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Volume 49 Issue 5
May  2022
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Article Contents

OsLTP47 may function in a lipid transfer relay essential for pollen wall development in rice

doi: 10.1016/j.jgg.2022.03.003
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This work was supported by grants from the Guangdong Natural Science Funds for Distinguished Young Scholars (2021B1515020089), the National Natural Science Foundation of China (32030080) and the Major Program of Guangdong Basic and Applied Research (2019B030302006).

  • Received Date: 2021-11-09
  • Accepted Date: 2022-03-05
  • Rev Recd Date: 2022-03-02
  • Publish Date: 2022-03-21
  • In plants, lipid transfer proteins (LTPs) transport pollen wall constituents from the tapetum to the exine, a process essential for pollen wall development. However, the functional cooperation of different LTPs in pollen wall development is not well understood. In this study, we have identified and characterized a grass-specific LTP gene, OsLTP47, an important regulator of pollen wall formation in rice (Oryza sativa). OsLTP47 encodes a membrane-localized LTP and in vitro lipid-binding assays confirms that OsLTP47 has lipid-binding activity. Dysfunction of OsLTP47 causes disordered lipid metabolism and defective pollen walls, leading to male sterility. Yeast two-hybrid and pull-down assays reveal that OsLTP47 physically interacts with another LTP, OsC6. These findings suggest that the plasma membrane-localized OsLTP47 may function as a mediator in a lipid transfer relay through association with cytosolic and/or locular OsC6 for pollen wall development and that various LTPs may function in a coordinated manner to transport lipid molecules during pollen wall development.
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  • Ariizumi, T., Toriyama, K., 2011. Genetic regulation of sporopollenin synthesis and pollen exine development. Annu. Rev. Plant Biol. 62, 437-460
    Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9, 86
    Bubert, H., Lambert, J., Steuernagel, S., Ahlers, F., and Wiermann, R. 2002. Continuous decomposition of sporopollenin from pollen of Typha angustifolia L. by acidic methanolysis. Z. Naturforsch. C J Biosci. 57, 1035-1041
    Chen, W.W., Yu, X.H., Zhang, K.S., Shi, J.X., De Oliveira, S., Schreiber, L., Shanklin, J., Zhang, D.B., 2011. Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol. 157, 842-853
    Choi, H., Jin, J.Y., Choi, S., Hwang, J.U., Kim, Y.Y., Suh, M.C., Lee, Y., 2011. An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J. 65, 181-193
    de Azevedo Souza, C., Kim, S.S., Koch, S., Kienow, L., Schneider, K., McKim, S.M., Haughn, G.W., Kombrink, E., Douglas, C.J., 2009. A novel fatty Acyl-CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21, 507–525
    Dobritsa, A.A., Shrestha, J., Morant, M., Pinot, F., Matsuno, M., Swanson, R., Moller, B.L., Preuss, D., 2009. CYP704B1 is a long-chain fatty acid ω-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol. 151, 574-589
    Domi´nguez, E., Mercado, J.A., Quesada, M.A., and Heredia, A. 1999. Pollen sporopollenin: degradation and structural elucidation. Sex. Plant Reprod. 12, 171-178
    Edlund, A.F., Swanson, R., Preuss, D., 2004. Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16, S84-S97
    Edstam, M.M., Edqvist, J., 2014. Involvement of GPI-anchored lipid transfer proteins in the development of seed coats and pollen in Arabidopsis thaliana. Physiol. Plant. 152, 32-42
    Ge, X.C., Chen, J.C., Li, N., Lin, Y., Sun, C.R., Cao, K.M., 2003. Resistance function of rice lipid transfer protein LTP110. J. Biochem. Mol. Biol. 36, 603-607
    Hu, L.F., Tan, H.X., Liang, W.Q., Zhang, D.B., 2010. The Post-meiotic Deficicent Anther1 (PDA1) gene is required for post-meiotic anther development in rice. J. Genet. Genomics 37, 37-46
    Huang, M.D., Chen, T.L., Huang, A.H., 2013. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol. 163, 1218-1229
    Huang, M.D., Wei, F.J., Wu, C.C., Hsing, Y.I., Huang, A.H., 2009. Analyses of advanced rice anther transcriptomes reveal global tapetum secretory functions and potential proteins for lipid exine formation. Plant Physiol. 149, 694-707
    Jiang, J., Zhang, Z., Cao, J., 2013. Pollen wall development: the associated enzymes and metabolic pathways. Plant Biol. 15, 249-263
    Kader, J.C., 1996. Lipid-transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 627-654
