Re-evaluation of the rice ‘Green Revolution’ gene: the weak allele SD1-EQ from japonica rice may be beneficial for super indica rice breeding in the post-Green Revolution era

Abstract

The Green Revolution of the 1960s introduced semi-dwarf cultivars of rice that had reduced lodging and increased harvest indexes. The mutant allele of Semi Dwarf 1 (SD1) is the gene underlying the Green Revolution advances in rice yield. Since that time, most of the commercial semi-dwarf cultivars carry a mutation in SD1. Unlike japonica rice cultivars containing weak functional SD1 alleles, indica rice cultivars owed their diminished stature to a null mutation in SD1. It has been proposed recently that increasing plant height and subsequently plant biomass will increase grain production in semi-dwarf cultivars used in super rice breeding programs. In this study, we evaluated the potential benefit of the weak functional allele of SD1 from japonica rice on yield improvement in the indica rice background. We found that the Green Revolution gene SD1 has pleiotropic effects on tiller number and spikelets per panicle, in addition to plant height in rice. The introduction of the weak allele SD1-EQ from the japonica cultivar ‘Nipponbare (Np)’ led not only to a substantial increase in plant height but also to an increase in yield per plant in the indica cultivar ‘9311’. This result was further confirmed in CRISPR/Cas9-mediated knockout mutants. In addition, heterosis for yield-related traits was detected at the SD1 locus, and SD1-EQ exhibited a potential improved yield in hybrid rice lines. This study provides evidence that the weak functional SD1 allele from japonica rice cultivar ‘Np’, SD1-EQ, is an excellent genetic resource for the improvement of indica rice lines with null alleles of SD1, in the post-Green Revolution era.

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References

  1. Asano K, Takashi T, Miura K, Qian Q, Kitano H, Matsuoka M, Ashikari M (2007) Genetic and molecular analysis of utility of sd1 alleles in rice breeding. Breed Sci 57(1):53–58

    Article  Google Scholar 

  2. Asano K, Yamasaki M, Takuno S, Miura K, Katagiri S, Ito T, Doi K, Wu J, Ebana K, Matsumoto T (2011) Artificial selection for a Green Revolution gene during japonica rice domestication. Proc Natl Acad Sci U S A 108(27):11034–11039

    PubMed  PubMed Central  Article  Google Scholar 

  3. Ashikari M, Sasaki A, Ueguchi-Tanaka M, Itoh H, Nishimura A, Datta S, Ishiyama K, Saito T, Kobayashi M, Khush GS (2002) Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice ‘Green Revolution’. Breed Sci 52(2):143–150

    Article  Google Scholar 

  4. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309(5735):741–745

    PubMed  PubMed Central  Article  Google Scholar 

  5. Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23(1):69–80

    PubMed  PubMed Central  Article  Google Scholar 

  6. Dai Z, Zhao B, Liu X, Xia G, Tan C, Zhang B, Zhang H (1997) Yangdao 6, a new indica variety with high quality, high yield and multi resistance. Jiangsu Agric Sci 4:13–14

    Google Scholar 

  7. Evenson RE, Gollin D (2003) Assessing the impact of the Green Revolution, 1960 to 2000. Science 300(5620):758–762

    PubMed  Article  Google Scholar 

  8. Ferrero-Serrano Á, Cantos C, Assmann SM (2019) The role of dwarfing traits in historical and modern agriculture with a focus on rice. Cold Spring Harb Perspect Biol 11(11): a034645. 

    PubMed  Article  Google Scholar 

  9. Hedden P (2003) The genes of the Green Revolution. Trends Genet 19(1):5–9

    PubMed  Article  Google Scholar 

  10. Hirano K, Ordonio RL, Matsuoka M (2017) Engineering the lodging resistance mechanism of post-Green Revolution rice to meet future demands. Proc Jpn Acad Ser B Phys Biol Sci 93(4):220–233

    PubMed  PubMed Central  Article  Google Scholar 

  11. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31(9):827–832

    PubMed  PubMed Central  Article  Google Scholar 

  12. Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537(7622):629–633

    PubMed  PubMed Central  Article  Google Scholar 

  13. Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, Yajima S, Kyozuka J, Ueguchi-Tanaka M, Matsuoka M, Shirasu K, Yamaguchi S, Asami T (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol 174(2):1250–1259

