Effect of ripeness on host-pathogen interactions of Penicillium spp. on stone fruits

Abstract

Stone fruits are susceptible to numerous postharvest pathogens. Penicillium expansum is a well-known concern to industry. Little information is available on other Penicillium spp. that cause decay of stone fruits. Pathogenicity of P. digitatum was recently described on pome fruits. Decay was associated with older fruit and specific cultivars. Preliminary trials revealed similarities on plum and nectarine. This led us to question the current understanding of pathogenicity and host specificity. Very little is known of the host-pathogen interactions of Penicillium spp. on stone fruits and less with regards to host ripeness. This study aimed to determine the pathogenicity of different Penicillium spp. on various nectarine and plum cultivars and further investigate the host-pathogen interactions of the most aggressive species on one plum and nectarine cultivar as model system. Different isolates, host ripeness levels, inoculum loads and storage conditions were considered. pH modulation and gene expression profiles of these Penicillium spp. were investigated. Penicillium digitatum was identified the most aggressive in terms of lesion diameter, followed by P. expansum, P. crustosum and P. solitum. Scanning electron microscopy provided additional information on different life stages of P. digitatum, P. expansum and P. crustosum on alternative hosts (nectarine, pear and lemon). Ripeness significantly increased lesion diameter and disease incidence of P. digitatum but not P. expansum. Irrespective of ripeness level, lesions caused by P. expansum were similar in size and disease incidence 100%. Penicillium digitatum was more sensitive to cold storage and greatly affected by inoculum load. Ripeness meaningfully affected pH modulation. Colonised tissue was acidic. A mechanism leading to alkalinisation of uncolonised tissue was discussed. This was specifically observed on plum. Higher pH at and beyond lesion borders potentially facilitate invasion, maceration and colonisation (nutrient uptake and growth) by/during acidification. The pH of colonised tissue was similar to the initial pH of the host (prior to infection). Localised alkalinisation can be accomplished by ammonium/ammonia accumulation but areas further away from lesions can be due to host ripening directly (elicited) or indirectly (ethylene stress) caused by pathogen attack. Ripeness had a large effect on the gene expression (especially PG) of the Penicillium spp. on nectarine. Penicillium digitatum downregulated ACCD (only) whereas P. expansum upregulated pacC and creA on plum. With nectarine, P. digitatum upregulated PG and creA while P. expansum downregulated PG and upregulated pacC. Fresh plum (1d postharvest) was already a more suitable host based on lesion diameter, disease incidence and the nonsignificant increase in PG expression. Unlike what is known on citrus, P. digitatum showed an opportunistic lifestyle on the stone fruits depending on host and environmental conditions. Rapid decay caused by P. digitatum highlighted it as a concern to industry. Further research is needed to identify the trigger/s leading to the significant shift in lesion size and disease incidence of P. digitatum on riper fruit. Host resistance should be considered. More research is needed to investigate the dual mechanism of pH modulation and truly link P. digitatum with stone fruit losses in industry.