Genomic Analyses of Penicillium Species Have Revealed Patulin and Citrinin Gene Clusters and Novel Loci Involved in Oxylipin Production

Abstract

Blue mold of apple is caused by several different Penicillium species, among which P. expansum and P. solitum are the most frequently isolated. P. expansum is the most aggressive species, and P. solitum is very weak when infecting apple fruit during storage. In this study, we report complete genomic analyses of three different Penicillium species: P. expansum R21 and P. crustosum NJ1, isolated from stored apple fruit; and P. maximae 113, isolated in 2013 from a flooded home in New Jersey, USA, in the aftermath of Hurricane Sandy. Patulin and citrinin gene cluster analyses explained the lack of patulin production in NJ1 compared to R21 and lack of citrinin production in all three strains. A Drosophila bioassay demonstrated that volatiles emitted by P. solitum SA and P. polonicum RS1 were more toxic than those from P. expansum and P. crustosum strains (R27, R11, R21, G10, and R19). The toxicity was hypothesized to be related to production of eight-carbon oxylipins. Putative lipoxygenase genes were identified in P. expansum and P. maximae strains, but not in P. crustosum. Our data will provide a better understanding of Penicillium spp. complex secondary metabolic capabilities, especially concerning the genetic bases of mycotoxins and toxic VOCs.

Comparative Penicillium spp. Transcriptomics: Conserved Pathways and Processes Revealed in Ungerminated Conidia and during Postharvest Apple Fruit Decay

“…P. expansum R19 contains an intact 40kb patulin gene cluster and produces patulin in vitro and in vivo, while RS1 lacks a complete cluster and thus does not produce patulin. This difference in toxigenic potential may indicate why we observed the increased differential expression of transporters in the R19 dataset compared to RS1 during apple fruit decay, as the R19 strain may rely on these transporters to export toxin produced in order to avoid self-toxicity [5,53]. Moreover, transport is also impacted by the apple phenolic, quercetin, which demonstrates one part of the apple fruits influence on fungal transcriptional regulation [54].…”

“…Lesion formation in the host has also been shown to be due to patulin production [35]. Interestingly, R19 has complete gene clusters for both, whereas RS1 only has partial biosynthetic gene clusters for each [53]. This could also contribute to lesion formation being larger for P. expansum.…”

“…Moreover, using the antiSMASH program, Wu et al [5] showed there are 66 predicted secondary metabolite clusters in P. expansum, compared to 58 predicted clusters in P. polonicum. Additional comparisons have been made regarding volatile organic compounds (VOCs) to specifically study differences in oxylipins [53]. Surprisingly, the less virulent RS1 produced more oxylipins than the more virulent R19, demonstrating that virulence in apple fruits and toxicity in other contexts do not always coincide.…”

Anti-Insect Properties of Penicillium Secondary Metabolites

“…VOCs emitted by strains of several Penicillium species, namely P. expansum , P. solitum , P. crustosum , P. polonicum and P. maximae , caused repellent and toxic effects on Drosophila larvae and adults [ 221 ]. Low concentrations of the vapor form of several eight carbon compounds, including oxylipins and 1-octen-3-ol, were found to be toxic to D. melanogaster in previous studies [ 222 , 223 , 224 ].…”

A highly quality genome sequence of Penicillium oxalicum species isolated from the root of Ixora chinensis in Vietnam

“…To date, 30 Penicillium genomes among 18 species/483 accepted species were reported. The most complete genome is from Penicilina ( Yin et al . 2021 ).…”