Heterochronic genes in plant evolution and development

Abstract

Evolution of morphology includes evolutionary shifts of developmental processes in space or in time. Heterochronic evolution is defined as a temporal shift. The concept of heterochrony has been very rewarding to investigators of both animal and plant developmental evolution, because it has strong explanatory power when trying to understand morphological diversity. While for animals, extensive literature on heterochrony developed along with the field of evolution of development, in plants the concept has been applied less often and is less elaborately developed. Yet novel genetic findings highlight heterochrony as a developmental and evolutionary process in plants. Similar to what has been found for the worm Caenorhabditis, a heterochronic gene pathway controlling developmental timing has been elucidated in flowering plants. Two antagonistic microRNA's miR156 and miR172 target two gene families of transcription factors, SQUAMOSA PROMOTOR BINDING PROTEIN-LIKE and APETALA2-like, respectively. Here, we propose that this finding now allows the molecular investigation of cases of heterochronic evolution in plants. We illustrate this point by examining microRNA expression patterns in the Antirrhinum majus incomposita and choripetala heterochronic mutants. Some of the more beautiful putative cases of heterochronic evolution can be found outside flowering plants, but little is known about the extent of conservation of this flowering plant pathway in other land plants. We show that the expression of an APETALA2-like gene decreases with age in a fern species. This contributes to the idea that ferns share some heterochronic gene functions with flowering plants.

Keywords: APETALA2; Ceratopteris; SPL; choripetala; heterochrony; incomposita; microRNA156; microRNA172.

FIGURE 1

The annual plant as viewed by Goethe (represented by Troll).

FIGURE 2

Illustrative examples of types of heterochronic evolution. (A) Schematic overview of the different types of heterochrony. Developmental time is the time span required to reach a certain developmental stage. In normal ancestral development (a) an organism requires time span t to reach development stage x. In Paedomorphosis development is reduced. Depending on the cause three subtypes can be distinguished. Delayed onset is the cause in post-displacement (b). In neoteny (c) development rate is slowed down. In progenesis (d) the normal time span is shortened, development will stop prematurely. In Peramorphosis an extended level of development is achieved. Again, we distinguish three subtypes. In pre-displacement (e) an earlier onset will result in a prolonged time span of development or in early maturation. In acceleration (f) developmental rate is increased. Finally, in hypermorphosis (g) development is continued after normal offset. (B) Hypothetical examples of heterochrony. Figure (a) shows a reference plant with different types of plant organs. Peramorphic develop “beyond” this, while paedomorphic plants retain juvenile features. In post-displacement (b), onset is later and an additional pair of cotyledons develops, in pre-displacement (e), onset is later and no cotyledons develop. In neoteny, less organs develop with larger internodes (c), while in acceleration (f), more organs develop with shorter internodes. In progenesis (d), offset is earlier and no bract develop, while in hypermorphosis (g), offset is later and additional bracts develop. (C) Examples of heterochrony taken from the literature. See text for explanation.

FIGURE 3

APETALA2-like expression in Ceratopteris richardii developmental time series. qRT-PCR of a putative miR172 target APETALA2-like gene with a putative miR172 binding site in gametophytes and sporophyte stages of development. Error bars are standard deviation of three biological replicates.

FIGURE 4

The heterochronic Antirrhinum mutant choripetala.(A) In incomposita, prophylls develop which are absent in wild-type Antirrhinum flowers. (B) Inco also occasionally develops petaloid sepals. (C) Petaloid sepals and an unfused corolla can also be observed in choripetala. (D) The expression pattern of miR156 (left axis) and miR172 (right axis) in Antirrhinum is similar to what has been observed for wild-type Arabidopsis and other species. Both in inco (E) and in cho (F), an early increase in miR172 can be observed late in adult development and lower expression levels are present in inflorescence tissue. Error bars represent standard errors of three technical replicates. A second biological replicate gave similar results.