Ecological and phylogenetic constraints determine the stage of anthetic ovule development in orchids

Abstract

Premise Unlike most flowering plants, orchid flowers have under‐developed ovules that complete development only after pollination. Classical studies reported variation in the stage in which ovule development is arrested, but the extent of this variation and its evolutionary and ecological significance are unclear. Methods Here, we used light microscopy to observe ovule development at anthesis for 39 species not previously studied and surveyed the literature gaining information on 94 orchid species. Tropical and temperate members of all five orchid subfamilies as well as species with contrasting pollination strategies (rewarding versus deceptive) and life forms (epiphytic versus terrestrial) were represented. We analyzed the data using statistical comparisons and a phylogenetic generalized least square (PGLS) analysis. Results Apostasioideae, the sister to the rest of the orchids, have mature ovules similar to other Asparagales, while under‐differentiated ovules are present in the other subfamilies. Ovule developmental stages showed high variation even among closely related groups. Ovules were more developed in terrestrial than in epiphytic, in temperate than in tropical, and in rewarding than in deceptive pollination orchid species. This latter comparison was also significant in the PGLS analysis. Conclusions These results suggest that ovule developmental stage in orchids can be shaped by ecological factors, such as seasonality and pollination strategy, and can be selected for optimizing female reproductive investment.

Apomixis beyond trees in the Brazilian savanna: new insights from the orchid Zygopetalum mackayi

“…The other two species, Z. mackayi and Cepridium acuminatum (as Malaxis walchitii ) ( Sood and Ram 1995 ), primarily exhibits a terrestrial habit in well-drained substrates, being occasionally observed as epiphytes. Ovules in terrestrial orchid species are more advanced in development at the time of pollination compared to their epiphytic counterparts ( Mayer et al 2021 ). This may explain the prevalence of apomixis in terrestrial species of the subfamily Orchidoideae.…”

Apomixis beyond trees in the Brazilian savanna: new insights from the orchid Zygopetalum mackayi

“…Contrary to other angiosperms, the endosperm in orchid seeds is non-functional, as it is never formed or degenerates after polar nuclei fertilization (Yeung 2017). Therefore, male sexual function must be conserved in orchids not for endosperm formation, but because pollination is necessary for ovule development (Mayer et al 2021).…”

Gymnadenia winkeliana—A New Orchid Species to Romanian Flora

“…In order for their development to progress further, it has been demonstrated that their survival significantly depends on the double fertilization of the sexual embryo sac [52,64,73]. This process not only generates the zygote and the triploid nucleus (resulting in reduced endosperm, in Orchidaceae) but also triggers the developmental start of the ovule [73][74][75]. This initiation is facilitated by complex nutrient and growth signals originating from both the egg cell and sperm cells [58,65,76].…”

“…Therefore, in most facultative apomicts, the formation of the embryo sac may still require the presence of pollen on the stigma to initiate the process of embryo sac development [77]. In orchids, in general, microsporogenesis proceeds normally, and the male sexual function is maintained not only for double and triple fertilisation, but also because pollination is essential for ovule development [75,78]. The reliance on pollination for ovule and embryo development might serve as an additional, yet underexplored, constraint influencing the scarcity of apomixis in orchids, which is a relatively rare phenomenon in the family [65,79].…”