5.9
CiteScore
5.9
Impact Factor
Volume 48 Issue 8
Aug.  2021
Turn off MathJax
Article Contents

Sporophytic control of anther development and male fertility by glucose-6-phosphate/phosphate translocator 1 (OsGPT1) in rice

doi: 10.1016/j.jgg.2021.04.013
Funds:

This research was supported by the grants from National Natural Science Foundation of China (31922005), Zhejiang Provincial Natural Science Foundation of China (LR18C020001), Zhejiang University K.P.Chao's High Technology Development Foundation (2018RC016), the Young Elite Scientist Sponsorship Program by CAST (2018QNRC001), and 111 Project (B14027) to J.X. The authors gratefully acknowledge the services and facilities supported by Dr. Zhenyu Qi of the Agricultural Experiment Station in Zhejiang University.

  • Received Date: 2020-11-10
  • Accepted Date: 2021-04-27
  • Rev Recd Date: 2021-04-26
  • Publish Date: 2021-08-20
  • Coordination between the sporophytic tissue and the gametic pollen within anthers is tightly controlled to achieve the optimal pollen fitness. Glucose-6-phosphate/phosphate translocator (GPT) transports glucose-6-phosphate, a key precursor of starch and/or fatty acid biosynthesis, into plastids. Here, we report the functional characterization of OsGPT1 in the rice anther development and pollen fertility. Pollen grains from homozygous osgpt1 mutant plants fail to accumulate starch granules, resulting in pollen sterility. Genetic analyses reveal a sporophytic effect for this mutation. OsGPT1 is highly expressed in the tapetal layer of rice anther. Degeneration of the tapetum, an important process to provide cellular contents to support pollen development, is impeded in osgpt1 plants. In addition, defective intine and exine are observed in the pollen from osgpt1 plants. Expression levels of multiple genes that are important to tapetum degeneration or pollen wall formation are significantly decreased in osgpt1 anthers. Previously, we reported that AtGPT1 plays a gametic function in the accumulation of lipid bodies in Arabidopsis pollen. This report highlights a sporophytic role of OsGPT1 in the tapetum degeneration and pollen development. The divergent functions of OsGPT1 and AtGPT1 in pollen development might be a result of their independent evolution after monocots and dicots diverged.

  • loading
  • Andriotis, V.M.E., Pike, M.J., Bunnewell, S., Hills, M.J., Smith, A.M., 2010. The plastidial glucose-6-phosphate/phosphate antiporter GPT1 is essential for morphogenesis in Arabidopsis embryos. Plant J. 64, 128-139.
    Ariizumi, T., Hatakeyama, K., Hinata, K., Inatsugi, R., Nishida, I., Sato, S., Kato, T., Tabata, S., Toriyama, K., 2004. Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J. 39, 170-181.
    Aya, K., Ueguchi-Tanaka, M., Kondo, M., Hamada, K., Yano, K., Nishimura, M., Matsuoka, M., 2009. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21, 1453-1472.
    Baune, M.C., Lansing, H., Fischer, K., Meyer, T., Charton, L., Linka, N., von Schaewen, A., 2020. The Arabidopsis plastidial glucose-6-phosphate transporter GPT1 is dually targeted to peroxisomes via the endoplasmic reticulum. Plant Cell 32, 1703-1726.
    Borg, M., Brownfield, L., Twell, D., 2009. Male gametophyte development: a molecular perspective. J. Exp. Bot. 60, 1465-1478.
    Chang, Z., Chen, Z., Yan, W., Xie, G., Lu, J., Wang, N., Lu, Q., Yao, N., Yang, G., Xia, J., 2016. An ABC transporter, OsABCG26, is required for anther cuticle and pollen exine formation and pollen-pistil interactions in rice. Plant Sci. 253, 21-30.
    Caspar, T., Huber, S.C., Somerville, C., 1985. Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis-thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol. 79, 11-17.
    Chang, Z.Y., Chen, Z.F., Wang, N., Xie, G., Lu, J.W., Yan, W., Zhou, J.L., Tang, X.Y., Deng, X.W., 2016. Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc. Natl. Acad. Sci. U. S. A. 113, 14145-14150.
    Chen, W., Yu, X., Zhang, K., Shi, J., De Oliveira, S., Schreiber, L., Shanklin, J., Zhang, D., 2011. Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol. 157, 842-853.
    Clough, S.J., Bent, A.F., 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
    Datta, R., Chamusco, K.C., Chourey, P.S., 2002. Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol. 130, 1645-1656.
    Feng, Z.Y., Zhang, B.T., Ding, W.N., Liu, X.D., Yang, D.L., Wei, P.L., Cao, F.Q., Zhu, S.H., Zhang, F., Mao, Y.F., 2013. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229-1232.
    Ferguson, A.C., Pearce, S., Band, L.R., Yang, C., Ferjentsikova, I., King, J., Yuan, Z., Zhang, D., Wilson, Z.A., 2017. Biphasic regulation of the transcription factor ABORTED MICROSPORES (AMS) is essential for tapetum and pollen development in Arabidopsis. New Phytol. 213, 778-790.
    Fischer, K., Weber, A., 2002. Transport of carbon in non-green plastids. Trends Plant Sci. 7, 345-351.
    Flugge, U.I., 1995. Phosphate translocation in the regulation of photosynthesis. J. Exp. Bot. 46, 1317-1323.
    Flugge, U.I., 1999. Phosphate translocators in plastids. Annu. Rev. Plant Physiol. 50, 27-45.
    Fu, Y., Li, M.Y., Zhang, S.T., Yang, Q., Zhu, E.G., You, C.J., Qi, J., Ma, H., Chang, F., 2020. Analyses of functional conservation and divergence reveal requirement of bHLH010/089/091 for pollen development at elevated temperature in Arabidopsis. J. Genet. Genomics 47, 477-492.
    Goldberg, R.B., Beals, T.P., Sanders, P.M., 1993. Anther development-basic principles and practical applications. Plant Cell 5, 1217-1229.
    Gomez, J.F., Talle, B., Wilson, Z.A., 2015. Anther and pollen development: a conserved developmental pathway. J. Integr. Plant Biol. 57, 876-891.
    Guan, Y., Meng, X., Khanna, R., LaMontagne, E., Liu, Y., Zhang, S., Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLoS Genet. e1004384.
    Han, M.J., Jung, K.H., Yi, G., An, G., 2011. Rice importin β 1 gene affects pollen tube elongation. Mol. Cell 31, 523-530.
    Heslop-Harrison, J., Heslop-Harrison, Y., 1970. Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol. 45, 15-20.
    Hill, L.M., Smith, A.M., 1991. Evidence that glucose-6-phosphate is imported as the substrate for starch synthesis by the plastids of developing pea embryos. Planta 185, 91-96.
    Hirose, T., Ohdan, T., Nakamura, Y., Terao, T., 2006. Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiol. Plantarum 128, 425-435.
    Hirose, T., Zhang, Z., Miyao, A., Hirochika, H., Ohsugi, R., Terao, T., 2010. Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. J. Exp. Bot. 61, 3639-3646.
    Huang, J.Y., Zhao, X.B., Cheng, K., Jiang, Y.H., Ouyang, Y.D., Xu, C.G., Li, X.H., Xiao, J.H., Zhang, Q.F., 2013. OsAP65, a rice aspartic protease, is essential for male fertility and plays a role in pollen germination and pollen tube growth. J. Exp. Bot. 64, 3351-3360.
    Huang, X., Run, M., Sun, M.X., 2019. OsGCD1, a novel player in rice intine construction. J. Genet. Genomics 46, 359-362.
    Jeong, C.Y., Kim, J.H., Lee, W.J., Jin, J.Y., Kim, J., Hong, S.W., Lee, H., 2018. AtMyb56 regulates anthocyanin levels via the modulation of AtGPT2 expression in response to sucrose in Arabidopsis. Mol. Cell 41, 351-361.
    Jiang, H.W., Dian, W.M., Liu, F.Y., Wu, P., 2003. Cloning and characterization of a glucose 6-phosphate/phosphate translocator from Oryza sativa. J. Zhejiang Univ. - Sci. 4, 331-335.
