Modifier Genes Challenge Traditional Views of Self-Incompatibility Breakdown

Plant love can be a tricky affair. When it comes to reproduction, some plant species, like the North American Arabidopsis lyrata, have evolved a fascinating strategy known as self-incompatibility, which prevents them from self-fertilizing, thereby promoting genetic diversity. But in certain cases, this self-incompatibility can break down, allowing the plant to self-fertilize. This botanical mystery was the focus of a recent study by Li and colleagues, published in the journal Nature Communications. 

The key findings of the research pivot around the role of what’s known as the S-locus. Traditionally, it’s been thought that mutations in the S-locus genes, responsible for self-pollen recognition, could cause the breakdown of self-incompatibility. However, Li and team have found that, in the case of Sand Cress, Arabidopsis lyrata, with S1S1 homozygous S-alleles, that is plants that have the same S1 gene from both parents, this isn’t the case. Rather, they propose that an S1-specific modifier unlinked to the S-locus might be responsible for the self-compatibility observed in certain self-fertilizing populations.

Self-incompatibility prevents self-fertilization in certain plants, thereby promoting genetic diversity – a key factor for survival in varying environmental conditions. North American Arabidopsis lyrata usually practices this strategy. However, some independent transitions to self-compatibility and selfing have been observed, linked to specific S-alleles (S1 and S19). The study further links this self-compatibility to these specific S-alleles, challenging the traditional view of self-incompatibility breakdown due to S-locus mutations.

“Self-pollinators have an increased potential to establish self-sustaining populations outside their natural range as invasive species and can survive without insect pollinators. Hence, a better understanding of the mechanisms that can lead to cross-pollinators becoming self-pollinators is of high ecological relevance,” explains Marc Stift, evolutionary ecologist at the University of Konstanz and one of the study authors in a press release.

Using a unique method involving crosses between self-compatible (SC) and self-incompatible (SI) plants, and further focusing on crosses involving SC plants from the two most common S-locus backgrounds associated with selfing, S1 and S19, Li and colleagues managed to provide strong evidence for their hypothesis. Their method relied on determining the breeding system of over 1,503 progeny from these crosses by calculating an SC-index. They calculated the success of breeding through measuring fruit length. In their article, Li and colleagues write:

After pollination, fruits elongate to accommodate the developing seeds, and attain their final length one to two weeks after pollination. Fruit length is a good proxy of seed number. Therefore, as seeds can only be counted reliably at least four weeks after pollination, we used fruit length at two weeks as a proxy of seed set to enable a higher throughput and allow screening of more plants.

Li et al. 2023

In their results, Li and colleagues found that crosses between self-compatible and self-incompatible plants yielded both self-compatible and self-incompatible progeny, with the S-alleles from the self-incompatible partner being crucial. In cases involving the S1 S-allele, the researchers found that self-compatibility could not be attributed to a mutation at the S-locus, instead suggesting the involvement of an unlinked S1-specific modifier.

In other words, the self-recognition genes were somehow involved in the breakdown of self-incompatibility in selfing sand cress, but not by the same mechanism as known from other species. On the contrary: “In fact, our experiments revealed progeny with identical self-recognition genes, of which some were self-incompatible, and others were completely self-fertile,” says Yan Li, who conducted the crossing experiments for her doctoral studies in Konstanz. This provides strong evidence for the previously unproven alternative mechanism involving a modifier gene.

“Now we will have to find out if this mechanism is unique to sand cress, or if it has also led to the transition from cross-pollinator to self-pollinator in other plant species,” Stift adds.

READ THE ARTICLE

Li, Y., Mamonova, E., Köhler, N., van Kleunen, M. and Stift, M. (2023) “Breakdown of self-incompatibility due to genetic interaction between a specific S-allele and an unlinked modifier,” Nature Communications, 14(1), p. 3420. Available at: https://doi.org/10.1038/s41467-023-38802-0.

Cover image: Arabidopsis lyrata flowers. Image: M. Stift