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Infection by Moniliophthora perniciosa reprograms tomato Micro-Tom physiology, establishes a sink, and increases secondary cell wall synthesis

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Paschoal, Daniele ; Costa, Juliana L. ; da Silva, Eder M. ; da Silva, Fabia B. ; Capelin, Diogo ; Ometto, Vitor ; Aricetti, Juliana A. ; Carvalho, Gabriel G. ; Pimpinato, Rodrigo F. ; de Oliveira, Ricardo F. ; Carrera, Esther ; Lopez-Diaz, Isabel ; Rossi, Monica L. ; Tornisielo, Valdemar ; Caldana, Camila ; Riano-Pachon, Diego M. ; Cesarino, Igor ; Teixeira, Paulo J. P. L. ; Figueira, Antonio
Total Authors: 19
Document type: Journal article
Source: Journal of Experimental Botany; v. 73, n. 11, p. 20-pg., 2022-02-21.
Abstract

Witches' broom disease of cacao is caused by the pathogenic fungus Moniliophthora perniciosa. By using tomato (Solanum lycopersicum) cultivar Micro-Tom (MT) as a model system, we investigated the physiological and metabolic consequences of M. perniciosa infection to determine whether symptoms result from sink establishment during infection. Infection of MT by M. perniciosa caused reductions in root biomass and fruit yield, a decrease in leaf gas exchange, and down-regulation of photosynthesis-related genes. The total leaf area and water potential decreased, while ABA levels, water conductance/conductivity, and ABA-related gene expression increased. Genes related to sugar metabolism and those involved in secondary cell wall deposition were up-regulated upon infection, and the concentrations of sugars, fumarate, and amino acids increased. C-14-glucose was mobilized towards infected MT stems, but not in inoculated stems of the MT line overexpressing CYTOKININ OXIDASE-2 (35S::AtCKX2), suggesting a role for cytokinin in establishing a sugar sink. The up-regulation of genes involved in cell wall deposition and phenylpropanoid metabolism in infected MT, but not in 35S::AtCKX2 plants, suggests establishment of a cytokinin-mediated sink that promotes tissue overgrowth with an increase in lignin. Possibly, M. perniciosa could benefit from the accumulation of secondary cell walls during its saprotrophic phase of infection. Infection by Moniliophthora perniciosaof tomato Micro-Tom induces a cytokinin-mediated nutrient sink at the stem and leads to vascular overgrowth and accumulation of secondary cell wall. (AU)

FAPESP's process: 13/04309-6 - Functional analysis of cacao signalling and defense genes in the interaction Moniliophthora perniciosa x Solanum lycopersicum
Grantee:Juliana Leles Costa
Support Opportunities: Scholarships in Brazil - Doctorate
FAPESP's process: 17/17000-4 - Analysis of the interaction Moniliophthora perniciosa x 'Micro-Tom' tomato: non-host type resistance, effects on the development and role of phytohormones in pathogenesis
Grantee:Eder Marques da Silva
Support Opportunities: Scholarships in Brazil - Post-Doctoral
FAPESP's process: 16/10498-4 - Investigation of strategies of adaptation to the pathogenic life style of fungi from the Moniliophthora genus at various levels of biological organizations: species, biotypes, and geographic lineages
Grantee:Antonio Vargas de Oliveira Figueira
Support Opportunities: Research Projects - Thematic Grants
FAPESP's process: 16/10524-5 - Transcriptional profile characterization in the Moniliophthora perniciosa x Solanum lycopersicum interaction
Grantee:Juliana Leles Costa
Support Opportunities: Scholarships abroad - Research Internship - Doctorate
FAPESP's process: 18/18711-4 - Functional analysis of genes potentially associated with resistance to the basidiomycete Moniliophthora perniciosa in tomato (Solanum lycopersicum) cv. 'Micro-Tom'
Grantee:Daniele Paschoal
Support Opportunities: Scholarships in Brazil - Doctorate