Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

• Published in: Environmental microbiology 2018-04, Vol.20 (4), p.1330-1349
• Main Authors: Lowe‐Power, Tiffany M., Hendrich, Connor G., von Roepenack‐Lahaye, Edda, Li, Bin, Wu, Dousheng, Mitra, Raka, Dalsing, Beth L., Ricca, Patrizia, Naidoo, Jacinth, Cook, David, Jancewicz, Amy, Masson, Patrick, Thomma, Bart, Lahaye, Thomas, Michael, Anthony J., Allen, Caitilyn
• Format: Article
• Language: English
• Subjects: Abundance; Carbon sources; Diseases; EPS; Inoculation; Laboratorium voor Fytopathologie; Laboratorium voor Phytopathologie; Laboratory of Phytopathology; Lycopersicon esculentum - microbiology; Metabolites; Metabolomics; Mineral nutrients; Nitrogen sources; Nutrient content; Nutrients; Ornithine; Ornithine decarboxylase; Plant bacterial diseases; Plant Diseases - microbiology; Putrescine; Putrescine - metabolism; Ralstonia solanacearum; Ralstonia solanacearum - metabolism; Ralstonia solanacearum - pathogenicity; Tomatoes; Virulence; Virulence Factors - metabolism; Wilt; Xylem; Xylem - metabolism; Xylem - microbiology
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.14020

Summary Ralstonia solanacearum thrives in plant xylem vessels and causes bacterial wilt disease despite the low nutrient content of xylem sap. We found that R. solanacearum manipulates its host to increase nutrients in tomato xylem sap, enabling it to grow better in sap from infected plants than in sap from healthy plants. Untargeted GC/MS metabolomics identified 22 metabolites enriched in R. solanacearum‐infected sap. Eight of these could serve as sole carbon or nitrogen sources for R. solanacearum. Putrescine, a polyamine that is not a sole carbon or nitrogen source for R. solanacearum, was enriched 76‐fold to 37 µM in R. solanacearum‐infected sap. R. solanacearum synthesized putrescine via a SpeC ornithine decarboxylase. A ΔspeC mutant required ≥ 15 µM exogenous putrescine to grow and could not grow alone in xylem even when plants were treated with putrescine. However, co‐inoculation with wildtype rescued ΔspeC growth, indicating R. solanacearum produced and exported putrescine to xylem sap. Intriguingly, treating plants with putrescine before inoculation accelerated wilt symptom development and R. solanacearum growth and systemic spread. Xylem putrescine concentration was unchanged in putrescine‐treated plants, so the exogenous putrescine likely accelerated disease indirectly by affecting host physiology. These results indicate that putrescine is a pathogen‐produced virulence metabolite.