Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa

Abstract

27Parallel adaptation results from independent evolution of similar traits between closely related 28 lineages and allows testing to which extent evolution is repeatable. Parallel adaptation often 29 involves similar gene expression changes but the identity of genes shaped by parallel selection 30 and the causes of expression parallelism remains largely unknown. By comparing genomes 31 and transcriptomes of four independent foothill-alpine population pairs across four 32 treatments, we addressed genetic basis, plasticity and functional consequences of gene 33 expression parallelism in alpine adaptation. Seeds of four population pairs of Arabidopsis 34 arenosa from distinct mountain regions were raised under four treatments that differed in 35 temperature and irradiance, factors varying strongly with elevation. Parallelism in gene 36 expression was quantified by RNA-seq in leaves of young plants. By manipulating 37temperature and irradiance, we also tested for parallelism in plasticity (gene-by-environment 38 interaction [GEI]). We found significant parallelism in differential gene expression across 39 four independently recruited alpine ecotypes with an overrepresentation of genes involved in 40 biotic stress response. In addition, we demonstrated significant parallelism in GEI indicating 41 shared response to environmental variation in our foothill and alpine populations. Fraction of 42 genes showing expression parallelism also encompassed genomic variants showing outlying 43 differentiation, with greater enrichment of such variants in cis-regulatory elements. In 44 summary, our results suggest frequent evolutionary repeatability in shaping expression 45 difference associated with colonization of an alpine environment and support the hypothesis 46 of an important role of genetic variation in cis-regulatory elements in gene expression 47 parallelism.48 49

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

“…Previous genetic and phenotypic investigations and follow-up analyses presented here showed that the scattered alpine forms of both species represent independent alpine colonization in each mountain range, followed by parallel phenotypic differentiation (Fig. 1 D and E) (44)(45)(46). Thus, we sequenced genomes from seven alpine and adjacent foothill population pairs, covering all European lineages encompassing the alpine ecotype.…”

Ploidy and local environment drive intraspecific variation in endoreduplication in Arabidopsis arenosa

“…We used RNA‐seq data from a previous study (Wos et al, 2021) using leaves from the third triplet of individual plants that were phenotyped for EF as described above. RNA‐seq data are available for eight (six tetraploid and two diploid populations) of the nine populations (RNA‐seq data for population D12 were not available) used for flow cytometry.…”

“…For this experiment, we used a subset of the plants from a previous common garden experiment that focused on overall transcriptome differentiation (Wos et al, 2021). Seeds of different mother plants from nine populations were collected in four mountain regions in Niedere Tauern (NT) in the Austrian Alps, Făgăraș (FG) Mountain in Romania, Vysoké (VT), and Zapadné (ZT) Tatry Mountain in Slovakia (Figure 1B; Appendix S1).…”

“…Because alpine areas of the ZT and VT regions have been colonized by plants with distinct ploidies, we considered each region as a separate unit in our main analysis. For each mountain region, we used seeds from one foothill and one alpine ecotype (eight populations; Wos et al, 2021), and for the VT region, we added one more foothill ecotype. Rearing conditions are the same as described by Wos et al (2021).…”

Niche differentiation following whole-genome duplication? The importance of considering the intricate evolutionary history of polyploids when assessing climatic niche evolution

“…Arabidopsis arenosa (Brassicaceae) is a diploid-autotetraploid species with a well-described evolutionary history of its lineages (see Fig. 1), that has recently become an interesting system not only to study polyploid evolution (Monnahan et al, 2019; Morgan et al, 2021a; 2021b; Bohutínská et al, 2021a), but also adaptation to extreme conditions (Konečná et al, 2021, Bohutínská et al, 2021b, Knotek et al, 2020, Wos et al, 2021). Multiple studies have addressed the role of niche differentiation in the autopolyploid evolution of this system, however, reaching strikingly inconsistent outcomes.…”