title: Carbon regulation of environmental pH by secreted small molecules that modulate pathogenicity in phytopathogenic fungi.
abstract: Fruit pathogens can contribute to the acidification or alkalinization of the host environment. This capability has been used to divide fungal pathogens into acidifying and/or alkalinizing classes. Here, we show that diverse classes of fungal pathogens-Colletotrichum gloeosporioides, Penicillium expansum, Aspergillus nidulans and Fusarium oxysporum-secrete small pH-affecting molecules. These molecules modify the environmental pH, which dictates acidic or alkaline colonizing strategies, and induce the expression of PACC-dependent genes. We show that, in many organisms, acidification is induced under carbon excess, i.e. 175 mm sucrose (the most abundant sugar in fruits). In contrast, alkalinization occurs under conditions of carbon deprivation, i.e. less than 15 mm sucrose. The carbon source is metabolized by glucose oxidase (gox2) to gluconic acid, contributing to medium acidification, whereas catalysed deamination of non-preferred carbon sources, such as the amino acid glutamate, by glutamate dehydrogenase 2 (gdh2), results in the secretion of ammonia. Functional analyses of Δgdh2 mutants showed reduced alkalinization and pathogenicity during growth under carbon deprivation, but not in high-carbon medium or on fruit rich in sugar, whereas analysis of Δgox2 mutants showed reduced acidification and pathogencity under conditions of excess carbon. The induction pattern of gdh2 was negatively correlated with the expression of the zinc finger global carbon catabolite repressor creA. The present results indicate that differential pH modulation by fruit fungal pathogens is a host-dependent mechanism, affected by host sugar content, that modulates environmental pH to enhance fruit colonization.
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.|Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, and Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, China.
authors.forename: Fangcheng
authors.initials: F
authors.lastname: Bi
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.|Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
authors.forename: Shiri
authors.initials: S
authors.lastname: Barad
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Dana
authors.initials: D
authors.lastname: Ment
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Neta
authors.initials: N
authors.lastname: Luria
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Amit
authors.initials: A
authors.lastname: Dubey
authors.affiliation: Department of Microbiology and Genetics, CIALE, Universidad de Salamanca, Salamanca, 37007, Spain.
authors.forename: Virginia
authors.initials: V
authors.lastname: Casado
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel.|Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
authors.forename: Nofar
authors.initials: N
authors.lastname: Glam
authors.affiliation: Department of Microbiology and Genetics, CIALE, Universidad de Salamanca, Salamanca, 37007, Spain.
authors.forename: Jose Diaz
authors.initials: JD
authors.lastname: Mínguez
authors.affiliation: Department of Molecular and Cellular Biology, Centro de Investigaciones Biológicas (C.I.B.), Madrid, 28040, Spain.
authors.forename: Eduardo A
authors.initials: EA
authors.lastname: Espeso
authors.affiliation: Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, 76100, Israel.
authors.forename: Robert
authors.initials: R
authors.lastname: Fluhr
authors.affiliation: Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel. dovprusk@volcani.agri.gov.il.
authors.forename: Dov
authors.initials: D
authors.lastname: Prusky
mesh_terms: D000468:Alkalies / Q000378:metabolism; D002244:Carbon / Q000378:metabolism*; D004777:Environment; D005110:Extracellular Space / Q000378:metabolism; D005638:Fruit / Q000382:microbiology; D005658:Fungi / Q000235:genetics / Q000378:metabolism* / Q000472:pathogenicity*; D015966:Gene Expression Regulation, Fungal; D006863:Hydrogen-Ion Concentration; D055442:Metabolome / Q000235:genetics
chemical_list: D000468:Alkalies; D002244:Carbon
keywords: carbon regulation of pathogenicity; pH regulation; pathogenicity