    PubMed  PubMed Central  Article  Google Scholar 

  14. Kao C, Zeng Z, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152(3):1203–1216

    PubMed  PubMed Central  CAS  Google Scholar 

  15. Khush G, Coffman W, Beachell H (2001) The history of rice breeding: IRRI’s contribution. In: rice research and production in the 21st century: symposium honouring Robert F. Chandler Jr. International Rice Research Institute, Manila, Philippines. pp. 117–135

  16. Lenaerts B, Collard BC, Demont M (2019) Improving global food security through accelerated plant breeding. Plant Sci 287:110207

    PubMed  PubMed Central  Article  Google Scholar 

  17. Li L, Mao D (2018) Deployment of cold tolerance loci from Oryza sativa ssp. Japonica cv. ‘Nipponbare’ in a high-yielding Indica rice cultivar ‘93-11’. Plant Breed 137(4):553–560

    Article  Google Scholar 

  18. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F (2003) Control of tillering in rice. Nature 422(6932):618–621

    PubMed  Article  Google Scholar 

  19. Li D, Huang Z, Song S, Xin Y, Mao D, Lv Q, Zhou M, Tian D, Tang M, Wu Q (2016) Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase. Proc Natl Acad Sci U S A 113(41):E6026

    PubMed  PubMed Central  Article  Google Scholar 

  20. Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang J, Liu Q, Hu M, Li H, Tong Y (2018) Modulating plant growth–metabolism coordination for sustainable agriculture. Nature 560(7720):595–600

    PubMed  PubMed Central  Article  Google Scholar 

  21. Liao Z, Yu H, Duan J, Yuan K, Yu C, Meng X, Kou L, Chen M, Jing Y, Liu G (2019) SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nat Commun 10(1):2738

    PubMed  PubMed Central  Article  Google Scholar 

  22. Lincoln S, Daly M, Lander E (1993) Mapping genes controlling quantitative traits using MAPMAKER/QTL version 1.1: a tutorial and reference manual. A White Institute for Biometrical Research Technical Report 2nd edn, Cambridge

  23. Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JA, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20(10):2603–2618

    PubMed  PubMed Central  Article  Google Scholar 

  24. Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q, Fu X, Wang Y, Li J (2013) Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25(10):3743–3759

    PubMed  PubMed Central  Article  Google Scholar 

  25. Lu Y, Ye X, Guo R, Huang J, Wang W, Tang J, Tan L, Zhu J, Chu C, Qian Y (2017) Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol Plant 10(9):1242–1245

    PubMed  Article  Google Scholar 

  26. Mackill D, Nguyen H, Zhang J (1999) Use of molecular markers in plant improvement programs for rainfed lowland rice. Field Crop Res 64(1):177–185

    Article  Google Scholar 

  27. Mao D, Yu L, Chen D, Li L, Zhu Y, Xiao Y, Zhang D, Chen C (2015) Multiple cold resistance loci confer the high cold tolerance adaptation of Dongxiang wild rice (Oryza rufipogon) to its high-latitude habitat. Theor Appl Genet 128(7):1359–1371

    PubMed  Article  Google Scholar 

  28. Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M, Sato M, Nasu S, Minobe Y (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “Green Revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9(1):11–17

    PubMed  Article  Google Scholar 

  29. Murai M, Tkamure I, Sato S, Tokutome T, Sato Y (2002) Effect of the dwarfing gene originating from ‘Dee-geo-woo-gen’ on yield and its related traits in rice. Breed Sci 52(2):95–100

    Article  Google Scholar 

  30. Nishimura A, Aichi I, Matsuoka M (2006) A protocol for Agrobacterium-mediated transformation in rice. Nat Protoc 1(6):2796–2802

    PubMed  Article  Google Scholar 

  31. Ogi Y, Kato H, Maruyama K, Kikuchi F (1993) The effects on the culm length and other agronomic characters caused by semidwarfing genes at the sd-1 locus in rice. Japon J Breed 43(2):267–275

    Article  Google Scholar 

  32. Ookawa T, Hobo T, Yano M, Murata K, Ando T, Miura H, Asano K, Ochiai Y, Ikeda M, Nishitani R, Ebitani T, Ozaki H, Angeles ER, Hirasawa T, Matsuoka M (2010) New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield. Nat Commun 1(1):132

