Advertisement

Euphytica

, 215:19 | Cite as

Evaluation of anaerobic germinability in various rice subpopulations: identifying genotypes suitable for direct-seeded rice cultivation

  • Muhammad Rauf
  • Yu-Mi Choi
  • Sukyeung Lee
  • Myung-Chul Lee
  • Sejong Oh
  • Do Yoon HyunEmail author
Article
  • 53 Downloads

Abstract

Anaerobic conditions in waterlogged soil lead to low germination rates, which significantly reduce crop yields. Good seed germination is prerequisite for direct-seeded cultivation of rice to obtain optimal yields not only in irrigated lowland but most importantly in rain-fed and waterlogged areas where water supply could be more than needed. Due to the limited availability of rice genotypes suitable for anaerobic germination, there is an urgent need to select diverse rice germplasm with enhanced anaerobic germinability. In this study, we evaluated 185 rice accessions from six subpopulations for germination rate (AGR) and coleoptile length (ACL) under anaerobic conditions. The highest average AGR (60%) and longest average ACL (2.13 cm) were observed in tropical japonica (TRJ) and temperate japonica (TEJ) germplasm, respectively. Meanwhile, the highest proportion of accessions with “very long” ACL was in the TEJ subpopulation, whereas those with the “highest” AGR were in the aus subpopulation based on our criteria. We selected seven strong accessions for anaerobic germinability (AG) based on AGR and ACL and analyzed the relative expression patterns of four AG-related genes in strong and weak accessions via qRT-PCR. In general, proton pyrophosphatase locus (OVP3) was expressed at the highest levels in strong accessions, whereas the expression level of rice ethylene response element binding protein locus (EREBP1) did not significantly differ among accessions under normal and anaerobic conditions. The relative expression results of rice alpha amylase locus (RAmy3D) and OVP3 showed distinct patterns and divided all strong accessions into two groups, suggesting that major genes involved in AG may vary depending on the germplasm. These findings could be helpful for breeders and lay the foundation for further genetic analysis.

Keywords

Anaerobic germination Rice subpopulation Evaluation Gene expression Direct-seeded rice 

Notes

Acknowledgements

This study was supported by the “Research Program for Agricultural Science and Technology Development (Project No. PJ010871)” of the National Institute of Agricultural Sciences, RDA.

