Abstract
To help learn how phytopathogens feed from their hosts, genes for nutrient transporters from the hemibiotrophic potato and tomato pest Phytophthora infestans were annotated. This identified 453 genes from 19 families. Comparisons with a necrotrophic oomycete, Pythium ultimum var. ultimum, and a hemibiotrophic fungus, Magnaporthe oryzae, revealed diversity in the size of some families although a similar fraction of genes encoded transporters. RNA-seq of infected potato tubers, tomato leaves, and several artificial media revealed that 56 and 207 transporters from P. infestans were significantly up- or down-regulated, respectively, during early infection timepoints of leaves or tubers versus media. About 17 were up-regulated >4-fold in both leaves and tubers compared to media and expressed primarily in the biotrophic stage. The transcription pattern of many genes was host-organ specific. For example, the mRNA level of a nitrate transporter (NRT) was about 100-fold higher during mid-infection in leaves, which are nitrate-rich, than in tubers and three types of artificial media, which are nitrate-poor. The NRT gene is physically linked with genes encoding nitrate reductase (NR) and nitrite reductase (NiR), which mobilize nitrate into ammonium and amino acids. All three genes were coregulated. For example, the three genes were expressed primarily at mid-stage infection timepoints in both potato and tomato leaves, but showed little expression in potato tubers. Transformants down-regulated for all three genes were generated by DNA-directed RNAi, with silencing spreading from the NR target to the flanking NRT and NiR genes. The silenced strains were nonpathogenic on leaves but colonized tubers. We propose that the nitrate assimilation genes play roles both in obtaining nitrogen for amino acid biosynthesis and protecting P. infestans from natural or fertilization-induced nitrate and nitrite toxicity.
Highlights
Successful pathogens must efficiently exploit the nutrients of their hosts to support their growth
To understand the interaction between the filamentous eukaryotic microbe Phytophthora infestans and its potato and tomato hosts, we mined the genome for genes encoding proteins involved in nutrient uptake and measured their expression in leaves, tubers, and three artificial media
When we blocked the expression of a nitrate transporter and two other genes involved in assimilating nitrate, we observed that those genes were required for successful colonization of nitrate-rich leaves but not nitrate-poor tissues, and that nitrate had become toxic to the silenced strains
Summary
Successful pathogens must efficiently exploit the nutrients of their hosts to support their growth. Pathogens accomplish this through mechanisms that include manipulating hosts to shift nutrients to sites of infection, generating feeding structures, expressing transporters for the nutrients, and making metabolic enzymes for assimilating the nutrients [1,2,3]. The nutritional strategies used by a plant pathogen may vary depending on the metabolic condition of its host, stage of infection, and lifestyle. While a role of oomycete haustoria in nutrition is not proved, sugar and amino acid transporters expressed in haustoria have been identified from rusts and powdery mildew fungi [5, 7]. The oomycete Phytophthora infestans, for example, behaves as a biotroph during much of its interaction with its potato and tomato hosts, but may shift to necrotrophy late in infection [11]
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