Research Article: Major-Effect Alleles at Relatively Few Loci Underlie Distinct Vernalization and Flowering Variation in Arabidopsis Accessions

Date Published: May 20, 2011

Publisher: Public Library of Science

Author(s): Amy Strange, Peijin Li, Clare Lister, Jillian Anderson, Norman Warthmann, Chikako Shindo, Judith Irwin, Magnus Nordborg, Caroline Dean, Miltos Tsiantis.

Abstract: We have explored the genetic basis of variation in vernalization requirement and
response in Arabidopsis accessions, selected on the basis of their phenotypic
distinctiveness. Phenotyping of F2 populations in different environments, plus
fine mapping, indicated possible causative genes. Our data support the
identification of FRI and FLC as candidates
for the major-effect QTL underlying variation in vernalization response, and
identify a weak FLC allele, caused by a Mutator-like
transposon, contributing to flowering time variation in two N. American
accessions. They also reveal a number of additional QTL that contribute to
flowering time variation after saturating vernalization. One of these was the
result of expression variation at the FT locus. Overall, our
data suggest that distinct phenotypic variation in the vernalization and
flowering response of Arabidopsis accessions is accounted for by variation that
has arisen independently at relatively few major-effect loci.

Partial Text: An important debate in evolutionary biology is the influence of few major-effect
versus many minor-effect changes in the adaptation of organisms to different
environments [1]. An
important adaptive trait in plants is the timing of flowering. This significantly
influences their fitness and so is tightly regulated, however, variation in this
trait is required to enable plants to adapt to different environmental conditions.
The regulatory network and molecular mechanisms mediating the impact of
environmental cues on the timing of the floral transition have been extensively
studied in Arabidopsis [2]. The data so far point to an integrated network of
pathways that converge on a set of common targets to quantitatively regulate genes
required to switch the vegetative apical meristem to a floral fate [2]. The natural
variation in Arabidopsis flowering is extensive and several loci have been
identified which contribute to this variation: FRIGIDA (FRI),
LOCUS T (FT) [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13], [14], [15]. We have focused on
vernalization, the acceleration of flowering by a prolonged period of cold, namely
winter. Different Arabidopsis accessions show variation in the length of cold
required to satisfy the vernalization requirement and this correlates with the
ability to epigenetically silence FLC[6]. Initial
analysis of four F2 populations mapped the QTL contributing to the variation in
FLC epigenetic silencing to broad genomic regions and concluded
that, unexpectedly, none of them corresponded to the trans-factors
currently known to regulate vernalization [10]. Further analysis was therefore
required to identify the genes involved.

Arabidopsis accessions provide an excellent resource in which to explore the
molecular basis of natural variation. We have been studying variation in flowering
time and vernalization response between Arabidopsis accessions to address how
Arabidopsis has adapted to growth in varying climates. In a previous study we
undertook a preliminary QTL analysis on populations derived from four winter annual
types, with very different vernalization responses crossed to the rapid cycler,
Columbia. We established that the variation in vernalization response did not appear
to map to any of the trans-factors currently known to mediate
vernalization. Unexpectedly, despite the varying phenotypes of the parents most of
the QTL mapped to very similar locations in the different populations. In this study
we specifically aimed to further define these QTL by additional phenotypic analysis
of the populations, both without vernalization and with longer, saturating, periods
of vernalization. We also extended the analysis to include two N. American
Arabidopsis accessions that showed interesting variation in flowering and
FLC levels [6]. Our data indicate that just a few major QTL account for a
large proportion of the flowering time variation in the six accessions analysed. The
map positions of these QTL and their response to different vernalization periods
suggest they may be caused by common loci. Smaller-effect QTL were also revealed
particularly after saturating vernalization, which is consistent with a recent
report based on genome wide association analysis of flowering time in natural
accessions [40].