Roger W Innes

Roger W Innes
Indiana University Bloomington | IUB · Department of Biology

PhD

About

217
Publications
28,653
Reads
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14,383
Citations
Additional affiliations
February 1988 - February 1991
University of California, Berkeley
Position
  • PostDoc Position
April 1991 - present
Indiana University Bloomington
Position
  • Professor (Full)

Publications

Publications (217)
Preprint
Full-text available
Most plant pathogens secrete effector proteins to circumvent host immune responses, thereby promoting pathogen virulence. One such pathogen is the fungus Fusarium graminearum, which causes Fusarium Head Blight (FHB) disease on wheat and barley. Transcriptomic analyses revealed that F. graminearum expresses many candidate effector proteins during ea...
Article
Full-text available
The soybean cyst nematode (SCN; Heterodera glycines) facilitates infection by secreting a repertoire of effector proteins into host cells to establish a permanent feeding site composed of a syncytium of root cells. Among the diverse proteins secreted by the nematode, we were specifically interested in identifying proteases to pursue our goal of eng...
Preprint
Full-text available
The soybean cyst nematode (SCN; Heterodera glycines) facilitates infection by secreting a repertoire of effector proteins into host cells to establish a permanent feeding site composed of a syncytium of root cells. Among the diverse proteins secreted by the nematode, we were specifically interested in identifying proteases to pursue our goal of eng...
Article
Hemibiotrophic fungi in the genus Colletotrichum employ a biotrophic phase invading host epidermal cells followed by a necrotrophic phase spreading through neighboring mesophyll and epidermal cells. We used serial block face scanning electron microscopy (SBF-SEM) to compare subcellular changes that occur in Medicago sativa (alfalfa) cotyledons duri...
Preprint
Full-text available
Transgenic expression of a double-stranded RNA in plants can induce silencing of homologous mRNAs in fungal pathogens. Although such host-induced gene silencing is well-documented, the molecular mechanisms by which RNAs can move from the cytoplasm of plant cells across the plasma membrane of both the host cell and fungal cell are poorly understood....
Preprint
Full-text available
Hemibiotrophic fungi in the genus Colletotrichum employ a biotrophic phase invading host epidermal cells followed by a necrotrophic phase spreading through neighboring mesophyll and epidermal cells. We used serial block face scanning electron microscopy (SBF-SEM) to compare subcellular changes that occur in Medicago sativa (alfalfa) cotyledons duri...
Preprint
Full-text available
Extracellular vesicles (EVs) secreted by mammalian cells are highly heterogenous in contents and function. Whether this is also true for EVs secreted by plant cells is not yet known. To address this knowledge gap, we used high-resolution density gradient ultracentrifugation to separate distinct subpopulations of Arabidopsis EVs. We analyzed the pro...
Article
Full-text available
Plant extracellular vesicles (EVs) are membrane-bound organelles involved mainly in intercellular communications and defense responses against pathogens. Recent studies have demonstrated the presence of proteins, nucleic acids including small RNAs, and lipids along with other metabolites in plant EVs. Here, we describe the isolation and characteriz...
Preprint
Full-text available
Plant extracellular vesicles (EVs) are membrane bound organelles involved mainly in intercellular communications and defense responses against pathogens. Recent studies have demonstrated the presence of proteins, nucleic acids including small RNAs, and lipids along with other metabolites in plant EVs. In this paper, we described the isolation and c...
Article
Full-text available
Extracellular vesicles (EVs) are nano-sized, lipid compartments that mediate the intercellular transport of lipids, proteins, nucleic acids and metabolites. During infectious diseases, EVs released by host cells promote immune responses, while those released by pathogens attempt to subvert host immunity. There is a growing body of research investig...
Article
Full-text available
Extracellular RNA (exRNA) has long been considered as cellular waste that plants can degrade and utilize to recycle nutrients. However, recent findings highlight the need to reconsider the biological significance of RNAs found outside of plant cells. A handful of studies suggest that the exRNA repertoire, which turns out to be an extremely heteroge...
