Transcriptomic heterochrony and completely cleistogamous flower development in the mycoheterotrophic orchid Gastrodia

Abstract

Cleistogamy, in which plants can reproduce via self-fertilization within permanently closed flowers, has evolved in > 30 angiosperm lineages; however, consistent with Darwin's doubts about its existence, complete cleistogamythe production of only cleistogamous flowershas rarely been recognized. Thus far, the achlorophyllous orchid genus, Gastrodia, is the only known genus with several plausible completely cleistogamous species.Here, we analyzed the floral developmental transcriptomes of two recently evolved, completely cleistogamous Gastrodia species and their chasmogamous sister species to elucidate the possible changes involved in producing common cleistogamous traits.The ABBA-BABA test did not support introgression and protein sequence convergence as evolutionary mechanisms leading to cleistogamy, leaving convergence in gene expression as a plausible mechanism. Regarding transcriptomic differentiation, the two cleistogamous species had common modifications in the expression of developmental regulators, exhibiting a gene family-wide signature of convergent expression changes in MADS-box genes. Our transcriptomic pseudotime analysis revealed a prolonged juvenile state and eventual maturation, a heterochronic pattern consistent with partial neoteny, in cleistogamous flower development.These findings indicate that transcriptomic partial neoteny, arising from changes in the expression of conserved developmental regulators, might have contributed to the rapid and repeated evolution of cleistogamous flowers in Gastrodia.

Gastrodia bawanglingensis (Orchidaceae, Epidendroideae), a new species from Hainan Island, China

“…We also found several other unpublished species that are different but very similar to G. bawanglingensis in our field survey in Hainan Island, which also confirms the above point of view. It is also notable that although lack of rostellum often facilitates selfing in the genus ( Suetsugu 2022 ; Suetsugu et al 2022 ), the new species has somewhat well-developed rostellum. Further observations are needed on how the species accomplishes autogamy.…”

“… Gastrodia is probably the only genus that contains species with completely cleistogamous flowers as confirmed by intensive monitoring. Self-pollination might be an adaptation to ensure reproduction, compensating for the defi- ciency of pollinators in the habitat ( Suetsugu 2022 ; Suetsugu et al 2022 ). Currently, complete cleistogamy has been reported in five Gastrodia species: G. clausa , G. takeshimensis , G. flexistyloides , G. kuroshimensis and G. amamiana ( Hsu et al 2012 ; Suetsugu 2013 , 2014 , 2016 , 2019 ), G. bawanglingensis is likely to be the sixth species reported.…”

Morphological, ecological, and molecular phylogenetic approaches reveal species boundaries and evolutionary history of Goodyera crassifolia (Orchidaceae, Orchidoideae) and its closely related taxa

“…We observed an association between the column and lip or rostellum shape; the lip and the rostellum appeared to be three-lobed when the lateral appendages are conspicuous (Figs 2E, F , 3E, F , 4G, H , 5E, G ). Given that the floral organ formation is explained mainly by the combined expression of ABCE-class MADS-box transcription factors ( Causier et al 2010 ; Hsu et al 2015 , 2021 ; Suetsugu et al 2022 ), the spatial expression of the factors underlying this distinctive morphology deserves further investigation. In particular, the enlarged staminodes indicate that G. crassifolia exhibits some radial symmetry, unlike most orchid flowers, which are typically zygomorphic.…”

Resurrection and emended description of Gastrodia foetida (Orchidaceae)

“…This notion is also based on the biological species concept, which defines a species as members of populations potentially interbreeding in nature because the completely cleistogamous status of G. takeshimensis blocks gene flow with its sympatric species G. foetida (Suetsugu 2022;Suetsugu et al 2023). Notably, G. foetida and G. nipponica are also reproductively isolated by their disjunct distribution (Fig.…”

“…1B). Intriguingly, several new taxa within the G. nipponica species complex have been described in recent years (Hsu & Kuo 2010;Suetsugu 2013Suetsugu , 2014Suetsugu , 2016Suetsugu , 2017Suetsugu , 2021, and the G. nipponica species complex is now recognized as an ideal model for understanding speciation and diversification of mycoheterotrophic plants (Kishikawa et al 2019;Ogaki et al 2019;Suetsugu 2022;Suetsugu et al 2023). Therefore, although a relatively long, narrow perianth tube (ca.…”