Apoplastic and intracellular plant sugars regulate developmental transitions in witches' broom disease of cacao

Author(s)

Barau, Joan ^[1] ; Grandis, Adriana ^[2] ; de Andrade Carvalho, Vinicius Miessler ^[1] ; Teixeira, Gleidson Silva ^[1] ; Alcala Zaparoli, Gustavo Henrique ^[1] ; Scatolin do Rio, Maria Carolina ^[1] ; Rincones, Johana ^[1] ; Buckeridge, Marcos Silveira ^[2] ; Guimaraes Pereira, Goncalo Amarante ^[1]

Affiliation

^[1] Univ Estadual Campinas Unicamp, Inst Biol, Dept Genet Evolucao & Bioagentes, Lab Genom & Expressao, BR-13083970 Campinas, SP - Brazil

^[2] Univ Sao Paulo, Inst Biociencias, Dept Bot, Lab Fisiol Ecol Plantas, BR-05508090 Sao Paulo, SP - Brazil

• Document type: Journal article
• Source: Journal of Experimental Botany; v. 66, n. 5, p. 1325-1337, MAR 2015.
• Web of Science Citations: 7

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. (AU)

• FAPESP's process: 09/50119-9 - Integrated and comparative study of three fungal diseases of cacao: witches' broom, frosty pod rot and brown-rot, aiming at understanding the pathogenic mechanisms for the development of control strategies
• Grantee: Gonçalo Amarante Guimarães Pereira
• Support Opportunities: Research Projects - Thematic Grants