A novel biosynthetic gene cluster across the Pantoea species complex is important for pathogenicity in onion

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Authors

Zhao, Mei
Shin, Gi Yoon
Stice, Shaun P.
Bown, Jonathon Luke
Metcalf, William W.
Gitaitis, Ron
Kvitko, Brian
Dutta, Bhabesh

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Volume Title

Publisher

American Phytopathological Society

Abstract

Onion center rot is caused by at least four species of genus Pantoea (P. ananatis, P. agglomerans, P. allii, and P. stewartii subsp. indologenes). Critical onion pathogenicity determinants for P. ananatis were recently described, but whether those determinants are common among other onion-pathogenic Pantoea species remains unknown. In this work, we report onion pathogenicity determinants in P. stewartii subsp. indologenes and P. allii. We identified two distinct secondary metabolite biosynthetic gene clusters present separately in different strains of onion-pathogenic P. stewartii subsp. indologenes. One cluster is similar to the previously described HiVir phosphonate biosynthetic cluster identified in P. ananatis and another is a novel putative phosphonate biosynthetic gene cluster, which we named Halophos. The Halophos gene cluster was also identified in P. allii strains. Both clusters are predicted to be phosphonate biosynthetic clusters based on the presence of a characteristic phosphoenolpyruvate phosphomutase (pepM) gene.The deletion of the pepM gene from either HiVir or Halophos clusters in P. stewartii subsp. indologenes caused loss of necrosis on onion leaves and red onion scales and resulted in significantly lower bacterial populations compared with the corresponding wild-type and complemented strains. Seven (halB to halH) of 11 genes (halA to halK) in the Halophos gene cluster are required for onion necrosis phenotypes. The onion nonpathogenic strain PNA15-2 (P. stewartii subsp. indologenes) gained the capacity to cause foliar necrosis on onion via exogenous expression of a minimal seven-gene Halophos cluster (genes halB to halH). Furthermore, cell-free culture filtrates of PNA14-12 expressing the intact Halophos gene cluster caused necrosis on onion leaves consistent with the presence of a secreted toxin. Based on the similarity of proteins to those with experimentally determined functions, we are able to predict most of the steps in Halophos biosynthesis. Together, these observations indicate that production of the toxin phosphonate seems sufficient to account for virulence of a variety of different Pantoea strains, although strains differ in possessing a single but distinct phosphonate biosynthetic cluster. Overall, this is the first report of onion pathogenicity determinants in P. stewartii subsp. indologenes and P. allii.

Description

Genome sequence data are available in the National Center for Biotechnology Information under the BioProject accession number PRJNA746326. The data that support the findings of this study are available from the corresponding author upon reasonable request.

Keywords

Halophos, HiVir, Pantoea allii, Pantoea stewartii subsp. indologenes, Phosphonate, Toxin, Onion center rot, SDG-02: Zero hunger, SDG-15: Life on land

Sustainable Development Goals

SDG-02:Zero Hunger
SDG-15:Life on land

Citation

Zhao, M., Shin, G.Y., Stice, S. 2023, 'A novel biosynthetic gene cluster across the pantoea species complex Is important for pathogenicity in onion', Molecular Plant-Microbe Interactions, vol. 36, no. 3, pp. 176-188. https://doi.org/10.1094/MPMI-08-22-0165-R.