Skip to main content
Log in

Pyramiding seed dormancy genes to improve resistance of semi-dwarf varieties to pre-harvest sprouting in rice

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

The quantitative trait locus SD1-2 for seed dormancy (SD) is identical to the semi-dawrf1 (sd1) gene prevailing in high-yield varieties of rice. However, sd1 alone appeared not sufficient to overcome the preharvest sprouting (PHS) problem in crop (or hybrid seed) production. This research aimed to address some genetic issues that may impact pyramiding of SD genes to improve semi-dwarf varieties for the PHS resistance. The isolated SD1-2, SD8, and SD10 loci were also associated with plant height (PH), awn or flowering time (FT), with the dormancy-enhancing alleles reducing stem elongation, increasing awned seeds, and promoting flowering, respectively. Allelic variants at SD1-2 and SD8 or SD10 were assembled in the same background as two digenic systems, each consisting of all the nine digenic genotypes. The two systems of plants were evaluated for the four traits and phenotypic data used to model trait correlations and the component additive, dominance, and epistatic effects of the two loci. FT was correlated with PH and germinability, but the correlations were opposite in direction between the two systems. Both additive and non-additive effects contributed to the variation for SD. All the three loci had effects on FT and PH in the digenic system(s). The SD10 alleles altered directions for effect on SD, with the late-flowering allele reducing germinability in the SD1-2 and SD10 system. This research demonstrated that genetic improvement of semi-dwarf cultivars for the PHS resistance involves proper selections for dormancy genes, recipient’s genetic backgrounds, and agronomic traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Data are available upon request.

References

  • Benech-Arnold RL, Rodriguez MV (2018) Pre-harvest sprouting and grain dormancy in Sorghum bicolor: what have we learned? Front Plant Sci 9:811

    Article  Google Scholar 

  • Bessho-Uehara K, Wang DR, Furuta T, Minami A, Nagai K, Gamuyao R, Asano K, Angeles-Shim RB, Shimizu Y, Ayano M, Komeda N, Doi K, Miura K, Toda Y, Kinoshita T, Okuda S, Higashiyama T, Nomoto M, Tada Y, Shinohara H, Matsubayashi Y, Greenberg A, Wu J, Yasui H, Yoshimura A, Mori H, McCouch SR, Ashikari M (2016) Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. Proc Natl Acad Sci U S A 113:8969–8974

    Article  CAS  Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    Article  CAS  Google Scholar 

  • Briggle LW (1980) Pre-harvest sprout damage in wheat in the U.S. Cereal Res Comm 8:245–250

    Google Scholar 

  • Chang TT, Tagumpay O (1973) Inheritance of grain dormancy in relation to growth duration in 10 rice crosses. SABRAO Newsl 5:87–94

    Google Scholar 

  • Chen X, Tian Y, Lu X (2018) Breeding of the dormant thermosensitive genic male-sterile lines of early rice to overcome pre-harvest sprouting of the hybrid seeds. Agronomy 8:191

    Article  CAS  Google Scholar 

  • Debieu M, Tang C, Stich B, Sikosek T, Effgen S, Josephs E, Schmitt J, Nordborg M, Koornneef M, de Meaux J (2013) Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLoS One 8:e61075

    Article  CAS  Google Scholar 

  • Derera NF, Bhatt GM, McMaster GJ (1977) On the problem of pre-harvest sprouting of wheat. Euphytica 26:299–308

    Article  CAS  Google Scholar 

  • Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936

    Article  CAS  Google Scholar 

  • Endo-Higashi N, Izawa T (2011) Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant Cell Physiol 52:1083–1094

    Article  CAS  Google Scholar 

  • Flintham JE, Gale MD (1982) The tom thumb dwarfing gene, Rht3 in wheat. I. Reduced pre-harvest damage to breadmaking quality. Theor Appl Genet 62:121–126

    Article  CAS  Google Scholar 

  • Gu XY, Kianian SF, Foley ME (2004) Multiple loci and epistases control genetic variation for seed dormancy in weedy rice (Oryza sativa). Genetics 166:1503–1516

