The evolution of gene regulatory networks controlling Arabidopsis thaliana L. trichome development

Alexey V Doroshkov,Dmitrii K Konstantinov,Dmitrii K Konstantinov,Dmitrij A Afonnikov,Dmitrii K Konstantinov,Konstantin V Gunbin,Konstantin V Gunbin,Konstantin V Gunbin,Konstantin V Gunbin

doi:10.1186/s12870-019-1640-2

Abstract

BackgroundThe variation in structure and function of gene regulatory networks (GRNs) participating in organisms development is a key for understanding species-specific evolutionary strategies. Even the tiniest modification of developmental GRN might result in a substantial change of a complex morphogenetic pattern. Great variety of trichomes and their accessibility makes them a useful model for studying the molecular processes of cell fate determination, cell cycle control and cellular morphogenesis. Nowadays, a large number of genes regulating the morphogenesis of A. thaliana trichomes are described. Here we aimed at a study the evolution of the GRN defining the trichome formation, and evaluation its importance in other developmental processes.ResultsIn study of the evolution of trichomes formation GRN we combined classical phylogenetic analysis with information on the GRN topology and composition in major plants taxa. This approach allowed us to estimate both times of evolutionary emergence of the GRN components which are mainly proteins, and the relative rate of their molecular evolution. Various simplifications of protein structure (based on the position of amino acid residues in protein globula, secondary structure type, and structural disorder) allowed us to demonstrate the evolutionary associations between changes in protein globules and speciations/duplications events. We discussed their potential involvement in protein-protein interactions and GRN function.ConclusionsWe hypothesize that the divergence and/or the specialization of the trichome-forming GRN is linked to the emergence of plant taxa. Information about the structural targets of the protein evolution in the GRN may predict switching points in gene networks functioning in course of evolution. We also propose a list of candidate genes responsible for the development of trichomes in a wide range of plant species.

Highlights

The variation in structure and function of gene regulatory networks (GRNs) participating in organisms development is a key for understanding species-specific evolutionary strategies
The central role in determining the cellular fate of cells with trichomes is played by the assembly of the trichome initiation MBW complex - (GL3/EGL3-GL1-TTG1), which initiates the expression of the gene GLABRA2 (GL2) encoding a transcription factor to initiate the cell transition to Doroshkov et al BMC Plant Biology 2019, 19(Suppl 1):53 differentiation into trichomes [5]
In addition to GL2, the MBW complex induces the expression of repressor genes (TRY/CPC), which can move between the cells and assemble into a complex (GL3/EGL3-CPC/TRY-TTG1) that is unable to initiate trichome formation

Summary

Introduction

The variation in structure and function of gene regulatory networks (GRNs) participating in organisms development is a key for understanding species-specific evolutionary strategies. To understand the processes of development and evolution of living organisms, the “gene regulatory networks”, or GRNs have to be taken into account The variability of such networks determines the diversity of organ forms and functions in plants and animals [1, 2]. Specialized trichome cells are useful as a model for studying the molecular processes of cell fate determination, cell cycle control and cellular morphogenesis [3] This model was instrumental in dissecting the mechanisms of epidermal morphogenesis in the model plant Arabidopsis thaliana L [4]. It is to be noted that the pattern of trichome formation is described by the widespread mechanism of lateral inhibition, which is known to exist in various plant and animal organisms It is responsible for the cyanobacterial heterocyst development [17, 18]

Methods

Results

Conclusion