The role of PCD in sexual dimorphism of dioecious Spinacia oleracea L.

Year 2023, Volume: 9 Issue: 3, 688 - 696, 20.09.2023

Özlem Aytürk , Özal Mutlu , Asuman Karadeniz Pekgöz

https://doi.org/10.28979/jarnas.1162623

Abstract

The formation of non-hermaphroditic, i.e. male or female, flowers is a rare event in the plant kingdom. S. oleracea provides an ideal unisexual floral developmental system for studying the structural development of floral organs. These species forms non-hermaphroditic flowers; the pistil is fertile in the female flower, but the development of the stamens stops at an early phase and this organ atrophies and becomes functionless, while the male flowers form four fertile stamens, however there is not any trace of the pistil, it aborts at a much early stage. We searched for the presence of programmed cell death (PCD) in the abortive tissues during the ontogenetic development of these flowers. These results show curicial information on how the fertile sex organ in spinach differentiates and develops while arresting the development of the other aborted sex organ ; the presence of PCD occur in unisexual flower development in rhe very early stage and continue short time. We also found that stamen development in the female flower and pistil development in the male flower were subject to changes that did not result in large-scale structural changes. The PCD data obtained are the first study of spinach in the literature. This type of studies are shedding additional light on the sexual specialization hypothesis. Moreover, the ability to manipulate or control the flowering of the dioecious plant by simple means holds great potential, both from an economic aspect and to increase food production for an ever-growing human population

Keywords

Spinach, unisexuality, flower, ontogeny, programmed cell death, TUNEL

Supporting Institution

Maltepe University

Project Number

FEN -E-100413-0125

Thanks

This research was supported by MUKKAM (Maltepe University Cancer and Stem Cell Research Centre). We thank MUKKAM for providing laboratory resources.