    Article  CAS  Google Scholar 

  • Gu XY, Kianian SF, Foley ME (2005a) Phenotypic selection for dormancy introduced a set of adaptive haplotypes from weedy into cultivated rice. Genetics 171:695–704

    Article  CAS  Google Scholar 

  • Gu XY, Kianian SF, Hareland GA, Hoffer BL, Foley ME (2005b) Genetic analysis of adaptive syndromes interrelated with seed dormancy in weedy rice (Oryza sativa). Theor Appl Genet 110:1108–1118

    Article  CAS  Google Scholar 

  • Gu XY, Pipatpongpinyo W, Zhang L, Zhou Y, Ye H, Feng J (2018) Two contrasting patterns and underlying genes for coadaptation of seed dormancy and flowering time in rice. Sci Rep 8:16813

    Article  Google Scholar 

  • Himi E, Noda K (2005) Red grain colour gene (R) of wheat is a Myb-type transcription factor. Euphytica 143:239–242

    Article  CAS  Google Scholar 

  • Hori K, Sato K, Takeda K (2007) Detection of seed dormancy QTL in multiple mapping populations derived from crosses involving novel barley germplasm. Theor Appl Genet 115:869–876

    Article  Google Scholar 

  • Jin J, Hua L, Zhu Z, Tan L, Zhao X, Zhang W, Liu F, Fu Y, Cai H, Sun X, Gu P, Xie D, Sun C (2016) GAD1 encodes a secreted peptide that regulates grain number, grain length, and awn development in rice domestication. Plant Cell 28:2453–2463

    Article  CAS  Google Scholar 

  • Johnson LPV (1935) The inheritance of delayed germination in hybrids of Avena fatua and A. sativa. Can J Res 13:367–387

    Article  Google Scholar 

  • Kammenga JE (2017) The background puzzle: how identical mutations in the same gene lead to different disease symptoms. FEBS J 284:3362–3373

    Article  CAS  Google Scholar 

  • Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822

    Article  CAS  Google Scholar 

  • Lee G-A, Jeon Y-A, Lee H-S, Hyun D-Y, Lee J-R, Lee M-C, Lee S-Y, Ma K-H, Koh H-J (2016) Variation in pre-harvest sprouting resistance, seed germination and changes in abscisic acid levels during grain development in diverse rice genetic resources. Plant Genet Resour 16:18–27

    Article  Google Scholar 

  • Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96:997–1003

    Article  CAS  Google Scholar 

  • Lumpkin TA (2015) How a gene from Japan revolutionized the world of wheat: CIMMYT’s quest for combining genes to mitigate threats to global food security. In: Ogihara Y, Takumi S, Handa H (eds) Advances in wheat genetics: from genome to field. Springer, Tokyo

    Google Scholar 

  • Mispan MS, Zhang L, Feng J, Gu XY (2013) Quantitative trait locus and haplotype analyses of wild and crop-mimic traits in U.S. weedy rice. G3 (Bethesda) 3:1049–1059

  • Nave M, Avni R, Ben-Zvi B, Hale I, Distelfeld A (2016) QTLs for uniform grain dimensions and germination selected during wheat domestication are co-located on chromosome 4B. Theor Appl Genet 129:1303–1315

    Article  CAS  Google Scholar 

  • Nelson SK, Steber CM (2016) Gibberellin hormone signal perception: down-regulating DELLA repressors of plant growth and development. In: Hedden P, Thomas SG (Eds), Annual plant reviews, volume 49, The Gibberellins (pp. 153–187). Chichester: Wiley Blackwell

  • Nilsson-Ehle H (1914) Zur Kenntnis der mit der Keimungsphy siologie des Weizens in Zusammenhang stehenden inneren Faktoren. Zeitschrift für Pflanzenzüchtung 2:153–187

    Google Scholar 

  • Olaerts H, Courtin CM (2018) Impact of preharvest sprouting on endogenous hydrolases and technological quality of wheat and bread: a review. Compr Rev Food Sci Food Saf 17:698–713

    Article  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  CAS  Google Scholar 

  • Rodriguez MV, Barrero JM, Corbineau F, Gubler F, Benech-Arnold RL (2015) Dormancy in cereals (not too much, not so little): about the mechanisms behind this trait. Seed Sci Res 25:99–119