Article
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Host-induced gene silencing (HIGS) refers to the silencing of genes in pathogens and pests by expressing homologous double-stranded RNAs (dsRNA) or artificial microRNAs (amiRNAs) in the host plant. The discovery of such trans-kingdom RNA silencing has enabled the development of RNA interference-based approaches for controlling diverse crop pathogen...
Article
Full-text available
Fungal phytopathogens secrete extracellular vesicles (EVs) associated with enzymes and phytotoxic metabolites. While these vesicles are thought to promote infection, defining the true contents and functions of fungal EVs, as well as suitable protein markers, is an ongoing process. To expand our understanding of fungal EVs and their possible roles d...
Article
Full-text available
Previously, we have shown that apoplastic wash fluid purified from Arabidopsis leaves contains small RNAs (sRNAs). To investigate whether these sRNAs are encapsulated inside extracellular vesicles (EVs), we treated EVs isolated from Arabidopsis leaves with the protease trypsin and RNase A, which should degrade RNAs located outside EVs but not those...
Preprint
Full-text available
Fungal phytopathogens secrete extracellular vesicles (EVs) associated with enzymes and phytotoxic metabolites. While these vesicles are thought to promote infection, defining the true contents and functions of fungal EVs, as well as suitable protein markers, is an ongoing process. To expand our understanding of fungal EVs and their possible roles d...
Preprint
Full-text available
Previously, we have shown that apoplastic wash fluid purified from Arabidopsis leaves contains small RNAs (sRNAs). To investigate whether these sRNAs are encapsulated inside extracellular vesicles (EVs), we treated EVs isolated from Arabidopsis leaves with the protease trypsin and RNase A, which should degrade RNAs located outside EVs but not those...
Article
Crop diseases caused by viruses, bacteria, fungi, oomycetes and nematodes constitute major costs for farmers in terms of control measures and yield losses. Enhancing resistance to these pathogens via genetic modification or genome editing represents an economically and environmentally attractive path forward. Recent advances in our understanding of...
Article
In this issue, Richard et al. report the identification of the Co-x disease resistance gene in common bean, which confers resistance against a highly virulent strain of the fungus Colletotrichum lindemuthianum. This fungus causes the disease anthracnose, which produces watery lesions on stems, leaves, pods, and seeds, and can cause up to 100% yield...
Article
Focusing on the discovery and characterization of the Arabidopsis disease resistance protein RPS5 and its guardee PBS1, this review discusses work done in the Innes laboratory from the initial identification of the RPS5 gene in 1995 to the recent deployment of the PBS1 decoy system in crops. This is done through discussion of the structure, functio...
Article
Full-text available
Extracellular vesicles (EVs) are small, membrane‐enclosed compartments that mediate the intercellular transport of proteins and small RNAs. In plants, EVs are thought to play a prominent role in immune responses and are being championed as the long‐sought‐after mechanism for host‐induced gene silencing. However, parallel research on mammalian EVs i...
Article
Stress signaling in plants is carefully regulated to ensure proper development and reproductive fitness. Overactive defense signaling can result in dwarfism as well as developmental defects. In addition to requiring a substantial amount of energy, plant stress responses place a burden upon the cellular machinery, which can result in the accumulatio...
Article
The Arabidopsis resistance protein RPS5 is activated by proteolytic cleavage of the protein kinase PBS1 by the Pseudomonas syringae effector protease AvrPphB. We have previously shown that replacing seven amino acids at the cleavage site of PBS1 with a motif cleaved by the NIa protease of turnip mosaic virus (TuMV) enables RPS5 activation upon TuMV...
Preprint
Full-text available
The Arabidopsis resistance protein RPS5 is activated by proteolytic cleavage of the protein kinase PBS1 by the Pseudomonas syringae effector protease AvrPphB. We have previously shown that replacing seven amino acids at the cleavage site of PBS1 with a motif cleaved by the NIa protease of turnip mosaic virus (TuMV) enables RPS5 activation upon TuMV...
Preprint
Full-text available
Stress signaling in plants is carefully regulated to ensure proper development and reproductive fitness. Overactive defense signaling can result in dwarfism as well as developmental defects. In addition to requiring a significant amount of energy, plant stress responses place a burden upon the cellular machinery, which can result in the accumulatio...
