The genetic basis of the recurrent evolutionary transition from outcrossing to selfing has been a major focus in evolutionary biology. The relationship between selfing and polyploidy has been debated for years. Polyploids, which are commonly found in plants, are suggested to self more frequently than their diploid relatives, although the underlying mechanism is still largely unknown.
The transition from outcrossing to selfing typically occurs through the breakdown of the self-incompatibility (SI) system. Sporophytic SI system prevents self-pollen tube growth via interactions between the male component, S-locus cysteine-rich protein (SCR) and the female component, S-locus receptor kinase (SRK) of the same S-haplogroups. While theories predict that mutations in male component, SCR, are more likely to be fixed as they have increased opportunities for outcrossing, empirical evidence is still lacking.
Here, we study the loss of SI in Arabidopsis kamchatica to reveal the molecular mechanisms underlying the evolution of self-compatibility in polyploids. A. kamchatica is a self-compatible allotetraploid species, originated through allopolyploidization between two predominantly outcrossing diploid species, Arabidopsis halleri and Arabidopsis lyrata. We applied high-throughput sequencing approach to isolate SCR genes from anther cDNAs, which has not been successful through conventional PCR method due to the short and highly polymorphic sequences among SCR genes of different S-haplogroups. Mutations were detected in SCR genes of A. kamchatica. Thus, transgenic method was developed to transform functionally restored SCR gene into A. kamchatica bearing functional female components. SI was recovered in transformed A. kamchatica, indicating that the degradation of SCR is primarily responsible for the loss of SI in A. kamchatica. This is in agreement with theoretical predictions that mutations in male components are more advantageous than mutations in female components. Moreover, dominance hierarchy among different S-haplogroups may be involved in the evolutionary loss of SI in allotetraploid A. kamchatica.