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Review
. 2018 Sep 18:9:1349.
doi: 10.3389/fpls.2018.01349. eCollection 2018.

The Times They Are A-Changin': Heterochrony in Plant Development and Evolution

Affiliations
Review

The Times They Are A-Changin': Heterochrony in Plant Development and Evolution

Manuel Buendía-Monreal et al. Front Plant Sci. .

Abstract

Alterations in the timing of developmental programs during evolution, that lead to changes in the shape, or size of organs, are known as heterochrony. Heterochrony has been widely studied in animals, but has often been neglected in plants. During plant evolution, heterochronic shifts have played a key role in the origin and diversification of leaves, roots, flowers, and fruits. Heterochrony that results in a juvenile or simpler outcome is known as paedomorphosis, while an adult or more complex outcome is called peramorphosis. Mechanisms that alter developmental timing at the cellular level affect cell proliferation or differentiation, while those acting at the tissue or organismal level change endogenous aging pathways, morphogen signaling, and metabolism. We believe that wider consideration of heterochrony in the context of evolution will contribute to a better understanding of plant development.

Keywords: cell cycle; developmental timing; heterochrony; miR156; plant development; plant evolution.

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Figures

FIGURE 1
FIGURE 1
Types of heterochrony. (A) Schematic representation of the 6 types of heterochrony. The black line represents the time required to reach a certain developmental stage in the ancestral ontogeny. Blue lines show the 3 types of paedomorphosis: progenesis (precocious offset), post-displacement (delayed onset) and neoteny (slower developmental rate). Red lines show the 3 types of peramorphosis: hypermorphosis (delayed offset), pre-displacement (precocious onset), and acceleration (higher developmental rate). Drawing in (A) is based on Alberch et al. (1979) and Geuten and Coenen (2013). (B) Heterochrony scenarios for embryogenesis. Arabidopsis embryogenesis is taken here as the hypothetical ancestral development, divided in four stages for illustrative purposes. A fifth stage, where the embryo has produced the first two leaves plus the two cotyledons (denoted embryonic seedling), is proposed as the final stage in peramorphic embryogenesis, whereas paedomorphic embryogenesis is expected to conclude at the heart stage. (C) Heterochrony scenarios for vegetative development. In this case, Arabidopsis vegetative development, where the plant continues producing cauline/reproductive leaves on the stem before flowering (drawn on the top), represents a hypothetical case of peramorphic vegetative development, compared to a hypothetical ancestor which flowers at the adult stage without producing cauline leaves. Paedomorphic vegetative development is predicted to result in plants flowering at the juvenile stage.
FIGURE 2
FIGURE 2
Mechanisms driving heterochrony in plants. (A) Cellular heterochrony. The sequence of rosette leaves produced during vegetative development is shown. The phenotype of Arabidopsis Columbia wild type plants is taken as a hypothetical ancestral state; a paedomorphic scenario (neoteny) and a peramorphic scenario (acceleration) are also shown. Arrows represent the direction of the wave of the cell division arrest in a basipetal gradient, where cells below the dotted line are still actively dividing whereas the cells above are expanding and/or differentiating. (B) Transcriptional and metabolic heterochrony. A graphic representation of the predicted abundance of the microRNA miR156/7 and its targets, the SPL genes, as well as sugar abundance along the time of vegetative development, corresponding to the phenotypes in (A). Dotted lines represent the threshold of miR156/7 and SPL abundance which leads to juvenility (above the threshold) or adulthood (below the threshold). In this case, a delay in the repression of miR156 and activation of SPL expression and sugar production results in paedomorphosis, whereas a precocious decay of miR156 and early activation of SPL expression and sugar production results in peramorphosis. These drawings are simplified representations, and do not reflect the exact abundances in nature. The actual pattern of miR156/SPL abundance is closer to that depicted for “peramorphosis” state.

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