Article
ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and PHYTOALEXIN DEFICIENT4 (PAD4) are sequence-related lipase-like proteins that function as a complex to regulate defense responses in Arabidopsis by both salicylic acid-dependent and independent pathways. Here we describe a gain-of-function mutation in PAD4 (S135F) that enhances resistance and cell death in...
Article
Full-text available
The Pseudomonas syringae effector protein AvrRpm1 activates the Arabidopsis (Arabidopsis thaliana) intracellular innate immune receptor protein RESISTANCE TO PSEUDOMONAS MACULICOLA1 (RPM1) via modification of a second Arabidopsis protein, RPM1-INTERACTING PROTEIN4 (AtRIN4). Prior work has shown that AvrRpm1 induces phosphorylation of AtRIN4, but ho...
Preprint
Full-text available
ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and PHYTOALEXIN DEFICIENT4 (PAD4) are sequence-related lipase-like proteins that function as a complex to regulate defense responses in Arabidopsis by both salicylic acid-dependent and independent pathways. Here we describe a gain-of-function mutation in PAD4 (S135F) that enhances resistance and cell death in...
Article
Full-text available
The Pseudomonas syringae effector protein AvrRpm1 activates the Arabidopsis thaliana intracellular innate immune receptor protein RESISTANCE TO PSEUDOMONAS MACULICOLA1 (RPM1) via modification of a second Arabidopsis protein, RPM1-INTERACTING PROTEIN4 (AtRIN4). Prior work has shown that AvrRpm1 induces phosphorylation of AtRIN4, but homology modelin...
Article
Full-text available
All living organisms secrete molecules for intercellular communication. Recent research has revealed that extracellular vesicles (EVs) play an important role in inter-organismal cell-to-cell communication by transporting diverse messenger molecules, including RNA, DNA, lipids and proteins. These discoveries have raised fundamental questions regardi...
Article
Full-text available
Small RNAs (sRNAs) that are 21 to 24 nucleotides (nt) in length are found in most eukaryotic organisms and regulate numerous biological functions, including transposon silencing, development, reproduction, and stress responses, typically via control of the stability and/or translation of target mRNAs. Major classes of sRNAs in plants include microR...
Article
Full-text available
In Arabidopsis, recognition of the AvrPphB effector protease from Pseudomonas syringae is mediated by the disease resistance (R) protein RPS5, which is activated by AvrPphB-induced cleavage of the Arabidopsis protein kinase PBS1. The recognition specificity of RPS5 can be altered by substituting the AvrPphB cleavage site within PBS1 with cleavage s...
Preprint
Full-text available
In Arabidopsis, recognition of the AvrPphB effector protease from Pseudomonas syringae is mediated by the disease resistance (R) protein RPS5, which is activated by AvrPphB-induced cleavage of the Arabidopsis protein kinase PBS1. The recognition specificity of RPS5 can be altered by substituting the AvrPphB cleavage site within PBS1 with cleavage s...
Article
RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads...
Article
Full-text available
The Pseudomonas syringae cysteine protease AvrPphB activates the Arabidopsis resistance protein RPS5 by cleaving a second host protein, PBS1. AvrPphB induces defense responses in other plant species, but the genes and mechanisms mediating AvrPphB recognition in those species have not been defined. Here, we show that AvrPphB induces defense response...
Preprint
Full-text available
Small RNAs (sRNAs) that are 21 to 24 nucleotides (nt) in length are found in most eukaryotic organisms and regulate numerous biological functions, including transposon silencing, development, reproduction, and stress responses, typically via control of the stability and/or translation of target mRNAs. Major classes of sRNAs in plants include microR...
Article
Full-text available
Subtelomeres of most eukaryotes contain fast-evolving genes usually involved in adaptive processes. In common bean (Phaseolus vulgaris), the Co-2 anthracnose resistance (R) locus corresponds to a cluster of nucleotide-binding-site leucine-rich-repeat (NL) encoding sequences, the prevalent class of plant R genes. To study the recent evolution of thi...
