Delayed differentiation of epidermal cells walls can underlie pedomorphosis in plants: the case of pedomorphic petals in the hummingbird-pollinated Caiophora hibiscifolia (Loasaceae, subfam. Loasoideae) species

Abstract

Background: Understanding the relationship between macroevolutionary diversity and variation in organism development is an important goal of evolutionary biology. Variation in the morphology of several plant and animal lineages is attributed to pedomorphosis, a case of heterochrony, where an ancestral juvenile shape is retained in an adult descendant. Pedomorphosis facilitated morphological adaptation in different plant lineages, but its cellular and molecular basis needs further exploration. Plant development differs from animal development in that cells are enclosed by cell walls and do not migrate. Moreover, in many plant lineages, the differentiated epidermis of leaves, and leaf-derived structures, such as petals, limits organ growth. We, therefore, proposed that pedomorphosis in leaves, and in leaf-derived structures, results from delayed differentiation of epidermal cells with respect to reproductive maturity. This idea was explored for petal evolution, given the importance of corolla morphology for angiosperm reproductive success. Results: By comparing cell morphology and transcriptional profiles between 5 mm flower buds and mature flowers of an entomophile and an ornitophile Loasoideae species (a lineage that experienced transitions from bee- to hummingbird-pollination), we show that evolution of pedomorphic petals of the ornithophile species likely involved delayed differentiation of epidermal cells with respect to flower maturity. We also found that developmental mechanisms other than pedomorphosis might have contributed to evolution of corolla morphology. Conclusions: Our results highlight a need for considering alternatives to the flower-centric perspective when studying the origin of variation in flower morphology, as this can be generated by developmental processes that are also shared with leaves. Graphical Abstract: [Figure not available: see fulltext.]