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POLLEN STERILITY, a novel suppressor of cell division, is required for timely tapetal programmed cell death in rice

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Abstract

Timely programmed cell death (PCD) of the tapetum supplying nutrients to microspores is a prerequisite for normal pollen development. Here we identified a unique mutant of rice (Oryza sativa L.), pollen sterility (post), which showed aborted pollens accompanied with extra-large husks. Due to failure of timely PCD of tapetal cells, post exhibited abnormal pollen wall patterning and defective pollen grains. By map-based cloning, we identified a causal gene, POST, encoding a novel protein which is ubiquitously localized in cells. RNA in situ hybridization showed that POST is highly detected in the tapetum and microspores at stages 8 and 9. Transcriptome analysis indicated that POST could function as an important regulator of the metabolic process involved in tapetal PCD. Compared with wild-type rice, post mutant has an increased cell number resulting from elevated expression of cell cycle associated genes in grain husks. Overexpression of POST inhibits grain size in wild type, while appropriate expression of POST in post mutant can recover the seed fertility but has little effect on the large grains, illustrating that fine-tuning of POST expression could be a potential strategy for rice yield improvement. The connection between cell division and cell death conferred by POST provides novel insights into the understanding of the tapetal PCD process.

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References

  • Aya, K., Ueguchi-Tanaka, M., Kondo, M., Hamada, K., Yano, K., Nishimura, M., and Matsuoka, M. (2009). Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21, 1453–1472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai, W., Wang, P., Hong, J., Kong, W., Xiao, Y., Yu, X., Zheng, H., You, S., Lu, J., Lei, D., et al. (2019). Earlier Degraded Tapetum1 (EDT1) encodes an ATP-citrate lyase required for tapetum programmed cell death. Plant Physiol 181, 1223–1238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhury, A.M. (1993). Nuclear genes controlling male fertility. Plant Cell 5, 1277–1283.

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng, B., Lu, D., Ma, X., Peng, Y., Sun, Y., Ning, G., and Ma, H. (2012). Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J 72, 612–624.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Z., Yu, J., Cheng, X., Zong, X., Xu, J., Chen, M., Li, Z., Zhang, D., and Liang, W. (2014). The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26, 1512–1524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg, R.B., Beals, T.P., and Sanders, P.M. (1993). Anther development: basic principles and practical applications. Plant Cell 5, 1217–1229.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray, J., Close, P.S., Briggs, S.P., and Johal, G.S. (1997). A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89, 25–31.

    Article  CAS  PubMed  Google Scholar 

  • Guo, J.X., and Liu, Y.G. (2012). Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54, 967–978.

    Article  CAS  PubMed  Google Scholar 

  • Helm, M., Schmid, M., Hierl, G., Terneus, K., Tan, L., Lottspeich, F., Kieliszewski, M.J., and Gietl, C. (2008). KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am J Bot 95, 1049–1062.

    Article  CAS  PubMed  Google Scholar 

  • Higginson, T., Li, S.F., and Parish, R.W. (2003). AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35, 177–192.

    Article  CAS  PubMed  Google Scholar 

  • Ito, T., and Shinozaki, K. (2002). The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43, 1285–1292.

    Article  CAS  PubMed  Google Scholar 

  • Ji, C., Li, H., Chen, L., Xie, M., Wang, F., Chen, Y., and Liu, Y.G. (2013). A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development. Mol Plant 6, 1715–1718.

    Article  CAS  PubMed  Google Scholar 

  • Jin, Y., Luo, Q., Tong, H., Wang, A., Cheng, Z., Tang, J., Li, D., Zhao, X., Li, X., Wan, J., et al. (2011). An AT-hook gene is required for palea formation and floral organ number control in rice. Dev Biol 359, 277–288.

