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).