title: Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves in mono- and dicotyledonous plants.
abstract: Microbes emit volatile compounds that affect plant growth and development. However, little or nothing is known about how microbial emissions may affect primary carbohydrate metabolism in plants. In this work we explored the effect on leaf starch metabolism of volatiles released from different microbial species ranging from Gram-negative and Gram-positive bacteria to fungi. Surprisingly, we found that all microbial species tested (including plant pathogens and species not normally interacting with plants) emitted volatiles that strongly promoted starch accumulation in leaves of both mono- and dicotyledonous plants. Starch content in leaves of plants treated for 2 d with microbial volatiles was comparable with or even higher than that of reserve organs such as potato tubers. Transcriptome and enzyme activity analyses of potato leaves exposed to volatiles emitted by Alternaria alternata revealed that starch overaccumulation was accompanied by up-regulation of sucrose synthase, invertase inhibitors, starch synthase class III and IV, starch branching enzyme and glucose-6-phosphate transporter. This phenomenon, designated as MIVOISAP (microbial volatiles-induced starch accumulation process), was also accompanied by down-regulation of acid invertase, plastidial thioredoxins, starch breakdown enzymes, proteins involved in internal amino acid provision and less well defined mechanisms involving a bacterial- type stringent response. Treatment of potato leaves with fungal volatiles also resulted in enhanced levels of sucrose, ADPglucose, UDPglucose and 3-phosphoglycerate. MIVOISAP is independent of the presence of sucrose in the culture medium and is strongly repressed by cysteine supplementation. The discovery that microbial volatiles trigger starch accumulation enhancement in leaves constitutes an unreported mechanism for the elicidation of plant carbohydrate metabolism by microbes.
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Mutiloako etorbidea z/g, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Ignacio
authors.initials: I
authors.lastname: Ezquer
authors.forename: Jun
authors.initials: J
authors.lastname: Li
authors.forename: Miroslav
authors.initials: M
authors.lastname: Ovecka
authors.forename: Edurne
authors.initials: E
authors.lastname: Baroja-Fernández
authors.forename: Francisco José
authors.initials: FJ
authors.lastname: Muñoz
authors.forename: Manuel
authors.initials: M
authors.lastname: Montero
authors.forename: Jessica
authors.initials: J
authors.lastname: Díaz de Cerio
authors.forename: Maite
authors.initials: M
authors.lastname: Hidalgo
authors.forename: María Teresa
authors.initials: MT
authors.lastname: Sesma
authors.forename: Abdellatif
authors.initials: A
authors.lastname: Bahaji
authors.forename: Ed
authors.initials: E
authors.lastname: Etxeberria
authors.forename: Javier
authors.initials: J
authors.lastname: Pozueta-Romero
mesh_terms: D000528:Alternaria / Q000737:chemistry*; D001419:Bacteria / Q000737:chemistry*; D050260:Carbohydrate Metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D018515:Plant Leaves / Q000378:metabolism*; D010940:Plant Proteins / Q000378:metabolism; D035281:Plant Tubers / Q000378:metabolism; D018749:RNA, Plant / Q000378:metabolism; D011198:Solanum tuberosum / Q000378:metabolism*; D013213:Starch / Q000032:analysis / Q000096:biosynthesis*; D055549:Volatile Organic Compounds / Q000494:pharmacology*
chemical_list: D010940:Plant Proteins; D018749:RNA, Plant; D055549:Volatile Organic Compounds; D013213:Starch