Long-term balancing selection drives evolution of immunity genes in Capsella

Koenig, Daniel; Hagmann, Jörg; Li, Rachel; Bemm, Felix; Slotte, Tanja; Neuffer, Barbara; Wright, Stephen I.; Weigel, Detlef

doi:10.7554/elife.43606

Cited by 93 publications

(71 citation statements)

References 112 publications

(150 reference statements)

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“…where the selfing species Capsella rubella shares variants with its outcrossing sister species Capsella grandiflora 47 . These trans-specific polymorphisms are predominantly found at loci involved in immune response 20 , which match our findings in C. elegans . Although it is likely that hyper-divergent regions also exist in outcrossing Caenorhabditis species, identifying them in selfers is expected to be easier for two reasons.…”

Section: Discussionsupporting

confidence: 89%

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Balancing selection maintains hyper-divergent haplotypes inC. elegans

Lee¹,

Zdraljevic²,

Stevens³

et al. 2020

Preprint

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Summary paragraphThe mating system of a species profoundly influences its evolutionary trajectory1–3. Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times4. The transition from outcrossing to selfing significantly decreases the effective population size, effective recombination rate, and heterozygosity within a species5. These changes lead to a reduction in the genetic diversity, and therefore adaptive potential, by intensifying the effects of random genetic drift and linked selection6,7. Selfing has evolved at least three times independently in the nematode genus Caenorhabditis8, including in the model organism Caenorhabditis elegans, and all three selfing species show substantially reduced genetic diversity relative to outcrossing species8,9. Selfing and outcrossing Caenorhabditis species are often found in the same niches, but we still do not know how selfing species with limited genetic diversity can adapt to and inhabit these same diverse environments. Here, we discovered previously uncharacterized levels and patterns of genetic diversity by examining the whole-genome sequences from 609 wild C. elegans strains isolated worldwide. We found that genetic variation is concentrated in punctuated hyper-divergent regions that cover 20% of the C. elegans reference genome. These regions are enriched in environmental response genes that mediate sensory perception, pathogen response, and xenobiotic stress. Population genomic evidence suggests that these regions have been maintained by balancing selection. Using long-read genome assemblies for 15 wild isolates, we found that hyper-divergent haplotypes contain unique sets of genes and show levels of divergence comparable to that found between Caenorhabditis species that diverged millions of years ago. Taken together, these results suggest that ancient genetic diversity present in the outcrossing ancestor of C. elegans has been maintained by long-term balancing selection since the evolution of selfing. These results provide an example for how species can avoid the evolutionary “dead end” associated with selfing by maintaining ancestral genetic diversity.

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Section: Discussionsupporting

confidence: 89%

“…Each point corresponds to one of 308 (d) or 251 (e,f) isotypes and is colored by the geographic origin. 20,193,267,244 of the N2 reference genome). The tree was inferred using SNVs and coloured by inferred haplotypes.…”

Section: Data and Code Availabilitymentioning

confidence: 99%

Balancing selection maintains hyper-divergent haplotypes inC. elegans

Lee¹,

Zdraljevic²,

Stevens³

et al. 2020

Preprint

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“…Seeds of Capsella rubella, collected from wild populations in Crete (Greece, coordinates 35.29, 24.42; accession 879) were previously described (Koenig et al, 2019). Seeds of Sisymbrium irio were collected from wild populations in Bellaterra (Barcelona, Spain, coordinates: 41.497731, 2.109558).…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

Light quality signals generated by vegetation shade facilitate acclimation to reduced light quantity in shade-avoider plants

Morelli

Paulišić

Qin

et al. 2020

Preprint

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SUMMARYWhen growing in search for light, plants can experience continuous or occasional shading by other plants. Plant proximity causes a decrease in the ratio of red to far red light (low R:FR) due to the preferential absorbance of red light and reflection of far red light by photosynthetic tissues of neighboring plants. This signal is often perceived before actual shading causes a reduction in photosynthetically active radiation (low PAR).Here we investigated elongation, photosynthesis and photoacclimation responses in several Brassicaceae species to explore the possible connections between low R:FR and low PAR.A negative correlation was found in shade-tolerant Cardamine hirsuta and shade-avoider Arabidopsis thaliana seedlings (e.g., shade-tolerance was associated with a good adaptation to low PAR but a poor or null response to low R:FR exposure). However, they could be genetically uncoupled. Most interestingly, exposure to low R:FR of shade-avoider plants improved their photoacclimation to low PAR by triggering changes in photosynthesis-related gene expression, pigment accumulation and chloroplast ultrastructure.These results indicate that low R:FR signaling unleashes molecular, metabolic and developmental responses that allow shade-avoider plants (including most crops) to adjust their photosynthetic capacity in anticipation of eventual shading by nearby plants.

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“…Approximately 1–2 Ma the self‐compatible Capsella orientalis diverged from a self‐incompatible C. grandiflora ‐like ancestor (Hurka et al ., ; Bachmann et al ., ), and c . 100 000–200 000 yr ago the self‐compatible C. rubella was derived from C. grandiflora (Foxe et al ., ; Guo et al ., ; Koenig et al ., ). In contrast to the outbreeding C. grandiflora , both selfing species form much smaller flowers and lack the strong floral scent of C. grandiflora .…”

Section: Introductionmentioning

confidence: 97%

Retracing the molecular basis and evolutionary history of the loss of benzaldehyde emission in the genus Capsella

et al. 2019

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The transition from pollinator-mediated outbreeding to selfing has occurred many times in angiosperms. This is generally accompanied by a reduction in traits attracting pollinators, including reduced emission of floral scent. In Capsella, emission of benzaldehyde as a main component of floral scent has been lost in selfing C. rubella by mutation of cinnamate-CoA ligase CNL1. However, the biochemical basis and evolutionary history of this loss remain unknown, as does the reason for the absence of benzaldehyde emission in the independently derived selfer Capsella orientalis.We used plant transformation, in vitro enzyme assays, population genetics and quantitative genetics to address these questions.CNL1 has been inactivated twice independently by point mutations in C. rubella, causing a loss of enzymatic activity. Both inactive haplotypes are found within and outside of Greece, the centre of origin of C. rubella, indicating that they arose before its geographical spread. By contrast, the loss of benzaldehyde emission in C. orientalis is not due to an inactivating mutation in CNL1.CNL1 represents a hotspot for mutations that eliminate benzaldehyde emission, potentially reflecting the limited pleiotropy and large effect of its inactivation. Nevertheless, even closely related species have followed different evolutionary routes in reducing floral scent.

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Long-term balancing selection drives evolution of immunity genes in Capsella

Cited by 93 publications

References 112 publications

Balancing selection maintains hyper-divergent haplotypes inC. elegans

Balancing selection maintains hyper-divergent haplotypes inC. elegans

Light quality signals generated by vegetation shade facilitate acclimation to reduced light quantity in shade-avoider plants

Retracing the molecular basis and evolutionary history of the loss of benzaldehyde emission in the genus Capsella

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