Natural variation in the C‐repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes

TLDR

Arabidopsis thaliana spans climates with widely varying winter temperatures, and accessions from colder northern latitudes are generally more freezing tolerant than those from warmer southern latitudes, a pattern linked to variation at the C‑repeat binding factor (CBF) locus that regulates a large freezing‑tolerance gene network. The study investigates whether differences in freezing tolerance, mediated by the CBF pathway, underlie local adaptation of Arabidopsis ecotypes. We find that the Italian ecotype has a non‑functional CBF2 protein, leading to reduced induction of the CBF regulon and lower freezing tolerance compared with the Swedish ecotype, demonstrating that natural variation in the CBF pathway drives adaptive evolution.

Abstract

The natural range of Arabidopsis thaliana (Arabidopsis) encompasses geographical regions that have greatly differing local climates, including harshness of winter temperatures. A question thus raised is whether differences in freezing tolerance might contribute to local adaptation in Arabidopsis. Consistent with this possibility is that Arabidopsis accessions differ in freezing tolerance and that those collected from colder northern latitudes are generally more tolerant to freezing than those collected from warmer southern latitudes. Moreover, recent studies with Arabidopsis genotypes collected from sites in Sweden (SW) and Italy (IT) have established that the two accessions are locally adapted, that the SW ecotype is more tolerant of freezing than the IT ecotype, and that genetic differences between the two ecotypes that condition local adaptation and freezing tolerance map to a region that includes the C-repeat binding factor (CBF) locus. The CBF locus includes three genes - CBF1, CBF2 and CBF3 - that are induced by low temperature and encode transcription factors that regulate a group of more than 100 genes, the CBF regulon, which impart freezing tolerance. Here we show that cold induction of most CBF regulon genes is lower in IT plants compared with SW plants, and that this is due to the IT CBF2 gene encoding a non-functional CBF2 protein. The non-functional IT CBF2 protein also contributes to the lower freezing tolerance of the IT plants compared with the SW plants. Taken together, studies on the SW and IT ecotypes provide evidence that natural variation in the CBF pathway has contributed to adaptive evolution in these Arabidopsis populations.