AI Chat Paper
Discover the SciOpen Platform and Achieve Your Research Goals with Ease.
Search articles, authors, keywords, DOl and etc.
{{expandStatus?'Exit ':''}}Advanced Search
Unreduced gametes through chromosome doubling play a major role in the process of plant polyploidization. Our previous work confirmed that Camellia oleifera can produce natural 2n pollen, and it is possible to induce the 2n pollen formation by high temperature treatment. This study focused on the optimization of the 2n pollen induction technique and the mechanisms of high temperature-induced 2n pollen formation in C. oleifera. We found that the optimal protocol for inducing 2n pollen via high temperature was to perform 45 ℃ with 4 h at the prophase I stage of the pollen mother cells (PMCs). Meanwhile, high temperature significantly decreased the yield and fertility of 2n pollen. Through the observation of meiosis, abnormal chromosome and cytological behaviour was discovered under high-temperature treatment, and we confirmed that the formation of 2n pollen is caused by abnormal cell plate. Based on weighted gene co-expression network analysis, fifteen hub genes related to cell cycle control were identified. After male flower buds were exposed to heat shock, polygalacturonase gene (CoPGX3) was significantly upregulated. We inferred that high temperature causes the CoPGX3 gene to be overexpressed and that CoPGX3 is redistributed into the cytosol where it degrades cytoplasmic pectin, which leads to an abnormal cell plate. Furthermore, abnormal cytokinesis resulted in the formation of dyads and triads, and PMCs divided to produce 2n pollen. Our findings provide new insights into the mechanism of 2n pollen induced by high temperature in a woody plant and lay a foundation for further ploidy breeding of C. oleifera.
Bai, X., Peirson, B.N., Dong, F., Xue, C., Makaroff, C.A., 1999. Isolation and characterization of SYN1 a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell, 11: 417-430.
Bhat, S.R., Gill, S.S., 1985. The implications of 2n egg gametes in nobilization and breeding of sugarcane. Euphytica, 34: 377-384.
Bomblies, K., Higgins, J.D., Yant, D., 2015. Meiosis evolves adaptation to external and internal environments. New Phytol, 208: 306-323.
Brown, R.C., Lemmon, B.E., 2001. The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma, 215: 35-49.
Brownfield, L., Khler, C., 2011. Unreduced gamete formation in plants mechanisms and prospects. J Exp Bot, 62: 1659-1668.
Cai, X., Dong, F.G., Edelmann, R.E., Makaroff, C.A., 2003. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci, 116: 2999-3007.
Camadro, E.L., Saffarano, S.K., Espinillo, J.C., Castro, M., Simon, P.W., 2008. Cytological mechanisms of 2n pollen formation in the wild potato Solanum okadae and pollen-pistil relations with the cultivated potato Solanum tuberosum. Genet Resour Crop Evol, 55: 471-477.
Conicella, C., Genualdo, G., Errico, A., Frusciante, L., Monti, L.M., 1996. Meiotic restitution mechanisms and 2n pollen formation in a Solanum tuberosum dihaploid and in dihaploid × wild species hybrids. Plant Breed, 115: 157-161.
Chen, C.G., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y.H., Xia, R., 2020. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 13: 1194-1202.
Chen, J.M., Yang, X.Q., Huang, X.M., Duan, S.H., Long, C., Chen, J.K., Rong, J., 2017. Leaf transcriptome analysis of a subtropical evergreen broadleaf plant, wild oil-tea camellia (Camellia oleifera), revealing candidate genes for cold acclimation. BMC Genom, 18: 211.
Cheng, S., Yao, P., Geng, X., Liu, C., Xie, L., 2022. High temperature treatment generates unreduced pollen in Paeonia suffruticosa. Acta Hortic Sin, 49: 581-589. (in Chinese)
Dewitte, A., Eeckhaut, T., Van Huylenbroeck, J., Van Bockstaele, E., 2010. Meiotic aberrations during 2n pollen formation in Begonia. Heredity, 104: 215-223.
Francis, K.E., Lam, Y., Copenhaver, G.P., 2006. Separation of Arabidopsis pollen tetrads is regulated by QUARTET1 a pectin methylesterase gene. Plant Physiol, 142: 1004-1013.