References

• Ainsworth, C., Parker, J., Buchanan-Wollaston, V. (1998). Sex determination in plants. Currient Topics in Development Biology, 38: 167-223.
• Aytürk, Ö., Unal, M. (2016). Comparison of Female, Gall and Male Flower Development with Microscopic and Molecular Tecniques in Dioecious Ficus carica L. PhD, Marmara University, Istanbul, Turkey.
• Aytürk, Ö., Ünal, M. (2012). Structural Analysis of Reproductive Development in Staminate Flowers of Laurus nobilis L. Notulae Scientia Biologicae, 4(1), 31-43
• Barrett, S.C.H. (2002). The evolution of plant sexual diversity. Nature Reviews Genetics, 3:274-284.
• Bartoli, G., Forino, L.M.C., Durante, M., Tagliasacchi, A.M. (2015). A lysigenic programmed cell death-dependent process shapes schizogenously formed aerenchyma in the stems of the waterweed Egeria densa. Annals of Botany, 116: 91-99
• Charlesworth, D., Geber, M.A., Dawson, T.E., Delph, L.F. (1999). Theories of the evolution of dioecy. In Gender and Sexual Dimorphism in Flowering Plants. Heidelberg: Springer, pp. 33-60
• Charlesworth, D., Charlesworth, B. (1978). A model for the evolution of dioecy and gynodioecy. The American Naturalist, 112: 975-997
• Cotter, T.G., Curtin, J.F. (2003). Apoptosis: Historical perspectives. In: Essays in Biochemistry. 39,1-162.
• Dellaporta, S.L., Calderon-Urrea , A. (1993). Sex determination in flowering plants. Plant Cell, 5 (10), 1241-1251.
• Diggle, P.K., Di Stilio, V.S., Gschwend, A.R., Golenberg, E.M., Moore, R.C., (2011). Multiple developmental processes underlie sex differentiation in angiosperms. Trends Genetics, 27: 368-376
• Di Stilio, V.S., Kramer ,E.M., Baum, D.A. (2005). Floral mads box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae)-a new model for the study of dioecy. The Plant Journal, 41: 755-766
• Duana, T., Xiaofang, D., Shi, C., Zhonglai, L., Zhongtao, Z., (2018). Evolution of sexual systems and growth habit in Mussaenda (Rubiaceae): Insights into the evolutionary pathways of dioecy. Molecular Phylogenetics and Evolution, 123: 113-122.
• Durand, B., Durand, R. (1991). Sex determination and reproductive organ differentiation in Mercurialis. Plant Science, 80: 49-65.
• Gorczyca, W., Bigman, K., Mittelman, A., Ahmed, T., Gong, J., (1993). Induction of DNA strand breaks associated with apoptosis during treatment of leukemias. Leukemia (Baltimore), in press
• Gunawardena, A.H.L.A.N. (2008). Programmed cell death and tissue emodelling in plants. Journal of Experimental Botany, 59: (3) 445-451
• Henry, I.M., Takashi, A., Ryutaro, T., Luca, C.1. (2018). One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants. Annual Review of Plant Biology, 69: 553-575.
• Huang, Y-T., Lowe, D.J., Churchman, G.J., Schipper, L.A., Cursons, R. (2016). DNA adsorption by nanocrystalline allophane spherules and nanoaggregates, and implications for carbon sequestration in Andisols. Applied Clay Science,120: 40-50.
• Janick, J., Stevenson, E.C. (1955). Genetics of the monoecious character in S. oleracea . Genetics, 40: 429-437
• Le Roux, L.G., Kellogg, E.A. (1999). Floral development and the formation of unisexual spikelets in the Andropogoneae (Poaceae). American Journal Botany, 86 (3): 354-366.
• Lloyd, D.G. (1982). Selection of combined versus separate sexes in seed plants. The American Naturalist, 120: 571-585
• Loo, D.T., Rillema, J.R. (1998). Measurement of cell death, in Methods in Cell Biology. (Mather J P and Barnes D, ed.), Academic Press, San Diego, CA, 57: 251-264.
• Michael, R., Robert ,L., Randall, J. M., Jeffrey, D.K. (2018). Plant Mating Systems Often Vary Widely Among Populations. Frontiers in Ecology and Evolution, 6: 38
• Nawkar, G.M., Maibam, P., Park, J.H., Sahi, V.P., Lee, S.Y. (2013). UV-Induced cell death in plants. International Journal of Molecular Sciences, 14: 1608-1628
• Naeger, J., Golenberg, E. (2016). Mode and tempo of sequence and floral evolution within the Anserineae. Plant Systematic Evolution, 302: 385-398.
• Ou, X.H., Li, S., Wang, Z.B., Li, M., Quan, S. (2012). Maternal insulin resistance causes oxidative stress and mitochondrial dysfunction in mouse oocytes. Human Reproduction, 27: 2130–2145.
• Renner, S.S. (2014). The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal Botany, 101: 1588-1596.
• Rosa, J. (1925). Sex expression in spinach. Hilgardia, 1: 259-274
• Sablowski, R. (2007). Flowering and determinacy in Arabidopsis. Journal of Experimental Botany, 58: 899-907
• Sather, D.N., York, A., Pobursky, K.J., Golenberg, E.M. (2005). Sequence evolution and sex-specific expression patterns of the C class floral identity gene,
• SpAGAMOUS, in dioecious Spinacia oleracea L. Planta, 222 (2): 284-92
• Sherry, R.A., Eckard, K.J., Lord, E.M. (1993). Flower development in dioecious Spinacia oleracea (Chenopodiaceae). American Journal Botany, 80: 283-291
• Tanurdzic, M., Banks, J.A. (2004). Sex-Determining Mechanisms in Land Plants. Plant Cell, 16: S61-S71
• Van der Vossen, H.A.M. (2004). Spinacia oleracea L. In: Grubben GJ, H, Denton OA (Eds), PROTA 2: Vegetables/Le´ gumes PROTA, Wageningen, Netherlands
• Vardar, F., Aytürk, Ö., Yanık, F. (2017). Programmed cell death evidence in wheat (Triticum aestivum L.) roots induced by aluminum oxide (Al2O3) nanoparticles. Caryologia, 70: (2), 112-119
• Wang C. L., Wu J., Xu G. H., Gao Y. B., Chen G., et. al. (2010). S-RNase disrupts tip-localized reactive oxygen species and induces nuclear DNA degradation in incompatible pollen tubes of Pyrus pyrifolia. Journal Cell Science, 123 (24): 4301–4309