33:749–753CrossRefGoogle Scholar
  44. Mackill DJ, Coffman WR, Garrity DP (1996) Rainfed lowland rice improvement. International Rice Research Institute, ManilaGoogle Scholar
  45. Mackill DJ, Ismail AM, Pamplona AM, Sanchez DL, Carandang JJ, Septiningsih E (2010) Stress tolerant rice varieties for adaptation to a changing climate. Crop Environ Bioinform 7:250–259Google Scholar
  46. Mackill DJ, Ismail AM, Singh US, Labios RV, Paris TR (2012) Development and rapid adoption of submergence-tolerant (Sub1) rice varieties. Adv Agron 115:299–352CrossRefGoogle Scholar
  47. Mackill DJ, Collard BCY, Atlin GN, Ismail AM, Sarkarung S (2013) Overview of and historical perspectives on the EIRLSBN. In: BCY C, Ismail AM, Hardy B (eds) EIRLSBN: twenty years of achievements in rice breeding. International Rice Research Institute, Manila, pp 1–6Google Scholar
  48. Nagai K, Kuroha T, Ayano M, Kurokawa Y, Angeles-Shim RB, Shim JH, Yasui H, Yoshimura A, Ashikari M (2012) Two novel QTLs regulate internode elongation in deepwater rice during the early vegetative stage. Breed Sci 62:178–185CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nagai K, Kondo Y, Kitaoka T, Noda T, Kuroha T, Angeles-Shim RB, Yasui H, Yoshimura A, Ashikari M (2014) QTL analysis of internode elongation in response to gibberellin in deepwater rice. AoB Plants 6:plu028CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nandi S, Subudhi PK, Senadhira D, Manigbas NL, Sen-Mandi S, Huang N (1997) Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective genotyping. Mol Gen Genet 255:1–8CrossRefPubMedGoogle Scholar
  51. Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BCY, Septiningsih EM, Vergara G, Sanchez D, Xu K, Ismail AM, Mackill DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767–776CrossRefPubMedGoogle Scholar
  52. Nemoto K, Ukai Y, Tang DQ, Kasai Y, Morita M (2004) Inheritance of early elongation ability in floating rice revealed by diallel and QTL analyses. Theor Appl Genet 109:42–47CrossRefPubMedGoogle Scholar
  53. Pearce DME, Hall KC, Jackson MB (1992) The effects of oxygen, carbon doxide and ethylene on ethylene biosynthesis in relation to shoot extension in seedlings of rice (Oryza sativa) and barnyard grass (Echinochloa oryzoides). Ann Bot 69:441–447CrossRefGoogle Scholar
  54. Prechachat C, Supapaj N, Limkanchanapon W, Jackson BR (1982) Farmer field yield trials for deepwater rice in Thailand, Proceedings of the 1981 International Deepwater Rice Workshop. International Rice Research Institute, Los Baños, pp 173–178Google Scholar
  55. Rao M, Grithlahre S, Bisen P, Pallavi, Singh NK, Dar MH, Singh US, Singh PK (2016) Genetics of marker assisted backcross progenies of the cross HUR 105 X Swarna-SUB1. Int J Agric Environ Biotechnol 9:499CrossRefGoogle Scholar
  56. Reddy JN, Patnaik SSC, Sarkar RK, Das SR, Singh VN, Dana I, Singh NK, Sharma RN, Ahmed T, Sharma KK, Verulkar S, Collard BCY, Pamplona AM, Singh US, Sarkarung S, Mackill DJ, Ismail AM (2013) Overview of the Eastern India Rainfed Lowland Shuttle Breeding Network (EIRLSBN). SABRAO J Breed Genet 45:57–66Google Scholar
  57. Richharia RH, Govindaswami S (1966) Rices of India. Scientific Book Company, PatnaGoogle Scholar
  58. Roychowdhury A (2016) Yes, the Sinhalese have their origins in Bengal, Odisha. Indian Express, New Delhi. http://indianexpress.com/article/research/yes-the-sinhalese-have-their-origins-in-bengal-odisha/ Google Scholar
  59. Rumanti IA, Nugraha Y, Wening RH, Gonzaga ZJC, Suwarno, Nasution A, Kusdiaman D, Septiningsih EM (2016) Development of high-yielding rice varieties suitable for swampy lands in Indonesia. Plant Breed Biotech 4:413–425CrossRefGoogle Scholar
  60. Schmitz AJ, Folsom JJ, Jikamaru Y, Ronald P, Walia H (2013) SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. New Phytol 198:1060–1070CrossRefPubMedGoogle Scholar
  61. Senaveratna JM (1997) The story of the Sinhalese from the most ancient times up to the end of “the Mahavansa” or great dynasty : Vijaya to Maha Sena, B.C. 543 to A.D.302. Asian Educational Services, New DelhiGoogle Scholar
  62. Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Ann Bot 103:151–160CrossRefPubMedGoogle Scholar
  63. Septiningsih EM, Sanchez DL, SIngh N, Sendon PM, Pamplona AM, Heuer S, Mackill DJ (2012) Identifying novel QTLs for submergence tolerance in rice cultivars IR72 and Madabaru. Theor Appl Genet 124:867–874CrossRefPubMedGoogle Scholar
  64. Septiningsih EM, Collard BCY, Heuer S, Bailey-Serres J, Ismail A, Mackill DJ (2013a) Applying genomics tools for breeding submergence tolerance in rice. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: volume 2 – improvement for abiotic stress, quality and yield improvement, Wiley, Hoboken, pp 9–30Google Scholar
  65. Septiningsih EM, Ignacio JCI, Sendon PMD, Sanchez DL, Ismail AM, Mackill DJ (2013b) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet 126:1357–1366CrossRefPubMedGoogle Scholar
