Landscape genomics meets karyotype evolution
Despite alleged limitations of RAD-seq genomic scanning to detect loci related to local adaptation (Lowry et al., 2017), our landscape genomic analyses have shown that 74 outlier loci are significantly correlated with climatic variables related to temperature (BIO4 and BIO6) and precipitation (BIO16 and BIO17). Interestingly, chromosome number was among these outliers and was also correlated with BIO6. Together with chromosome number we also identified four loci significantly correlated with BIO6 and with similar associations with RDA1 and RDA2 axes as chromosome number (Fig. 3b).
One of the four loci is linked to genome regions with high amounts of repetitive DNA. This is unsurprising as highly repetitive sequences can be found at centromeres and telomeres, which play critical roles in genome integrity maintenance throughout the cell cycle (Onishi-Seebacher & Korbel, 2011). Repetitive DNA sequences were previously referred to as “junk DNA” because few discernible functions could be assigned to these regions, but recent studies have shown that they have important functional roles in genome organization and evolution (von Sternberg & Shapiro, 2005; Biscotti et al., 2015). Although the precise functions of repetitive regions in the genome are still poorly understood, in plants they have been associated with abiotic stress resistance or adaptation to the environment. For example, repetitive non-coding DNA has proven to be susceptible to environmental stress, which can induce specific quantitative modifications on the affected genome fraction (Bassi et al., 2015). Repetitive DNA has been associated with ectopic recombination (González & Petrov, 2012), also in holocentric organisms (Höök et al., 2023), which could result in chromosomal fission and fusion rearrangements and explain, at least partially, the resulting patterns of karyotype variation. In this way, very recently, the genomic architecture of fission and fusion has been deciphered for holocentric sedges (Hofstaetter et al., 2022; Escudero et al., 2023) and butterflies (Höök et al., 2023), which is characterized by a high density of repetitive DNA.
The other three significantly correlated loci were associated with genes involved in important metabolic routes, being kinases specially relevant (three hits) and associated to two of the three loci. Among these, diacylglycerol kinase (DGK) genes are of special relevance given that they are involved in the modulation of plant growth, development, and adaptation in both biotic and abiotic stress conditions (Kue Foka et al., 2020). Additionally, DGK plays an important role in generating membrane-derived oligosaccharides that protect cells against osmotic stress conditions (Jefferson et al., 2013). Furthermore, glycerophospholipids (GPL), which are synthesized by DGK, have been linked with adaptation to high-altitude cold environments (Wei et al., 2022). Kinase domains seem to be associated with stress response and adaptation to the environment in plants. Receptor-like kinases (RLKs) and histidine kinases have been found to play a role in plant response to abiotic stresses (Osakabe et al., 2013). Additionally, calcium-dependent protein kinases (CDPKs) are essential for plant development and stress responses (Alves et al., 2021). SNF1-related protein kinases have been found to have a unique function in plant glucose and stress signaling (Lumbreras et al., 2001). Furthermore, receptor-like kinases have been found to play significant roles in plant growth regulation and responses to stresses (Fenglian et al., 2012). Finally, kinase domains have also been found to function in plant growth and salt-stress responses (Zhou et al., 2006).
Remarkably, different chromosome numbers (which are related to linkage groups and recombination rates) are significantly associated with allelic variants at these loci (with important genes), which in turn are also significantly associated with environmental climatic variables. This study is a step forward in supporting the hypothesis that cytogenetic variation (chromosome number, linkage groups and recombination rates) in species with holocentric chromosomes are selected towards different optima of climatic regimes (Escudero et al., 2012, 2013b; Spalink et al., 2018; Márquez-Corro et al., 2021).