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MS1 is essential for male fertility by regulating the microsporocyte cell plate expansion in soybean

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Abstract

Male sterility is an essential trait in hybrid seed production, especially for monoclinous and autogamous food crops. Soybean male-sterile ms1 mutant has been known for more than 50 years and could be instrumental in making hybrid seeds. However, the gene responsible for the male-sterile phenotype has remained unknown. Here, we report the map-based cloning and characterization of the MS1 gene in soybean. MS1 encodes a kinesin protein and localizes to the nucleus, where it is required for the male meiotic cytokinesis after telophase II. We further substantiated that MS1 colocalizes with microtubules and is essential for cell plate formation in soybean male gametogenesis through immunostaining. Both ms1 and CRISPR/Cas9 knockout mutants show complete male sterility but are otherwise phenotypically normal, making them perfect tools for producing hybrid seeds. The identification of MS1 has the practical potential for assembling the sterility system and speeding up hybrid soybean breeding.

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Data availability

Data supporting the findings of this work are available within the paper and its Supplementary Information files. The RNA-seq data supporting this research have been deposited in the NCBI SRA with the accession number PRJNA726823.

References

  • Albertsen, M.C., and Palmer, R.G. (1979). A comparative light- and electron-microscopic study of microsporogenesis in male sterile (MS1) and male fertile soybeans (Glycine max (L.) Merr.). Am J Bot 66, 253–265.

    Article  Google Scholar 

  • Brim, C.A., and Young, M.F. (1971). Inheritance of a male-sterile character in soybeans. Crop Sci 11, 564–566.

    Article  Google Scholar 

  • Chang, F., Wang, Y., Wang, S., and Ma, H. (2011). Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14, 66–73.

    Article  CAS  PubMed  Google Scholar 

  • Chen, L., and Liu, Y.G. (2014). Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65, 579–606.

    Article  CAS  PubMed  Google Scholar 

  • Chen, S., Zhou, Y., Chen, Y., and Gu, J. (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davis, W.H. (1985). Route to hybrid soybean production. US Patent, 4545146.

  • Echlin, P., and Godwin, H. (1968). The ultrastructure and ontogeny of pollen in Helleborus Foetidus L. J Cell Sci 3, 175–186.

    Article  CAS  PubMed  Google Scholar 

  • Fang, X., Zhao, Y., Ma, Q., Huang, Y., Wang, P., Zhang, J., Nian, H., and Yang, C. (2013). Identification and comparative analysis of cadmium tolerance-associated miRNAs and their targets in two soybean genotypes. PLoS ONE 8, e81471.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang, X., Han, Y., Liu, M., Jiang, J., Li, X., Lian, Q., Xie, X., Huang, Y., Ma, Q., Nian, H., et al. (2021). Modulation of evening complex activity enables north-to-south adaptation of soybean. Sci China Life Sci 64, 179–195.

    Article  CAS  PubMed  Google Scholar 

  • Hackenberg, D., and Twell, D. (2019). The evolution and patterning of male gametophyte development. In: Grossniklaus, U., ed. Current Topics in Developmental Biology. New York: Academic Press. 257–298.

    Google Scholar 

  • Ho, C.M.K., Hotta, T., Guo, F., Roberson, R.W., Lee, Y.R.J., and Liu, B. (2011). Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65–3 in Arabidopsis. Plant Cell 23, 2909–2923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, Y., Wang, H., Huang, X., Wang, Q., Wang, J., An, D., Li, J., Wang, W., and Wu, Y. (2019). Maize VKS1 regulates mitosis and cytokinesis during early endosperm development. Plant Cell 31, 1238–1256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, B., Chen, L., Yang, C., Wu, T., Yuan, S., Wu, C., Zhang, M., Gai, J., Han, T., Hou, W., et al. (2021). The cloning and CRISPR/Cas9-mediated mutagenesis of a male sterility gene MS1 of soybean. Plant Biotechnol J 19, 1098–1100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, Y.J., and Zhang, D. (2018). Molecular control of male fertility for crop hybrid breeding. Trends Plant Sci 23, 53–65.

    Article  CAS  PubMed  Google Scholar 

  • Lawrence, C.J., Dawe, R.K., Christie, K.R., Cleveland, D.W., Dawson, S. C., Endow, S.A., Goldstein, L.S.B., Goodson, H.V., Hirokawa, N., Howard, J., et al. (2004). A standardized kinesin nomenclature. J Cell Biol 167, 19–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewers, K.S., and Palmer, R.G. (1997). Recurrent selection in soybean. Plant Breed Rev 15, 275–313.

