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Title: The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development

item THOMAZELLA, DANIELA - Universidade De Campinas (UNICAMP)
item TEIXEIRA, PAULA JOSE - Universidade De Campinas (UNICAMP)
item DE OLIVEIRA, HALLEY CAIXETA - Universidade De Campinas (UNICAMP)
item SAVIANI, ELIZIRA - Universidade De Campinas (UNICAMP)
item RINCONES, JOHANA - Universidade De Campinas (UNICAMP)
item TONI, ISABELA - Universidade De Campinas (UNICAMP)
item OSVALDO, REIS - Universidade De Campinas (UNICAMP)
item GARCIA, ODALYS - Universidade De Campinas (UNICAMP)
item Meinhardt, Lyndel
item SALGADO, IONE - Universidade De Campinas (UNICAMP)
item PEREIRA, GONCALO - Universidade De Campinas (UNICAMP)

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/11/2012
Publication Date: 3/23/2012
Citation: Thomazella, D.P., Teixeira, P., De Oliveira, H., Saviani, E., Rincones, J., Toni, I., Osvaldo, R., Garcia, O., Meinhardt, L.W., Salgado, I., Pereira, G.A. 2012. The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development. New Phytologist. 194(4):1025-1034.

Interpretive Summary: Cacao (Theobroma cacao) is a tropical commodity and is economically important as the source of chocolate. Fungal diseases limit the production of cacao in many countries around the world. To understand one of these diseases (witches broom disease) and attempt to reduce yield loses, we studied how the fungus survives in the plant. We discovered that the mitochondria (which is the organelle that generated the energy for the fungus) has a special protein (AOX) that allows it to survive plant defenses. When this protein is inhibited the fungus stops growing. Tests showed that when the inhibitor of this protein is sprayed onto plants prior to infection, the disease is prevented. These findings will provide researchers with new protein targets in a number of fungal pathogens that can be used to develop new fungicides and/or new control methods. This research will benefit researchers, extension personnel, and ultimately farmers around the world.

Technical Abstract: The mitochondrial alternative oxidase (AOX) is a non-energy conserving ubiquinol oxidase found in most fungal genomes studied to date. With the development of fungicides containing cytochrome-dependent respiratory chain (CRC) inhibitors, a strong interest in studying AOX functions in phytopathogenic fungi has arisen. Here, we report the characterization of an aox gene (Mp-aox) identified in the genome of the hemibiotrophic fungus Moniliophthora perniciosa, which causes one of the most devastating diseases of cacao, the Witches’ Broom Disease (WBD). In the biotrophic (infective) phase, M. perniciosa showed an increased expression of Mp-aox gene, as well as a high sensitivity to AOX inhibitors. Interestingly, the in vitro transition from the biotrophic to the necrotrophic phase of this fungus could be prevented by inhibition of the CRC pathway with the fungicide azoxystrobin. Thereby, we propose AOX might play a role during the development of the biotrophic mycelium and, consequently, during the primary stage of WBD. Considering that a burst of nitric oxide (NO) was detected at the beginning of WBD, we speculated that the maintenance of the biotrophic phase in planta may be dependent on the inhibitory effects of NO on the cytochrome respiratory pathway. Finally, we verified that the application of an AOX inhibitor with the CRC inhibitor azoxystrobin impaired the in vitro growth of M. perniciosa as well as the WBD development in cacao seedlings. These results point to AOX as a key target to disrupt the hemibiotrophic cycle of this fungus and AOX inhibitors as promising molecules to control WBD.