Gao, C., Yuan, D.Y., Wang, B.F., Yang, Y., liu, D.M., Han, Z.Q., 2015. A cytological study of anther and pollen development in Camellia oleifera. Genet Mol Res, 14: 8755-8765.
Gu, X.F., Luo, Z.R., 2003. Sutdies on abnormal meiosis producing 2n pollens in nonastgringent persimmon (Diospyros kaki Thunb.). Acta Hortic Sin, 30: 135-140. (in Chinese)
Gu, Y., Rasmussen, C.G., 2022. Cell biology of primary cell wall synthesis in plants. Plant Cell, 34: 103-128.
Han, Z.Q., Geng, X.N., Kang, X.Y., Xu, C.P., Yao, P.Q., Bai, F.Y., Kang, X.Y., 2018. Analysis of genetic composition and transmitted parental heterozygosity of natural 2n gametes in Populus tomentosa based on SSR markers. Planta, 247: 1407-1421.
Hu, Y., Gao, C., Deng, Q.E., Qiu, J., Wei, H.L., Yan, L., Xie, J.J., Liao, D.S., 2021. Anatomical characteristics of petalized anther abortion in male sterile Camellia oleifera plants. J Am Soc Hortic Sci, 146: 411-423.
Jacob, Y., Pierret, V., 2000. Pollen size and ploidy level in the genus Rosa. Acta Hortic, 508: 289-292.
Kang, X.Y., Zhu, Z.T., Zhang, Z.Y., 2000. Suitable Period of High Temperature Treatment for 2n Pollen of Populus Tomentosa×P. Bolleana. J Beijing For Univ, 22: 1-4. (in Chinese)
Khan, N., Fatima, F., Haider, M.S., Shazadee, H., Liu, Z., Zheng, T., Fang, J., 2019. Genome-wide identification and expression profiling of the polygalacturonase (PG) and pectin methylesterase (PME) genes in grapevine (Vitis vinifera L). Int J Mol Sci, 20: 3180.
Kim, D., Langmead, B., Salzberg, S.L., 2015. HISAT a fast spliced aligner with low memory requirements. Nat Methods, 12: 357-360.
Kosetsu, K., Matsunaga, S., Nakagami, H., Colcombet, J., Sasabe, M., Soyano, T., Takahashi, Y., Hirt, H., Machida, Y., 2010. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell, 22: 3778-3790.
Langfelder, P., Horvath, S., 2008. WGCNA an R package for weighted correlation network analysis. BMC Bioinf, 9: 1-13.
Lei, X.N., Ning, Y.J., Elesawi, L., Yang, K., Chen, L., Wang, C., Liu, B., 2020. Heat stress interferes with chromosome segregation and cytokinesis during male meiosis in Arabidopsis thaliana. Plant Signal Behav, 15: 1746985.
Li, J.B., Xiong, C.W., Ruan, D., Du, W., Li, H., Ruan, C.J., 2023. Identification of Camellia oleifera WRKY transcription factor genes and functional characterization of CoWRKY78. Front Plant Sci, 14: 1110366.
Li, Y., Wang, Y., Wang, P.Q., Yang, J., Kang, X.Y., 2016. Induction of unreduced megaspores in Eucommia ulmoides by high temperature treatment during megasporogenesis. Euphytica, 212: 515-524.
Liu, C.Y., Peng, C.F., Cheng, S.P., Yao, P.Q., Geng, X.X., Xie, L.H., 2023. Creation of triploid germplasm in Paeonia ostii ‘Fengdan’ through 2n female gametes inducing with high temperature treatment. Acta Hortic Sin, 50: 1455-1466. (in Chinese)
Lu, M., Zhang, P.D., Wang, J., Kang, X.Y., Wu, J.Y., Wang, X.J., Chen, Y., 2014. Induction of tetraploidy using high temperature exposure during the first zygote division in Populus adenopoda Maxim. Plant Growth Regul, 72: 279-287.
Luan, F., Zeng, J.S., Yang, Y., He, X.R., Wang, B.J., Gao, Y.B., Zeng, N., 2020. Recent advances in Camellia oleifera Abel a review of nutritional constituents biofunctional properties and potential industrial applications. J Funct Foods, 75: 104242.
