Secondary Evolution of a Self-incompatibility Locus in the Brassicaceae Genus Leavenworthia
Affiliations
Self-incompatibility (SI) is the flowering plant reproductive system in which self pollen tube growth is inhibited, thereby preventing self-fertilization. SI has evolved independently in several different flowering plant lineages. In all Brassicaceae species in which the molecular basis of SI has been investigated in detail, the product of the S-locus receptor kinase (SRK) gene functions as receptor in the initial step of the self pollen-rejection pathway, while that of the S-locus cysteine-rich (SCR) gene functions as ligand. Here we examine the hypothesis that the S locus in the Brassicaceae genus Leavenworthia is paralogous with the S locus previously characterized in other members of the family. We also test the hypothesis that self-compatibility in this group is based on disruption of the pollen ligand-producing gene. Sequence analysis of the S-locus genes in Leavenworthia, phylogeny of S alleles, gene expression patterns, and comparative genomics analyses provide support for both hypotheses. Of special interest are two genes located in a non-S locus genomic region of Arabidopsis lyrata that exhibit domain structures, sequences, and phylogenetic histories similar to those of the S-locus genes in Leavenworthia, and that also share synteny with these genes. These A. lyrata genes resemble those comprising the A. lyrata S locus, but they do not function in self-recognition. Moreover, they appear to belong to a lineage that diverged from the ancestral Brassicaceae S-locus genes before allelic diversification at the S locus. We hypothesize that there has been neo-functionalization of these S-locus-like genes in the Leavenworthia lineage, resulting in evolution of a separate ligand-receptor system of SI. Our results also provide support for theoretical models that predict that the least constrained pathway to the evolution of self-compatibility is one involving loss of pollen gene function.
Ferrer M, Vasquez-Cruz M, Verde-Caceres M, Magana Rosado U, Magana-Rosado U, Good S Ann Bot. 2024; 135(1-2):25-42.
PMID: 38716780 PMC: 11805948. DOI: 10.1093/aob/mcae056.
Molecular insights into self-incompatibility systems: From evolution to breeding.
Zhang D, Li Y, Zhao X, Zhang C, Liu D, Lan S Plant Commun. 2023; 5(2):100719.
PMID: 37718509 PMC: 10873884. DOI: 10.1016/j.xplc.2023.100719.
Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae.
Novikova P, Kolesnikova U, Scott A Plant Reprod. 2022; 36(1):125-138.
PMID: 36282331 PMC: 9957919. DOI: 10.1007/s00497-022-00451-6.
Mora-Carrera E, Stubbs R, Keller B, Leveille-Bourret E, de Vos J, Szovenyi P Mol Ecol. 2021; 32(1):61-78.
PMID: 34761469 PMC: 10078681. DOI: 10.1111/mec.16270.
Abdallah D, Baraket G, Perez V, Salhi Hannachi A, Hormaza J Hortic Res. 2020; 7:170.
PMID: 33082976 PMC: 7527504. DOI: 10.1038/s41438-020-00392-z.