    PubMed  PubMed Central  Article  Google Scholar 

  33. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F (1999) ‘Green Revolution’ genes encode mutant gibberellin response modulators. Nature 400(6741):256–261

    PubMed  Article  Google Scholar 

  34. Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS (2002) A mutant gibberellin–synthesis gene in rice. Nature 416(6882):701–702

    PubMed  Article  Google Scholar 

  35. Serrano-Mislata A, Bencivenga S, Bush M, Schiessl K, Boden S, Sablowski R (2017) DELLA genes restrict inflorescence meristem function independently of plant height. Nat Plants 3(9):749–754

    PubMed  PubMed Central  Article  Google Scholar 

  36. Shen YJ, Jiang H, Jin JP, Zhang ZB, Xi B, He YY, Wang G, Wang C, Qian L, Li X (2004) Development of genome-wide DNA polymorphism database for map-based cloning of rice genes. Plant Physiol 135(3):1198–1205

    PubMed  PubMed Central  Article  Google Scholar 

  37. Song X, Lu Z, Yu H, Shao G, Xiong J, Meng X, Jing Y, Liu G, Xiong G, Duan J, Yao XF, Liu CM, Li H, Wang Y, Li J (2017) IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 27(9):1128–1141

    PubMed  PubMed Central  Article  Google Scholar 

  38. Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “Green Revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci U S A 99(13):9043–9048

    PubMed  PubMed Central  Article  Google Scholar 

  39. Terao T, Hirose T (2015) Control of grain protein contents through SEMIDWARF1 mutant alleles: sd1 increases the grain protein content in Dee-geo-woo-gen but not in Reimei. Mol Gen Genomics 290(3):939–954

    Article  Google Scholar 

  40. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2000) MapQTL 4.0: software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, the Netherlands

  41. Wang S, Basten C, Zeng Z (2005) Windows QTL cartographer version 2.5. Statistical genetics North Carolina State University, Raleigh

  42. Wang LM, Zhang JP, Dang Z, Pei XW, Dang ZH (2016) The analysis of the parental combining ability and heterosis on two-line hybrid flax. Sci Agric Sin 49(6):1047–1059

    CAS  Google Scholar 

  43. Wang Y, Shang L, Yu H, Zeng L, Hu J, Ni S, Rao Y, Li S, Chu J, Meng X, Wang L, Hu P, Yan J, Kang S, Qu M, Lin H, Wang T, Wang Q, Hu X, Chen H, Qian Q (2020) A Strigolactone Biosynthesis Gene Contributed to the Green Revolution in Rice. Mol Plant 13(6):923–932

  44. Wu Y, Wang Y, Mi XF, Shan JX, Li XM, Xu JL, Lin HX (2016) The QTL GNP1 encodes GA20ox1, which increases grain number and yield by increasing cytokinin activity in rice panicle meristems. PLoS Genet 12(10):e1006386

    PubMed  PubMed Central  Article  Google Scholar 

  45. Yano K, Ookawa T, Aya K, Ochiai Y, Hirasawa T, Ebitani T, Takarada T, Yano M, Yamamoto T, Fukuoka S, Wu J, Ando T, Ordonio RL, Hirano K, Matsuoka M (2015) Isolation of a novel lodging resistance QTL gene involved in strigolactone signaling and its pyramiding with a QTL gene involved in another mechanism. Mol Plant 8(2):303–314

    PubMed  Article  Google Scholar 

  46. 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: genes, genomes. Genetics 3(2):323–331

    CAS  Google Scholar 

  47. 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(3):2152–2165

    PubMed  PubMed Central  CAS  Google Scholar 

  48. Yuan LP (1998) Hybrid rice breeding in China. Adv Hybrid Rice Technol:27–33

  49. Yuan LP (2014) Development of hybrid rice to ensure food security. Rice Sci 21(1):1–2

    Article  Google Scholar 

  50. Zhang QF (2007) Strategies for developing green super rice. Proc Natl Acad Sci U S A 104(42):16402–16409

    PubMed  PubMed Central  Article  Google Scholar 

  51. Zhang F, Jiang YZ, Yu SB, Ali J, Paterson A, Khush G, Xu JL, Gao YM, Fu BY, Lafitte R (2013) Three genetic systems controlling growth, development and productivity of rice (Oryza sativa L.): a reevaluation of the ‘Green Revolution’. Theor Appl Genet 126(4):1011–1024

