Characterization of a gene co-expression network associated with MGST, the pollen modifier gene of gametophytic self-incompatibility in sweet cherry (Prunus avium L.)

Most sweet cherry (Prunus avium L.) cultivars exhibit S-RNase-based gametophytic self-incompatibility ( SI), a major obstacle for fruit production. Clarifying the molecular mechanism behind the SI reaction will contribute to future improvements in sweet cherry productivity. Although the S haplotype combination of pollen and seed parent determines SI specificity in Prunus, as in other S-RNase-based SI plants, accumulated experimental results imply the presence of a Prunus-specific SI mechanism. The sweet cherry cultivar 'Cristobalina', with a functional S locus, shows pollen-part self-compatibility (SC) owing to the downregulated expression of an SI modifier in pollen. This modifier has been identified as M-locus-encoded glutathione Stransferase-like ( MGST), but it has not been well characterized. In this study, we investigated the transcriptomic profiles of pollen with relatively higher and lower MGST expression levels, M-pollen and m-pollen, respectively. 'Cristobalina' (Mm) F1 populations segregating for SC (Mm) and SI (MM), 'Cristobalina' selfed progeny of the mm genotype (SC), and diverse SI sweet cherry cultivars (MM) were used. Illumina mRNA-seq reads obtained from a pollen grain or germinated pollen tube of each sample were mapped to the sweet cherry reference-coding sequence. A differential expression analysis among the genotypic combinations yielded 985 and 853 differentially expressed genes in the pollen-grain and germinated pollen-tube stages, respectively; however, only MGST was detected in all the pollen-grain comparisons. This supported our hypothesis that MGST functions in the S-RNase activation of pollen. However, a differentially expressed gene clustering analysis and a weighted gene co-expression network analysis revealed significant correlations between MGST's expression and the expression levels of functional gene sets, such as those involved in lipid metabolism and stress responses. Thus, it is also possible that MGST may function in some pollen development- or viability-related processes. Further analyses are necessary to elucidate the molecular function of MGST in the Prunus-specific SI reaction.