PhD Thesis: Tracing Molecular Patterns of Adaptation in Arctic Brassicaceae

Extreme environments can function as natural laboratories for studying how different organisms adapt to similar selection pressures at the genetic level. This thesis explores how three Arctic plant species independently adapted to some of the coldest biomes on Earth, and how they evolved similar suites of adaptations to extremes in light and temperature. It addresses fundamental questions in plant evolutionary biology, such as the extent to which adaptation follows the same genetic trajectories in different species, and the genetic basis for plant adaptation to extreme environments. The thesis has two main objectives that are addressed through three papers (Papers I-III): 1) estimate the degree of adaptive molecular convergence in the three Arctic Brassicaceae Cardamine bellidifolia, Cochlearia groenlandica, and Draba nivalis, and 2) identify putative molecular adaptations to the Arctic environment in the same three species.

Approach. The first two papers examine the degree of evolutionary repeatability in how C. bellidifolia, C. groenlandica, and D. nivalis adapted to the Arctic environment at the genetic level (objective 1). In Paper I, we estimated molecular convergence at the level of codons, genes, and functional pathways, by comparing genome-wide patterns of positive selection and identifying convergent substitutions in the three species. In Paper II, we conducted a time series experiment to examine the transcriptional responses of the Arctic Brassicaceae to low temperatures, and to identify potential convergent expression patterns in cold response.

All three papers identify putative molecular adaptations to extremes in light and temperature (objective 2). In Paper I, we identified candidate genes for adaptation to the Arctic environment by searching for positively selected genes associated with abiotic stresses common in the Arctic. In Paper II, we explored the molecular basis of cold tolerance in Arctic Brassicaceae, and described how their cold-induced transcriptomes differ from that of the temperate model species, Arabidopsis thaliana. In Paper III, we assembled the genome of D. nivalis and explored the genomic characteristics of Arctic plant adaptation, by conducting comparative analyses of chromosomal evolution and functional genomics with other species in the Brassicaceae.

Main findings and discussion. The findings in Papers I-II suggests that the three Arctic Brassicaceae have adapted to the Arctic environment through independent genetic trajectories (objective 1). In Paper I, we found that positive selection has been acting on different genes, but similar functional pathways in the three species. The positively selected genes sets showed convergent functional profiles associated with abiotic stresses common in the Arctic. However, we found little evidence for convergent substitutions at the same sites, or for positive selection acting on the same genes in the three species. In Paper II, we found that the cold-response of C. bellidifolia, C. groenlandica, and D. nivalis was highly species-specific. Most cold-induced genes were unique for each species, and the number of genes shared by the three Arctic species and the temperate A. thaliana was higher than the number of genes shared by the Arctic species alone. This suggests that the cold response in Arctic Brassicaceae mainly evolved independently, but with some components likely conserved across the family. The low levels of molecular convergence could be explained by the many evolutionary trajectories leading to better performance under temperature and light stress in plants, and/or less repeatable patterns of adaptation in highly polygenic traits such as cold tolerance.

Papers I-III presents some of the first molecular evidence for putative plant adaptations to the Arctic environment (objective 2). In Paper I, we found multiple candidate genes for Arctic adaptation associated with cold stress, freezing stress, oxidative stress and light stress in all species. Adaptations associated with the plasma membrane seemed to be particularly important in all species, possibly due to its crucial role in freezing tolerance. In Paper II, we found that the Arctic cold response followed similar trends as in the temperate A. thaliana, but a few genes and characteristics were specific for the Arctic species alone. In Paper III, we presented a 302 Mb assembly of D. nivalis that is highly contiguous with 91.6 % assembled into eight chromosomes (the base chromosome of the species). We found that the D. nivalis genome contains expanded suites of genes associated with common Arctic stresses, and the expansion of these gene families appear to partly be driven by the activity of transposable elements.

Conclusion. The results from this dissertation provide a framework for studies that aim to test the existence of a functional syndrome of Arctic adaptation in Brassicaceae and other flowering plants. The D. nivalis genome assembly may also become an important tool in studies of Arctic plant evolution in general.