Accumulation of the Mycotoxin Patulin in the Presence of Gluconic Acid Contributes to Pathogenicity of Penicillium expansum

Abstract

Penicillium expansum, the causal agent of blue mold rot, causes severe postharvest fruit maceration through secretion of D-gluconic acid (GLA) and secondary metabolites such as the mycotoxin patulin in colonized tissue. GLA involvement in pathogenicity has been suggested but the mechanism of patulin accumulation and its contribution to P. expansum pathogenicity remain unclear. The roles of GLA and patulin accumulation in P. expansum pathogenicity were studied using i) glucose oxidase GOX2-RNAi mutants exhibiting decreased GOX2 expression, GLA accumulation, and reduced pathogenicity; ii) IDH-RNAi mutants exhibiting downregulation of IDH (the last gene in patulin biosynthesis), reduced patulin accumulation, and no effect on GLA level; and iii) PACC-RNAi mutants exhibiting downregulation of both GOX2 and IDH that reduced GLA and patulin production. Present results indicate that conditions enhancing the decrease in GLA accumulation by GOX2-RNAi and PACC-RNAi mutants, and not low pH, affected patulin accumulation, suggesting GLA production as the driving force for further patulin accumulation. Thus, it is suggested that GLA accumulation may modulate patulin synthesis as a direct precursor under dynamic pH conditions modulating the activation of the transcription factor PACC and the consequent pathogenicity factors, which contribute to host-tissue colonization by P. expansum.

How Does Host Carbon Concentration Modulate the Lifestyle of Postharvest Pathogens during Colonization?

“…The results obtained under acidification and alkalization conditions are consistent with the observation that ΔpacC mutants of C. gloeosporioides, C. acutatum, F. oxysporum, P. expansum , and S. sclerotiorum are less virulent than the wild type (Caracuel et al, 2003a; Rollins, 2003; You et al, 2007; Miyara et al, 2008; Zhang et al, 2013; Barad et al, 2014). This suggests the importance of gene regulation by PacC in acidifying and alkalizing pathogens.…”

“…S. sclerotiorum and B. cinerea decrease host pH by secreting significant amounts of oxalic acid (OA; Rollins and Dickman, 2001; Manteau et al, 2003); gluconic acid (GLA) is secreted by Phomopsis mangiferae (Davidzon et al, 2010), and combinations of gluconic and citric acids are mainly secreted by Penicillium (Prusky et al, 2004) and Aspergillus (Ruijter et al, 1999). In P. expansum , reduced GLA accumulation has been related to reduced pathogenicity (Barad et al, 2014). …”

Biocontrol Agents Increase the Specific Rate of Patulin Production by Penicillium expansum but Decrease the Disease and Total Patulin Contamination of Apples

“…The assessment of the role of PAT in the interaction between apple and P. expansum is beyond the scope of the present study. However, this role has recently been a matter of debate (Sanzani et al, 2012; Barad et al, 2014; Ballester et al, 2015; Li et al, 2015). Our results seem to suggest that PAT could be involved in the aggressiveness of P. expansum (defined as the disease incidence and development of symptoms rather than the fungal biomass growth).…”

PCPPI: a comprehensive database for the prediction of Penicillium–crop protein–protein interactions

“…GOX2 , IDH ) have been reported to be involved in the initial signaling cascades that stimulate the growth of P. expansum on crops (10, 11). Although these enzymes may have a role in pathogenicity, there is evidence that more complex interactions are taking place during the initial stages of infection and diseases development (10).…”

“…GOX2 , IDH ) have been reported to be involved in the initial signaling cascades that stimulate the growth of P. expansum on crops (10, 11). Although these enzymes may have a role in pathogenicity, there is evidence that more complex interactions are taking place during the initial stages of infection and diseases development (10). To facilitate an effective approach for studying such complex interactions, bioinformatics has been suggested and employed to study the protein interaction networks at a genome-wide scale (12).…”