S-LOCUS EARLY FLOWERING 3 Is Exclusively Present in the Genomes of Short-Styled Buckwheat Plants that Exhibit Heteromorphic Self-Incompatibility

Abstract

The different forms of flowers in a species have attracted the attention of many evolutionary biologists, including Charles Darwin. In Fagopyrum esculentum (common buckwheat), the occurrence of dimorphic flowers, namely short-styled and long-styled flowers, is associated with a type of self-incompatibility (SI) called heteromorphic SI. The floral morphology and intra-morph incompatibility are both determined by a single genetic locus named the S-locus. Plants with short-styled flowers are heterozygous (S/s) and plants with long-styled flowers are homozygous recessive (s/s) at the S-locus. Despite recent progress in our understanding of the molecular basis of flower development and plant SI systems, the molecular mechanisms underlying heteromorphic SI remain unresolved. By examining differentially expressed genes from the styles of the two floral morphs, we identified a gene that is expressed only in short-styled plants. The novel gene identified was completely linked to the S-locus in a linkage analysis of 1,373 plants and had homology to EARLY FLOWERING 3. We named this gene S-LOCUS EARLY FLOWERING 3 (S-ELF3). In an ion-beam-induced mutant that harbored a deletion in the genomic region spanning S-ELF3, a phenotype shift from short-styled flowers to long-styled flowers was observed. Furthermore, S-ELF3 was present in the genome of short-styled plants and absent from that of long-styled plants both in world-wide landraces of buckwheat and in two distantly related Fagopyrum species that exhibit heteromorphic SI. Moreover, independent disruptions of S-ELF3 were detected in a recently emerged self-compatible Fagopyrum species and a self-compatible line of buckwheat. The nonessential role of S-ELF3 in the survival of individuals and the prolonged evolutionary presence only in the genomes of short-styled plants exhibiting heteromorphic SI suggests that S-ELF3 is a suitable candidate gene for the control of the short-styled phenotype of buckwheat plants.

The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations

“…Two genes completely linked to the distyly locus have, however, been identified in buckwheat ( Fagopyrum esculentum ), and studies of plants from natural populations showed that some variants in these genes are specific to the S allele, which is strong evidence that recombination with the long style allele ( s ) is very rare (Yasui et al. ). This study sequenced about 610 kb around one of the genes, which included at least one other gene and also repetitive transposable element sequences; the repeats make assembly difficult, and the fully S‐linked region must be larger than the total length of current contigs.…”

Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses

“…Efficient fertilization is only possible in inter-morph crosses. A candidate for a causal distyly gene has been described from Fagopyrum (Yasui et al, 2012); also, S- locus linked sequences have been identified from Primula and Turnera (Labonne and Shore, 2011; Labonne et al, 2009; Li et al, 2007, 2015; Nowak et al, 2015). However, in Primula no causal distyly gene has been isolated, and no plausible mechanistic explanation for style length dimorphism is available in any species, hampering progress in understanding the evolution of the S -locus supergene.

10.7554/eLife.17956.003Figure 1.Identification of CYP734A50 as an S-morph and style-specific gene.( A ) Dissected P. veris L- (left) and S-morph flowers (right), showing reciprocal differences in style length and anther position (yellow arrowheads).

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Genetic Control of Floral Morph and Petal Pigmentation in <i>Linum grandiflorum</i> Desf., a Heterostylous Flax

“…The tight linkage and convergent evolution of SI and floral characteristics in heterostylous plants have been attracting the interest of geneticists and evolutionary biologists since the age of Charles Darwin (Darwin, 1877). Many attempts to isolate the S gene have been reported in Primula, Fagopyrum, and Turnera, but the S gene has never been identified (Labonne and Shore, 2011;Li et al, 2011;Manfield et al, 2005;Yasui et al, 2012). We have also studied heterostyly in Linum in order to isolate the S gene and reported a good S gene candidate (Ushijima et al, 2012).…”