Hoarau, G. | bioRxiv Science

bioRxiv2024

Origin and evolutionary trajectories of brown algal sex chromosomes

Sex chromosomes fall into three classes: XX/XY, ZW/ZZ and U/V systems. The rise, evolution and demise of U/V systems has remained an evolutionary enigma. Here, we analyse genomes spanning the entire brown algal phylogeny to decipher their sex-determination evolutionary history. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN located in a discrete region in proto-U and proto-V chromosomes ceased recombining. Over time, nested inversions led to step-wise expansions of the sex locus, accompanying increasing morphological complexity and sexual differentiation of brown seaweeds. Unlike XX/XY and ZW/ZZ, brown algal U/V evolve mainly by gene gain, showing minimal degeneration. They are structurally dynamic and act as genomic cradles fostering the birth of new genes, potentially from ancestrally non coding sequences. Our analyses demonstrate that hermaphroditism arose from ancestral males that acquired U-specific genes by ectopic recombination, and that in the transition from a U/V to an XX/XY system, V-specific genes moved down the genetic hierarchy of sex determination. Both events lead to the demise of U and V and erosion of their specific genomic characteristics. Taken together, our findings offer a comprehensive model of U/V sex chromosome evolution.

evolutionary biology↗

bioRxiv2019

Methylation variation promotes phenotypic diversity and evolutionary potential in a millenium-old clonal seagrass meadow

Evolutionary theory predicts that clonal organisms are more susceptible to extinction than sexually reproducing organisms, due to low genetic variation and slow rates of evolution. In agreement, conservation management considers genetic variation as the ultimate measure of a populations ability to survive over time. However, clonal plants are among the oldest living organisms on our planet. Here, we test the hypothesis that clonal seagrass meadows display epigenetic variation that complements genetic variation as a source of phenotypic variation. In a clonal meadow of the seagrass Zostera marina we characterized DNA methylation among 42 shoots. We also sequenced the whole genome of 10 shoots to correlate methylation patterns with photosynthetic performance under exposure to, and recovery from 27{degrees}C, while controlling for somatic mutations. Here, we show for the first time that clonal seagrass shoots display DNA methylation variation that is associated with variation in fitness-related traits: photosynthetic performance and heat stress resilience. The co-variation in DNA methylation and phenotype may be linked via gene expression because methylation patterns varied in functionally relevant genes involved in photosynthesis, and in the repair and prevention of heat-induced protein damage. A >five week epigenetic heat stress memory may heat-harden previously heat-exposed shoots. While genotypic diversity has been shown to enhance stress resilience in seagrass meadows, we suggest that epigenetic variation plays a similar role in meadows dominated by a single genotype. Consequently, conservation management of clonal plants should consider epigenetic variation as indicator of resilience and stability, and restoration efforts may benefit from stress-priming transplanted seeds or shoots.

evolutionary biology↗