The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background

Abstract

The timing of flowering initiation is a fundamental trait for the adaptation of annual plants to different environments. Large amounts of intraspecific quantitative variation have been described for it among natural accessions of many species, but the molecular and evolutionary mechanisms underlying this genetic variation are mainly being determined in the model plant Arabidopsis thaliana. To find novel A. thaliana flowering QTL, we developed introgression lines from the Japanese accession Fuk, which was selected based on the substantial transgression observed in an F2 population with the reference strain Ler. Analysis of an early flowering line carrying a single Fuk introgression identified Flowering Arabidopsis QTL1 (FAQ1). We fine-mapped FAQ1 in an 11 kb genomic region containing the MADS transcription factor gene SHORT VEGETATIVE PHASE (SVP). Complementation of the early flowering phenotype of FAQ1-Fuk with a SVP-Ler transgen demonstrated that FAQ1 is SVP. We further proved by directed mutagenesis and transgenesis that a single amino acid substitution in SVP causes the loss-of-function and early flowering of Fuk allele. Analysis of a worldwide collection of accessions detected FAQ1/SVP-Fuk allele only in Asia, with the highest frequency appearing in Japan, where we could also detect a potential ancestral genotype of FAQ1/SVP-Fuk. In addition, we evaluated allelic and epistatic interactions of SVP natural alleles by analysing more than one hundred transgenic lines carrying Ler or Fuk SVP alleles in five genetic backgrounds. Quantitative analyses of these lines showed that FAQ1/SVP effects vary from large to small depending on the genetic background. These results support that the flowering repressor SVP has been recently selected in A. thaliana as a target for early flowering, and evidence the relevance of genetic interactions for the intraspecific evolution of FAQ1/SVP and flowering time. © 2013 Méndez-Vigo et al.

[Author Summary] In many plant species, the timing of flowering initiation shows abundant quantitative variation among natural varieties, which reflects the importance of this trait for adaptation to different environments. Currently, a major goal in plant biology is to determine the molecular and evolutionary bases of this natural genetic variation. In this study we demonstrate that the central flowering regulator SHORT VEGETATIVE PHASE (SVP), encoding a MADS transcription factor, is involved in the flowering natural variation of the model organism Arabidopsis thaliana. In particular, we prove that a structural change caused by a single amino acid substitution generates a SVP early flowering allele that is distributed only in Asia. Furthermore, genetic interactions have been shown to be a component of the natural variation for many important adaptive traits. However, very few studies, either in animals or plants, have systematically addressed the extent of genetic interactions among specific alleles responsible for the natural variation of complex traits. Our study shows that the flowering effects of SVP natural alleles depend significantly on the genetic background; and, subsequently, we demonstrate the relevance of epistasis for the evolution of this crucial transcription factor and flowering time.