Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Groen, Simon C.; Humphrey, Parris T.; Chevasco, Daniela; Ausubel, Frederick M.; Pierce, Naomi E.; Whiteman, Noah K.

doi:10.1016/j.jinsphys.2015.07.011

Cited by 24 publications

(13 citation statements)

References 125 publications

(266 reference statements)

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“…Trophic depletion of 15 N has been observed in fluid-feeding herbivorous insects (34,35) , but it is inconsistent with a diet consisting primarily of plant-associated microbes. Our finding that S. flava primarily derives nutrients from living plant tissue is further supported by previous findings that larval feeding and growth rates are not directly enhanced by elevated bacterial loads in their diet, although larvae do benefit indirectly through bacterial suppression of plant defenses (36) . Overall, these experiments show that S. flava is an obligate herbivore that consumes and acquires nutrients from living plant tissue.…”

Section: An Obligately Herbivorous Drosophilidsupporting

confidence: 89%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

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SIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly ( Drosophila melanogaste r), the "wasabi fly" ( Scaptomyza flava ), that evolved to consume mustard plants including Arabidopsis thaliana . The yeast-to-mustard dietary transition remodeled the fly's gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals. Gloss et al. 2019 1ABSTRACT One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana ) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila . We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains ("blooms") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase ( Gst ) and cytochrome P450 ( Cyp450 ) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1 ) and Gst (N=5 for GstE5-8 ) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro . One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis , helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

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Section: An Obligately Herbivorous Drosophilidsupporting

confidence: 89%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

Self Cite

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“…Differential coexpression analysis can boost the study of plant immune response-related transcriptomics and provide new insights into deciphering the molecular mechanisms of plant-pathogen interactions (Jiang et al, 2016). More qualitative studies has the potential to give further insights into the synergistic effects of ROS and GSL metabolites in view of improving plant immunity (Groen et al, 2015;Groen et al, 2013;Gloss et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

“…Brader et al (2006) showed that Arabidopsis, which expresses the sorghum gene CYP79A1, endogenous CYP79A2 gene or benzyl GSL respectively, showed increased resistance towards PSM. Using a series of physiological and genetic tools, Groen et al (2015) showed that PSM enhances the feeding of infected plant parts by the herbivore, Scaptomyza flava partly by suppressing anti-herbivore defense mechanisms triggered by ROS burst. Stahl et al (2016) showed that indol-3ylmethylamine (I3A) was one of the three major accumulating compounds and is also produced via IGSL breakdown by pathways dependent and independent of the myrosinase PEN2.…”

Section: Phytophthora Brassicae De Cock and Man In't Veldmentioning

confidence: 99%

Progress and prospects of glucosinolate pathogen resistance in some brassica plants

Evivie

Ogwu

Cang

et al. 2019

JANS

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Plants are constantly defending themselves against an array of assaults by pathogenic organisms. This has led to the evolution of precise and elaborate chemical defense systems involving glucosinolates (GSLs) in cruciferous plants. These GSLs and their hydrolysis products are biologically active and are implicated as enabling formidable plant defense processes in certain economically important members of Brassicaceae like broccoli, cabbage and mustard seed. This review provides a comprehensive report of how indole and aliphatic GSLs mitigate incidents of plant pathogenesis. By evaluating the roles of GSLs in plant-pathogen interaction of some brassica plants, this review highlights the associated mechanism that culminates in disease suppression. Moreover, seven economically important brassica pathogens were reviewed in terms of their ability to disrupt proper plant functioning as well as the mechanisms by which GSLs and their hydrolysis products in Brassica lower the susceptibility to them. Future perspectives of the application of GSLs in plant pathogen resistance using advanced molecular techniques are also discussed.

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“…Insects could be an especially important species pool to consider as certain insects, including Scaptomyza spp. and Mamestra brassicae, have been reported to vector bacteria between plants as they feed on leaves (58,70). Honeybee species have been shown to have LAB in their intestinal tracts (59), and although bees do not usually feed on leaves, they could have other interactions with plant leaves that might transfer bacteria into the phyllosphere.…”

Section: Discussionmentioning

confidence: 99%

Establishment Limitation Constrains the Abundance of Lactic Acid Bacteria in the Napa Cabbage Phyllosphere

Miller

Kearns

Niccum

et al. 2019

Appl Environ Microbiol

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Patterns of phyllosphere diversity have become increasingly clear with high-throughput sequencing surveys, but the processes that control phyllosphere diversity are still emerging. Through a combination of lab and field experiments using Napa cabbage and lactic acid bacteria (LAB), we examined how dispersal and establishment processes shape the ecological distributions of phyllosphere bacteria. We first determined the abundance and diversity of LAB on Napa cabbage grown at three sites using both culture-based approaches and 16S rRNA gene amplicon sequencing. Across all sites, LAB made up less than 0.9% of the total bacterial community abundance. To assess whether LAB were low in abundance in the Napa cabbage phyllosphere due to a limited abundance in local species pools (source limitation), we quantified LAB in leaf and soil samples across 51 vegetable farms and gardens throughout the northeastern United States. Across all sites, LAB comprised less than 3.2% of the soil bacterial communities and less than 1.6% of phyllosphere bacterial communities. To assess whether LAB are unable to grow in the phyllosphere even if they dispersed at high rates (establishment limitation), we used a gnotobiotic Napa cabbage system in the lab with experimental communities mimicking various dispersal rates of LAB. Even at high dispersal rates, LAB became rare or completely undetectable in experimental communities, suggesting that they are also establishment limited. Collectively, our data demonstrate that the low abundance of LAB in phyllosphere communities may be explained by establishment limitation. IMPORTANCE The quality and safety of vegetable fermentations are dependent on the activities of LAB naturally present in the phyllosphere. Despite their critical role in determining the success of fermentation, the processes that determine the abundance and diversity of LAB in vegetables used for fermentation are poorly characterized. Our work demonstrates that the limited ability of LAB to grow in the cabbage phyllosphere environment may constrain their abundance on cabbage leaves. These results suggest that commercial fermentation of Napa cabbage proceeds despite low and variable abundances of LAB across different growing regions. Propagule limitation may also explain ecological distributions of other rare members of phyllosphere microbes.

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Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Cited by 24 publications

References 125 publications

Evolution of herbivory remodels aDrosophilagenome

Evolution of herbivory remodels aDrosophilagenome

Progress and prospects of glucosinolate pathogen resistance in some brassica plants

Establishment Limitation Constrains the Abundance of Lactic Acid Bacteria in the Napa Cabbage Phyllosphere

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