Mitotic recombination between homologous chromosomes drives genomic diversity in diatoms

Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific genetic variability in natural populations. However, the contribution of various mechanisms generating such diversity is unknown. Here we estimated the genetic micro-diversity within a natural diatom popu...

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Bibliographic Details
Published in:Current biology 2021-08, Vol.31 (15), p.3221-3232.e9
Main Authors: Bulankova, Petra, Sekulić, Mirna, Jallet, Denis, Nef, Charlotte, van Oosterhout, Cock, Delmont, Tom O., Vercauteren, Ilse, Osuna-Cruz, Cristina Maria, Vancaester, Emmelien, Mock, Thomas, Sabbe, Koen, Daboussi, Fayza, Bowler, Chris, Vyverman, Wim, Vandepoele, Klaas, De Veylder, Lieven
Format: Article
Language:English
Subjects:
Biochemistry, Molecular Biology
copy number variation
diatom
genetic variability
haplotypes diversity
Life Sciences
loss of heterozygosity
recombination
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Summary:Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific genetic variability in natural populations. However, the contribution of various mechanisms generating such diversity is unknown. Here we estimated the genetic micro-diversity within a natural diatom population and mapped the genomic changes arising within clonally propagated diatom cell cultures. Through quantification of haplotype diversity by next-generation sequencing and amplicon re-sequencing of selected loci, we documented a rapid accumulation of multiple haplotypes accompanied by the appearance of novel protein variants in cell cultures initiated from a single founder cell. Comparison of the genomic changes between mother and daughter cells revealed copy number variation and copy-neutral loss of heterozygosity leading to the fixation of alleles within individual daughter cells. The loss of heterozygosity can be accomplished by recombination between homologous chromosomes. To test this hypothesis, we established an endogenous readout system and estimated that the frequency of interhomolog mitotic recombination was under standard growth conditions 4.2 events per 100 cell divisions. This frequency is increased under environmental stress conditions, including treatment with hydrogen peroxide and cadmium. These data demonstrate that copy number variation and mitotic recombination between homologous chromosomes underlie clonal variability in diatom populations. We discuss the potential adaptive evolutionary benefits of the plastic response in the interhomolog mitotic recombination rate, and we propose that this may have contributed to the ecological success of diatoms. [Display omitted] •Diatom clonal cultures rapidly accumulate genomic diversity•At the single-cell level loss of heterozygosity and copy number variation are observed•Genomic changes correlate with the occurrence of mitotic interhomolog recombination•The frequency attains 4.2 events per 100 cell divisions and increases under stress Bulankova et al. show that recombination between homologous chromosomes in vegetative cells of diatom Phaeodactylum tricornutum results in genomic diversity in clonal populations. This diversity includes the appearance of recombined haplotypes, loss of heterozygosity, and copy number variation between individual cells.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2021.05.013