    PubMed  Article  Google Scholar 

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Acknowledgments

We appreciate Dr. Caiyan Chen for the critical advice of the manuscript and Dr. David Zaitlin for language improvement. We would like to express our gratitude to anonymous reviewers and editor for their careful work and thoughtful suggestions that have helped improve this paper substantially.

Funding

This work was supported by grants from the National Natural Science Foundation of China (31371603) and partly supported by Youth Innovation Promotion Association of Chinese Academy of Sciences (2018398).

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YY, XH and YZ performed the experiments. YY and DM analyzed the data and wrote the manuscript. DM conceived and designed the experiments.

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Correspondence to Donghai Mao.

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Supplementary Figure 1

Flow diagram showing the population development strategy used in this study. MAS, marker-assisted selection; 9311, an indica rice cultivar; Nipponbare, a japonica rice cultivar; 9311-SD1NpSD1Np, the NIL for SD1Np in the indica rice cultivar ‘9311’; Np-SD19311SD19311, the NIL for SD19311 in the japonica rice cultivar ‘Np’; F1-SD1NpSD1Np, F1-SD19311SD19311, F1-SD1NpSD19311, and F1-SD19311SD1cr: four kinds of F1 hybrids carrying different genotypes of SD1, the two homozygous types SD1NpSD1Np and SD19311SD19311, and the heterozygous type SD1NpSD19311 and SD19311SD1cr, respectively (JPG 95 kb)

Supplementary Figure 2

Morphology of a CRISPR/Cas9 knockout mutant, the two SD1 NILs, of the parental lines 9311 and ‘Np’ grown in the field at Sanya city in the summer of 2018 and 2020. a WT, wild-type ‘Np’; cr-sd1-1, the CRISPR/Cas9 SD1 knockout mutant; 9311-SD1NpSD1Np, the ‘9311’ backcross line carrying SD1NpSD1Np; Np-SD19311SD19311, the ‘Np’ backcross line carrying SD19311SD19311. In the field at Sanya city in the summer of 2018, b 9311-SD1NpSD1Np, the ‘9311’ backcross line carrying SD1NpSD1Np; CK1, a rice cultivar as control check 1 in the same field; CK2, another rice cultivar as control check 2 in the same field. In the field at Sanya city in the summer of 2020 (JPG 442 kb)

Supplementary Figure 3

Phenotypic comparisons and statistical analyses of the F1 hybrids with different SD1 genotypes, the homozygous NILs, and the parental inbred lines ‘Np’ and ‘9311’. The dotted line represents the mid-parent value (MPV) (JPG 257 kb)

Supplementary Figure 4

Statistical analyses of plant height and yield-related traits in two hybrid rice lines. F1-SD19311SD1cr, the F1 hybrid derived from a cross between ‘9311’ and cr-sd1-1; F1-SD1NpSD19311, the F1 hybrid derived from a cross between ‘9311’ and ‘Np’. ns, no significant difference; *p < 0.05 and **p < 0.01, as determined by Student’s t test (JPG 76 kb)

Supplementary Figure 5

Comparison of plant heights between Np-SD19311SD19311 and the CRISPR/Cas9 knockout line cr-sd1-1. ns, no significant difference at the 0.05 level (Student’s t test) (JPG 19 kb)

Supplementary Figure 6

Hypothetical model showing how SD1 regulates plant height, tiller number, and spikelet number in rice (JPG 167 kb)

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Yu, Y., Hu, X., Zhu, Y. et al. Re-evaluation of the rice ‘Green Revolution’ gene: the weak allele SD1-EQ from japonica rice may be beneficial for super indica rice breeding in the post-Green Revolution era. Mol Breeding 40, 84 (2020). https://doi.org/10.1007/s11032-020-01164-2

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Keywords

  • Rice
  • Subspecies
  • OsGA20ox-2 (SD1)
  • Tiller number
  • Spikelets per panicle