References

  1. 3K RGP (2014) The 3,000 rice genomes project. Gigascience 3:7CrossRefGoogle Scholar
  2. Adachi Y, Sugiyama M, Sakagami JI, Fukuda A, Ohe M, Watanabe H (2015) Seed germination and coleoptile growth of new rice lines adapted to hypoxic conditions. Plant Prod Sci 18:471–475CrossRefGoogle Scholar
  3. 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
  4. Atwell BJ, Waters I, Greenway H (1982) The effect of oxygen and turbulence on elongation of coleoptiles of submergence-tolerant and -intolerant rice cultivars. J Exp Bot 33:1030–1044CrossRefGoogle Scholar
  5. Atwell BJ, Greenway H, Colmer TD (2015) Efficient use of energy in anoxia-tolerant plants with focus on germinating rice seedlings. New Phytol 206:36–56PubMedCrossRefGoogle Scholar
  6. Baltazar MD, Ignacio JC, Thomson MJ, Ismail AM, Mendioro MS, Septiningsih EM (2014) QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197:251–260CrossRefGoogle Scholar
  7. Civáň P, Craig H, Cox CJ, Brown TA (2015) Three geographically separate domestications of Asian rice. Nat Plants 1:1–5Google Scholar
  8. Das KK, Sarkar RK, Ismail AM (2005) Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice. Plant Sci 168:131–136CrossRefGoogle Scholar
  9. Eizenga GC, Ali ML, Bryant RJ, Yeater KM, McClung AM, McCouch SR (2014) Registration of the rice diversity panel 1 for genomewide association studies. J Plant Regist 8:109–116CrossRefGoogle Scholar
  10. Farooq M, Siddique KH, Rehman H, Aziz T, Lee DJ, Wahid A (2011) Rice direct seeding: experiences, challenges and opportunities. Soil Tillage Res 111:87–98CrossRefGoogle Scholar
  11. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638PubMedPubMedCentralCrossRefGoogle Scholar
  12. Gibbs J, Morrell S, Valdez A, Setter TL, Greenway H (2000) Regulation of alcoholic fermentation in coleoptiles of two rice cultivars differing in tolerance to anoxia. J Exp Bot 51:785–796PubMedCrossRefGoogle Scholar
  13. Hsu SK, Tung CW (2015) Genetic mapping of anaerobic germination associated QTLs controlling coleoptile elongation in rice. Rice 8:1–12CrossRefGoogle Scholar
  14. 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 8:762PubMedPubMedCentralCrossRefGoogle Scholar
  15. Huang J, Yamaguchi J, Akita S (2000) Expression of the ar-amylase gene RAmy3D in rice (Oryza sativa L.) under aerobic, hypoxic and anoxic conditions. Plant Prod Sci 3:213–218CrossRefGoogle Scholar
  16. Huang S, Colmer TD, Millar AH (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci 13:221–227PubMedCrossRefGoogle Scholar
  17. 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 L.). Ann Bot 103:197–209PubMedCrossRefGoogle Scholar
  18. Ismail AM, Johnson DE, Ella ES, Vergara GV, Baltazar AM (2012) Adaptation to flooding during emergence and seedling growth in rice and weeds, and implications for crop establishment. AoB Plants 2012:1–18CrossRefGoogle Scholar
  19. Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot 91:227–241PubMedPubMedCentralCrossRefGoogle Scholar
  20. Jiang L, Hou M, Wang C, Wan J (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa L.). Rice Sci 11:238–244Google Scholar
  21. Kordan HA (1974) The rice shoot in relation to oxygen supply and root growth in seedlings germinating under water. New Phytol 73:695–697CrossRefGoogle Scholar
  22. Kumar V, Ladha JK (2011) Direct seeding of rice: recent developments and future research needs. Adv Agron 111:297–413CrossRefGoogle Scholar
  23. Ladha JK, Kumar V, Alam MM, Sharma S, Gathala M, Chandna P, Saharawat YS, Balasubramanian V (2009) Integrating crop and resource management technologies for enhanced productivity, profitability, and sustainability of the rice-wheat system in South Asia. In: Ladha JK, Singh Y, Erenstein O, Hardy B (eds) Integrated crop and resource management in the rice-wheat system of south Asia. International Rice Research Institute, Los Banos, pp 69–108Google Scholar
  24. Liu Q, Shang Q, Burton RA, Shirley NJ, Atwell BJ (2010) Expression of vacuolar H+-pyrophosphatase (OVP3) is under control of an anoxia-inducible promoter in rice. Plant Mol Biol 72:47–60PubMedCrossRefGoogle Scholar
  25. Magneschi L, Perata P (2009) Rice germination and seedling growth in the absence of oxygen. Ann Bot 103:181–196PubMedCrossRefGoogle Scholar
  26. Manangkil OE, Vu HT, Yoshida S, Mori N, Nakamura C (2008) A simple, rapid and reliable bioassay for evaluating seedling vigor under submergence in indica and japonica rice (Oryza sativa L.). Euphytica 163:267–674CrossRefGoogle Scholar
  27. McGraw-Hill C (2008) Statistix 8.1 Analytical Software, Tallahassee, Florida Maurice/Thomas text. Analytical Software, Tallahassee. ISBN 0073402818Google Scholar
  28. 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 4:1–18CrossRefGoogle Scholar
