Novel Cytological Findings on Gametophyte Development and Embryogenesis in Wheat (Triticum aestivum L.)

Document Type : Research Article

Authors

1 Department of Biology, Faculty of Science, Bu-Ali Sina University, Hamedan, Iran

2 Department of Plant Protection, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran

Abstract

A step-by-step study of the anther and ovule developments, sporogenesis, from pre-meiotic stages to anthesis in anthers and seed development in the ovary, was done in Triticum aestivum L. The results showed that the wall development at tetrasporangiate anthers was consistent with the monocotyledonous type. The anther locule was surrounded by two inner temporal cell layers, including the tapetal cells and the middle layer, and two outer permanent layers, including the endothecium and epidermis. Tapetum cells were observed as uni- or bi-nucleated in the maturity stage. Asynchronous cytokinesis during the meiosis of microsporocytes caused the formation of tetragonal tetrads. The mature pollen grains were monoporated and three-celled type. Different origins of the tapetum cells, the polarity of the tapetum cells, and callose formation around the microsporangial cells were novel findings. The ovule was bitegmic, tenuinucellate, and orthotropous initially, and anatropous in the late developmental stages. Chalazal megaspore was functional causing the formation of monosporic embryo sac type. Due to the proliferation of the antipodal cells, a modified Polygonum type of embryo sac was observed. The first zygote division occurred before the endosperm mother cell division and gave rise to equal cells. The nuclear endosperm was formed by dividing the nucleus of the endosperm mother cell. However, it became cellular in later stages. The endosperm involved three types of cells: an aleurone layer around the embryo sac, the endosperm cells around the embryo with dense cytoplasm, and the more giant and vacuolated endosperm cells away from the embryo. Deposition of the residual callose in the micropylar opening wall of the megaspores tetrad stage, variation in endosperm cell type, and some details of the developmental process are among the novel findings.