    Kawahara, Y., et al., 2013. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6, 4
    Li, F.S., Phyo, P., Jacobowitz, J., Hong, M., and Weng, J.K. 2019. The molecular structure of plant sporopollenin. Nat. Plants 5, 41-46
    Li, H., Kim, Y.J., Yang, L., Liu, Z., Zhang, J., Shi, H., Huang, G., Persson, S., Zhang, D., Liang, W., 2020. Grass-specific EPAD1 is essential for pollen exine patterning in rice. Plant Cell 32, 3961-3977
    Li, H., Pinot, F., Sauveplane, V., Werck-Reichhart, D., Diehl, P., Schreiber, L., Franke, R., Zhang, P., Chen, L., Gao, Y.W., 2010. Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22, 173-190
    Li, Y.L., Li, D.D., Guo, Z.L., Shi, Q.S., Xiong, S.X., Zhang, C., Zhu, J., Yang, Z.N., 2016. OsACOS12, an orthologue of Arabidopsis acyl-CoA synthetase5, plays an important role in pollen exine formation and anther development in rice. BMC Plant Biol. 16, 256
    Liu, W.Z., Xie, X.R., Ma, X.L., Li, J., Chen, J.H., Liu, Y.G., 2015. DSDecode: A web-based tool for decoding of sequencing chromatograms for genotyping of targeted mutations. Mol. Plant 8, 1431-1433
    Ma, H., 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393-434
    Ma, X.L., Zhang, Q.Y., Zhu, Q.L., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z.F., Li, H.Y., Lin, Y.R., 2015. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274-1284
    McCormick, S., 1993. Male gametophyte development. Plant Cell 5, 1265-1275
    Morant, M., Jorgensen, K., Schaller, H., Pinot, F., Moller, B.L., Werck-Reichhart, D., Bak, S., 2007. CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19, 1473-1487
    Quilichini, T.D., Douglas, C.J., Samuels, A.L., 2014a. New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann. Bot. 114, 1189-1201
    Quilichini, T.D., Samuels, A.L., Douglas, C.J., 2014b. ABCG26-mediated polyketide trafficking and hydroxycinnamoyl spermidines contribute to pollen wall exine formation in Arabidopsis. Plant Cell 26, 4483-4498
    Quilichini, T.D., Grienenberger, E., and Douglas, C.J. 2015. The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113, 170-182
    Shi, J.X., Cui, M.H., Yang, L., Kim, Y.J., Zhang, D.B., 2015. Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci. 20, 741-753
    Shi, J., Tan, H.X., Yu, X.H., Liu, Y.Y., Liang, W.Q., Ranathunge, K., Franke, R.B., Schreiber, L., Wang, Y.J., Kai, G.Y., 2011. Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23, 2225-2246
    Tao, Y., Zou, T., Zhang, X., Liu, R., Chen, H., Yuan, G.Q., Zhou, D., Xiong, P.P., He, Z.Y., Li, G.W., 2021. Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development. Plant J. 108, 358-377
    Tsirigos K.D., Peters C., Shu N., Kall L., Elofsson A., 2015. The TOPCONS web server for combined membrane protein topology and signal peptide prediction. Nucleic Acids Res. 43, W401-W407
    Tsou, C.H., Cheng, P.C., Tseng, C.M., Yen, H.J., Fu, Y.L., You, T.R., Walden, D.B., 2015. Anther development of maize (Zea mays) and longstamen rice (Oryza longistaminata) revealed by cryo-SEM, with foci on locular dehydration and pollen arrangement. Plant Reprod. 28, 47-60
    Xie, X.R., Ma, X.L., Zhu, Q.L., Zeng, D.C., Li, G.S., Liu, Y.G., 2017. CRISPR-GE: A convenient software toolkit for CRISPR-based genome editing. Mol. Plant 10, 1246-1249
    Xie, X.R., Zhang, Z.X., Zhao, Z., Xie, Y.Y., Li, H.Y., Ma, X.L., Liu, Y.G., and Chen, L.T., 2020. The mitochondrial aldehyde dehydrogenase OsALDH2b negatively regulates tapetum degeneration in rice. J. Exp. Bot. 71, 2551-2560
    Xu, J., Ding, Z.W., Vizcay-Barrena, G., Shi, J.X., Liang, W.Q., Yuan, Z., Werck-Reichhart, D., Schreiber, L., Wilson, Z.A., Zhang, D.B., 2014. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26, 1544-1556
    Xue, J.-S., Zhang, B., Zhan, H., Lv, Y.-L., Jia, X.-L., Wang, T., Yang, N.-Y., Lou, Y.-X., Zhang, Z.-B., Hu, W.-J., et al. 2020. Phenylpropanoid derivatives are essential components of sporopollenin in vascular plants. Mol. Plant 13, 1644-1653
    Yang, X.J., Wu, D., Shi, J.X., He, Y., Pinot, F., Grausem, B., Yin, C.S., Zhu, L., Chen, M.J., Luo, Z.J., 2014. Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J. Integr. Plant Biol. 56, 979-994
    Zhang, D.S., Liang, W.Q., Yin, C.S., Zong, J., Gu, F.W., Zhang, D.B., 2010. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol. 154, 149-162
    Zhang, D.B., Shi, J.X., Yang, X.J., 2016. Role of lipid metabolism in plant pollen exine development. Subcell. Biochem. 86, 315-337
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