Repeatome evolution across space and time: Unravelling repeats dynamics in the plant genus Erythrostemon Klotzsch (Leguminosae Juss).

Abstract

Fluctuations in genomic repetitive fractions (repeatome) are known to impact several facets of evolution, such as ecological adaptation and speciation processes. Therefore, investigating the divergence of repetitive elements can provide insights into an important evolutionary force. However, it is not clear how the different repetitive element clades are impacted by the different factors such as ecological changes and/or phylogeny. To discuss this, we used the Neotropical legume genus Erythrostemon (Caesalpinioideae) as a model, given its ancient origin (~33 Mya), lineage-specific niche conservatism, macroecological heterogeneity, and disjunct distribution in Meso- and South American (MA and SA respectively) lineages. We performed a comparative repeatomic analysis of 18 Erythrostemon species to test the impact of environmental variables over repeats diversification. Overall, repeatome composition was diverse, with high abundances of satDNAs and Ty3/gypsy-Tekay transposable elements, predominantly in the MA and SA lineages respectively. However, unexpected repeatome profiles unrelated to the phylogeny/biogeography were found in a few MA (E. coccineus, E. pannosus and E. placidus) and SA (E. calycinus) species, related to reticulate evolution and incongruence between nuclear and plastid topology, suggesting ancient hybridizations. The plesiomorphic Tekay and satDNA pattern was altered in the MA-sensu stricto subclade with a striking genomic differentiation (expansion of satDNA and retraction of Tekay) associated with the colonization of a new environment in Central America around 20 Mya. Our data reveal that the current species-specific Tekay pool was the result of two bursts of amplification probably in the Miocene, with distinct patterns for the MA and SA repeatomes. This suggests a strong role of the Tekay elements as modulators of the genome-environment interaction in Erythrostemon, providing macroevolutionary insights about mechanisms of repeatome differentiation and plant diversification across space and time.