TY - JOUR
T1 - A phosphonate natural product made by pantoea ananatis is necessary and sufficient for the hallmark lesions of onion center rot
AU - Polidore, Alexander L.A.
AU - Furiassi, Lucia
AU - Hergenrother, Paul J.
AU - Metcalf, William W.
N1 - Funding Information:
We thank T. Stack, C. Ting, and X. Guan for helpful discussions and assistance with NMR experiments, H. Yao (School of Chemical Sciences Mass Spectrometry Lab, UIUC) for HRMS experiments, the UIUC Core Sequencing Facility for sequencing, and M. Burke (Chemistry Department, UIUC) and J. Imlay (Microbiology Department, UIUC) for providing fungal strains. We would especially like the thank J. Zhang for training on the fungicide assays. This work was funded by the National Institutes of Health (grant no. R01 GM127659 to W.W.M.). The NMR spectra were recorded on an instrument purchased with support from NIH grant S10 RR028833. Experiments were designed and planned by W.W.M. and A.L.A.P. Bioinformatics analyses, molecular genetics, compound purifications, structural analyses, and plant and microorganism bioactivity assays were performed by A.L.A.P. Human cell line bioactivity screening was performed by L.F. Data were analyzed and manuscript written by A.L.A.P. and W.W.M. W.W.M. is coowner and cofounder of the natural products discovery company MicroMgx.
Funding Information:
This work was funded by the National Institutes of Health (grant no. R01 GM127659 to W.W.M.). The NMR spectra were recorded on an instrument purchased with support from NIH grant S10 RR028833.
Publisher Copyright:
© 2021 Polidore et al.
PY - 2021/2
Y1 - 2021/2
N2 - Pantoea ananatis is the primary cause of onion center rot. Genetic data suggest that a phosphonic acid natural product is required for pathogenesis; however, the nature of the molecule is unknown. Here, we show that P. ananatis produces at least three phosphonates, two of which were purified and structurally characterized. The first, designated pantaphos, was shown to be 2-(hydroxy[phosphono] methyl)maleate; the second, a probable biosynthetic precursor, was shown to be 2(phosphonomethyl)maleate. Purified pantaphos is both necessary and sufficient for the hallmark lesions of onion center rot. Moreover, when tested against mustard seedlings, the phytotoxic activity of pantaphos was comparable to the widely used herbicides glyphosate and phosphinothricin. Pantaphos was also active against a variety of human cell lines but was significantly more toxic to glioblastoma cells. Pantaphos showed little activity when tested against a variety of bacteria and fungi. IMPORTANCE Pantoea ananatis is a significant plant pathogen that targets a number of important crops, a problem that is compounded by the absence of effective treatments to prevent its spread. Our identification of pantaphos as the key virulence factor in onion center rot suggests a variety of approaches that could be employed to address this significant plant disease. Moreover, the general phytotoxicity of the molecule suggests that it could be developed into an effective herbicide to counter the alarming rise in herbicide-resistant weeds.
AB - Pantoea ananatis is the primary cause of onion center rot. Genetic data suggest that a phosphonic acid natural product is required for pathogenesis; however, the nature of the molecule is unknown. Here, we show that P. ananatis produces at least three phosphonates, two of which were purified and structurally characterized. The first, designated pantaphos, was shown to be 2-(hydroxy[phosphono] methyl)maleate; the second, a probable biosynthetic precursor, was shown to be 2(phosphonomethyl)maleate. Purified pantaphos is both necessary and sufficient for the hallmark lesions of onion center rot. Moreover, when tested against mustard seedlings, the phytotoxic activity of pantaphos was comparable to the widely used herbicides glyphosate and phosphinothricin. Pantaphos was also active against a variety of human cell lines but was significantly more toxic to glioblastoma cells. Pantaphos showed little activity when tested against a variety of bacteria and fungi. IMPORTANCE Pantoea ananatis is a significant plant pathogen that targets a number of important crops, a problem that is compounded by the absence of effective treatments to prevent its spread. Our identification of pantaphos as the key virulence factor in onion center rot suggests a variety of approaches that could be employed to address this significant plant disease. Moreover, the general phytotoxicity of the molecule suggests that it could be developed into an effective herbicide to counter the alarming rise in herbicide-resistant weeds.
KW - Biosynthesis
KW - Herbicide
KW - Natural products
KW - Onion
KW - Pantoea
KW - Phosphonate
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U2 - 10.1128/mBio.03402-20
DO - 10.1128/mBio.03402-20
M3 - Article
C2 - 33531390
AN - SCOPUS:85100265856
SN - 2161-2129
VL - 12
SP - 1
EP - 18
JO - mBio
JF - mBio
IS - 1
M1 - e03402-20
ER -