Natural genetic variation in GLK1-mediated photosynthetic acclimation in response to light

Abstract

Background: GOLDEN-like (GLK) transcription factors are central regulators of chloroplast biogenesis in Arabidopsis and other species. Findings from Arabidopsis show that these factors also contribute to photosynthetic acclimation, e.g. to variation in light intensity, and are controlled by retrograde signals emanating from the chloroplast. However, the natural variation of GLK1-centered gene-regulatory networks in Arabidopsis is largely unexplored.

Results: By evaluating the activities of GLK1 target genes and GLK1 itself in vegetative leaves of natural Arabidopsis accessions grown under standard conditions, we uncovered variation in the activity of GLK1 centered regulatory networks. This is linked with the ecogeographic origin of the accessions, and can be associated with a complex genetic variation across loci acting in different functional pathways, including photosynthesis, ROS and brassinosteroid pathways. Our results identify candidate upstream regulators that contribute to a basal level of GLK1 activity in rosette leaves, which can then impact the capacity to acclimate to different environmental conditions. Indeed, accessions with higher GLK1 activity, arising from habitats with a high monthly variation in solar radiation levels, may show lower levels of photoinhibition at higher light intensities.

Conclusions: Our results provide evidence for natural variation in GLK1 regulatory activities in vegetative leaves. This variation is associated with ecogeographic origin and can contribute to acclimation to high light conditions.

Keywords: Acclimation; Arabidopsis thaliana; GLK1; Natural variation.

Fig. 1

Gene expression diversity of GLK1 candidate target genes across 727 Arabidopsis accessions. A Heatmap showing the relative gene expression of the candidate target genes (n = 136) of the top 100 GLK1 binding events across 727 Arabidopsis accessions. Rows represent genes and column accessions. Three clusters of accessions and three clusters of genes were identified and labeled in the heatmap depending on their particular expression patterns. B Expression of GLK1 in the three clusters identified in Fig. 1A. The expression is significantly different (t-test; p-value< 2*10⁻¹⁶) between A1 vs A2, and A1 vs A3, and slightly significant (p-value< 0.03) between A2 vs A3. C Distribution of the monthly standard deviation (SD) of solar radiation of the coordinates from the regions where the accessions were collected. Groups A1 and A2 were significantly different (p-value< 10⁻⁷; t-test). D Map representing the location of the 727 Arabidopsis accessions. Only a subsection of the map is plotted, see Suppl. Fig. 1 for a complete map. A1 accessions are plotted in blue, A2 in red, and A3 in green

Fig. 2

Differential gene expression signature in clusters A1 vs A2. A Scatterplot showing the average expression of all genes in cluster A1 vs A2. In blue are indicated differentially expressed genes (FDR < 0.01 & abs log2FC > 2), and in red the potential direct targets of GLK1 represented in Fig. 1A. B GO analysis (Biological process, ShinyGO) of genes with a significantly increased expression in A1 vs A2. C) GO analysis (Biological process, ShinyGO) of genes with a significantly increased expression in A2 vs A1

Fig. 3

Genetic variation behind the different GLK1 activity. Heatmap showing SNPs among the Arabidopsis accessions studied. Only SNPs differently associated with A1 and A2 accession groups and with a predicted high or moderate impact on gene function are shown. Genes predicted to have a high impact and mentioned in the manuscript are labeled on the right side

Fig. 4

Gene regulatory network differences. A Predicted GRN around GLK1 in the A2 group of accessions. B Interaction strength predicted in the A2 accessions (y-axis) versus A1 accessions (x-axis) for all possible interactions of the genes depicted in A. The continuous black line is the diagonal, dotted black lines represent a difference of 0.2 points from the diagonal line. Red points indicate the interactions whose strength is the difference of 0.2 points indicated by the dotted black lines

Fig. 5

Photosynthetic activity measures across Arabidopsis accessions. The two groups of accessions studied have different photosynthetic activity. A Average photosynthetic value (column) among the accession groups and environmental conditions considered (rows). B Distributions for QY_max, the distributions for A2 accessions are not significantly different between the conditions studied (t-test, p-value< 0.543). A1 accessions are significantly different when growing in the two environments (t-test, p-value< 0.010). C Distributions for NPQ_Lss, the distributions for A1 accessions are not significantly different between the conditions studied, however, A2 accessions are significantly different when growing in different environments considered (t-test, p-value< 2.6*10⁻⁵). D Distributions for the parameter QY_Lss in the A1 and A2 accession groups for the two different sets of conditions