Abstract
Gynodioecy, the coexistence of hermaphrodites and females (i.e. male-sterile plants) in natural plant populations, most often results from polymorphism at genetic loci involved in a particular interaction between the nuclear and cytoplasmic genetic compartments (cytonuclear epistasis): cytoplasmic male sterility (CMS). Although CMS clearly contributes to the coevolution of involved nuclear loci and cytoplasmic genomes in gynodioecious species, the occurrence of CMS genetic factors in the absence of sexual polymorphism (cryptic CMS) is not easily detected and rarely taken in consideration. We found cryptic CMS in the model plant Arabidopsis thaliana after crossing distantly related accessions, Sha and Mr-0. Male sterility resulted from an interaction between the Sha cytoplasm and two Mr-0 genomic regions located on chromosome 1 and chromosome 3. Additional accessions with either nuclear sterility maintainers or sterilizing cytoplasms were identified from crosses with either Sha or Mr-0. By comparing two very closely related cytoplasms with different male-sterility inducing abilities, we identified a novel mitochondrial ORF, named orf117Sha, that is most likely the sterilizing factor of the Sha cytoplasm. The presence of orf117Sha was investigated in worldwide natural accessions. It was found mainly associated with a single chlorotype in accessions belonging to a clade predominantly originating from Central Asia. More than one-third of accessions from this clade carried orf117Sha, indicating that the sterilizing-inducing cytoplasm had spread in this lineage. We also report the coexistence of the sterilizing cytoplasm with a non-sterilizing cytoplasm at a small, local scale in a natural population; in addition a correlation between cytotype and nuclear haplotype was detected in this population. Our results suggest that this CMS system induced sexual polymorphism in A. thaliana populations, at the time when the species was mainly outcrossing.
Highlights
Cytoplasmic male sterility (CMS) is known to spontaneously evolve in plant natural populations, where it leads to the coexistence of females and hermaphrodites
A case of cryptic CMS was recently revealed after hybridization of two Mimulus species whereas no gynodioecy was observed in M. guttatus, the sterilizing cytoplasm donor [11]
Cytoplasmic Male Sterility Arose in a cross Between Distantly–related Arabidopsis Accessions
Summary
Cytoplasmic male sterility (CMS) is known to spontaneously evolve in plant natural populations, where it leads to the coexistence of females (i.e. male-sterile individuals) and hermaphrodites. Such populations are called gynodioecious [1,2]. In this reproductive system, the plant sexual phenotype results from the epistatic interaction between the cytoplasm, either sterilizing or not, and nuclear genes whose alleles may either restore male fertility in the presence of the sterilizing cytoplasm (restorer, Rf) or allow the expression of male sterility (maintainer). Nuclear restorers seem to be common in M. guttatus, the sterilizing cytoplasm is almost exclusively restricted to the population where it was originally described [12]
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