Time-resolved dual transcriptomics reveal early induced Nicotiana benthamiana root genes and conserved infection-promoting Phytophthora palmivora effectors

Abstract

BackgroundPlant-pathogenic oomycetes are responsible for economically important losses in crops worldwide. Phytophthora palmivora, a tropical relative of the potato late blight pathogen, causes rotting diseases in many tropical crops including papaya, cocoa, oil palm, black pepper, rubber, coconut, durian, mango, cassava and citrus.Transcriptomics have helped to identify repertoires of host-translocated microbial effector proteins which counteract defenses and reprogram the host in support of infection. As such, these studies have helped in understanding how pathogens cause diseases. Despite the importance of P. palmivora diseases, genetic resources to allow for disease resistance breeding and identification of microbial effectors are scarce.ResultsWe employed the model plant Nicotiana benthamiana to study the P. palmivora root infections at the cellular and molecular levels. Time-resolved dual transcriptomics revealed different pathogen and host transcriptome dynamics. De novo assembly of P. palmivora transcriptome and semi-automated prediction and annotation of the secretome enabled robust identification of conserved infection-promoting effectors. We show that one of them, REX3, suppresses plant secretion processes. In a survey for early transcriptionally activated plant genes we identified a N. benthamiana gene specifically induced at infected root tips that encodes a peptide with danger-associated molecular features.ConclusionsThese results constitute a major advance in our understanding of P. palmivora diseases and establish extensive resources for P. palmivora pathogenomics, effector-aided resistance breeding and the generation of induced resistance to Phytophthora root infections. Furthermore, our approach to find infection-relevant secreted genes is transferable to other pathogen-host interactions and not restricted to plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0379-1) contains supplementary material, which is available to authorized users.

Comparative analyses of saprotrophy in Salisapilia sapeloensis and diverse plant pathogenic oomycetes reveal lifestyle-specific gene expression

“…In contrast the transition between biotrophy to necrotrophy requires a switch from a transcriptional program that is outlined to keep a host alive to a transcriptional program outlined to kill a host. In agreement hemibiotrophic pathogens show strong transcriptional shifts between their biotrophic and necrotrophic phases [23,37,38]. Hence, a strong transcriptional difference between a saprotrophic interaction, in which S. sapeloensis feeds on dead plant tissue, compared to the biotrophic phase in the hemibiotroph P. infestans , where its physiology is optimized to keep the host alive, is only expected.…”

Time‐resolved dissection of the molecular crosstalk driving Fusarium head blight in wheat provides new insights into host susceptibility determinism

“…Secreted proteins and especially effectors are closely related to the infection success, facilitating pathogen entry into the plant host tissues, suppressing plant immune responses, and manipulating plant physiology for pathogen's benefit (Giraldo & Valent, ; Stergiopoulos & de Wit, ; Toruño, Stergiopoulos, & Coaker, ). Although some effectors and their functions have already been described in several plant–microbe‐interacting systems (Boller & He, ; Evangelisti et al, ), their diversity and their dynamics during infection are still unknown, especially in filamentous fungi (Alfano, ). In this study, one third of the regulated Fg proteins harbouring representative domains of effectors proved to be accumulated at specific stages of infection (Figure ).…”

Centrin-anchored hydrodynamic shape changes underpin active nuclear rerouting in branched hyphae of an oomycete pathogen

“…Indeed, loss of transketolase function results in depletion of ATP content and slowing down of TOR signaling pathway (Fernandez et al, 2014) . Whether an expressed transketolase ortholog of TKL1 in P. palmivora (PLTG_04838) (Evangelisti et al, 2017) is also involved in early infection processes remains to be addressed.…”

“…Plates were then flooded with 5 mL sterile water and incubated at room temperature for another 30 min. N. benthamiana growth conditions were described previously (Evangelisti et al, 2017) .…”

“…RNA quality was assessed by electrophoresis on agarose gel. Conditions for quantitative PCR were described previously (Evangelisti et al, 2017) .…”