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, 117 (5), 2526-2534

Functional Variants of DOG1 Control Seed Chilling Responses and Variation in Seasonal Life-History Strategies in Arabidopsis thaliana

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Functional Variants of DOG1 Control Seed Chilling Responses and Variation in Seasonal Life-History Strategies in Arabidopsis thaliana

Alejandra Martínez-Berdeja et al. Proc Natl Acad Sci U S A.

Abstract

The seasonal timing of seed germination determines a plant's realized environmental niche, and is important for adaptation to climate. The timing of seasonal germination depends on patterns of seed dormancy release or induction by cold and interacts with flowering-time variation to construct different seasonal life histories. To characterize the genetic basis and climatic associations of natural variation in seed chilling responses and associated life-history syndromes, we selected 559 fully sequenced accessions of the model annual species Arabidopsis thaliana from across a wide climate range and scored each for seed germination across a range of 13 cold stratification treatments, as well as the timing of flowering and senescence. Germination strategies varied continuously along 2 major axes: 1) Overall germination fraction and 2) induction vs. release of dormancy by cold. Natural variation in seed responses to chilling was correlated with flowering time and senescence to create a range of seasonal life-history syndromes. Genome-wide association identified several loci associated with natural variation in seed chilling responses, including a known functional polymorphism in the self-binding domain of the candidate gene DOG1. A phylogeny of DOG1 haplotypes revealed ancient divergence of these functional variants associated with periods of Pleistocene climate change, and Gradient Forest analysis showed that allele turnover of candidate SNPs was significantly associated with climate gradients. These results provide evidence that A. thaliana's germination niche and correlated life-history syndromes are shaped by past climate cycles, as well as local adaptation to contemporary climate.

Keywords: delay of germination; genome-wide association; germination niche; seed dormancy; stratification.

Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
(A) PC scores of germination variables (base, and cold treatments: 4, 8, 11, 15, 22, and 32 d at 4 and 10 °C). Percent variance explained by each axis: PC1germ = 83%, PC2germ = 7%. (B) Mean percent germination in each treatment for the lines with the 10% highest and lowest scores on PC1germ and PC2germ. Colors indicate the amino acid sequence at the DOG1 self-binding domain (53), which we use to define haplotypes, and grey color indicates accessions for which we were not able to assign a haplotype.
Fig. 2.
Fig. 2.
Correlations between PC2germ and DTF (A) and DTS (B). Colors indicate the amino acid sequence at the self-binding domain for different DOG1 haplotypes.
Fig. 3.
Fig. 3.
Chromosome location (Mb) and association P value from GWAS for the SNPs on PC1germ, PC2germ, and DTF (permutation-based significance thresholds are shown by dotted horizontal lines). The vertical dashed grey line indicates the location of DOG1 gene.
Fig. 4.
Fig. 4.
(A) Bayesian phylogeny of DOG1 haplotypes. Haplotype names represent amino acid sequence at the self-binding domain of DOG1. Triangle clade heights represent the number of individuals carrying a redundant sequence. The A. lyrata outgroup used to root the phylogeny is not shown. (B) Ages estimated from pairwise nucleotide divergence of DOG1 haplotype groups with Pleistocene deuterium isotope records (103). Confidence intervals represent a range of generation times from 1.3 (±0.3) y per generation. Pairwise divergence of D-RY appears older in B as branch lengths are not weighted by number of individuals during tree-building (Materials and Methods). In both plots, points reflect divergence of haplotypes or groups of haplotypes. Temperatures are presented as deviations from the last 1,000-y average.
Fig. 5.
Fig. 5.
Average cumulative importance functions of mean temperature of the wettest quarter for the index SNPs of the top 100 SNPs with the highest association with the first 2 PCs of germination for 752 accessions. Genomic controls are shown in grey, representing the 100 cumulative functions of 150 random SNPs with MAF > 0.01.

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