Mai, Y.N., Li, H.W., Suo, Y.J., Fu, J.M., Sun, P., Han, W.J., Diao, S.F., Li, F.D., 2019. High temperature treatment generates unreduced pollen in persimmon (Diospyros kaki Thunb). Sci Hortic, 258: 108774.
Mason, A.S., Nelson, M.N., Yan, G.L., Cowling, W.A., 2011. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol, 11: 103.
Miyazaki, W.Y., Orr-Weaver, T.L., 1994. Sister-chromatid cohesion in mitosis and meiosis. Annu Rev Genet, 28: 167-187.
Nystrom, S.L., McKay, D.J., 2021. Memes: a motif analysis environment in R using tools from the MEME Suite. PLoS Comput Biol, 17: e1008991.
Ortiz, R., Iwanaga, M., Mendoza, H.A., 1988. Combining ability and parental effects in 4x-2x crosses for potato breeding. Potato Res, 31: 643-650.
Pereira, E.O., Kolotilin, I., Conley, A.J., Menassa, R., 2014. Production and characterization of in planta transiently produced polygalacturanase from Aspergillus niger and its fusions with hydrophobin or ELP tags. BMC Biotechnol, 14: 59.
Qi, W.Q., Zhang, C.L., Wang, W.J., Cao, Z., Li, S., Li, H., Zhu, W., Huang, Y.Q., Bao, M.Z., He, Y.H., Zheng, R.R., 2021. Comparative transcriptome analysis of different heat stress responses between self-root grafting line and heterogeneous grafting line in rose. Hortic Plant J, 7: 243-255.
Quan, W.X., Wang, A.P., Gao, C., Li, C.C., 2022. Applications of Chinese Camellia oleifera and its by-products a review. Front Chem, 10: 921246.
Ramsey, J., 2007. Unreduced gametes and neopolyploids in natural populations of Achillea borealis (Asteraceae). Heredity, 98: 143-150.
Rhee, S.Y., Osborne, E., Poindexter, P.D., Somerville, C.R., 2003. Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol, 133: 1170-1180.
Rodomiro, O., 1997. Occurrence and inheritance of 2n pollen in Musa. Ann Bot, 79: 449-453.
Shamina, N., Dorogova, N., Trunova, S., 2000. Radial spindle and the phenotype of the maize meiotic mutant, dv. Cell Biol Int, 24: 729-736.
Shamina, N.V., Gordeeva, E.I., Kovaleva, N.M., Seriukova, E.G., Dorogova, N.V., 2007. Formation and function of phragmoplast during successive cytokinesis stages in higher plant meiosis. Cell Biol Int, 31: 626-635.
Song, X.M., Wang, J.P., Sun, P.C., Ma, X., Yang, Q.H., Hu, J.J., Wang, X.Y., 2020. Preferential gene retention increases the robustness of cold regulation in Brassicaceae and other plants after polyploidization. Hortic Res, 7: 20.
Storme, N.D., Copenhaver, G.P., Geelen, D., 2012. Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol (Wash D C), 160: 1808-1826.
Storme, N.D., Geelen, D., 2013a. Cytokinesis in plant male meiosis. Plant Signal Behav, 8: e23394.
Storme, N.D., Geelen, D., 2013b. Sexual polyploidization in plants cytological mechanisms and molecular regulation. New Phytol, 198: 670-684.
Storme, N.D., Geelen, D., 2014. The impact of environmental stress on male reproductive development in plants biological processes and molecular mechanisms. Plant Cell Environ, 37: 1-18.
Storme, N.D., Geelen, D., 2020. High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana. Commun Biol, 3: 187.
Taschett, O.M., Pagliarini, M.S., 2003. Occurrence of 2n and jumbo pollen in the Brazilian ginseng (Pfaffia glomerata and P. tuberosa). Euphytica, 133: 139-145.
Tavoletti, S., Mariani, A., Veronesi, F., 1991. Cytological analysis of macro and microsporogenesis of a diploid alfalfa clone producing male and female 2n gametes. Crop Sci, 31: 1258-1263.
