Partial redundancy and functional specialization of E-class SEPALLATA genes in an early-diverging eudicot

Abstract

Plant MADS-box genes have duplicated extensively, allegedly contributing to the immense diversity of floral form in angiosperms. In Arabidopsis thaliana (a core eudicot model plant), four SEPALLATA (SEP) genes comprise the E-class from the extended ABCE model of flower development. They are redundantly involved in the development of the four types of floral organs (sepals, petals, stamens and carpels) and in floral meristem determinacy. E-class genes have been examined in other core eudicots and monocots, but have been less investigated in non-core eudicots. Our goal was to functionally characterize the E-class genes in the early-diverging eudicot Thalictrum thalictroides (Ranunculaceae), whose flowers are apetalous. We identified four SEP orthologs, which when placed in a phylogenetic context, resulted from a major gene duplication event before the origin of angiosperms and a subsequent duplication at the origin of the Ranunculales. We used Virus-Induced Gene Silencing (VIGS) to down-regulate the three expressed paralogs individually and in combination to investigate their function and to determine the degree of conservation versus divergence of this important plant transcription factor. All loci were partially redundant in sepal and stamen identity and in promoting petaloidy of sepals, yet the SEP3 ortholog had a more pronounced role in carpel identity and development. The two other paralogs appear to have subfunctionalized in their cadastral roles to keep the boundaries between either sepal and stamen zones or stamen and carpel zones. Double knockdowns had enhanced phenotypes and the triple knockdown had an even more severe phenotype that included partial to complete homeotic conversion of stamens and carpels to sepaloid organs and green sepals, highlighting a role of E-class genes in petaloidy of sepals in this species. While no floral meristem determinacy defects were observed, this could be due to residual amounts of gene expression in the VIGS experiments being sufficient to perform this function or to the masking role of a redundant gene.

Identification of novel seed longevity genes related to oxidative stress and seed coat by genome‐wide association studies and reverse genetics

“…They interact with other MAD-box proteins to determine flowering and ovule development (Favaro et al, 2003;Hugouvieux et al, 2018). They are not completely redundant as they differ in DNA-binding patterns (Jetha, Theißen, & Melzer, 2014;Soza, Snelson, Hewett Hazelton, & Di Stilio, 2016).…”

A renaissance in plant development

“…If selection acts against a set of pleiotropic effects, evolution will be limited by gene duplication allowing for subfunctionalization or neofunctionalization to bypass the constraint. Soza et al (Soza et al, 2016) describe such a scenario for SEPALLATA genes in an earlydiverging eudicot without petals, Thalictrum (Ranunculaceae). These genes resulted from gene duplication events before the angiosperm diversification and before the origin of Ranunculales.…”

Facilitating candidate gene discovery in an emerging model plant lineage: Transcriptomic and genomic resources forThalictrum(Ranunculaceae)

“…Thalictrum is a temperate genus of circa 200 species with floral diversity that encompasses unisexual and wind-pollinated flowers, in association with polyploidy (Soza et al, 2012(Soza et al, , 2013. Certain species, mainly T. thalictroides, are amenable to virus-induced gene silencing (Di Stilio et al, 2010), which has enabled functional studies of ABC model floral MADS-box genes (Di Galimba and Di Stilio, 2015;Galimba et al, 2012Galimba et al, , 2018Soza et al, 2016). Two chloroplast genomes have been assembled to date for the genus, for T. coreanum (Park et al, 2015) and T. thalictroides (from this dataset, Morales Briones et al, 2019).…”