The 124202 candidate effector of Melampsora larici-populina interacts with membranes in Nicotiana and Arabidopsis

Gaouar, Ouassila; Morency, Marie-Josée; Letanneur, Claire; Séguin, Armand; Germain, Hugo

doi:10.1080/07060661.2016.1153523

Cited by 12 publications

(10 citation statements)

References 71 publications

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“…As such, recent research efforts have identified and initiated the characterization of M . larici-populina candidate effectors using transcriptomics and functional screens in heterologous plant systems such as Nicotiana benthamiana and Arabidopsis thaliana 21,22,24,32 . These studies highlighted that M .…”

Section: Introductionmentioning

confidence: 99%

“…larici-populina candidate effector proteins. To this end, we used Escherichia coli as an heterologous system to express eleven candidate effectors that were previously described to target particular cell compartments and/or to interact with specific plant proteins and/or that are homologues of known rust avirulence effectors 21,22,24,32 . Among the eleven selected proteins, three were successfully produced and purified from E .…”

Section: Introductionmentioning

confidence: 99%

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Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds

Guillen

Lorrain

Tsan

et al. 2019

Sci Rep

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Rust fungi are plant pathogens that secrete an arsenal of effector proteins interfering with plant functions and promoting parasitic infection. Effectors are often species-specific, evolve rapidly, and display low sequence similarities with known proteins. How rust fungal effectors function in host cells remains elusive, and biochemical and structural approaches have been scarcely used to tackle this question. In this study, we produced recombinant proteins of eleven candidate effectors of the leaf rust fungus Melampsora larici-populina in Escherichia coli. We successfully purified and solved the three-dimensional structure of two proteins, MLP124266 and MLP124017, using NMR spectroscopy. Although both MLP124266 and MLP124017 show no sequence similarity with known proteins, they exhibit structural similarities to knottins, which are disulfide-rich small proteins characterized by intricate disulfide bridges, and to nuclear transport factor 2-like proteins, which are molecular containers involved in a wide range of functions, respectively. Interestingly, such structural folds have not been reported so far in pathogen effectors, indicating that MLP124266 and MLP124017 may bear novel functions related to pathogenicity. Our findings show that sequence-unrelated effectors can adopt folds similar to known proteins, and encourage the use of biochemical and structural approaches to functionally characterize effector candidates.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds

Guillen

Lorrain

Tsan

et al. 2019

Sci Rep

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“…Agrobacterium-mediated heterologous expression or Pseudomonas-mediated delivery of tagged effectors in leaf cells are methods of choice for the study of effectors in planta (Torto et al, 2003;Vleeshouwers et al, 2008). Confocal imaging of green fluorescent protein (GFP) fusions has been widely used to determine the cellular compartments targeted by effectors (Caillaud et al, 2012;Gaouar et al, 2016;Schornack et al, 2010;Takemoto et al, 2012). More recently, Nicotiana benthamiana has been used to identify cellular compartments targeted by M. larici-populina candidate effectors as well as putative plant-interacting proteins (Petre et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

Infection assays in Arabidopsis reveal candidate effectors from the poplar rust fungus that promote susceptibility to bacteria and oomycete pathogens

Germain

Joly

Mireault

et al. 2017

Molecular Plant Pathology

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SUMMARYFungi of the Pucciniales order cause rust diseases which, altogether, affect thousands of plant species worldwide and pose a major threat to several crops. How rust effectors-virulence proteins delivered into infected tissues to modulate host functionscontribute to pathogen virulence remains poorly understood. Melampsora larici-populina is a devastating and widespread rust pathogen of poplar, and its genome encodes 1184 identified small secreted proteins that could potentially act as effectors. Here, following specific criteria, we selected 16 candidate effector proteins and characterized their virulence activities and subcellular localizations in the leaf cells of Arabidopsis thaliana. Infection assays using bacterial (Pseudomonas syringae) and oomycete (Hyaloperonospora arabidopsidis) pathogens revealed subsets of candidate effectors that enhanced or decreased pathogen leaf colonization. Confocal imaging of green fluorescent protein-tagged candidate effectors constitutively expressed in stable transgenic plants revealed that some protein fusions specifically accumulate in nuclei, chloroplasts, plasmodesmata and punctate cytosolic structures. Altogether, our analysis suggests that rust fungal candidate effectors target distinct cellular components in host cells to promote parasitic growth.

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“…Discussion Effector biologists have tackled both the identification and the functional characterization of candidate effectors (CEs) [14, 35], as this is a key step towards a better understanding of plant-microbe interactions. In rust fungi, different approaches are used in the functional characterization of these proteins, including analysis of subcellular localization in planta[19,25,28,30,31], infection assays in true host or in a model plant, and induction/repression of plant cell death[19,30,36,37]. The transcriptome or metabolome of the host in responses to the pathogen are frequently evaluated[38][39][40][41][42][43], but the assessment of the role of individual CEs in these processes is not easily measured and seldom analyzed[22,44].Here we investigated 14 CEs from Melampsora larici-populina by evaluating their individual impact on the transcriptome and metabolome of stable transgenic Arabidopsis plants.…”

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Differential alteration of plant functions by homologous fungal candidate effectors

Kcg

Pelletier

Séguin

et al. 2020

Preprint

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Rust fungi are plant pathogens that cause epidemics that threaten the production of important plant species, such as wheat, soy, coffee and poplar. Melampsora larici-populina (Mlp) causes the poplar rust and encodes at least 1 184 candidate effectors (CEs), however their functions are poorly known. In this study, we used Arabidopsis plants constitutively expressing CEs of Mlp to discover processes targeted by these fungal proteins. For this purpose, we sequenced the transcriptome and used mass spectrometry to analyse the metabolome of Arabidopsis plants expressing individually one of the 14 selected CEs and of a control line. We found 2 299 deregulated genes across the experiment. Among the down-regulated genes, the KEGG pathways "MAPK signaling pathway" and "Plant-pathogen interaction" were respectively over-represented in six and five of the 14 transgenic lines. Moreover, genes related to hormone response and defense were down-regulated across all transgenic lines are. We further observed that there were 680 metabolites deregulated in at least one CE-expressing transgenic line, with highly unsaturated and phenolic compounds enriched in up-regulated metabolites and peptides enriched among down-regulated metabolites. Interestingly, we found that 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. Taken together, our results indicate that the sequence of effectors and their belonging to families may not be a good predictor of their impact on the plant.

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The 124202 candidate effector of Melampsora larici-populina interacts with membranes in Nicotiana and Arabidopsis

Cited by 12 publications

References 71 publications

Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds

Structural genomics applied to the rust fungus Melampsora larici-populina reveals two candidate effector proteins adopting cystine knot and NTF2-like protein folds

Infection assays in Arabidopsis reveal candidate effectors from the poplar rust fungus that promote susceptibility to bacteria and oomycete pathogens

Differential alteration of plant functions by homologous fungal candidate effectors

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