The Nuclear Component of a Cytonuclear Hybrid Incompatibility in Mimulus Maps to a Cluster of Pentatricopeptide Repeat Genes

Abstract

Characterizing the genetic and molecular basis of hybrid incompatibilities is a first step toward understanding their evolutionary origins. We fine mapped the nuclear restorer (Rf ) of cytoplasm-dependent anther sterility in Mimulus hybrids by identifying and targeting regions of the Mimulus guttatus genome containing large numbers of candidate pentatricopeptide repeat genes (PPRs). The single Mendelian locus Rf was first isolated to a 1.3-cM region on linkage group 7 that spans the genome's largest cluster of PPRs, then split into two tightly linked loci (Rf1 and Rf2) by ,10 recombination events in a large (N ¼ 6153) fine-mapping population. Progeny testing of fertile recombinants demonstrated that a dominant M. guttatus allele at each Rf locus was sufficient to restore fertility. Each Rf locus spans a physical region containing numerous PPRs with high homology to each other, suggesting recent tandem duplication or transposition. Furthermore, these PPRs have higher homology to restorers in distantly related taxa (petunia and rice) than to PPRs elsewhere in the Mimulus genome. These results suggest that the cytoplasmic male sterility (CMS)-PPR interaction is highly conserved across flowering plants. In addition, given our theoretical understanding of cytonuclear coevolution, the finding that hybrid CMS results from interactions between a chimeric mitochondrial transcript that is modified by Rf loci identified as PPRs is consistent with a history of selfish mitochondrial evolution and compensatory nuclear coevolution within M. guttatus.

Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

“…Phytozome.net/). For completeness, a handful of markers were also added from published fine-mapping studies of particular genomic regions (Barr and Fishman, 2010).…”

Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

“…To fine-map the nuclear component of cytonuclear male sterility, we previously generated lines with the M. guttatus cytoplasm (IM62 line, Iron Mountain, OR, USA), a nearly isogenic M. nasutus nuclear background (SF line; Sherar's Falls, OR, USA) and heterozygous introgressions for the Rf region on Linkage Group 7 (LG7) Barr and Fishman, 2010). Two independent fourth generation introgression lines were selfed to generate a large mapping population (CSBG; N ¼ 6153) segregating as F 2 hybrids for the Rf region.…”

“…Two independent fourth generation introgression lines were selfed to generate a large mapping population (CSBG; N ¼ 6153) segregating as F 2 hybrids for the Rf region. These individuals were genotyped at markers across the Rf region and scored for male sterility to finemap the tightly linked Rf1 and Rf2 loci (Barr and Fishman, 2010).…”

“…In hybrids between outcrosser Mimulus guttatus (dam) and closely related selfer Mimulus nasutus (sire), anther sterility is caused by a chimeric mitochondrial gene (Case and Willis, 2008) and epistatically restored by two tightly linked Rf loci that act as a single Mendelian locus in F 2 hybrids Barr and Fishman, 2010). This type of sexual system is called cytoplasmic male sterility (CMS) and is widespread in the plant kingdom (Budar et al, 2003).…”

“…However, we did not have sufficient mapping resolution at that time to determine whether the reduced corolla size of male-sterile flowers was due to linkage or pleiotropy. In this study, we use nearly isogenic lines (NILs) segregating for male sterility (Barr and Fishman, 2010) to explicitly test for pleiotropic effects of CMS on corolla size (length and width) and gynoecium length. To uncouple the effects of Rf genotype from linked genes, we used a set of NILs with introgressions that only overlapped in the Rf region (that is, some lines segregated for Rf and genes to the right, whereas others segregated for Rf and genes to the left).…”