A Remarkable Expansion of Oligopeptide Transporter Genes in Rust Fungi (Pucciniales) Suggests a Specialization in Nutrient Acquisition for Obligate Biotrophy

Abstract

Nutrients acquisition by rust fungi during their biotrophic growth has been assigned to a few transporters expressed in haustorial infection structures. We performed a comparative genomic analysis of all transporter genes (hereafter termed transportome) classified according to the Transporter Classification Database (TCDB) focusing specifically on rust fungi (order Pucciniales) versus other species in the Dikarya. We also surveyed expression of transporter genes in the poplar rust fungus for which transcriptomics data are available across the whole life cycle. Despite a significant increase in gene number, rust fungi presented a reduced transportome compared to a vast majority of fungi in the Dikarya. However, a few transporter families in the subclass Porters showed significant expansions. Noteworthy, three metal transport-related families involved in the import, export and sequestration of metals were expanded in Pucciniales and expressed at various stages of the rust life cycle suggesting a tight regulation of metal homeostasis. The most remarkable gene expansion in the Pucciniales was observed for the oligopeptide transporter (OPT) family with 25 genes in average compared to seven to 14 genes in the other surveyed taxonomical ranks. A phylogenetic analysis showed several specific expansion events at the root of the order Pucciniales with subsequent expansions in rust taxonomical families. The OPT genes showed dynamic expression patterns along the rust life cycle and more particularly during infection of the poplar host tree, suggesting a possible specialization for the acquisition of nitrogen and sulfur through the transport of oligopeptides from the host during biotrophic growth.

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“…Previous studies utilizing comparative genomics information, gene expression data and signatures of diversifying selection uncovered protein families uniquely linked to pathogenic fungi, including rusts (Sperschneider et al ., 2014 ). Recently, a comparison of the total set of transporter genes in the order Pucciniales with other dikarya fungi revealed that the genomes of rusts show a global reduction in their repertoire of transporter genes (Guerillot et al ., 2023 ). However, a marked expansion of specific transporter gene families compared with other dikarya was found, specifically for oligopeptide transporters (OPT) and three families related with metal transport (Guerillot et al ., 2023 ).…”

“…Recently, a comparison of the total set of transporter genes in the order Pucciniales with other dikarya fungi revealed that the genomes of rusts show a global reduction in their repertoire of transporter genes (Guerillot et al ., 2023 ). However, a marked expansion of specific transporter gene families compared with other dikarya was found, specifically for oligopeptide transporters (OPT) and three families related with metal transport (Guerillot et al ., 2023 ). These findings may reflect rust specialties related with adaptation to biotrophy in terms of nutrient acquisition and control of metal homeostasis.…”