Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication.

Li-Jia Qu,Keiko Sakakibara,John L Bowman,Chihiro Furumizu,John Paul Alvarez

doi:10.1371/journal.pgen.1004980

Li-Jia Qu, Keiko Sakakibara + Show 3 more

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https://doi.org/10.1371/journal.pgen.1004980

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Abstract

Neofunctionalization following gene duplication is thought to be one of the key drivers in generating evolutionary novelty. A gene duplication in a common ancestor of land plants produced two classes of KNOTTED-like TALE homeobox genes, class I (KNOX1) and class II (KNOX2). KNOX1 genes are linked to tissue proliferation and maintenance of meristematic potentials of flowering plant and moss sporophytes, and modulation of KNOX1 activity is implicated in contributing to leaf shape diversity of flowering plants. While KNOX2 function has been shown to repress the gametophytic (haploid) developmental program during moss sporophyte (diploid) development, little is known about KNOX2 function in flowering plants, hindering syntheses regarding the relationship between two classes of KNOX genes in the context of land plant evolution. Arabidopsis plants harboring loss-of-function KNOX2 alleles exhibit impaired differentiation of all aerial organs and have highly complex leaves, phenocopying gain-of-function KNOX1 alleles. Conversely, gain-of-function KNOX2 alleles in conjunction with a presumptive heterodimeric BELL TALE homeobox partner suppressed SAM activity in Arabidopsis and reduced leaf complexity in the Arabidopsis relative Cardamine hirsuta, reminiscent of loss-of-function KNOX1 alleles. Little evidence was found indicative of epistasis or mutual repression between KNOX1 and KNOX2 genes. KNOX proteins heterodimerize with BELL TALE homeobox proteins to form functional complexes, and contrary to earlier reports based on in vitro and heterologous expression, we find high selectivity between KNOX and BELL partners in vivo. Thus, KNOX2 genes confer opposing activities rather than redundant roles with KNOX1 genes, and together they act to direct the development of all above-ground organs of the Arabidopsis sporophyte. We infer that following the KNOX1/KNOX2 gene duplication in an ancestor of land plants, neofunctionalization led to evolution of antagonistic biochemical activity thereby facilitating the evolution of more complex sporophyte transcriptional networks, providing plasticity for the morphological evolution of land plant body plans.

Highlights

Gene duplication is thought to be one of the key drivers in generating evolutionary novelty
We show that the two subclasses resulting from the gene duplication event act to pattern, in a complementary manner, most above ground organs of the diploid stage of the flowering plant Arabidopsis
As phylogenetic analyses place KNAT7 in a clade sister to the remaining Arabidopsis KNOX2 genes [9], we focused on KNAT3 (AT5G25220), KNAT4 (AT5G11060), and KNAT5 (AT4G32040) genes in this study (Fig. 1B, S1 and S2 Figs.)

Summary

Introduction

Gene duplication is thought to be one of the key drivers in generating evolutionary novelty. Paralogs can undergo a process of neofunctionalization, supplying a genetic basis for morphological novelty [1,2,3]. Transcription factors can undergo neofunctionalization via either a change in expression pattern or an alteration in functionality, e.g. the derivation of a repressor or inhibitor from an ancestral activator, or vice versa Three amino acid loop extension (TALE) homeodomain transcriptional factors, characterized by having a homeodomain that has three extra amino acids between helices 1 and 2, are found in all eukaryotic lineages [5,6,7]. KNOX genes of flowering plants have been studied for over two decades, the functional consequences of the KNOX gene duplication have been largely unexplored

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