The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana - PubMed
- ️Invalid Date
The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana
Sureshkumar Balasubramanian et al. Nat Genet. 2006 Jun.
Abstract
Light has an important role in modulating seedling growth and flowering time. We show that allelic variation at the PHYTOCHROME C (PHYC) photoreceptor locus affects both traits in natural populations of A. thaliana. Two functionally distinct PHYC haplotype groups are distributed in a latitudinal cline dependent on FRIGIDA, a locus that together with FLOWERING LOCUS C explains a large portion of the variation in A. thaliana flowering time. In a genome-wide scan for association of 65 loci with latitude, there was an excess of significant P values, indicative of population structure. Nevertheless, PHYC was the most strongly associated locus across 163 strains, suggesting that PHYC alleles are under diversifying selection in A. thaliana. Our work, together with previous findings, suggests that photoreceptor genes are major agents of natural variation in plant flowering and growth response.
Figures

Identification of a defective PHYC allele in Fr-2. (a) Expression profiles of genes that are differentially expressed between Fr-2 and Col across 34 wild strains. The genomic interval that co-segregates with early flowering of Fr-2 were analyzed for differentially expressed genes using the AtGenExpress dataset of expression data from 34 strains. Of 112 genes in this interval represented on the ATH1 microarray, 11 were differentially expressed between Col-0 and Fr-2, and are shown here. (b) Expression profile of PHYC (At5g38540) in the 34 strains shown in (a). (c) Red light response of Fr-2, Col-0 and phyB-9 in Col-0. The response of Fr-2 is similar to that of phyB-9, indicating reduced red light sensitivity. (d) Flowering under short days of different parental lines and their F1 progeny.

Quantitative complementation analysis with different parental lines. Col-0 was used as the wild type and the null allele phyC-2 in the Col-0 background as a tester for the crosses. An ANOVA was performed with the following model: TLN~ Line + Cross + Line x Cross. The Line x Cross interaction was significant in all three combinations (p < 0.0001). However, the proportion of total variance accounted for by the Line x Cross interaction varies (shown as R2), which is consistent with the Ler allele being intermediate in activity between the Col-0 and Fr-2 alleles.

PHYC haplotypes. A representative unrooted phylogenetic tree generated from PHYC coding sequences is shown on top. Numbers indicate bootstrap values above 60. The amino acid changes that delineate the two haplotype groups are given below. Unique changes compared to the outgroup A. lyrata are found in both haplotypes. Amino acids that are conserved in other phytochromes (Q or E at position 735, and E at position 822), but changed in either the Col-0- or Ler-type haplotype, are boxed. See Supplementary Table 6 online for provenance of strains.

Latitudinal cline of PHYC alleles. (a) Proportion of Ler-type (black) and Col-0-type (white) PHYC alleles at different latitudes among apparently FRI functional strains. The absolute numbers for each of the classes is given on top of the histograms. (b) Distribution of p-values of a nominal logistic regression model with latitude as a factor and genotypes as response. Allele information of 65 random SNP markers with similar allele frequency as that of PHYC was available in a set of 163 strains. This information was used as a response. Note genome-wide skew towards small p-values. (c) Distribution of p-values for interaction of a given random marker with FRI in an interaction model with latitude as the response and FRI and marker genotypes as factors with interaction.

Markers used for mapping of the early flowering phenotype in Fr- 2. About 80 early plants were genotyped for all markers and linkage of the phenotype to MSat 5.22 and SO191 was confirmed with 60 additional early plants.

Flowering behavior of populations segregating for different PHYC alleles. (a) Distribution of flowering time in an F2 population derived from Ler x Fr-2 cross showing a continuous distribution, in contrast to a bimodal distribution observed in an F2 population derived from the Col x Fr-2 cross (see Lempe, J. et al. Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet. 1, e6 [2005]). (b) Average flowering times of plants with different allelic combinations at PHYC in F2 populations derived from Ler x Fr-2 and Col x Fr-2. A single copy of the Col-0 allele delays flowering much more than a single Ler allele. (c) Genetic complementation analysis with Ler.Flowering times of F1 progeny in short days along with parental lines are shown.

