Evolution of major fowering pathway integrators in Orchidaceae

Abstract

ABSTRACT: The Orchidaceae is a mega-diverse plant family with ca. 29,000 species with a large variety of life forms that can colonize transitory habitats. Despite this diversity, little is known about their fowering integrators in response to specifc environmental factors. During the reproductive transition in fowering plants a vegetative apical meristem (SAM) transforms into an inforescence meristem (IM) that forms bracts and fowers. In model grasses, like rice, a fowering genetic regulatory network (FGRN) controlling reproductive transitions has been identifed, but little is known in the Orchidaceae. In order to analyze the players of the FRGN in orchids, we performed comprehensive phylogenetic analyses of CONSTANS-like/CONSTANS- like 4 (COL/COL4), FLOWERING LOCUS D (FD), FLOWERING LOCUS C/FRUITFULL (FLC/FUL) and SUPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) gene lineages. In addition to PEBP and AGL24/SVP genes previously analyzed, here we identify an increase of orchid homologs belonging to COL4, and FUL gene lineages in comparison with other monocots, including grasses, due to orchid-specifc gene lineage duplications. Contrariwise, local duplications in Orchidaceae are less frequent in the COL, FD and SOC1 gene lineages, which points to a retention of key functions under strong purifying selection in essential signaling factors. We also identifed changes in the protein sequences after such duplications, variation in the evolutionary rates of resulting paralogous clades and targeted expression of isolated homologs in diferent orchids. Interestingly, vernalization-response genes like VERNALIZATION1 (VRN1) and FLOWERING LOCUS C (FLC) are completely lacking in orchids, or alternatively are reduced in number, as is the case of VERNALIZATION2/GHD7 (VRN2). Our fndings point to non-canonical factors sensing temperature changes in orchids during reproductive transition. Expression data of key factors gathered from Elleanthus auratiacus, a terrestrial orchid in high Andean mountains allow us to characterize which copies are actually active during fowering. Altogether, our data lays down a comprehensive framework to assess gene function of a restricted number of homologs identifed more likely playing key roles during the fowering transition, and the changes of the FGRN in neotropical orchids in comparison with temperate grasses.