Changes in cis-regulatory elements of a key floral regulator are associated with divergence of inflorescence architectures

Abstract

Higher plant species diverged extensively with regard to the moment (flowering time) and position (inflorescence architecture) at which flowers are formed. This seems largely caused by variation in the expression patterns of conserved genes that specify floral meristem identity (FMI), rather than changes in the encoded proteins. Here, we report a functional comparison of the promoters of homologous FMI genes from Arabidopsis, petunia, tomato and Antirrhinum. Analysis of promoter-reporter constructs in petunia and Arabidopsis, as well as complementation experiments, showed that the divergent expression of LEAFY (LFY) and the petunia homolog ABERRANT LEAF AND FLOWER (ALF) results from alterations in the upstream regulatory network rather than cis-regulatory changes. The divergent expression of UNUSUAL FLORAL ORGANS (UFO) from Arabidopsis, and the petunia homolog DOUBLE TOP (DOT), however, is caused by the loss or gain of cis-regulatory promoter elements, which respond to trans-acting factors that are expressed in similar patterns in both species. Introduction of pUFO:UFO causes no obvious defects in Arabidopsis, but in petunia it causes the precocious and ectopic formation of flowers. This provides an example of how a change in a cis-regulatory region can account for a change in the plant body plan.

The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation

“…S16), suggesting a complex interaction between cis-and trans-regulatory factors are required to explain the evolutionary shift from single-flowered tobacco to multiflowered tomato. This is perhaps not surprising given the amount of heterochronic changes in expression observed in our analyses, as well as numerous other documented variation in gene regulatory sequences that affect shoot architecture diversity across flowering plants (Studer et al 2011;Meyer and Purugganan 2013;Kusters et al 2015;Xu et al 2015).…”

Petunia, Your Next Supermodel?

“…Even though the end result of a biological process might be very similar in different species, the underlying regulatory gene networks may have diverged more than generally thought. Some very clear examples of network divergence between Arabidopsis and petunia can be found in the mechanisms that pattern homeotic gene expression in the flower ( Cartolano et al, 2007 ), and in the regulation of floral meristem identity genes ( Kusters et al, 2015 ). Thus, even if clear orthologs for all individual components of a regulatory gene network identified in one species can be found back in another species, it does not guarantee that a similar network architecture will control the same biological process in the two species.…”

Conservation vs divergence in LEAFY and APETALA1 functions between Arabidopsis thaliana and Cardamine hirsuta

“…LFY interacts with the F-box protein UNUSUAL FLORAL ORGANS (UFO) in A. thaliana and this interaction is conserved among orthologues of these proteins in different flowering plants Chae et al, 2008;Souer et al, 2008). However, divergence in the spatiotemporal expression of these two genes played a major role in determining the various inflorescence architectures found in different species (Hake, 2008;McKim & Hay, 2010;Moyroud et al, 2010;Park et al, 2014;Kusters et al, 2015). For example, A. thaliana and A. majus have a raceme architecture with lateral flowers, and LFY/FLO expression is the limiting factor for acquisition of floral fate in these flowers (Coen et al, 1990;Bl azquez et al, 1997).…”