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Slowing development restores the fertility of thermo-sensitive male-sterile plant lines

Abstract

Temperature-sensitive genic male sterility (TGMS) lines are widely used in the breeding of hybrid crops1,2, but by what means temperature as a general environmental factor reverses the fertility of different TGMS lines remains unknown. Here, we identified an Arabidopsis TGMS line named reversible male sterile (rvms) that is fertile at low temperature (17 °C) and encodes a GDSL lipase. Cytological observations and statistical analysis showed that low temperature slows pollen development. Further screening of restorers of rvms, as well as crossing with a slow-growth line at normal temperature (24 °C), demonstrate that slowing of development overcomes the defects of rvms microspores and allows them to develop into functional pollen. Several other Arabidopsis TGMS lines were identified, and their fertility was also restored by slowing of development. Given that male reproductive development is conserved3, we propose that slowing of development is a general mechanism applicable to the sterility–fertility conversion of TGMS lines from different plant species.

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Fig. 1: rvms, a mutant of a GDSL lipase, displays temperature-dependent male sterility.
Fig. 2: Pollen development is slower at low temperature.
Fig. 3: res1 exhibits delayed and asynchronous cell division during meiosis in the restoration of rvms fertility.
Fig. 4: Slow pollen development is a general mechanism capable of restoring fertility in other Arabidopsis TGMS mutants.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We thank H. Huang, L. Xu, J.-D. Rochaix, S. McCormick, J. Xu, L.-W. Peng and L. Zhang for discussions about this manuscript. This work was supported by grants from the National Key Research and Development Program of China (no. 2016YFD0100902), National Science Foundation of China (nos. 31770348 and 31600243), Science and Technology Commission of Shanghai Municipality (nos. 18DZ2260500 and 17DZ2252700) and the Innovation Program of Shanghai Municipal Education Commission (no. 2019-01-07-00-02-E00006).

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Authors and Affiliations

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Contributions

The project leader is Z.-N.Y. Z.-N.Y. and J.Z. conceived the experiments. J.Z. and Y.L. performed thermo-sensitive phenotype analysis. Q.-S.S. and J.Z. performed statistical analysis of microspore development. Q.-S.S. contributed to analysis of restorers of rvms-2. S.Z. contributed fine mapping of RVMS. W.-T.Z. contributed enzyme activity assays. J.Y. and Y.L. performed genetic complementation. J.-Q.H. and J.-Q.W. detected the expression of RES1. C.Z., T.X., J.-L.L. and L.Z. analysed fertility restoration of pollen-wall-related mutants. X.-H.H contributed BAS-seq analysis. J.Z. and Y.L. wrote the paper with input from Z.-N.Y. S.W. and X.-Z.Y. revised the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Zhong-Nan Yang.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Danny Geelen, Yidan Ouyang, Dabing Zhang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–26 and Tables 1–3.

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Zhu, J., Lou, Y., Shi, QS. et al. Slowing development restores the fertility of thermo-sensitive male-sterile plant lines. Nat. Plants 6, 360–367 (2020). https://doi.org/10.1038/s41477-020-0622-6

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