  66. Septiningsih EM, Hidayatun N, Sanchez DL, Nugraha Y, Carandang J, Pamplona AM, Collard BCY, Ismail AM, Mackill DJ (2015) Accelerating the development of new submergence tolerant rice varieties: the case of Ciherang-Sub1 and PSB Rc18-Sub1. Euphytica 202:259–268CrossRefGoogle Scholar
  67. Setter TL, Ella ES, Valdez AP (1994) Relationship between coleoptile elongation and alcoholic fermentation in rice exposed to anoxia. 2. Cultivar differences. Ann Bot 74:273–279CrossRefGoogle Scholar
  68. Singh S, Mackill DJ, Ismail AM (2009) Responses of SUB1 rice introgression lines to submergence in the field: yield and grain quality. Field Crop Res 113:12–23CrossRefGoogle Scholar
  69. Singh N, Dang TTM, Vergara GV, Pandey DM, Sanchez D, Neeraja CN, Septiningsih EM, Mendioro M, Tecson-Mendoza EM, Ismail AM, Mackill DJ, Heuer S (2010) Molecular marker survey and expression analyses of the rice submergence-tolerance gene SUB1A. Theor Appl Genet 121:1441–1453CrossRefPubMedGoogle Scholar
  70. Singh S, Mackill DJ, Ismail AM (2011) Tolerance of longer-term partial stagnant flooding is independent of the SUB1 locus in rice. Field Crop Res 121:311–323CrossRefGoogle Scholar
  71. Singh D, Tsiang M, Rajaratnam B, Diffenbaugh NS (2014) Observed changes in extreme wet and dry spells during the South Asian summer monsoon season. Nat Clim Chang 4:456–461CrossRefGoogle Scholar
  72. Singh R, Singh Y, Xalaxo S, Verulkar S, Yadav N, Singh S, Singh N, Prasad KS, Kondayya K, Rao PV, Rani MG, Anuradha T, Suraynarayana Y, Sharma PC, Krishnamurthy SL, Sharma SK, Dwivedi JL, Singh AK, Singh PK, Nilanjay, Singh NK, Kumar R, Chetia SK, Ahmad T, Rai M, Perraju P, Pande A, Singh DN, Mandal NP, Reddy JN, Singh ON, Katara JL, Marandi B, Swain P, Sarkar RK, Singh DP, Mohapatra T, Padmawathi G, Ram T, Kathiresan RM, Paramsivam K, Nadarajan S, Thirumeni S, Nagarajan M, Singh AK, Vikram P, Kumar A, Septiningshih E, Singh US, Ismail AM, Mackill D, Singh NK (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 242:278–287CrossRefPubMedGoogle Scholar
  73. Singh A, Carandang J, Gonzaga ZJC, Collard BCY, Ismail AM, Septiningsih EM (2017) Identification of QTLs for yield and agronomic traits in rice under stagnant flooding conditions. Rice 10:15Google Scholar
  74. Toledo AMU, Ignacio JCI, Casal C Jr, Gonzaga ZJ, Mendioro MS, Septiningsih EM (2015) Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breed Biotech 3:77–87CrossRefGoogle Scholar
  75. Toojinda T, Siangliw M, Tragoonrung S, Vanavichit A (2003) Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot 91:243–253CrossRefPubMedPubMedCentralGoogle Scholar
  76. Vergara BS, Mazaredo A (1975) Screening for resistance to submergence under greenhouse conditions, Proceedings of the International Seminar on Deepwater Rice, August 1974. Bangladesh Rice Research Institute, Dhaka, pp 67–70Google Scholar
  77. Vergara GV, Nugraha Y, Esguerra MQ, Mackill DJ, Ismail AM (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:plu055CrossRefPubMedPubMedCentralGoogle Scholar
  78. Wake B (2013) Flooding costs. Nat Clim Chang 3:778–778CrossRefGoogle Scholar
  79. Williams JF, Roberts SR, Hill JE, Scardaci SC, Tibbits G (1990) Managing water for weed control in rice. Calif Agric 44(5):6–10Google Scholar
  80. Xu K, Mackill DJ (1996) A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed 2:219–224CrossRefGoogle Scholar
  81. Xu K, Xu X, Ronald PC, Mackill DJ (2000) A high-resolution linkage map in the vicinity of the rice submergence tolerance locus Sub1. Mol Gen Genet 263:681–689CrossRefPubMedGoogle Scholar
  82. Xu K, Xia X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene response factor-like gene that confers submergence tolerance to rice. Nature 442:705–708CrossRefPubMedGoogle Scholar
  83. Yamauchi M, Herradura PS, Aguilar AM (1994) Genotype difference in rice postgermination growth under hypoxia. Plant Sci 100:105–113CrossRefGoogle Scholar
  84. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by Trehalose-6-phosphate. Plant Physiol 149:1860–1871CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zhang M, Lu Q, Wu W, Niu X, Wang C, Feng Y, Xu Q, Wang S, Yuan X, Yu H, Wang Y, Wei X (2017) Association mapping reveals novel genetic loci contributing to flooding tolerance during germination in indica rice. Front Plant Sci 8:678CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zhou X, Zhang ZL, Park J, Tyler L, Yusuke J, Qiu K, Nam EA, Lumba S, Desveaux D, McCourt P, Kamiya Y, Sun TP (2016) The ERF11 transcription factor promotes internode elongation by activating gibberellin biosynthesis and signaling. Plant Physiol 171:2760–2770PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Soil and Crop SciencesTexas A&M UniversityCollege StationUSA
  2. 2.MARS Inc. and Department of Plant SciencesUniversity of CaliforniaDavisUSA

Personalised recommendations