Preprint
Full-text available
The Pseudomonas syringae cysteine protease AvrPphB activates the Arabidopsis resistance protein RPS5 by cleaving a second host protein, PBS1. AvrPphB induces defense responses in other plant species, but the genes and mechanisms mediating AvrPphB recognition in those species have not been defined. Here, we show that AvrPphB induces defense response...
Article
Salicylic acid (SA) is a potent inducer of defense gene expression in plants, but how SA activates transcription has been controversial. In this issue of Cell, Ding et al. show that the SA-binding proteins NPR3 and NPR4 function as transcriptional co-repressors, with this activity being blocked by SA.
Article
This letter describes a newly discovered confounding effect of bacterial titer in a previously published type III delivery-based assay of the fungal effector BEC1019. The original publication has been retracted as a consequence of this discovery. The letter tabulates the affected and unaffected figures and conclusions in the original publication, a...
Article
Extracellular vesicles (EVs) are lipid compartments capable of trafficking proteins, lipids, RNA and metabolites between cells. Plant cells have been shown to secrete EVs during immune responses, but virtually nothing is known about their formation, contents or ultimate function. Recently developed methods for isolating plant EVs have revealed that...
Article
Extracellular vesicles (EVs) play an important role in intercellular communication by transporting proteins and RNA. While plant cells secrete EVs, they have only recently been isolated and questions regarding their biogenesis, release, uptake and function remain unanswered. Here, we present a detailed protocol for isolating EVs from the apoplastic...
Article
Full-text available
Reader Comments The white paper reports the deliberations of a workshop focused on biotic challenges to plant health held in Washington, D.C. in September 2016. Ensuring health of food plants is critical to maintaining the quality and productivity of crops and for sustenance of the rapidly growing human population. There is a close linkage between...
Article
Exosomes are extracellular vesicles (EVs) that play a central role in intercellular signaling in mammals by transporting proteins and small RNAs. Plants are also known to produce EVs, particularly in response to pathogen infection. The contents of plant EVs have not been analyzed, however, and their function is unknown. Here we describe a method fo...
Article
Full-text available
Soybean hosts a wide variety of pathogens that cause significant yield losses. The importance of soybean as a major oilseed crop has led to research focused on its interactions with pathogens, such as Soybean mosaic virus, Pseudomonas syringae, Phytophthora sojae, Phakopsora pachyrhizi, and Heterodera glycines. Pioneering work on soybean's interact...
Article
Improving plant disease responses Disease resistance in plants depends on genes that allow them to recognize when they are infected by a pathogen so that they can mount a timely defense response. Unfortunately, pathogens can often overcome endogenous disease resistance genes by evolving new virulence strategies that escape detection. Kim et al. mod...
Article
Intracellular nucleotide-binding leucine-rich repeat (NLR) receptors play central roles in human and plant innate immunity. In this issue of Cell Host & Microbe, Wang et al. (2015) show that a single plant NLR can detect diverse pathogen effectors by partnering with different scaffolding proteins, which can each recognize distinct effector targets.
Article
Full-text available
Jasmonate (JA) signaling in plants is mediated by the JASMONATE ZIM-DOMAIN (JAZ) proteins that repress the activity of several transcription factors regulating JA-inducible gene expression. The hormone JA-isoleucine triggers the interaction of JAZ repressor proteins with the F-box protein CORONATINE INSENSITIVE1 (COI1), part of a Skp1/Cullin1/F-box...
Article
The interaction of barley, Hordeum vulgare L., with the powdery mildew fungus, Blumeria graminis f. sp. hordei, is a well-developed model to investigate resistance and susceptibility to obligate biotrophic pathogens. The 130-Mb Blumeria genome encodes ca. 540 predicted effectors, which are hypothesized to suppress or induce host processes to promot...
Article
The Pseudomonas syringae effector AvrB triggers a hypersensitive resistance response in Arabidopsis and soybean plants expressing the disease resistance (R) proteins RPM1 and Rpg1b respectively. In Arabidopsis, AvrB induces the host kinase RIPK to phosphorylate a disease regulator known as RIN4, which subsequently activates RPM1-mediated defenses....
