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

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          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.

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          Most cited references49

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          FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.

          Winter-annual ecotypes of Arabidopsis are relatively late flowering, unless the flowering of these ecotypes is promoted by exposure to cold (vernalization). This vernalization-suppressible, late-flowering phenotype results from the presence of dominant, late-flowering alleles at two loci, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC). In this study, we report that flc null mutations result in early flowering, demonstrating that the role of active FLC alleles is to repress flowering. FLC was isolated by positional cloning and found to encode a novel MADS domain protein. The levels of FLC mRNA are regulated positively by FRI and negatively by LUMINIDEPENDENS. FLC is also negatively regulated by vernalization. Overexpression of FLC from a heterologous promoter is sufficient to delay flowering in the absence of an active FRI allele. We propose that the level of FLC activity acts through a rheostat-like mechanism to control flowering time in Arabidopsis and that modulation of FLC expression is a component of the vernalization response.
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            Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.

            Vernalization, the acceleration of flowering by a long period of cold temperature, ensures that many plants overwinter vegetatively and flower in spring. In Arabidopsis, allelic variation at the FRIGIDA (FRI) locus is a major determinant of natural variation in flowering time. Dominant alleles of FRI confer late flowering, which is reversed to earliness by vernalization. We cloned FRI and analyzed the molecular basis of the allelic variation. Most of the early-flowering ecotypes analyzed carry FRI alleles containing one of two different deletions that disrupt the open reading frame. Loss-of-function mutations at FRI have thus provided the basis for the evolution of many early-flowering ecotypes.
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              Activation tagging of the floral inducer FT.

              FLOWERING LOCUS T (FT), which acts in parallel with the meristem-identity gene LEAFY (LFY) to induce flowering of Arabidopsis, was isolated by activation tagging. Like LFY, FT acts partially downstream of CONSTANS (CO), which promotes flowering in response to long days. Unlike many other floral regulators, the deduced sequence of the FT protein does not suggest that it directly controls transcription or transcript processing. Instead, it is similar to the sequence of TERMINAL FLOWER 1 (TFL1), an inhibitor of flowering that also shares sequence similarity with membrane-associated mammalian proteins.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                20 May 2011
                : 6
                : 5
                : e19949
                Affiliations
                [1 ]Department of Cell and Developmental Biology, John Innes Centre, Norwich, England, United Kingdom
                [2 ]Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
                [3 ]Department of Molecular and Computational Biology, University of Southern California, Los Angeles, California, United States of America
                University of Oxford, United Kingdom
                Author notes

                Conceived and designed the experiments: CD AS PL. Performed the experiments: AS PL CL JI CS. Analyzed the data: CD AS PL JI MN. Contributed reagents/materials/analysis tools: AS JA NW. Wrote the paper: CD PL. Helped with experiments: JA. Developed the molecular markers: NW. Gave interpretation of the experiments and results: JI MN. Supervised the work: CD.

                [¤a]

                Current address: Wellcome Trust Centre for Human Genetics, Oxford, England, United Kingdom

                [¤b]

                Current address: Bayer Crop Science, Monheim am Rhein, Germany

                [¤c]

                Current address: Gregor Mendel Institute, Vienna, Austria

                Article
                PONE-D-11-02809
                10.1371/journal.pone.0019949
                3098857
                21625501
                837fa6ff-41e6-47eb-aeec-15e1f8ee3dd2
                Strange et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 28 January 2011
                : 7 April 2011
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Evolutionary Genetics
                Genetics
                Population Genetics
                Genetic Polymorphism
                Genetic Mutation
                Plant Genetics
                Plant Science
                Plant Genetics

                Uncategorized
                Uncategorized

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