Abstract
Sexual reproduction remains an understudied feature of oomycete biology. To expand our knowledge of this process, we used RNA-seq and quantitative proteomics to examine matings in Phytophthora infestans. Exhibiting significant changes in mRNA abundance in three matings between different A1 and A2 strains compared to nonmating controls were 1170 genes, most being mating-induced. Rising by >10-fold in at least one cross were 455 genes, and 182 in all three crosses. Most genes had elevated expression in a self-fertile strain. Many mating-induced genes were associated with cell wall biosynthesis, which may relate to forming the thick-walled sexual spore (oospore). Several gene families were induced during mating including one encoding histidine, serine, and tyrosine-rich putative wall proteins, and another encoding prolyl hydroxylases which may strengthen the extracellular matrix. The sizes of these families vary >10-fold between Phytophthora species and one exhibits concerted evolution, highlighting two features of genome dynamics within the genus. Proteomic analyses of mature oospores and nonmating hyphae using isobaric tags for quantification identified 835 shared proteins, with 5% showing >2-fold changes in abundance between the tissues. Enriched in oospores were β-glucanases potentially involved in digesting the oospore wall during germination. Despite being dormant, oospores contained a mostly normal complement of proteins required for core cellular functions. The RNA-seq data generated here and in prior studies were used to identify new housekeeping controls for gene expression studies that are more stable than existing normalization standards. We also observed >2-fold variation in the fraction of polyA+ RNA between life stages, which should be considered when quantifying transcripts and may also be relevant to understanding translational control during development.
Highlights
Sexual reproduction contributes to the survival of many species
In 2006, we reported the results of a microarray study of P. infestans that identified 87 unigenes induced >10-fold during mating [13]
Four A1 and three A2 strains of P. infestans were mated in all combinations in order to identify pairings that yielded well-defined mating zones, in which oospore production is maximized and sporulating aerial hyphae is minimized
Summary
Sexual reproduction contributes to the survival of many species. In the filamentous microbial eukaryotes known as oomycetes, sexual development culminates in the formation of oospores. These are made both by homothallic (self-fertile) species and in pairings of the two mating types of heterothallics, which are called A1 and A2 in Phytophthora [1]. The sexual cycle contributes to fitness by yielding new genotypes. This is well-described in the potato late blight system, where recombination between strains of the pathogen, Phytophthora infestans, has led to more aggressive genotypes [6, 7]
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