A Small Cysteine-Rich Protein from the Asian Soybean Rust Fungus, Phakopsora pachyrhizi, Suppresses Plant Immunity

Qi, Mingsheng; Link, Tobias; Müller, Manuel; Daniela, Hirschburger; Pudake, Ramesh Namdeo; Pedley, Kerry F.; Braun, E. J.; Voegele, Ralf T.; Baum, Thomas J.; Whitham, Steven A.

doi:10.1371/journal.ppat.1005827

Cited by 62 publications

(59 citation statements)

References 84 publications

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“…Cell death symptom elicited by VmE02 recombinant protein was monitored 2-4 d post infiltration for N. benthamiana, S. lycopersicum, Arabidopsis, apple and wheat. Trypan blue staining was performed as described (Qi et al, 2016). The experiments were repeated at least three times, and each assay consisted of at least three plant seedlings or leaves.…”

Section: A Tumefaciens Infiltration and Trypan Blue Stainingmentioning

confidence: 99%

A small cysteine‐rich protein from two kingdoms of microbes is recognized as a novel pathogen‐associated molecular pattern

et al. 2019

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Summary Pathogen‐associated molecular patterns (PAMPs) are conserved molecules that are crucial for normal life cycle of microorganisms. However, the diversity of microbial PAMPs is little known. During screening of cell‐death‐inducing factors from the necrotrophic fungus Valsa mali, we identified a novel PAMP VmE02 that is widely spread in oomycetes and fungi. Agrobacterium tumefaciens‐mediated transient expression or infiltration of recombinant protein produced by Escherichia coli was performed to assay elicitor activity of the proteins tested. Virus‐induced gene silencing in Nicotiana benthamiana was used to determine the components involved in VmE02‐triggered cell death. The role of VmE02 in virulence and conidiation of V. mali were characterized by gene deletion and complementation. We found that VmE02, together with some of its homologues from both oomycete and fungal species, exhibited cell‐death‐inducing activity in N. benthamiana. VmE02‐triggered cell death was shown to be dependent on BRI1‐ASSOCIATED KINASE‐1, SUPPRESSOR OF BIR1‐1, HSP90 and SGT1 in N. benthamiana. Deletion of VmE02 in V. mali greatly attenuated pathogen conidiation but not virulence, and treatment of N. benthamiana with VmE02 enhances plant resistance to Sclerotinia sclerotiorum and Phytophthora capsici. We conclude that VmE02 is a novel cross‐kingdom PAMP produced by several fungi and oomycetes.

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Section: A Tumefaciens Infiltration and Trypan Blue Stainingmentioning

confidence: 99%

A small cysteine‐rich protein from two kingdoms of microbes is recognized as a novel pathogen‐associated molecular pattern

et al. 2019

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“…Another clade-II member, GmSPL12l from soybean, was shown to be a target of the Phakopsora pachyrhizi (Asian soybean rust) effector PpEC23 (Qi et al , 2016). This effector suppressed the hypersensitive response (HR) in soybean and tobacco and also interacted with other clade-II members from N. benthamiana and Arabidopsis: NbSPL1 and AtSPL1 (Qi et al , 2016). In another study, the N immune receptor of N. benthamiana was found to associate with the SBP transcription factor NbSPL6 upon activation of HR.…”

Section: Discussionmentioning

confidence: 99%

An inhibitor of apoptosis (SfIAP) interacts with SQUAMOSA promoter binding protein (SBP) transcription factors that exhibit pro-cell death characteristics

Kessens

Sorensen

Kabbage

2018

Preprint

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Highlights: SBP transcription factors SlySBP8b and SlySBP12a from tomato interact with an insect inhibitor of apoptosis protein (SfIAP). Both exhibit pro-cell death characteristics while SlySBP12a activity may be regulated through ER membrane tethering. AbstractDespite the functional conservation of programmed cell death (PCD) across broad evolutionary distances, an understanding of the molecular machinery underpinning this fundamental program in plants remains largely elusive. This is despite its critical importance to development, homeostasis, and proper responses to stress. Progress in plant PCD has been hindered by the fact that many core regulators of animal PCD are absent in plant genomes. Remarkably, numerous studies have shown that the ectopic expression of animal anti-PCD genes in plants can suppress cell death imposed by many stresses. In this study, we capitalize on the ectopic expression of an insect inhibitor of apoptosis (SfIAP) to identify novel cell death regulators in plants. A yeast two-hybrid assay was conducted using SfIAP as bait to screen a tomato cDNA library. This screen identified several transcription factors of the SQUAMOSA promoter binding protein (SBP) family as potential SfIAP binding partners. We confirmed this interaction in vivo for our top two interactors, SlySBP8b and SlySBP12a, using coimmunoprecipitation. Interestingly, overexpression of SlySBP8b and SlySBP12a induced spontaneous cell death in Nicotiana benthamiana leaves. Overexpression of these two transcription factors also induced the accumulation of reactive oxygen species and enhanced the growth of the necrotrophic pathogen Alternaria alternata. Fluorescence microscopy confirmed the nuclear localization of both SlySBP8b and SlySBP12a, while SlySBP12a was also localized to the ER membrane. These results support a pro-death role for SlySBP8b and SlySBP12a and provide potential targets that can be utilized to improve stress tolerance in crop plants.3

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“…Interaction of PpEC23 with the soybean transcription repressor GmSPL12I was shown by yeast two-hybrid and pull-down. PpEC23 interacts with itself in the cytoplasm and it localizes in the nucleus when it interacts with GmSPL12I (Qi et al, 2016). With this large effectoromic screen, the authors were able to propose a shortlist of 17 P. pachyrhizi priority candidates that can now be specifically addressed in dedicated efforts .…”

Section: Effectoromics Of the Asian Soybean Rust Fungus P Pachyrhizimentioning

confidence: 99%

Advances in understanding obligate biotrophy in rust fungi

et al. 2019

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Summary Rust fungi (Pucciniales) are the largest group of plant pathogens and represent one of the most devastating threats to agricultural crops worldwide. Despite the economic importance of these highly specialized pathogens, many aspects of their biology remain obscure, largely because rust fungi are obligate biotrophs. The rise of genomics and advances in high‐throughput sequencing technology have presented new options for identifying candidate effector genes involved in pathogenicity mechanisms of rust fungi. Transcriptome analysis and integrated bioinformatics tools have led to the identification of key genetic determinants of host susceptibility to infection by rusts. Thousands of genes encoding secreted proteins highly expressed during host infection have been reported for different rust species, which represents significant potential towards understanding rust effector function. Recent high‐throughput in planta expression screen approaches (effectoromics) have pushed the field ahead even further towards predicting high‐priority effectors and identifying avirulence genes. These new insights into rust effector biology promise to inform future research and spur the development of effective and sustainable strategies for managing rust diseases.

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A Small Cysteine-Rich Protein from the Asian Soybean Rust Fungus, Phakopsora pachyrhizi, Suppresses Plant Immunity

Cited by 62 publications

References 84 publications

A small cysteine‐rich protein from two kingdoms of microbes is recognized as a novel pathogen‐associated molecular pattern

A small cysteine‐rich protein from two kingdoms of microbes is recognized as a novel pathogen‐associated molecular pattern

An inhibitor of apoptosis (SfIAP) interacts with SQUAMOSA promoter binding protein (SBP) transcription factors that exhibit pro-cell death characteristics

Advances in understanding obligate biotrophy in rust fungi

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