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

Agradecimentos: The authors are grateful for the assistance of Dr Lauro Tatsuo Kubota and Dr Jailson Cardoso Dias in the chromatographic detection and analysis of carbohydrates of cacao apoplastic fluid, and Marcelo Carazzolle, Osvaldo Reis Junior, and Gustavo Gilson Lacerda Costa for the bioinformatics support and management of databases consulted in the conduct of this work. This work was financially supported by CNPq (472710/2008-7) and FAPESP (2006/56942-0, 2009/17507-5, and 2009/50119-9). The authors declare no conflicts of interest 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 CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO - CNPQ FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP Fechado