Leptosphaeria biglobosa inhibits the production of sirodesmin PL by L. maculans

Abstract

BACKGROUNDPhoma stem canker is caused by two coexisting pathogens, Leptosphaeria maculans and L. biglobosa. They coexist because of their temporal and spatial separations, which are associated with the differences in timing of their ascospore release. L. maculans produces sirodesmin PL, while L. biglobosa does not. However, their interaction/coexistence in terms of secondary metabolite production is not understood.RESULTSSecondary metabolites were extracted from liquid cultures, L. maculans only (Lm only), L. biglobosa only (Lb only), L. maculans and L. biglobosa simultaneously (Lm&Lb) or sequentially 7 days later (Lm+Lb). Sirodesmin PL or its precursors were identified in extracts from ‘Lm only’ and ‘Lm+Lb’, but not from ‘Lm&Lb’. Metabolites from ‘Lb only’, ‘Lm&Lb’ or ‘Lm+Lb’ caused significant reductions in L. maculans colony area. However, only the metabolites containing sirodesmin PL caused a significant reduction to L. biglobosa colony area. When oilseed rape cotyledons were inoculated with conidia of ‘Lm only’, ‘Lb only’ or ‘Lm&Lb’, ‘Lm only’ produced large gray lesions, while ‘Lm&Lb’ produced small dark lesions similar to lesions caused by ‘Lb only’. Sirodesmin PL was found only in the plant extracts from ‘Lm only’. These results suggest that L. biglobosa prevents the production of sirodesmin PL and its precursors by L. maculans when they grow simultaneously in vitro or in planta.CONCLUSIONFor the first time, L. biglobosa has been shown to inhibit the production of sirodesmin PL by L. maculans when interacting simultaneously with L. maculans either in vitro or in planta. This antagonistic effect of interspecific interaction may affect their coexistence and subsequent disease progression and management. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Co‐inoculation timing affects the interspecific interactions between phoma stem canker pathogens Leptosphaeria maculans and Leptosphaeria biglobosa

“…29 However, when L. biglobosa was co-inoculated sequentially 7 days after L. maculans in liquid culture, the production of sirodesmin PL by L. maculans was not inhibited. 29 Previous work showed that it took approximately 3 days for L. maculans to produce sirodesmin PL. [28][29][30] We hypothesised that the timing when L. maculans and L. biglobosa meet influences the outcome of the interspecific competition related to sirodesmin PL production and pathogen growth.…”

“…Leptosphaeria maculans produces a non-host selective epipolythiodioxopiperazine (ETP) phytotoxin called sirodesmin PL, while L. biglobosa does not. [27][28][29] Sirodesmin PL has antimicrobial and antifungal properties. 27,28 The sirodesmin PL produced by L. maculans was shown to inhibit the growth of L. biglobosa in vitro.…”

“…27,28 The sirodesmin PL produced by L. maculans was shown to inhibit the growth of L. biglobosa in vitro. 29,30 The in vitro growth of L. biglobosa was inhibited when it was inoculated with liquid culture containing sirodesmin PL. 29 Previous work showed that a mutant isolate of L. maculans that did not produce sirodesmin PL was still able to cause disease symptoms on oilseed rape, only with reduced antimicrobial and antifungal activity, suggesting that sirodesmin PL is produced as an interference competition strategy, but not required for disease development.…”

“…29,30 The in vitro growth of L. biglobosa was inhibited when it was inoculated with liquid culture containing sirodesmin PL. 29 Previous work showed that a mutant isolate of L. maculans that did not produce sirodesmin PL was still able to cause disease symptoms on oilseed rape, only with reduced antimicrobial and antifungal activity, suggesting that sirodesmin PL is produced as an interference competition strategy, but not required for disease development. 30 Similar studies were done for another ETP, gliotoxin, which is produced by Aspergillus fumigatus, the causative agent of pulmonary aspergillosis.…”

“…29 Previous work showed that it took approximately 3 days for L. maculans to produce sirodesmin PL. [28][29][30] We hypothesised that the timing when L. maculans and L. biglobosa meet influences the outcome of the interspecific competition related to sirodesmin PL production and pathogen growth. The aim of this research was therefore to investigate the effects of sequential co-inoculation on interspecific interactions between L. maculans and L. biglobosa in terms of production of sirodesmin PL and relative growth of the two pathogens in vitro, and the impact of the interspecific interactions on phoma stem canker management.…”