    Article  CAS  Google Scholar 

  • Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H, Iwahori S, Matsuoka M (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516

    Article  CAS  Google Scholar 

  • SAS Institute Inc. (2016) Cary, NC, USA

  • Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) A mutant gibberellin-synthesis gene in rice. Nature 416:701–702

    Article  CAS  Google Scholar 

  • Simpson GM (1990) Seed dormancy in grasses. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Tao L, Wang X, Tan H, Chen H, Yang C, Zhuang J, Zheng K (2007) Physiological analysis on pre-harvest sprouting in recombinant inbred rice lines. Front Agric China 1:24–29

    Article  Google Scholar 

  • Van De Velde K, Chandler PM, Van Der Straeten D, Rohde A (2017) Differential coupling of gibberellin responses by Rht-B1c suppressor alleles and Rht-B1b in wheat highlights a unique role for the DELLA N-terminus in dormancy. J Exp Bot 68:443–455

    Google Scholar 

  • Vidigal DS, Marques AC, Willems LA, Buijs G, Méndez-Vigo B, Hilhorst HW, Bentsink L, Picó FX, Alonso-Blanco C (2016) Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana. Plant Cell Environ 39:1737–1748

    Article  CAS  Google Scholar 

  • Wang X, Liu H, Liu G, Mia MS, Siddique KHM, Yan G (2019) Phenotypic and genotypic characterization of near-isogenic lines targeting a major 4BL QTL responsible for pre-harvest sprouting in wheat. BMC Plant Biol 19:348. https://doi.org/10.1186/s12870-019-1961-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye H, Foley ME, Gu XY (2010) New seed dormancy loci detected from weedy rice-derived advanced populations with major QTL alleles removed from the background. Plant Sci 179:612–619

    Article  CAS  Google Scholar 

  • Ye H, Beighley DH, Feng J, Gu XY (2013) Genetic and physiological characterization of two clusters of quantitative trait loci associated with seed dormancy and plant height in rice. G3 (Bethesda) 3:323-331

  • Ye H, Feng J, Zhang L, Zhang J, Mispan MS, Cao Z, Beighley DH, Yang J, Gu XY (2015) Map-based cloning of seed dormancy1-2 identified a gibberellin synthesis gene regulating the development of endosperm-imposed dormancy in rice. Plant Physiol 169:2152–2165

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of Rice, Ed 3. International Rice Research Institute, Manila

    Google Scholar 

  • Zhang L, Lou J, Foley ME, Gu XY (2017) Comparative mapping of seed dormancy loci between tropical and temperate ecotypes of weedy rice (Oryza sativa L.). G3 7:2605-2614

  • Zhu D, Qian Z, Wei H, Guo B, Xu K, Dai Q, Zhang H, Huo Z (2019) The effects of field pre-harvest sprouting on the morphological structure and physicochemical properties of rice (Oryza sativa L.) starch. Food Chem 278:10–16

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Christian De Guzman, Chad Mike, and Ahmed Charif for their technical supports to the field management experiment and seed storage.

Funding

This research was supported by grants from the United States Department of Agriculture-National Institute of Food and Agriculture (2019-67014-29238 and 2018-33522-28795) and American Seed Research Foundation and from the South Dakota Agricultural Extension Station. Missouri Rice Research Farm provided a field for part of this research.

Author information

Authors and Affiliations

Authors

Contributions

UK and WP and JW and MG developed and collected data from the SD1-2 and SD8 and the SD1-2 and SD10 system, respectively; they all participated in the data analyses; XG conceived this research, participated in the data analysis, and wrote the paper. All authors read and approved this paper.

Corresponding author

Correspondence to Xing-You Gu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical standards

The authors declare that the present work complies with ethical standards of South Dakota State University.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Korkmaz, U., Guo, M. et al. Pyramiding seed dormancy genes to improve resistance of semi-dwarf varieties to pre-harvest sprouting in rice. Mol Breeding 40, 93 (2020). https://doi.org/10.1007/s11032-020-01172-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-020-01172-2

Keywords

Navigation