    Jung, K.H., Han, M.J., Lee, Y.S., Kim, Y.W., Hwang, I., Kim, M.J., Kim, Y.K., Nahm, B.H., An, G., 2005. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705-2722.
    Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A., Flugge, U.I., 1998. Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10, 105-117.
    Kaneko, M., Inukai, Y., Ueguchi-Tanaka, M., Itoh, H., Izawa, T., Kobayashi, Y., Hattori, T., Miyao, A., Hirochika, H., Ashikari, M., 2004. Loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development. Plant Cell 16, 33-44.
    Kossmann, J., Lloyd, J., 2000. Understanding and influencing starch biochemistry. Crit. Rev. Plant Sci. 19, 171-226.
    Kunz, H.H., Hausler, R.E., Fettke, J., Herbst, K., Niewiadomski, P., Gierth, M., Bell, K., Steup, M., Flugge, U.I., Schneider, A., 2010. The role of plastidial glucose-6-phosphate/phosphate translocators in vegetative tissues of Arabidopsis thaliana mutants impaired in starch biosynthesis. Plant Biol. 12, 115-128.
    Lee, Y., Kim, E.S., Choi, Y., Hwang, I., Staiger, C.J., Chung, Y.Y., Lee, Y., 2008. The Arabidopsis phosphatidylinositol 3-kinase is important for pollen development. Plant Physiol. 147, 1886-1897.
    Li, N., Zhang, D.S., Liu, H.S., Yin, C.S., Li, X.X., Liang, W.Q., Yuan, Z., Xu, B., Chu, H.W., Wang, J., 2006. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
    Li, X., Gao, X., Wei, Y., Deng, L., Ouyang, Y., Chen, G., Li, X., Zhang, Q., Wu, C., 2011. Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-box adenosine 5'-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23, 1416-1434.
    Liu, Y., Liu, X., Chen, H., Zheng, P., Wang, W., Wang, L., Zhang, J., Tu, J., 2017. A plastid-localized pentatricopeptide repeat protein is required for both pollen development and plant growth in rice. Sci. Rep. 7, 1-12.
    Liu, Z., Lin, S., Shi, J., Yu, J., Zhu, L., Yang, X., Zhang, D., Liang, W., 2017. Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning. Plant J. 91, 263-277.
    Ma, H., 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393-434.
    Mccormick, S., 1993. Male gametophyte development. Plant Cell 5, 1265-1275.
    Nelson, B.K., Cai, X., Nebenfuhr, A., 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
    Neuhaus, H.E., Henrichs, G., Scheibe, R., 1993. Characterization of glucose-6-phosphate incorporation into starch by isolated intact cauliflower-bud plastids. Plant Physiol. 101, 573-578.
    Ni, E., Zhou, L., Li, J., Jiang, D., Wang, Z., Zheng, S., Qi, H., Zhou, Y., Wang, C., Xiao, S., 2018. OsCER1 plays a pivotal role in very-long-chain alkane biosynthesis and affects plastid development and programmed cell death of tapetum in rice (Oryza sativa L.). Front. Plant Sci. 9, 1217.
    Niewiadomski, P., Knappe, S., Geimer, S., Fischer, K., Schulz, B., Unte, U.S., Rosso, M.G., Ache, P., Flugge, U.I., Schneider, A., 2005. The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17, 760-775.
    Niu, N., Liang, W., Yang, X., Jin, W., Wilson, Z.A., Hu, J., Zhang, D., 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 4, 1445.
    Nonomura, K., Miyoshi, K., Eiguchi, M., Suzuki, T., Miyao, A., Hirochika, H., Kurata, N., 2003. The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728-1739.
    Pacini, E., Guarnieri, M., Nepi, M., 2006. Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228, 73-77.
    Papini, A., Mosti, S., Brighigna, L., 1999. Programmed-cell death events during tapetum development of angiosperms. Protoplasma 207, 213-221.
    Perrone, I., Pagliarani, C., Lovisolo, C., Chitarra, W., Roman, F., Schubert, A., 2012. Recovery from water stress affects grape leaf petiole transcriptome. Planta 235, 1383-1396.