  29. Miro B, Longkumer T, Entila FD, Kohli A, Ismail AM (2017) Rice seed germination underwater: morpho-physiological responses and the bases of differential expression of alcoholic fermentation enzymes. Front Plant Sci 8:1–17CrossRefGoogle Scholar
  30. Miura K, Lin SY, Yano M, Nagamine T (2001) Mapping quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Breed Sci 51:293–299CrossRefGoogle Scholar
  31. Mohan A, Schillinger WF, Gill KS (2013) Wheat seedling emergence from deep planting depths and its relationship with coleoptile length. PLoS ONE 8:1–9CrossRefGoogle Scholar
  32. Mori S, Fujimoto H, Watanabe S, Ishioka G, Okabe A, Kamei M, Yamauchi M (2012) Physiological performance of iron-coated primed rice seeds under submerged conditions and the stimulation of coleoptile elongation in primed rice seeds under anoxia. Soil Sci Plant Nutr 58:469–478CrossRefGoogle Scholar
  33. Ogiwara H, Terashima K (2001) A varietal difference in coleoptile growth is correlated with seedling establishment of direct-seeded rice in submerged field under low temperature conditions. Plant Prod Sci 4:166–172CrossRefGoogle Scholar
  34. Pandey S, Velasco L (2002) Economics of direct seeding in Asia: patterns of adoption and research priorities. In: Pandey S, Mortimer M, Wade L, Tuong TP, Lopez K, Hardy B (eds) Direct seeding: research strategies and opportunities. International Rice Research Institute, Los Banos, pp 3–14Google Scholar
  35. Perata P, Pozueta-Romero J, Akazawa T, Yamaguchi J (1992) Effect of anoxia on starch breakdown in rice and wheat seeds. Planta 188:611–618PubMedCrossRefGoogle Scholar
  36. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time qRT-PCR. Nucleic Acids Res 29:e45PubMedPubMedCentralCrossRefGoogle Scholar
  37. Plaxton WC, Podesta FE (2006) The functional organisation and control of plant respiration. Crit Rev Plant Sci 25:159–198CrossRefGoogle Scholar
  38. Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015PubMedPubMedCentralCrossRefGoogle Scholar
  39. Rahman ANM, Zhang J (2016) Flood and drought tolerance in rice: opposite but may coexist. Food Energy Secur 5:76–88CrossRefGoogle Scholar
  40. Redoña ED, Mackill DJ (1996) Molecular mapping of quantitative trait loci in japonica rice. Genome 39:395–403PubMedCrossRefGoogle Scholar
  41. Roy SC, Sharma BD (2014) Assessment of genetic diversity in rice (Oryza sativa L.) germplasm based on agro-morphology traits and zinc-iron content for crop improvement. Physiol Mol Biol Plants 20:209–224PubMedPubMedCentralCrossRefGoogle Scholar
  42. Septiningsih EM, Collard BCY, Heuer S, Bailey-Serres J, Ismail AM, Mackill DJ (2013a) Applying genomics tools for breeding submergence tolerance in rice. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: improvement for abiotic stress, quality and yield improvement, vol 2. Wiley-Blackwell, Hoboken, pp 9–30CrossRefGoogle Scholar
  43. Septiningsih EM, Ignacio JC, Sendon PM, 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 126:1357–1366PubMedCrossRefGoogle Scholar
  44. Seshu DV, Krishnasamy V, Siddique SB (1988) Seed vigor in rice. Rice seed health. International Rice Research Institute, Los Banos, pp 315–329Google Scholar
  45. Setter TL, Ellis M, Laureles CV, Ella ES, Senadhira D, Mishra SB et al (1997) Physiology and genetics of submergence tolerance in rice. Ann Bot 79:67–77CrossRefGoogle Scholar
  46. Takahashi H, Greenway H, Matsumura H, Tsutsumi N, Nakazono M (2014) Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water. Ann Bot 113:851–859PubMedPubMedCentralCrossRefGoogle Scholar
  47. Vu HTT, Nguyen GT, Nguyen TT, Vo TTM, Nakamura C (2016) Contribution of seedling vigour and anoxia/hypoxia-responsive genes to submergence tolerance in Vietnamese lowland rice (Oryza sativa L.). Biotechnol Biotechnol Equip 30:842–852CrossRefGoogle Scholar
  48. XLSTAT (2017) Data analysis and statistical solution for Microsoft excel. Addinsoft, ParisGoogle Scholar
  49. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S et al (2006) Sub1A is an ethylene response factor like gene that confers submergence tolerance to rice. Nature 442:705–708PubMedCrossRefGoogle Scholar
  50. Yamauchi M, Winn T (1996) Rice seed vigor and seedling establishment in anaerobic soil. Crop Sci 36:680–686CrossRefGoogle Scholar
  51. Yamauchi M, Aguilar AM, Vaughan DA, Seshu DV (1993) Rice (Oryza sativa L.) germplasm suitable for direct sowing under flooded soil surface. Euphytica 67:177–184CrossRefGoogle Scholar
  52. Yamauchi M, Herradura PS, Aguilar AM (1994) Genotype difference in rice post germination growth under hypoxia. Plant Sci 100:105–113CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Muhammad Rauf
    • 1
  • Yu-Mi Choi
    • 1
  • Sukyeung Lee
    • 1
  • Myung-Chul Lee
    • 1
  • Sejong Oh
    • 1
  • Do Yoon Hyun
    • 1
    Email author
  1. 1.National Agrobiodiversity CenterNational Institute of Agricultural Sciences, RDAJeonjuRepublic of Korea

Personalised recommendations