Advertisement

Euphytica

, 215:44 | Cite as

Identifying the genes around Rf5 and Rf6 loci for the fertility restoration of WA-type cytoplasmic male sterile japonica rice (Oryza sativa) lines

  • Honggen Zhang
  • Xiaojun Cheng
  • Lijia Zhang
  • Qiaoquan Liu
  • Minghong Gu
  • Shuzhu TangEmail author
Article
  • 1 Downloads

Abstract

Wild abortive (WA)-type, Honglian (HL)-type, and Chinsurah Boro II-type cytoplasm are three typical sterile cytoplasms used to generate three-line hybrid rice, and the fertility restorer (Rf) genes are considered to have specificity for fertility restoration of cytoplasmic male sterility (CMS) lines. ‘93-11’, an HL-type indica restorer line used widely in China, shows a weak ability to restore the fertility of WA-type CMS lines. Rf5 and Rf6, the fertility restorer genes for HL-type CMS, are members of a multigene cluster that encodes pentatricopeptide repeat proteins in ‘93-11’. In the present study, we studied the function of Rf genes around Rf5 and Rf6 loci on fertility restoration to WA-type CMS lines. We generated plants carrying WA-type cytoplasm and different genotypes at the Rf5 and Rf6 loci. All plants exhibited no seed setting on bagged panicles but had different anther and pollen grain morphologies. Plants with the genotypes of Rf5rf5rf6rf6, Rf5Rf5rf6rf6, rf5rf5Rf6rf6, rf5rf5Rf6Rf6, and Rf5rf5Rf6rf6 exhibited degraded anthers and typical abortive pollen grains, which were same as those of WA-NipA plants (rf5rf5rf6rf6); however, plants with the genotypes Rf5rf5Rf6Rf6, Rf5Rf5Rf6rf6, and Rf5Rf5Rf6Rf6 displayed restored anthers and pollen grains. These results indicated that Rf genes around the Rf5 and Rf6 loci had minor effects on the fertility restoration of WA-type CMS lines, which were mediated by dosage effects. Furthermore, these Rf genes functioned to decrease the WA352 (the mitochondrial gene conferring CMS-WA) transcript levels. Our findings will promote the development of three-line hybrids.

Keywords

Rice Cytoplasmic male sterility Fertility restorer Gene effect 

Notes

Acknowledgements

This study was supported financially by The National Natural Science Foundation of China (Grant No. 31771743), The National Key Research and Development Program (2016YFD0101107), and a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author contributions

HZ analyzed the data and drafted the manuscript. XC and LZ completed the phenotypic evaluations and data analyses. QL and MG were involved in designing the study. ST designed the study and revised the manuscript. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10681_2019_2368_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)

