Abstract
BackgroundUnderstanding 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.ResultsBy 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.ConclusionsOur 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
Highlights
Understanding the relationship between macroevolutionary diversity and variation in organism development is an important goal of evolutionary biology
We propose that the evolution of large flowers with an unexpanded petal base in hummingbird-pollinated Loasoideae species resulted from delayed development of basipetal cell wall lobeyness (Fig. 2)
Cell geometry and cell number in petals of L. heterophylla and C. hibiscifolia Triple interaction terms between PAMR developmental stage and species were significant in the regressions describing the patterning of Cell lobeyness (CL), log(CA) and cell length-to-width ratio (CLWR) along the petal midrib (t = 3.806, P < 0.0005; t = 3.347, P < 0.0005; t = 3.685, P < 0.0005 for interaction with the linear term; t = − 3.365, P < 0.0005; t = − 4.048, P < 0.0001; t = − 2.880, P < 0.005 for interaction with the quadratic term)
Summary
Understanding the relationship between macroevolutionary diversity and variation in organism development is an important goal of evolutionary biology. We 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. Heterochronic variation in the observable morphology of organisms is generated by alteration of developmental trajectories involving shifts in the timing of somatic differentiation relative to the timing of reproductive maturity [1] This could result either in ‘overdeveloped’ somatic morphologies, i.e., peramorphosis, or in ‘underdeveloped’ somatic morphologies, i.e., pedomorphosis in the descendant lineage [3]. Reproductive maturity can, be defined at the whole plant level, e.g., inflorescence initiation, and for separate plant reproductive modules, e.g., anther dehiscence and stigma receptivity in a flower
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