Abstract

Rust fungi cause epidemics that threaten the production of important plant species, such as wheat and soy. Melampsora larici-populina (Mlp) causes the poplar rust and encodes at least 1184 candidate effectors (CEs) whose functions are poorly known. In this study, we sequenced the transcriptome and used mass spectrometry to analyze the metabolome of Arabidopsis plants constitutively expressing 14 Mlp CEs and of a control line to discover alterations leading to plant susceptibility. We found 2299 deregulated genes across the experiment. Genes involved in pattern-triggered immunity, such as FRK1, PR1, RBOHD, and WRKY33, as well as AUX/IAA genes were down-regulated. We further observed that 680 metabolites were deregulated in at least one CE-expressing transgenic line, with “highly unsaturated and phenolic compounds” and “peptides” enriched among down- and up-regulated metabolites. Interestingly, transgenic lines expressing unrelated CEs had correlated patterns of gene and metabolite deregulation, while expression of CEs belonging to the same family deregulated different genes and metabolites. Thus, our results uncouple effector sequence similarity and function. This supports that effector functional investigation in the context of their virulence activity and effect on plant susceptibility requires the investigation of the individual effector and precludes generalization based on sequence similarity.

Highlights

  • Plants must defend themselves against different types of pathogens

  • In Planta Expression of Candidate Fungal Effectors Results in Important Deregulation at the Melampsora larici-populina candidate effectors (CEs) have been previously studied in heterologous systems for functional characterization [22,24,27,30,50]

  • They were selected from the set of small secreted proteins from M. laricipopulina, characterized for their small size, the presence of a signal peptide, the absence of a transmembrane domain and no sequence similarity to proteins outside the Pucciniales order [9]

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Summary

Introduction

Plants must defend themselves against different types of pathogens. Their first line of defense consists of passive barriers, such as the cuticle and cell wall, which prevent pathogens from entering the plant tissue and its cells. Upon successful entry of a pathogen, conserved pathogenic motifs, called Microbe-Associated Molecular Patterns (MAMPs), may be detected and activate the Pattern-Triggered Immunity (PTI) [1]. Microorganisms secrete effectors into their host to modulate the host metabolism in favor of the pathogen. If detected, these effectors will activate the Effector-Triggered Immunity (ETI), leading to plant cell death in order to avoid the pathogen spreading to surrounding cells [4]

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