Occurrence of pyrrocidine and dihydroresorcylide production amongAcremonium zeaepopulations from maize grown in different regions

Abstract

Acremonium zeae is recognized as a protective endophyte of maize (Zea mays). Thus, it is a potential confounding variable in maize variety trials for resistance to pathogenic microbes and their mycotoxins. This fungus grows systemically in maize and produces pyrrocidines A and B, polyketide -amino acid derived antibiotics exhibiting potent in vitro activity against major stalk-and ear-rot pathogens of maize. An evaluation of a number of A. zeae isolates accessioned by the USDA Agricultural Research Service Culture Collection (NRRL) and CBS Culture Collections from 1969 to 1992 revealed that pyrrocidines were produced by 5 of 11 isolates from maize grown in regions sharing a milder temperate climate with cold winters (e.g., Illinois, Nebraska, and Germany) and by 10 of 12 isolates from maize grown in warmer regions (e.g., North Carolina and Georgia, USA; Iran; and India). Cultures of A. zeae representing 13 populations isolated from maize seeds harvested from different regions and years were grown on potato dextrose agar in Petri dishes. Excised portions of the developing colony and underlying agar were extracted and analyzed by liquid chromatography -atmospheric pressure chemical ionization interface -mass spectrometry. Among 52 isolates representing four A. zeae populations from regions associated with drought and temperature stress (e.g., Arizona, California, and Texas) 49 isolates (94%) produced pyrrocidine A in amounts ranging from 1 to 248 ng (mean 29 ng), and 51 isolates (98%) produced pyrrocidine B in amounts ranging from 2 to 440 ng (mean 137 ng). In contrast, among 102 isolates representing nine A. zeae populations from the midwestern corn belt (e.g., Illinois, Indiana, Iowa, Kentucky, Michigan, and Nebraska), only one isolate produced pyrrocidine A (280 ng) and pyrrocidine B (411 ng). During the population study, a new secondary metabolite of A. zeae, dihydroresorcylide, was discovered, and its distribution among the population is described. Clonal populations of A. zeae endophytes differing in their ability to produce pyrrocidines may be distributed with seed of maize cultivars grown in commercial plantings. Résumé : Acremonium zeae est reconnu en tant que champignon endophyte protecteur du maïs. Il s'agit par conséquent d'un facteur confusionnel potentiel dans les essais de variété effectués sur le maïs afin d'en évaluer la résistance aux microbes pathogènes et à leurs mycotoxines. A. zeae pousse systématiquement sur le maïs et produit des pyrrocidines A et B, c'est-à-dire des antibiotiques polykétides dérivés d'acides aminés qui affichent une forte activité in vitro contre les principaux agents pathogènes causant la fusariose de l'épi et la pourriture des tiges chez le maïs. Une évaluation d'un nombre d'isolats d'A. zeae, répertoriés, de 1969 à 1992, par l'Agricultural Research Service Culture Collection NRRL et le CBS Culture Collection a démontré que 5 des 11 isolats obtenus de plants de maïs cultivés dans des régions qui connaissent des étés doux et des hivers froids (p. ex., Illinois, Nebraska, A...

Fungal endophytes of Panicum maximum and Pennisetum purpureum: isolation, identification, and determination of antifungal potential

“…This genus was established in 1975 (Gams and Hawksworth, 1975); however, it was only recently delimited as a monophyletic group and shown to contain several species formerly classified in the morphogenus Acremonium (Summerbell et al, 2011;Giraldo et al, 2015). These findings highlight the common association of Sarocladium species with plants in the Poaceae family, including the rice sheet rot pathogen Sarocladium oryzae and the putative plant-protective endophytes Sarocladium zeae (formerly Acremonium zeae) from maize (Wicklow et al, 2008) and Sarocladium implicatum (formerly Acremonium implicatum) from Brachiaria brizantha (Kelemu et al, 2001). Two Sarocladium species were recently described from collections of grass endophytes, Sarocladium spinificis from Spinifex littoreus, a grass found on the Taiwanese coast (Yeh and Kirschner, 2014), and Sarocladium brachiariae, from B. brizantha grass, collected in China (Liu et al, 2017).…”

Sarocladium and Lecanicillium Associated with Maize Seeds and Their Potential to Form Selected Secondary Metabolites

“…The authors reported that Pyrrocidine A and B were detected in nine of the cultures, while pyrrocidine B alone was detected in three cultures. Subsequent studies by Wicklow et al [ 42 ] confirmed the variation in the distribution of pyrrocidines in the populations of maize endophytes S. zeae and supported that the ability of these fungi to form pyrrocidine A and B appeared to be isolate-specific and not species-specific. These findings are consistent with the observations from the present study.…”

“…It is noteworthy that pyrrocidines A and B were discovered to be the metabolites accounting for S. zeae antifungal activity against Aspergillus flavus and Fusarium verticillioides [ 6 , 43 ]. Moreover, Wicklow et al [ 42 ] documented that Pyrrocidine A displayed in vitro activity against major stalk and ear rot pathogens of maize, including F. graminearum , Nigrospora oryzae , Stenocarpella ( Diplodia ) maydis , and Rhizoctonia zeae as well as seed-infecting colonists of the phylloplane Alternaria alternata , Cladosporium cladosporioides , and Curvularia lunata , which produces a damaging leaf spot disease and seed-rotting saprophyte Eupenicillium ochrosalmoneum . Following the suggestion of Wicklow et al [ 6 , 42 ] that the ability of fungal endophytes to produce pyrrocidine A and B may be important for their interaction with competing microorganisms, it can be assumed that the capacity of maize seed-associated Sarocladium and Lecanicillium isolates to synthesize these and other antibiotics (bassianolide, vericillian A) observed in present study may also signal their antagonistic potential towards other fungi.…”

Xenoacremones D–H, Bioactive Tyrosine-decahydrofluorene Analogues from the Plant-Derived Fungus Xenoacremonium sinensis

“…These PKS-NRPS hybrids were isolated from various fungal species, some of which were from the family Nectriaceae, such as Hirsutella spp. [9,17], Neonectria ramulariae [12,18] and Acremonium zeae [19]. They share a structural skeleton that contains a fused [6,5,6] tricarbocyclic decahydrofluorene, a γ-lactam and a 13-membered para-cyclophane ether ring system, and they possess antitumor, antifungal, antibacterial and antitubercular activities [20].…”