Effectors of plant-colonizing fungi and beyond

Uhse, Simon; Djamei, Armin

doi:10.1371/journal.ppat.1006992

Cited by 89 publications

(88 citation statements)

References 53 publications

(60 reference statements)

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“…Effectors can be classified into apoplastic, cytoplasmic and nuclear categories based on their subcellular localization and action inside hosts [70]. Since software LOCALIZER can only predict the location of chloroplast, mitochondria and nuclei [71], those with their targets unpredictable were considered as apoplastic effectors.…”

Section: Discussionmentioning

confidence: 99%

Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identifies avirulence gene candidates

Xia

Wang

et al. 2020

BMC Genomics

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Background: The stripe rust pathogen, Puccinia striiformis f. sp. tritici (Pst), threats world wheat production. Resistance to Pst is often overcome by pathogen virulence changes, but the mechanisms of variation are not clearly understood. To determine the role of mutation in Pst virulence changes, in previous studies 30 mutant isolates were developed from a least virulent isolate using ethyl methanesulfonate (EMS) mutagenesis and phenotyped for virulence changes. The progenitor isolate was sequenced, assembled and annotated for establishing a high-quality reference genome. In the present study, the 30 mutant isolates were sequenced and compared to the wide-type isolate to determine the genomic variation and identify candidates for avirulence (Avr) genes. Results: The sequence reads of the 30 mutant isolates were mapped to the wild-type reference genome to identify genomic changes. After selecting EMS preferred mutations, 264,630 and 118,913 single nucleotide polymorphism (SNP) sites and 89,078 and 72,513 Indels (Insertion/deletion) were detected among the 30 mutant isolates compared to the primary scaffolds and haplotigs of the wild-type isolate, respectively. Deleterious variants including SNPs and Indels occurred in 1866 genes. Genome wide association analysis identified 754 genes associated with avirulence phenotypes. A total of 62 genes were found significantly associated to 16 avirulence genes after selection through six criteria for putative effectors and degree of association, including 48 genes encoding secreted proteins (SPs) and 14 non-SP genes but with high levels of association (P ≤ 0.001) to avirulence phenotypes. Eight of the SP genes were identified as avirulence-associated effectors with high-confidence as they met five or six criteria used to determine effectors. Conclusions: Genome sequence comparison of the mutant isolates with the progenitor isolate unraveled a large number of mutation sites along the genome and identified high-confidence effector genes as candidates for avirulence genes in Pst. Since the avirulence gene candidates were identified from associated SNPs and Indels caused by artificial mutagenesis, these avirulence gene candidates are valuable resources for elucidating the mechanisms of the pathogen pathogenicity, and will be studied to determine their functions in the interactions between the wheat host and the Pst pathogen.

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Section: Discussionmentioning

confidence: 99%

Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identifies avirulence gene candidates

Xia

Wang

et al. 2020

BMC Genomics

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“…Given that the chloroplast plays a key role in plant immunity, it is reasonable that the organelle would be a prime target of effector proteins introduced by pathogens [8]. Plant pathogens secrete a cocktail of effector proteins or virulence factors that are known to act in the apoplast or the cytoplasm, where they may target specific organelles [7,[61][62][63][64][65][66] (Figure 1). While effector proteins are very diverse, with different mechanisms of action, ultimately, what they have in common is their ability to facilitate pathogen proliferation in the host in the absence of direct or indirect detection by corresponding compatible resistance proteins (R) to trigger ETI.…”

Section: Effectors and Chloroplastsmentioning

confidence: 99%

“…While effector proteins are very diverse, with different mechanisms of action, ultimately, what they have in common is their ability to facilitate pathogen proliferation in the host in the absence of direct or indirect detection by corresponding compatible resistance proteins (R) to trigger ETI. In compatible interactions, effectors contribute to virulence by suppressing the plant immune response, by interfering with the host's physiology to promote nutrient acquisition, by influencing organelle function and gene expression, or by as yet unknown mechanisms [64,66,67].…”

Section: Effectors and Chloroplastsmentioning

confidence: 99%

Chloroplasts and Plant Immunity: Where Are the Fungal Effectors?

et al. 2019

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Chloroplasts play a central role in plant immunity through the synthesis of secondary metabolites and defense compounds, as well as phytohormones, such as jasmonic acid and salicylic acid. Additionally, chloroplast metabolism results in the production of reactive oxygen species and nitric oxide as defense molecules. The impact of viral and bacterial infections on plastids and chloroplasts has been well documented. In particular, bacterial pathogens are known to introduce effectors specifically into chloroplasts, and many viral proteins interact with chloroplast proteins to influence viral replication and movement, and plant defense. By contrast, clear examples are just now emerging for chloroplast-targeted effectors from fungal and oomycete pathogens. In this review, we first present a brief overview of chloroplast contributions to plant defense and then discuss examples of connections between fungal interactions with plants and chloroplast function. We then briefly consider well-characterized bacterial effectors that target chloroplasts as a prelude to discussing the evidence for fungal effectors that impact chloroplast activities.

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“…Plant-microbe interactions have evolved over hundreds of millions of years, generating a diversity of associations covering a broad spectrum from pathogenic to mutualistic coexistence (Martin et al, 2017;Uhse and Djamei, 2018). Although these various lifestyles incur different needs, they all bear in common the use of secreted molecules, which enable interacting partners to communicate and have an impact on each other and on their environment, and vice versa.…”

Section: Discussionmentioning

confidence: 99%

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

2020

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The plant secretome is usually considered in the frame of proteomics, aiming at characterizing extracellular proteins, their biological roles and the mechanisms accounting for their secretion in the extracellular space. In this review, we aim to highlight recent results pertaining to secretion through the conventional and unconventional protein secretion pathways notably those involving plant exosomes or extracellular vesicles. Furthermore, plants are well known to actively secrete a large array of different molecules from polymers (e.g. extracellular RNA and DNA) to small compounds (e.g. ATP, phytochemicals, secondary metabolites, phytohormones). All of these play pivotal roles in plant-fungi (or oomycetes) interactions, both for beneficial (mycorrhizal fungi) and deleterious outcomes (pathogens) for the plant. For instance, recent work reveals that such secretion of small molecules by roots is of paramount importance to sculpt the rhizospheric microbiota. Our aim in this review is to extend the definition of the plant and fungal secretomes to a broader sense to better understand the functioning of the plant/microorganisms holobiont. Fundamental perspectives will be brought to light along with the novel tools that should support establishing an environment-friendly and sustainable agriculture.

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Effectors of plant-colonizing fungi and beyond

Cited by 89 publications

References 53 publications

Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identifies avirulence gene candidates

Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identifies avirulence gene candidates

Chloroplasts and Plant Immunity: Where Are the Fungal Effectors?

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

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