Conference Paper
Full-text available
There are 22 additional places for researchers to attend the meeting (registration 350 €, accommodation ~ 350 €). Please send title and abstract (250 words) to Simone Gieraths (gieraths@mpipz.mpg.de) by Feb. 20th 2015 for selection by Feb. 27th 2015. Advanced PhD and postdoctoral scientists are especially encouraged to apply.
Article
Protein palmitoylation is the post-translational modification of proteins via the attachment of palmitate through acyl linkages. The nucleophile sulfhydryl group of cysteines is the common palmitoylation site. Covalent attachment of palmitate occurs on numerous proteins and is usually associated with directing protein localization to the endomembra...
Article
The IC-MPMI was held in Rhodes, Greece from July 6-10, 2014. A new feature of the meeting was the inclusion of a “Student Travel Workshop”. In honor of our late colleague Ko Shimamoto, a student travel fellowship program was initiated to enrich graduate student and postdoctoral participation at this congress. The fellowship program was generously s...
Article
Loss-of-function mutations in the Arabidopsis thaliana ENHANCED DISEASE RESISTANCE1 (EDR1) gene confer enhanced programmed cell death under a variety of abiotic and biotic stress conditions. All edr1 mutant phenotypes can be suppressed by missense mutations in the KEEP ON GOING gene, which encodes a trans-Golgi network/early endosome (TGN/EE)-local...
Article
Full-text available
Rpg1b and Rpg1r are soybean disease resistance (R) genes responsible for conferring resistance to Pseudomonas syringae strains expressing the effectors AvrB and AvrRpm1, respectively. The study of these cloned genes would be greatly facilitated by the availability of a suitable transient expression system. The commonly used Niciotiana benthamiana-b...
Article
Full-text available
In Arabidopsis, the Pseudomonas syringae effector proteins AvrB and AvrRpm1 are both detected by the RPM1 disease resistance (R) protein. In contrast, soybean can distinguish between these effectors, with AvrB and AvrRpm1 being detected by the Rpg1b and Rpg1r R proteins, respectively. We have been using these genes to investigate the evolution of R...
Article
Plant resistance (R) genes are a crucial component in plant defence against pathogens. Although R genes often fail to provide durable resistance in an agricultural context, they frequently persist as long-lived balanced polymorphisms in nature. Standard theory explains the maintenance of such polymorphisms through a balance of the costs and benefit...
Article
Full-text available
The IC-MPMI was held in Rhodes, Greece from July 6-10, 2014. A new feature of the meeting was the inclusion of a "Student Travel Workshop". In honor of our late colleague Ko Shimamoto, a student travel fellowship program was initiated to enrich graduate student and postdoctoral participation at this congress. The fellowship program was generously s...
Article
Full-text available
The recognition of pathogen effector proteins by plants is typically mediated by intracellular receptors belonging to the nucleotide binding-leucine rich repeat (NLR) family. NLR proteins often detect pathogen effector proteins indirectly by detecting modification of their targets. How NLR proteins detect such modifications is poorly understood. To...
Article
Full-text available
Nucleotide-binding domain leucine-rich repeat (NLR) proteins play a central role in the innate immune systems of plants and vertebrates. In plants, NLR proteins function as intracellular receptors that detect pathogen effector proteins directly, or indirectly by recognizing effector-induced modifications to other host proteins. NLR activation trigg...
Article
Full-text available
In plants, the trans-Golgi network and early endosomes (TGN/EE) function as the central junction for major endomembrane trafficking events, including endocytosis and secretion. Here, we demonstrate that the KEEP ON GOING (KEG) protein of Arabidopsis thaliana localizes to the TGN/EE and plays an essential role in multiple intracellular trafficking p...
Article
Full-text available
We used a comparative genomics approach to investigate the evolution of a complex nucleotide-binding (NB)-leucine-rich repeat (LRR) gene cluster found in soybean (Glycine max) and common bean (Phaseolus vulgaris) that is associated with several disease resistance (R) genes of known function, including Rpg1b (for Resistance to Pseudomonas glycinea1b...