Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait - PubMed (original) (raw)

Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait

Ana L Caicedo et al. Proc Natl Acad Sci U S A. 2004.

Abstract

Epistatic gene interactions are believed to be a major factor in the genetic architecture of evolutionary diversification. In Arabidopsis thaliana, the FRI and FLC genes mechanistically interact to control flowering time, and here we show that this epistatic interaction also contributes to a latitudinal cline in this life history trait within the species. Two major FLC haplogroups (FLC(A) and FLC(B)) are associated with flowering time variation in A. thaliana in field conditions, but only in the presence of putatively functional FRI alleles. Significant differences in latitudinal distribution of FLC haplogroups in Eurasia and North Africa also depend on the FRI genotype. There is significant linkage disequilibrium between FRI and FLC despite their location on separate chromosomes. Although no nonsynonymous polymorphisms differentiate FLC(A) and FLC(B), vernalization induces the expression of an alternatively spliced FLC transcript that encodes a variant protein with a radical amino acid replacement associated with the two FLC haplogroups. Numerous polymorphisms differentiating the FLC haplogroups also occur in intronic regions implicated in the regulation of FLC expression. The features of the regulatory gene interaction between FRI and FLC in contributing to the latitudinal cline in A. thaliana flowering time are consistent with the maintenance of this interaction by epistatic selection. These results suggest that developmental genetic pathways and networks provide the molecular basis for epistasis, contributing to ecologically important phenotypic variation in natural populations and to the process of evolutionary diversification.

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Figures

Fig. 1.

Schematic representation of genetic pathways of flowering time in A. thaliana. Lines with arrows denote up-regulation of gene expression; lines with bars denote repression of gene expression.

Fig. 2.

Polymorphisms observed in the sequenced FLC region. Site numbering is based on our alignment and includes indels. Polymorphisms in mononucleotide repeats longer than 4-bp and long dinucleotide repeats are not included. Positions highlighted in gray, along with the Da (1)-12 type insert (not shown), were used in genotyping.

Fig. 3.

FLC haplotype network. The tree represents one of four mostparsimonious arrangements; relationships among major haplotype groups do not change with alternative trees. Each line represents a single mutational step corresponding to a SNP or an indel. Mutations marked with lower-case letters are homoplasious. Characters 1919 and 7207, which are highly homoplasious (consistency index ≤ 0.333), were excluded from the tree. Shaded boxes indicate haplogroups. Haplogroup and haplotype frequencies are based on genotyping 353 A. thaliana accessions.

Fig. 4.

Associations between FRI FLC genotype and flowering time. Bars that differ in roman numerals are significantly different at P < 0.006 by Fisher's protected least-significant difference test. Error bars indicate standard error. (A) Short-day growth chamber conditions. (B) Long-day growth chamber conditions. (C and D) Vernalized over-wintering field conditions.

Fig. 5.

Alternative splicing at FLC. (A) RT-PCR of FLC under different treatments. Plants at V0 were collected soon after germination and were not subjected to vernalization. Plants at V15 were grown at 4°C for 15 days after germination. (B) Structure of the alternative-splice FLC transcript. The upper gene model encompasses the region sequenced for FLC. White boxes represent UTRs, black boxes represent exon regions, and lines represent introns and promoter regions. Slender bars indicate splice sites of the alternative FLC product. The lower gene model represents the alternative transcript after splicing has occurred. (C) Predicted protein of the FLC alternative splice transcript, indicating the amino acid replacement polymorphism between the FLCA and FLCB haplogroups.

References

1. Fenster, C. B., Galloway, L. F. & Chao, L. (1997) Trends Ecol. Evol. 12, 282-286. - PubMed
1. Wade, M. J., Winther, R. G., Agrawal, A. F. & Goodnight, C. J. (2001) Trends Ecol. Evol. 16, 498-504.
1. Fisher, R. A. (1930) The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford).
1. Wright, S. (1931) Genetics 16, 97-159. - PMC - PubMed
1. Weinig, C., Dorn, L. A., Kane, N. C., German, Z. M., Halldorsdottir, S. S., Ungerer, M. C., Toyonaga, Y., Mackay, T. F., Purugganan, M. D. & Schmitt, J. (2003) Genetics 165, 321-329. - PMC - PubMed

Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait - PubMed (original) (raw)