    Google Scholar 

  • Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, S., Zhang, M., Feng, F., and Tian, Z. (2020). Toward a “Green Revolution” for soybean. Mol Plant 13, 688–697.

    Article  CAS  PubMed  Google Scholar 

  • Liu, W., Wang, C., Wang, G., Ma, Y., Tian, J., Yu, Y., Dong, L., and Kong, Z. (2019). Towards a better recording of microtubule cytoskeletal spatial organization and dynamics in plant cells. J Integr Plant Biol 61, 388–393.

    Article  CAS  PubMed  Google Scholar 

  • Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15, 550.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu, P., Chai, M., Yang, J., Ning, G., Wang, G., and Ma, H. (2014). The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol 164, 1893–1904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, H. (2005). Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56, 393–434.

    Article  CAS  PubMed  Google Scholar 

  • Ma, X., Zhang, Q., Zhu, Q., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z., Li, H., Lin, Y., et al. (2015). A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8, 1274–1284.

    Article  CAS  PubMed  Google Scholar 

  • McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010). The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 20, 1297–1303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadeem, M., Chen, A., Hong, H., Li, D., Li, J., Zhao, D., Wang, W., Wang, X., and Qiu, L. (2021). GmMs1 encodes a kinesin-like protein essential for male fertility in soybean (Glycine max L.). J Integr Plant Biol 63, 1054–1064.

    Article  CAS  PubMed  Google Scholar 

  • Naito, Y., Hino, K., Bono, H., and Ui-Tei, K. (2015). CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 31, 1120–1123.

    Article  CAS  PubMed  Google Scholar 

  • Nebenführ, A., and Dixit, R. (2018). Kinesins and myosins: molecular motors that coordinate cellular functions in plants. Annu Rev Plant Biol 69, 329–361.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nie, Z., Zhao, T., Liu, M., Dai, J., He, T., Lyu, D., Zhao, J., Yang, S., and Gai, J. (2019). Molecular mapping of a novel male-sterile gene msNJ in soybean [Glycine max (L.) Merr.]. Plant Reprod 32, 371–380.

    Article  PubMed  Google Scholar 

  • Nishihama, R., Soyano, T., Ishikawa, M., Araki, S., Tanaka, H., Asada, T., Irie, K., Ito, M., Terada, M., Banno, H., et al. (2002). Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109, 87–99.

    Article  CAS  PubMed  Google Scholar 

  • Palmer, R.G., Winger, C.L., and Albertsen, M.C. (1978). Four independent mutations at the ms1, locus in soybeans. Crop Sci 18, 727–729.

    Article  Google Scholar 

  • Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.C., Mendell, J.T., and Salzberg, S.L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33, 290–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea, M., Kim, D., Pertea, G.M., Leek, J.T., and Salzberg, S.L. (2016). Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11, 1650–1667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutley, N., and Twell, D. (2015). A decade ofpollen transcriptomics. Plant Reprod 28, 73–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasabe, M., and Machida, Y. (2012). Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton 69, 913–918.

    Article  CAS  PubMed  Google Scholar 

  • Sasabe, M., Soyano, T., Takahashi, Y., Sonobe, S., Igarashi, H., Itoh, T.J., Hidaka, M., and Machida, Y. (2006). Phosphorylation of NtMAP65–1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 20, 1004–1014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spielman, M., Preuss, D., Li, F.L., Browne, W.E., Scott, R.J., and Dickinson, H.G. (1997). TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124, 2645–2657.

    Article  CAS  PubMed  Google Scholar 

  • Sun, H., Zhao, L., and Huang, M. (1993). A study on the cytoplasm-nuclear male sterile soybean line (in Chinese). Chin Sci Bull 38, 1535–1536.

    Google Scholar 

  • Tanaka, H., Ishikawa, M., Kitamura, S., Takahashi, Y., Soyano, T., Machida, C., and Machida, Y. (2004). The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells 9, 1199–1211.

    Article  CAS  PubMed  Google Scholar 

  • Tester, M., and Langridge, P. (2010). Breeding technologies to increase crop production in a changing world. Science 327, 818–822.