References

  1. Ahmadikhah A, Karlov GI (2006) Molecular mapping of the fertility-restoration gene Rf4 for WA-cytoplasmic malesterility in rice. Plant Breed 125:363–367CrossRefGoogle Scholar
  2. Chen LT, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefGoogle Scholar
  3. Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966CrossRefGoogle Scholar
  4. Dill CL, Wise RP, Schnable PS (1997) Rf8 and Rf* mediate unique T-Urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147:1367–1379PubMedPubMedCentralGoogle Scholar
  5. Hu J, Wang K, Huang WC, Liu G, Gao Y, Wang JM, Huang Q, Ji YX, Qin XJ, Wan L, Zhu RS, Li SQ, Yang DC, Zhu YG (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122CrossRefGoogle Scholar
  6. Huang WC, Hu J, Yu CC, Huang Q, Wan L, Wang LL, Qin XJ, Ji YX, Zhu RS, Li SQ, Zhu YG (2012) Two non-allelic nuclear genes restore fertility in a gametophytic pattern and enhance abiotic stress tolerance in the hybrid rice plant. Theor Appl Genet 124:799–807CrossRefGoogle Scholar
  7. Huang JZ, E ZG, Zhang HL, Shu QY (2014) Workable male sterility systems for hybrid rice: genetics, biochemistry, molecular biology, and utilization. Rice 7:13CrossRefGoogle Scholar
  8. Huang WC, Yu CC, Hu J, Wang LL, Dan ZW, Zhou W, He CL, Zeng YF, Yao GX, Qi JZ, Zhang ZH, Zhu RS, Chen XF, Zhu YG (2015) Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility. Proc Natl Acad Sci USA 112:14984–14989CrossRefGoogle Scholar
  9. Jing RC, Li XM, Yi P, Zhu YG (2001) Mapping fertility restoring genes of rice WA cytoplasmic male sterility using SSLP markers. Bot Bull Acad Sin 42:167–171Google Scholar
  10. Komori T, Ohta S, Murai NY, Kuraya Y, Suzuki S, Hiei Y (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37:315–325CrossRefGoogle Scholar
  11. Li SQ, Yang DC, Zhu YG (2007) Characterization and use of male sterility in hybrid rice breeding. J Integr Plant Biol 49:791–804CrossRefGoogle Scholar
  12. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  13. Luo DP, Xu H, Liu ZL, Guo JX, Li HY, Chen LT, Fang C, Zhang QY, Bai M, Yao N, Wu H, Ji CH, Zheng HQ, Chen YL, Ye S, Li XY, Zhao XC, Li RQ, Liu YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577CrossRefGoogle Scholar
  14. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le RM, Martin ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103CrossRefGoogle Scholar
  15. Ngangkham U, Parida SK, De S, Anand RKK, Singh AK, Singh SK, Mohapatra T (2010) Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice. Mol Breed 26:275–292CrossRefGoogle Scholar
  16. Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76CrossRefGoogle Scholar
  17. Tan YP, Li SQ, Wang L, Liu G, Hu J, Zhu YG (2008) Genetic analysis of fertility-restorer genes in rice. Biol Plant 52:469–474CrossRefGoogle Scholar
  18. Tang HW, Luo DP, Zhou DG, Zhang QY, Tian DS, Zheng XM, Chen LT, Liu YG (2014) The rice restorer Rf4 for wild-abortive cytoplasmic male sterility encodes a mitochondrial-localized PPR protein that functions in reduction of WA352 transcripts. Mol Plant 7:1497–1500CrossRefGoogle Scholar
  19. Tang HW, Xie YY, Liu YG, Chen LT (2017) Advances in understanding the molecular mechanisms of cytoplasmic male sterility and restoration in rice. Plant Reprod 30:179–184CrossRefGoogle Scholar
  20. Wang ZH, Zou YJ, Li XY, Zhang QY, Chen LT, Wu H, Su DH, Chen YL, Guo JX, Luo D, Long YM, Zhong Y, Liu YG (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687CrossRefGoogle Scholar
  21. Wise RP, Gobelman-Werner K, Pei D, Dill CL, Schnable PS (1999) Mitochondrial transcript processing and restoration of male fertility in T-cytoplasm maize. J Hered 90:380–385CrossRefGoogle Scholar
  22. Yao FY, Xu CJ, Yu SB, Li JX, Gao YJ, Li XH, Zhang QF (1997) Mapping and genetic analysis of two fertility restorer loci in the wild-abortive cytoplasmic male sterility system of rice (Oryza sativa L.). Euphytica 98:183–187CrossRefGoogle Scholar
  23. Yuan LP (2014) Development of hybrid rice to ensure food security. Rice Sci 21:1–2CrossRefGoogle Scholar
  24. Zhang G, Lu Y, Bharaj TS, Virmani SS, Huang N (1997) Mapping of the Rf-3 nuclear fertility-restoring gene for WA cytoplasmic male sterility in rice using RAPD and RFLP markers. Theor Appl Genet 94:27–33CrossRefGoogle Scholar
  25. Zhang H, Zhao Q, Sun ZZ, Zhang CQ, Feng Q, Tang SZ, Liang GH, Gu MH, Han B, Liu QQ (2011) Development and high-throughput genotyping of substitution lines carring the chromosome segments of indica 9311 in the background of japonica Nipponbare. J Genet Genom 38:603–611CrossRefGoogle Scholar
  26. Zhang HG, Zhang LJ, Si H, Ge YS, Liang GH, Gu MH, Tang SZ (2016) Rf5 is able to partially restore fertility to Honglian-type cytoplasmic male sterile japonica rice (Oryza sativa) lines. Mol Breed 36:1–10CrossRefGoogle Scholar
  27. Zhang HG, Che JL, Ge YS, Pei Y, Zhang LJ, Liu QQ, Gu MH, Tang SZ (2017) Ability of Rf5 and Rf6 to restore fertility of chinsurah boro II-type cytoplasmic male sterile Oryza sativa (ssp. japonica) lines. Rice 10:2CrossRefGoogle Scholar
  28. Zhu ZB, Zhang HG, Liu C, Li P, Yi CD, Tang SZ, Gu MH (2010) Comparative study on breeding utilization characteristics of the isonuclear alloplasmic japonica CMS lines Liuqianxin A with four different cytoplasm sources. Acta Agron Sin 36:1–8Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Jiangsu Key Laboratory of Crop Genetics and Physiology/Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular BreedingAgricultural College of Yangzhou UniversityYangzhouChina
  2. 2.Jiangsu Co-Innovation Center for Modern Production Technology of Grain CropsYangzhou UniversityYangzhouChina

Personalised recommendations