    Article  CAS  PubMed  Google Scholar 

  • Jung, K.H., Han, M.J., Lee, Y.S., Kim, Y.W., Hwang, I., Kim, M.J., Kim, Y. K., Nahm, B.H., and An, G. (2005). Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705–2722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapoor, S., Kobayashi, A., and Takatsuji, H. (2002). Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14, 2353–2367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolattukudy, P.E., and Rogers, L. (1986). Acyl-CoA reductase and acyl-CoA: fatty alcohol acyl transferase in the microsomal preparation from the bovine meibomian gland. J Lipid Res 27, 404–411.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S., Jung, K.H., An, G., and Chung, Y.Y. (2004). Isolation and characterization of a rice cysteine protease gene, OsCP1, using T-DNA gene-trap system. Plant Mol Biol 54, 755–765.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Yuan, Z., Vizcay-Barrena, G., Yang, C., Liang, W., Zong, J., Wilson, Z.A., and Zhang, D. (2011). PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156, 615–630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, N., Zhang, D.S., Liu, H.S., Yin, C.S., Li, X., Liang, W., Yuan, Z., Xu, B., Chu, H.W., Wang, J., et al. (2006). The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999–3014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, S.F., Higginson, T., and Parish, R.W. (1999). A novel MYB-related gene from Arabidopsis thaliana expressed in developing anthers. Plant Cell Physiol 40, 343–347.

    Article  CAS  PubMed  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, Y., Liu, L., Zhu, C., Sun, C., Xu, B., Fang, J., Tang, J., Luo, A., Cao, S., Li, G., et al. (2009). Molecular analysis of rice plants harboring a multi-functional T-DNA tagging system. J Genet Genomics 36, 267–276.

    Article  CAS  PubMed  Google Scholar 

  • Millar, A.A., and Gubler, F. (2005). The Arabidopsis GAMYB-Like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17, 705–721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu, N., Liang, W., Yang, X., Jin, W., Wilson, Z.A., Hu, J., and Zhang, D. (2013). EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4, 1445.

    Article  PubMed  CAS  Google Scholar 

  • Pan, X., Yan, W., Chang, Z., Xu, Y., Luo, M., Xu, C., Chen, Z., Wu, J., and Tang, X. (2020). OsMYB80 regulates anther development and pollen fertility by targeting multiple biological pathways. Plant Cell Physiol 61, 988–1004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phan, H.A., Iacuone, S., Li, S.F., and Parish, R.W. (2011). The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23, 2209–2224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phan, H.A., Li, S.F., and Parish, R.W. (2012). MYB80, a regulator of tapetal and pollen development, is functionally conserved in crops. Plant Mol Biol 78, 171–183.

    Article  CAS  PubMed  Google Scholar 

  • Schneider-Belhaddad, F., and Kolattukudy, P. (2000). Solubilization, partial purification, and characterization of a fatty aldehyde decarbonylase from a higher plant, Pisum sativum. Arch Biochem Biophys 377, 341–349.

    Article  CAS  PubMed  Google Scholar 

  • Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., and Levine, A. (1999). The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11, 431–443.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorensen, A., Guerineau, F., Canales-Holzeis, C., Dickinson, H.G., and Scott, R.J. (2002). A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29, 581–594.

    Article  CAS  PubMed  Google Scholar 

  • Sorensen, A.M., Kröber, S., Unte, U.S., Huijser, P., Dekker, K., and Saedler, H. (2003). The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33, 413–423.

    Article  CAS  PubMed  Google Scholar 

  • Than, M.E., Helm, M., Simpson, D.J., Lottspeich, F., Huber, R., and Gietl, C. (2004). The 2.0 Å crystal structure and substrate specificity of the KDEL-tailed cysteine endopeptidase functioning in programmed cell death of ricinus communis endosperm. J Mol Biol 336, 1103–1116.

    Article  CAS  PubMed  Google Scholar 

  • Tsuchiya, T., Toriyama, K., Ejiri, S., and Hinata, K. (1994). Molecular characterization of rice genes specifically expressed in the anther tapetum. Plant Mol Biol 26, 1737–1746.