    Article  CAS  PubMed  Google Scholar 

  • Thu, S.W., Rai, K.M., Sandhu, D., Rajangam, A., Balasubramanian, V.K., Palmer, R.G., and Mendu, V. (2019). Mutation in a PHD-finger protein MS4 causes male sterility in soybean. BMC Plant Biol 19, 378.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wan, X., Wu, S., Li, Z., Dong, Z., An, X., Ma, B., Tian, Y., and Li, J. (2019). Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Mol Plant 12, 321–342.

    Article  CAS  PubMed  Google Scholar 

  • Wang, K., Li, M., and Hakonarson, H. (2010). ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38, e164.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whitford, R., Fleury, D., Reif, J.C., Garcia, M., Okada, T., Korzun, V., and Langridge, P. (2013). Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64, 5411–5428.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, Z.A., and Zhang, D.B. (2009). From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60, 1479–1492.

    Article  CAS  PubMed  Google Scholar 

  • Wu, G., Fanzo, J., Miller, D.D., Pingali, P., Post, M., Steiner, J.L., and Thalacker-Mercer, A.E. (2014). Production and supply of high-quality food protein for human consumption: sustainability, challenges, and innovations. Ann NY Acad Sci 1321, 1–19.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Y., Fox, T.W., Trimnell, M.R., Wang, L., Xu, R.J., Cigan, A.M., Huffman, G.A., Garnaat, C.W., Hershey, H., and Albertsen, M.C. (2016). Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J 14, 1046–1054.

    Article  CAS  PubMed  Google Scholar 

  • Xu, X., Walter, W.J., Liu, Q., Machens, I., and Nick, P. (2018). A rice class-XIV kinesin enters the nucleus in response to cold. Sci Rep 8, 3588.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang, C.Y., Spielman, M., Coles, J.P., Li, Y., Ghelani, S., Bourdon, V., Brown, R.C., Lemmon, B.E., Scott, R.J., and Dickinson, H.G. (2003a). TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34, 229–240.

    Article  CAS  PubMed  Google Scholar 

  • Yang, X., Makaroff, C.A., and Ma, H. (2003b). The ArabidopsisMALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15, 1281–1295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Y., Speth, B.D., Boonyoo, N., Baumert, E., Atkinson, T.R., Palmer, R.G., and Sandhu, D. (2014). Molecular mapping of three male-sterile, female-fertile mutants and generation of a comprehensive map of all known male sterility genes in soybean. Genome 57, 155–160.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, D., Luo, X., and Zhu, L. (2011). Cytological analysis and genetic control of rice anther development. J Genet Genomics 38, 379–390.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, L., Sun, H., Wang, S., Wang, Y., Huang, M., and Li, J. (2004). Breeding of hybrid soybean HybSoy1 (in Chinese). Chin J Oil Crop Sci 26, 15–17.

    Google Scholar 

  • Zhu, C., and Dixit, R. (2012). Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249, 887–899.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32072084, 31871648, and 31971969). We gratefully acknowledge Zhaosheng Kong from the Institute of Microbiology, Chinese Academy of Sciences, for sharing the pTUB6::mCherry-TUB6 transgenic Arabidopsis seeds and useful discussions. We would like to thank Dr. Ali Muhammad for editing and improving the manuscript.

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  1. Contributed equally to this work

Authors and Affiliations

  1. Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou, 510006, China

    Xiaolong Fang, Xiaoyuan Sun, Wenjun Gong, Yifan Wang, Lu Liu, Baohui Liu, Fanjiang Kong & Meina Li

  2. Soybean Research Institute, National Engineering Research Center for Soybean, Jilin Academy of Agricultural Sciences, Changchun, 130033, China

    Xiangdong Yang, Chunjing Lin, Limei Zhao & Chunbao Zhang

  3. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 311401, China

    Qing Li

  4. Core Facility and Technical Service Center for SLSB, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Jie Xu

  5. Cereal & Oil Crop Institute, Hebei Academy of Agricultural and Forestry Sciences, Shijiazhuang, 050031, China

    Jun Qin & Mengchen Zhang

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  1. Xiaolong Fang
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  2. Xiaoyuan Sun
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Correspondence to Jun Qin, Mengchen Zhang, Chunbao Zhang, Fanjiang Kong or Meina Li.

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Fang, X., Sun, X., Yang, X. et al. MS1 is essential for male fertility by regulating the microsporocyte cell plate expansion in soybean. Sci. China Life Sci. 64, 1533–1545 (2021). https://doi.org/10.1007/s11427-021-1973-0

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