Latitudinal cline of PHYC alleles. (a) Distribution of p-values of a nominal logistic regression model with latitude as a factor and genotype as response. Allele information of 69 random SNP markers with similar allele frequency as that of PHYC was available in a set of 56 strains. This information was used as a response. Note genome-wide skew towards small p-values. (c) Distribution of p-values for interaction of a given random marker with FRI in an interaction model with latitude as the response and FRI and marker genotypes as factors with interaction. PHYC falls in the top bin for both associations and the p-values for PHYC are smaller than those for FLC.
Comment in
-
Mathews S. Mathews S. Nat Genet. 2006 Jun;38(6):606-8. doi: 10.1038/ng0606-606. Nat Genet. 2006. PMID: 16736011 No abstract available.
Similar articles
-
Discordant longitudinal clines in flowering time and phytochrome C in Arabidopsis thaliana.
Samis KE, Heath KD, Stinchcombe JR. Samis KE, et al. Evolution. 2008 Dec;62(12):2971-83. doi: 10.1111/j.1558-5646.2008.00484.x. Epub 2008 Aug 26. Evolution. 2008. PMID: 18752603
-
Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C. Méndez-Vigo B, et al. Plant Physiol. 2011 Dec;157(4):1942-55. doi: 10.1104/pp.111.183426. Epub 2011 Oct 11. Plant Physiol. 2011. PMID: 21988878 Free PMC article.
-
Scarcelli N, Kover PX. Scarcelli N, et al. Mol Ecol. 2009 May;18(9):2039-49. doi: 10.1111/j.1365-294X.2009.04145.x. Epub 2009 Mar 20. Mol Ecol. 2009. PMID: 19317844
-
Monte E, Alonso JM, Ecker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH. Monte E, et al. Plant Cell. 2003 Sep;15(9):1962-80. doi: 10.1105/tpc.012971. Plant Cell. 2003. PMID: 12953104 Free PMC article.
-
Bloomer RH, Dean C. Bloomer RH, et al. J Exp Bot. 2017 Nov 28;68(20):5439-5452. doi: 10.1093/jxb/erx270. J Exp Bot. 2017. PMID: 28992087 Review.
Cited by
-
Linkage and association mapping of Arabidopsis thaliana flowering time in nature.
Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. Brachi B, et al. PLoS Genet. 2010 May 6;6(5):e1000940. doi: 10.1371/journal.pgen.1000940. PLoS Genet. 2010. PMID: 20463887 Free PMC article.
-
Ikeda H, Fujii N, Setoguchi H. Ikeda H, et al. Genetics. 2009 Jun;182(2):603-14. doi: 10.1534/genetics.109.102152. Epub 2009 Apr 10. Genetics. 2009. PMID: 19363127 Free PMC article.
-
Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light.
Filiault DL, Wessinger CA, Dinneny JR, Lutes J, Borevitz JO, Weigel D, Chory J, Maloof JN. Filiault DL, et al. Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):3157-62. doi: 10.1073/pnas.0712174105. Epub 2008 Feb 14. Proc Natl Acad Sci U S A. 2008. PMID: 18287016 Free PMC article.
-
Brennan AC, Méndez-Vigo B, Haddioui A, Martínez-Zapater JM, Picó FX, Alonso-Blanco C. Brennan AC, et al. BMC Plant Biol. 2014 Jan 10;14:17. doi: 10.1186/1471-2229-14-17. BMC Plant Biol. 2014. PMID: 24411008 Free PMC article.
-
Life history in a model system: opening the black box with Arabidopsis thaliana.
Metcalf CJ, Mitchell-Olds T. Metcalf CJ, et al. Ecol Lett. 2009 Jul;12(7):593-600. doi: 10.1111/j.1461-0248.2009.01320.x. Epub 2009 May 18. Ecol Lett. 2009. PMID: 19473216 Free PMC article.
References
-
- Chen M, Chory J, Fankhauser C. Light signal transduction in higher plants. Annu Rev Genet. 2004;38:87–117. - PubMed
-
- Johanson U, et al. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science. 2000;290:344–347. - PubMed
-
- Aukerman MJ, Amasino RM. Molecular genetic analysis of flowering time in Arabidopsis. Sem Cell Dev Biol. 1996;7:427–433.
-
- El-Assal SED, Alonso-Blanco C, Peeters AJ, Raz V, Koornneef M. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet. 2001;29:435–40. - PubMed
-
- Maloof JN, et al. Natural variation in light sensitivity of Arabidopsis. Nat Genet. 2001;29:441–6. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases