Comparative transcriptomics reveals conserved infection-associated gene expression in Phytophthora agathidicida across its natural gymnosperm host kauri and the model angiosperm host Nicotiana benthamiana.

Abstract

Phytophthora species cause many devastating diseases of plants, including those of forest trees. Agathis australis (New Zealand kauri) is an ancient and culturally significant tree species that is susceptible to a lethal root and collar rot caused by Phytophthora agathidicida. Functional characterisation of P. agathidicida virulence factors is limited by difficulties in working with its natural host. The angiosperm Nicotiana benthamiana is widely used as a model plant host for studying plant-pathogen interactions, including P. agathidicida. To help determine whether N. benthamiana is a reliable model for the gymnosperm A. australis, we analysed P. agathidicida gene expression in leaves and roots of N. benthamiana and compared this to an earlier transcriptomic analysis in A. australis. A core set of 1129 genes upregulated in both hosts and organs was enriched for secreted RXLR effector, CAZyme and elicitin proteins, indicating a conserved infection-associated transcriptional programme. Similarities between the suites of genes expressed in leaves and roots support the approach of performing assays of gene function on leaves which are technically easier to use than roots. While many genes were similarly expressed across hosts, there were also some differences. A CAP protein, highly expressed only in N. benthamiana, increased P. agathidicida growth in N. benthamiana but not in A. australis under the conditions tested. These findings suggest that P. agathidicida deploys a largely conserved molecular strategy to colonise gymnosperm and angiosperm hosts, supporting the use of N. benthamiana as a model system for functional studies, while also highlighting pathogen genes that are highly expressed and upregulated in each of the hosts.