    Scott, R., Hodge, R., Paul, W., Draper, J., 1991. The molecular-biology of anther differentiation. Plant Sci. 80, 167-191.
    Silva, A., Noronha, H., Dai, Z.W., Delrot, S., Geros, H., 2017. Low source-sink ratio reduces reserve starch in grapevine woody canes and modulates sugar transport and metabolism at transcriptional and enzyme activity levels. Planta 246, 525-535.
    Tauberger, E., Fernie, A.R., Emmermann, M., Renz, A., Kossmann, J., Willmitzer, L., Trethewey, R.N., 2000. Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant J. 23, 43-53.
    Toyota, K., Tamura, M., Ohdan, T., Nakamura, Y., 2006. Expression profiling of starch metabolism-related plastidic translocator genes in rice. Planta 223, 248-257.
    White, J.A., Todd, T., Newman, T., Focks, N., Girke, T., de Ilarduya, O.M., Jaworski, J.G., Ohlrogge, J.B., Benning, C., 2000. A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. Plant Physiol. 124, 1582-1594.
    Wilson, Z.A., Zhang, D.B., 2009. From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479-1492.
    Wu, H.M., Cheung, A.Y., 2000. Programmed cell death in plant reproduction. Plant Mol. Biol. 44, 267-281.
    Xu, J., Yang, C.Y., Yuan, Z., Zhang, D.S., Gondwe, M.Y., Ding, Z.W., Liang, W.Q., Zhang, D.B., Wilson, Z.A., 2010. The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22, 91-107.
    Zhang, D.S., Liang, W.Q., Yuan, Z., Li, N., Shi, J., Wang, J., Liu, Y.M., Yu, W.J., Zhang, D.B., 2008. Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol. Plant 1, 599-610.
    Zhang, D., Liang, W., Yin, C., Zong, J., Gu, F., Zhang, D., 2010. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol. 154, 149-162.
    Zhang, D.B., Luo, X., Zhu, L., 2011. Cytological analysis and genetic control of rice anther development. J. Genet. Genomics 38, 379-390.
    Zhang, Y., Su, J., Duan, S., Ao, Y., Dai, J., Liu, J., Wang, P., Li, Y., Liu, B., Feng, D., 2011. A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7, 30.
    Zhang, H., Wang, M., Li, Y., Yan, W., Chang, Z., Ni, H., Chen, Z., Wu, J., Xu, C., Deng, X.W., 2020. GDSL esterase/lipases OsGELP34 and OsGELP110/OsGELP115 are essential for rice pollen development. J. Integr. Plant Biol. 62, 1574-1593.
    Zhang, M., Xu, X., Zheng, Y., Zhang, Y., Deng, X., Luo, S., Wu, Q., Xu, J., Zhang, S., 2020. Expression of a plastid-localized sugar transporter in the suspensor is critical to embryogenesis. Plant Physiol. 185, 1021-1038.
    Zhao, G.C., Shi, J.X., Liang, W.Q., Xue, F.Y., Luo, Q., Zhu, L., Qu, G.R., Chen, M.J., Schreiber, L., Zhang, D.B., 2015. Two ATP binding cassette G transporters, rice ATP binding cassette G26 and ATP binding cassette G15, collaboratively regulate rice male reproduction. Plant Physiol. 169, 2064-2079.
    Zheng, Y., Deng, X., Qu, A., Zhang, M., Tao, Y., Yang, L., Liu, Y., Xu, J., Zhang, S., Regulation of pollen lipid body biogenesis by MAP kinases and downstream WRKY transcription factors in Arabidopsis. PLoS Genet. e1007880.
    Zhou, S.R., Wang, Y., Li, W.C., Zhao, Z.G., Ren, Y.L., Wang, Y., Gu, S.H., Lin, Q.B., Wang, D., Jiang, L., 2011. Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23, 111-129.
    Zhu, X., Yu, J., Shi, J., Tohge, T., Fernie, A.R., Meir, S., Aharoni, A., Xu, D., Zhang, D., Liang, W., 2017. The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice. J. Integr. Plant Biol. 59, 612-628.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (249) PDF downloads (41) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return