Keywords


Albert B, Ressayre A, Nadot S. 2011. Correlation between pollen aperture pattern and callose deposition in late tetrad stage in three species producing atypical pollen grains. Am J Bot 98(2): 189-196.‏
An LH, You RL. 2004. Studies on nuclear degeneration during programmed cell death of synergid and antipodal cells in Triticum aestivum Sex Plant Reprod 17(4): 195-201.‏
Bennett MD, Rao MK, Smith JB, Bayliss MW. 1973. Cell development in the anther, the ovule, and the young seed of Triticum aestivum L. var. Chinese Spring. Phil Trans Roy Soc B 266(875): 39-81.
Browne RG, Iacuone S, Li SF, Dolferus R, Parish RW. 2018. Anther morphological development and stage determination in Triticum aestivum. Front Plant Sci 9: 228.
Cass DD, Peteya DJ, Robertson BL. 1985. Megagametophyte development in Hordeum vulgare. 1. Early megagametogenesis and the nature of cell wall formation. Can J Bot 63(12): 2164-2171.‏
Chehregani A, Malayeri B,Yousefi N. 2009. Developmental stages of ovule and megagametophyte in Chenopodium botrys L. (Chenopodiaceae). Turk J Bot 33(2): 75-81.
Christensen JE. 1972. Developmental aspects of microsporogenesis in Sorghum bicolor.‏ Iowa State University.
Clayton WD. 1990. The spikelet. In: Chapman GP (ed). Reproductive Versatility in the Grasses. Cambridge, UK: Cambridge University Press 32-51.
Davis GL. 1966. Systematic Embryology of the Angiosperms. John Willey & Sons. Inc, USA.‏
Dover GA. 1972. The organization and polarity of pollen mother cells of Triticum aestivum. J Cell Sci 11(3): 699-711.‏
Drews GN, Koltunow A M. 2011. The female gametophyte. The Arabidopsis book/American Society of Plant Biologists 9.‏
Ekici N, Dane F. 2004. Polarity during sporogenesis and gametogenesis in plants. Biologia (Bratislava) 59: 687-696.‏
El‐Ghazaly G, Jensen WA. 1987. Development of wheat (Triticum aestivum) pollen. II. Histochemical differentiation of wall and Ubisch bodies during development. Am J Bot 74(9): 1396-1418.‏
Greene CW. 1984. Sexual and apomictic reproduction in Calamagrostis (Gramineae) from eastern North America. American Journal of Botany 71(3): 285-293.‏
Heslop-Harrison J. 1964. Cell walls, cell membranes and protoplasmic connections during meiosis and pollen development. In Pollen Physiology and Fertilization Edited by Linskens HF. North-Holland, Amsterdam.
Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima SY, Kuroiwa H, Kuroiwa T. 2001. Pollen tube attraction by the synergid cell. Science 293(5534): 1480-1483.‏
Itoh JI, Nonomura KI, Ikeda K, Yamaki S, Inukai Y, Yamagishi H et al. 2005. Rice plant development: from zygote to spikelet. Plant Cell Physiol 46(1): 23-47.‏
Lausser A, Kliwer I, Srilunchang KO, Dresselhaus T. 2009. Sporophytic control of pollen tube growth and guidance in maize. J Exp Bot 61(3): 673-682.‏
Lausser A, Dresselhaus T. 2010. Sporophytic control of pollen tube growth and guidance in grasses.‏ Biochem Soc Trans 38(2): 631-634.
Leblanc O, Peel MD, Carman JG, Savidan Y. 1995. Megasporogenesis and megagametogenesis in several Tripsacum species (Poaceae). Am J Bot 82(1): 57-63.‏
Lovisolo MR, Galati BG. 2007. Ultrastructure and development of the megagametophyte in Eleusine tristachya (Lam.) Lam. (Poaceae). Flora 202(4): 293-301.‏
Mahalingappa MS. 1977. Gametophytes of Eleusine compressa [millets, India]. Phytomorph‏ 27: 231-239.
Manning JC, Linder HP. 1990. Cladistic analysis of patterns of endothecial thickenings in the Poales/Restionales. Am J Bot 77(2): 196-210.
Musiał K, Kościńska-Pająk M, Antolec R, Joachimiak AJ. 2015. Deposition of callose in young ovules of two Taraxacum species varying in the mode of reproduction. Protoplasma 252(1): 135-144.‏
Nakamura AT, Longhi-Wagner HM, Scatena VL. 2010. Anther and pollen development in some species of Poaceae (Poales). Braz J Biol 70(2): 351-360.‏
Nelson MR, Band LR, Dyson RJ, Lessinnes T, Wells DM, Yang C, …, Wilson ZA. 2012. A biomechanical model of anther opening reveals the roles of dehydration and secondary thickening. New Phytol 196(4): 1030-1037.‏
Prieu C, Toghranegar Z, Matamoro-Vidal A, Nadot S, Albert B. 2017. Additional callose deposits are located at the future apertural regions in sulcate, ulcerate, porate, colporate, colpate and syncolpate pollen grains. Bot J Linn Soc 183(2): 271-279.‏
Quilichini TD, Samuels AL, Douglas CJ. 2014. ABCG26-mediated polyketide trafficking and hydroxycinnamoyl spermidines contribute to pollen wall exine formation in Arabidopsis. Plant Cell 26(11): 4483-4498.‏
Ramezani H, Chehregani Rad A, Karamian R. 2018. Development of the male and female gametophyte in Capsicum annuum L. var. California Wonder. Plant Biosyst 152(6): 1-10.‏
Rodkiewicz B. 1970. Callose in cell walls during megasporogenesis in angiosperms. Planta 93(1): 39-47.‏
Saarela JM, Burke SV, Wysocki WP, Barrett MD, Clark LG, Craine JM, …, Duvall MR. 2018. A 250 plastome phylogeny of the grass family (Poaceae): topological support under different data partitions. Peer J 6: e4299.
Schwab CA. 1971. Floral structure and embryology of Diarrhena (Gramineae).‏ Iowa State University.
Shewry PR, Halford NG. 2002. Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53(370): 947-958.‏
Shirkhani Z, Chehregani Rad A, Gholami M. 2019. Sporogenesis and gametophytes development in Datura stramonium L. (Solanaceae). Braz J Bot 42(1): 107-117.‏
Soreng RJ, Peterson PM, Romaschenko K, Davidse G, Teisher JK, Clark LG, …, Zuloaga FO. 2017. A worldwide phylogenetic classification of the Poaceae (Gramineae) II: An update and a comparison of two 2015 classifications. J Syst Evol 55(4): 259-290.‏
Takeuchi H, Higashiyama T. 2012. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10(12): e1001449.‏
Teng N, Huang Z, Mu X, Jin B, Hu Y, Lin J. 2005. Microsporogenesis and pollen development in Leymus chinensis with emphasis on dynamic changes in callose deposition. Flora 200(3): 256-263.‏
Ünal M, Vardar F, Aytürk Ö. 2013. Callose in plant sexual reproduction. In Current progress in biological research. IntechOpen.
Wang, A, Xia Q, Xie W, Datla R, Selvaraj G. 2003. The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc Natl Acad Sci USA 100(24): 14487-14492.‏
Wang H, Mao Y, Yang J, He Y. 2015. TCP24 modulates secondary cell wall thickening and anther endothecium development. Front Plant Sci 6: 436.‏
Wang R, Dobritsa AA. 2018. Exine and aperture patterns on the pollen surface: Their formation and roles in plant reproduction. Annu plant rev online 1(2): 589-628.
Wu CC, Diggle PK, Friedman WE. 2011. Female gametophyte development and double fertilization in Balsas teosinte, Zea mays subsp. parviglumis (Poaceae). Sex Plant Reprod 24(3): 219-229.‏
You R, Jensen WA. 1985. Ultrastructural observations of the mature megagametophyte and the fertilization in wheat (Triticum aestivum). Can J Bot 63(2): 163-178.
Zhou LZ, Juranić M, Dresselhaus T. 2017. Germline development and fertilization mechanisms in maize. Mol Plant 10(3): 389-401.