title: Apoplastic and intracellular plant sugars regulate developmental transitions in witches' broom disease of cacao.
abstract: Witches' broom disease (WBD) of cacao differs from other typical hemibiotrophic plant diseases by its unusually long biotrophic phase. Plant carbon sources have been proposed to regulate WBD developmental transitions; however, nothing is known about their availability at the plant-fungus interface, the apoplastic fluid of cacao. Data are provided supporting a role for the dynamics of soluble carbon in the apoplastic fluid in prompting the end of the biotrophic phase of infection. Carbon depletion and the consequent fungal sensing of starvation were identified as key signalling factors at the apoplast. MpNEP2, a fungal effector of host necrosis, was found to be up-regulated in an autophagic-like response to carbon starvation in vitro. In addition, the in vivo artificial manipulation of carbon availability in the apoplastic fluid considerably modulated both its expression and plant necrosis rate. Strikingly, infected cacao tissues accumulated intracellular hexoses, and showed stunted photosynthesis and the up-regulation of senescence markers immediately prior to the transition to the necrotrophic phase. These opposite findings of carbon depletion and accumulation in different host cell compartments are discussed within the frame of WBD development. A model is suggested to explain phase transition as a synergic outcome of fungal-related factors released upon sensing of extracellular carbon starvation, and an early senescence of infected tissues probably triggered by intracellular sugar accumulation.
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Joan
authors.initials: J
authors.lastname: Barau
authors.affiliation: Laboratório de Fisiologia Ecológica de Plantas, Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo-USP, CP 11461, Rua do Matão 277, São Paulo-SP, CEP 05508-090, Brazil.
authors.forename: Adriana
authors.initials: A
authors.lastname: Grandis
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Vinicius Miessler de Andrade
authors.initials: VM
authors.lastname: Carvalho
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Gleidson Silva
authors.initials: GS
authors.lastname: Teixeira
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Gustavo Henrique Alcalá
authors.initials: GH
authors.lastname: Zaparoli
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Maria Carolina Scatolin
authors.initials: MC
authors.lastname: do Rio
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil.
authors.forename: Johana
authors.initials: J
authors.lastname: Rincones
authors.affiliation: Laboratório de Fisiologia Ecológica de Plantas, Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo-USP, CP 11461, Rua do Matão 277, São Paulo-SP, CEP 05508-090, Brazil.
authors.forename: Marcos Silveira
authors.initials: MS
authors.lastname: Buckeridge
authors.affiliation: Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas-UNICAMP, CP 6109, Campinas-SP, CEP 13083-970, Brazil goncalo@unicamp.br.
authors.forename: Gonçalo Amarante Guimarães
authors.initials: GA
authors.lastname: Pereira
mesh_terms: D000363:Agaricales / Q000502:physiology*; D002099:Cacao / Q000166:cytology / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D006601:Hexoses / Q000378:metabolism*; D015388:Organelles / Q000235:genetics / Q000378:metabolism*; D010788:Photosynthesis; D010935:Plant Diseases / Q000382:microbiology*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism
chemical_list: D006601:Hexoses; D010940:Plant Proteins
keywords: Autophagy; Moniliophthora perniciosa; Theobroma cacao.; hemibiotrophic; senescence; starvation