Abstract
Angiosperms are renown for their diversity of flower colors. Often considered adaptations to pollinators, the most common underlying pigments, anthocyanins, are also involved in plants’ stress response. Although the anthocyanin biosynthetic pathway is well characterized across many angiosperms and is composed of a few candidate genes, the consequences of blocking this pathway and producing white flowers has not been investigated at the transcriptome scale. We take a transcriptome-wide approach to compare expression differences between purple and white petal buds in the arctic mustard, Parrya nudicaulis, to determine which genes’ expression are consistently correlated with flower color. Using mRNA-Seq and de novo transcriptome assembly, we assembled an average of 722 bp per gene (49.81% coding sequence based on the A. thaliana homolog) for 12,795 genes from the petal buds of a pair of purple and white samples. Our results correlate strongly with qRT-PCR analysis of nine candidate genes in the anthocyanin biosynthetic pathway where chalcone synthase has the greatest difference in expression between color morphs (P/W = ∼7×). Among the most consistently differentially expressed genes between purple and white samples, we found 3× more genes with higher expression in white petals than in purple petals. These include four unknown genes, two drought-response genes (CDSP32, ERD5), a cold-response gene (GR-RBP2), and a pathogen defense gene (DND1). Gene ontology analysis of the top 2% of genes with greater expression in white relative to purple petals revealed enrichment in genes associated with stress responses including cold, drought and pathogen defense. Unlike the uniform downregulation of chalcone synthase that may be directly involved in the loss of petal anthocyanins, the variable expression of several genes with greater expression in white petals suggest that the physiological and ecological consequences of having white petals may be microenvironment-dependent.
Highlights
The loss of floral anthocyanins in white flowers provides an unparalleled opportunity to examine the genes underlying a distinctive phenotypic transition
To disentangle the roles of pollinator and non-pollinator agents of selection on flower color, we studied a habitat in interior Alaska, where pollinators are exceedingly rare [10,11] and non-pollinator agents of selection are predicted to be paramount [12]
Genome Size Estimation Since recent polyploidy can complicate transcriptome analysis due to genome-wide paralogy, we examined the genome size of six P. nudicaulis samples from three populations using fresh leaf tissue extracts on a flow cytometer
Summary
The loss of floral anthocyanins in white flowers provides an unparalleled opportunity to examine the genes underlying a distinctive phenotypic transition. The purple-white flower color polymorphism in the arctic mustard, Parrya nudicaulis, offers a unique perspective on potential non-pollinator agents of selection (Fig. 1; [13]). Since the frequency of white individuals is positively correlated with the length of the growing season, we suspect climatic factors (or correlated, non-pollinator selective agents) interacting with the petal color contribute to the maintenance of this polymorphism [13]. We have detected selection against individuals with lighter colored petals along the Arctic Coastal Plain, but not in interior Alaska where the climate during the growing season is more benign [14]
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