Terefe, N.S., Gamage, M., Vilkhu, K., Simons, L., Mawson, R., Versteeg, C., 2009. The kinetics of inactivation of pectin methylesterase and polygalacturonase in tomato juice by thermosonication. Food Chem, 117: 20-27.
Tian, M.D., Zhang, L., Kang, X.Y., Zhang, P.D., 2018. High temperature exposure did not affect induced 2n pollen viability in Populus. Plant Cell Environ, 41: 1383-1393.
Tommasini, D., Fogel, B.L., 2023. multiWGCNA: an R package for deep mining gene co-expression networks in multi-trait expression data. BMC Bioinf, 24: 115.
Wang, J., Li, D.L., Shang, F.N., Kang, X.Y., 2017. High temperature-induced production of unreduced pollen and its cytological effects in Populus. Sci Rep, 7: 5281.
Wu, H.C., Hsu, S.F., Luo, D.L., Chen, S.J., Huang, W.D., Lur, H.S., Jinn, T.L., 2010. Recovery of heat shock-triggered released apoplastic Ca2+ accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. J Exp Bot, 61: 2843-2852.
Wu, T., Jia, R., Yang, S.H., Zhao, X., Yu, X.N., Guo, Y., Ge, H., 2022. Research advances and prospects on Phalaenopsis polyploid breeding. Acta Hortic Sin, 49: 448-462. (in Chinese)
Yang, Y., Anderson, C.T., Cao, J., 2021. Polygalacturonase45 cleaves pectin and links cell proliferation and morphogenesis to leaf curvature in Arabidopsis thaliana. Plant J, 106: 1493-1508.
Yao, P.Q., Li, G.H., Long, Q.Y., He, L.G., Kang, X.Y., 2017. Microsporogenesis and induction of unreduced pollen with high temperatures in rubber tree clone RRIM 600. Forests, 8: 152.
Zamariola, L., Tiang, C.L., Storme, N.D., Pawlowski, W., Geelen, D., 2014. Chromosome segregation in plant meiosis. Front Plant Sci, 5: 279.
Zhang, J.F., Wei, Z.Z., Li, D., Li, B.L., 2009. Using SSR markers to study the mechanism of 2n pollen formation in Populus × euramericana (Dode) Guinier and P. × popularis. Ann For Sci, 66: 1-10.
Zhang, P.D., Kang, X.Y., 2017. Occurrence and cytological mechanism of numerically unreduced pollen in diploid Populus euphratica. Silvae Genet, 62: 285-291.
Zhang, Q., Huang, L., Liu, T.T., Yu, X.L., Cao, J.S., 2008. Functional analysis of a pollen-expressed polygalacturonase gene BcMF6 in Chinese cabbage (Brassica campestris L. ssp. chinensis Makino). Plant Cell Rep, 27: 1207-1215.
Zhang, X.Y., Tong, H.L., Han, Z.Q., Huang, L., Tian, J., Fu, Z.X., Yuan, D.Y., 2021. Cytological and morphology characteristics of natural microsporogenesis within Camellia oleifera. Physiol Mol Biol Plants, 27: 959-968.
Zhang, Z.H., Kang, X.Y., 2010. Cytological characteristics of numerically unreduced pollen production in Populus tomentosa Carr. Euphytica, 173: 151-159.
Zhao, C.G., Li, Y.J., Zhang, P.D., Kang, X.Y., 2015. Cytological mechanism of unreduced 2n pollen formation in Populus euphratica. J Nanjing For Univ (Nat Sci Ed), 39: 40-44.
Zhou, X.H., Mo, X.J., Gui, M., Wu, X.W., Jiang, Y.L., Ma, L.L., Tang, W.R., 2015. Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L. Plant Physiol Biochem (Issy les Moulineaux, Fr), 97: 255-263.
Zhou, Q., Cheng, X.T., Kong, B., Zhao, F., Li, Z.Q., Sang, Y.R., Wu, J., Zhang, P.D., 2022. Heat shock-induced failure of meiosis I to meiosis II transition leads to 2n pollen formation in a woody plant. Plant Physiol, 189: 2110-2127.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
京公网安备11010802044758号