Development of Commercial Thermo-sensitive Genic Male Sterile Rice Accelerates Hybrid Rice Breeding Using the CRISPR/Cas9-mediated TMS5 Editing System

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zhou, Hai ^a,b,c   He, Ming ^a,b,c   Li, Jing ^a,b,c   Chen, Liang ^a,b,c   Huang, Zhifeng ^a,b,c   Zheng, Shaoyan ^a,b,c   Zhu, Liya ^a,b,c   Ni, Erdong ^a,b,c   Jiang, Dagang ^a,b,c   Zhao, Bingran ^d   Zhuang, Chuxiong ^a,b,c  

^a State Key Laboratory for Conservation and Utilization of Subtropical Agro bioresources   (China)

^b Key Laboratory of Plant Functional Genomics and Biotechnology of Education Department   (China)

^c SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^d HUNAN HYBRID RICE RESEARCH CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GUIDE RNA;

ANATOMY AND HISTOLOGY; BREEDING; CRISPR CAS SYSTEM; GENE EDITING; GENETICS; HYBRIDIZATION; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; ORYZA; PLANT INFERTILITY; POLLEN; PROCEDURES; TEMPERATURE; TRANSGENIC PLANT;

BASE SEQUENCE; BREEDING; CRISPR-CAS SYSTEMS; GENE EDITING; HYBRIDIZATION, GENETIC; MUTATION; ORYZA; PLANT INFERTILITY; PLANTS, GENETICALLY MODIFIED; POLLEN; RNA, GUIDE; TEMPERATURE;

EID: 84996802204     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37395     Document Type: Article

References (53)

1. Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42, 545-549 (2010).
2. Kusano, M. et al. Using metabolomic approaches to explore chemical diversity in rice. Mol Plant 8, 58-67 (2015).
3. Khush, G. S. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol 59, 1-6 (2005).
4. Su, N. et al. Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant Physiol 159, 227-238 (2012).
5. Normile, D. Agricultural research. Reinventing rice to feed the world. Science 321, 330-333 (2008).
6. Yuan, L. Development of hybrid rice to ensure food security. Rice Science 21, 1-2 (2014).
7. Cheng, S. H., Zhuang, J. Y., Fan, Y. Y., Du, J. H., Cao, L. Y. Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100, 959-966 (2007).
8. Chen, L., Liu, Y. G. Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579-606 (2014).
9. Lin, S. C., Yuan, L. P. Hybrid rice breeding in China, In Innovative Approaches to Rice Breeding (Manila, Philippines: International Rice Research Institute), 35-51 (1980).
10. Deng, X. W. et al. Hybrid rice breeding welcomes a new era of molecular crop design. Sci Sin: Life Sci 864-868 (2013).
11. Yuan, L. P. Progress of two-line system hybrid rice breeding. Sci Agr Sin 23, 1-6 (2013).
12. Zhang, Q. et al. Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc Natl Acad Sci USA 91, 8675-8679 (1994).
13. Zhou, H. et al. Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22, 649-660 (2012).
14. Zhang, H. et al. Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci USA 110, 76-81 (2013).
15. Zhou, H. et al. RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5, 4884 (2014).
16. Huang, J. Z., E., Z. G., Zhang, H. L., Shu, Q. Y. Workable male sterility systems for hybrid rice: Genetics, biochemistry, molecular biology, and utilization. Rice 7, 13 (2014).
17. Liu, N. et al. Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Mol Genet & Genomics 266, 271-275 (2001).
18. Ding, J. et al. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109, 2654-2659 (2012).
19. Chen, R. et al. Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19, 847-861 (2007).
20. Zhang, H. L. et al. Identification and transition analysis of photo-/thermo-sensitive genic male sterile genes in two-line hybrid rice in China. Sci Agr Sin 48, 1-9 (2015).
21. Luo, X. H., Qiu, Z. Z. Pei-Ai64S-a dual-purpose sterile line whose sterility is induced by low critical temperature. Hybrid Rice 7, 27-29 (1992).
22. Yang, Z. et al. Breeding of fine quality PTGMS line Guangzhan 63S in medium indica rice. Hybrid Rice 17, 4-6 (2002).
23. Deng, Q. Y. Breeding of the PTGMS line Y58S with wide adaptability in rice. Hybrid Rice 20, 15-18 (2005).
24. LU, Z. M. Highlights and difficulties in hybrid rice breeding in China. Chinese Journal of Rice Science 25, 231-235 (2011).
25. Zhang, H. et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol 12, 797-807 (2014).
26. Ma, X. et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8, 1274-1284 (2015).
27. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
28. Feng, Z. et al. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23, 1229-1232 (2013).
29. Hwang, W. Y. et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31, 227-229 (2013).
30. Jiang, W. et al. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41, e188 (2013).
31. Li, J. F. et al. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31, 688-691 (2013).
32. Miao, J. et al. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23, 1233-1236 (2013).
33. Shan, Q. et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31, 686-688 (2013).
34. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
35. Feng, Z. et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA 111, 4632-4637 (2014).
36. Shan, Q., Wang, Y., Li, J., Gao, C. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9, 2395-2410 (2014).
37. Wang, T., Wei, J. J., Sabatini, D. M., Lander, E. S. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343, 80-84 (2013).
38. Li, Q. L. et al. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genomics doi: 10.1016/j.jgg.2016.04.011.
39. Huang, S., Weigel, D., Beachy, R. N., Li, J. A proposed regulatory framework for genome-edited crops. Nat Genet 48 109-111 (2016).
40. Boettcher, M., McManus, M. T. Choosing the right tool for the Job: RNAi, TALEN, or CRISPR. Mol Cell 58, 575-585 (2015).
41. Xu, R. F. et al. Generation of inheritable and "transgene clean" targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep 5, 11491 (2015).
42. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31, 822-826 (2013).
43. Lei, D., Tang, W., Xie, Z., Liu, H., Chen, L. Solutions to insecurity problems in seed production of two-line hybrid rice. Agr Sci & Technol 15, 1160-1166 1187 (2014).
44. Levings, C. R. The Texas cytoplasm of maize: cytoplasmic male sterility and disease susceptibility. Science 250, 942-947 (1990).
45. Huang, Q., He, Y., Jing, R., Zhu, R., Zhu, Y. Mapping of the nuclear fertility restorer gene for HL cytoplasmic male sterility in rice using microsatellite markers. Chinese Sci Bull 45, 430-432 (2000).
46. Zhong, B. Q., Yang, Z. L., He, G. H. Analysis of restoring and maintaining ability of thirty-three American rice varieties (Oryza Sativa L.). Journal of Southwest Agricultural University 26, 554-555 559 (2004).
47. Ruan, R. C., Chen, H. C., Yang, Y. S., Jin, T. Y., You, J. M. Screening of rice (Oryza sativa) germplasm with restoring genes to CMS from local varieties collected in Guizhou. Guizhou Agr Sci 27, 34-37 (1999).
48. Deng, H. F. et al. Status and technical strategy on development of japonica hybrid rice in China. Hybrid Rice 21, 1-6 (2006).
49. Makarova, K. S. et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9, 467-477 (2011).
50. Li, J. et al. Expression of RNA-interference/antisense transgenes by the cognate promoters of target genes is a better gene-silencing strategy to study gene functions in rice. PLoS One 6, e17444 (2011).
51. Dellaporta, S. L., Wood, J., Hicks, J. B. A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1, 19-21 (1983).
52. Ma, X., Chen, L., Zhu, Q., Chen, Y., Liu, Y. G. Rapid decoding of sequence-specific nuclease-induced heterozygous and biallelic mutations by direct sequencing of PCR products. Mol Plant 8, 1285-1287 (2015).
53. Li, X. et al. Identification and validation of rice reference proteins for western blotting. J Exp Bot 62, 4763-4772 (2011).