    Article  CAS  PubMed  Google Scholar 

  • Tsuchiya, T., Toriyama, K., Nasrallah, M.E., and Ejiri, S. (1992). Isolation of genes abundantly expressed in rice anthers at the microspore stage. Plant Mol Biol 20, 1189–1193.

    Article  CAS  PubMed  Google Scholar 

  • Uzair, M., Xu, D., Schreiber, L., Shi, J., Liang, W., Jung, K.H., Chen, M., Luo, Z., Zhang, Y., Yu, J., et al. (2020). PERSISTENT TAPETAL CELL2 is required for normal tapetal programmed cell death and pollen wall patterning. Plant Physiol 182, 962–976.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, Z.A., Morroll, S.M., Dawson, J., Swarup, R., and Tighe, P.J. (2001). The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28, 27–39.

    Article  CAS  PubMed  Google Scholar 

  • Wu, H., and Cheun, A.Y. (2000). Programmed cell death in plant reproduction. Plant Mol Biol 44, 267–281.

    Article  PubMed  Google Scholar 

  • Xie, H.T., Wan, Z.Y., Li, S., and Zhang, Y. (2014). Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26, 2007–2023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, J., Yang, C., Yuan, Z., Zhang, D., Gondwe, M.Y., Ding, Z., Liang, W., Zhang, D., and Wilson, Z.A. (2010). The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22, 91–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanouchi, U., Yano, M., Lin, H., Ashikari, M., and Yamada, K. (2002). A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99, 7530–7535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Z., Liu, L., Sun, L., Yu, P., Zhang, P., Abbas, A., Xiang, X., Wu, W., Zhang, Y., Cao, L., et al. (2019a). OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Mol Biol 99, 175–191.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Sun, L., Zhang, P., Zhang, Y., Yu, P., Liu, L., Abbas, A., Xiang, X., Wu, W., Zhan, X., et al. (2019b). TDR INTERACTING PROTEIN 3, encoding a PHD-finger transcription factor, regulates Ubisch bodies and pollen wall formation in rice. Plant J 99, 844–861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, D., Liu, D., Lv, X., Wang, Y., Xun, Z., Liu, Z., Li, F., and Lu, H. (2014). The cysteine protease CEP1, a key executor involved in tapetal programmed cell death, regulates pollen development in Arabidopsis. Plant Cell 26, 2939–2961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, D.B., and Wilson, Z.A. (2009). Stamen specification and anther development in rice. Chin Sci Bull 54, 2342–2353.

    Article  CAS  Google Scholar 

  • Zhang, D.S., Liang, W.Q., Yuan, Z., Li, N., Shi, J., Wang, J., Liu, Y.M., Yu, W.J., and Zhang, D.B. (2008). Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1, 599–610.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, W., Sun, Y., Timofejeva, L., Chen, C., Grossniklaus, U., and Ma, H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133, 3085–3095.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z.B., Zhu, J., Gao, J.F., Wang, C., Li, H., Li, H., Zhang, H.Q., Zhang, S., Wang, D.M., Wang, Q.X., et al. (2007). Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52, 528–538.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J., Chen, H., Li, H., Gao, J.F., Jiang, H., Wang, C., Guan, Y.F., and Yang, Z.N. (2008). Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55, 266–277.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J., Zhang, G.Q., Chang, Y.H., Li, X.C., Yang, J., Huang, X.Y., Yu, Q. B., Chen, H., Wu, T.L., and Yang, Z.N. (2010). AMYB103 is a crucial regulator of several pathways affecting Arabidopsis anther development. Sci China Life Sci 53, 1112–1122.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31801338), and the Major Program of Guangdong Basic and Applied Research (2019B030302006).

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Correspondence to Hongning Tong or Chengcai Chu.

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Che, R., Hu, B., Wang, W. et al. POLLEN STERILITY, a novel suppressor of cell division, is required for timely tapetal programmed cell death in rice. Sci. China Life Sci. 65, 1235–1247 (2022). https://doi.org/10.1007/s11427-021-2011-2

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