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

Joan Barau,Johana Rincones,Maria Carolina Scatolin Do Rio,Adriana Grandis,Vinicius Miessler De Andrade Carvalho,Gleidson Silva Teixeira,Marcos Silveira Buckeridge,Gonçalo Amarante Guimarães Pereira,Gustavo Henrique Alcalá Zaparoli

doi:10.1093/jxb/eru485

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.

Highlights

Nutrition is a key component of the trade-offs involved in the evolution of parasitism, and this importance is highlighted by the remarkable diversity of strategies that parasites exploit in order to feed at their host’s expense (Newton et al, 2010; Olson et al, 2012)
In order to obtain a view of the soluble carbon sources available to M. perniciosa in the apoplast during infection, quantitative analysis was performed in a time course experiment spanning the whole biotrophic and the initial transition to the necrotrophic phase of Witches’ broom disease (WBD) in cacao seedlings
Apoplastic soluble sugars in the rhythmic growth of cacao and WBD development Aiming for the characterization of the carbohydrates available for M. perniciosa in the apoplastic fluid of cacao, a concentration pattern that matched the periodic growth of healthy cacao seedlings was unexpectedly found (Fig. 1A, C; Supplementary Fig. S3 at JXB online)

Summary

Introduction

Nutrition is a key component of the trade-offs involved in the evolution of parasitism, and this importance is highlighted by the remarkable diversity of strategies that parasites exploit in order to feed at their host’s expense (Newton et al, 2010; Olson et al, 2012). Hemibiotrophs present features of both strategies, initially deriving nutrients from living plant tissues, and requiring host cell death to grow and complete their life cycle (Munch et al, 2008). This short-term colonization of living tissues requires interaction-specific. This allowed the in vivo testing of the hypothesis that phase transition is prompted by carbon availability, followed by a stepwise collection of further physiological and molecular data depicting in unprecedented spatial–temporal detail the complex relationships of carbohydrate metabolism and WBD developmental transitions

Materials and methods

Results

Discussion