A fungal endophyte induces transcription of genes encoding a redundant fungicide pathway in its host plant

Abstract

BackgroundTaxol is an anti-cancer drug harvested from Taxus trees, proposed ecologically to act as a fungicide. Taxus is host to fungal endophytes, defined as organisms that inhabit plants without causing disease. The Taxus endophytes have been shown to synthesize Taxol in vitro, providing Taxus with a second potential biosynthetic route for this protective metabolite. Taxol levels in plants vary 125-fold between individual trees, but the underlying reason has remained unknown.ResultsComparing Taxus trees or branches within a tree, correlations were observed between Taxol content, and quantity of its resident Taxol-producing endophyte, Paraconiothyrium SSM001. Depletion of fungal endophyte in planta by fungicide reduced plant Taxol accumulation. Fungicide treatment of intact plants caused concomitant decreases in transcript and/or protein levels corresponding to two critical genes required for plant Taxol biosynthesis. Taxol showed fungicidal activity against fungal pathogens of conifer wood, the natural habitat of the Taxol-producing endophyte. Consistent with other Taxol-producing endophytes, SSM001 was resistant to Taxol.ConclusionsThese results suggest that the variation in Taxol content between intact Taxus plants and/or tissues is at least in part caused by varying degrees of transcriptional elicitation of plant Taxol biosynthetic genes by its Taxol-producing endophyte. As Taxol is a fungicide, and the endophyte is resistant to Taxol, we discuss how this endophyte strategy may be to prevent colonization by its fungal competitors but at minimal metabolic cost to itself.

Diversity, distribution and biotechnological potential of endophytic fungi

“…Thus, it has been surmised that endophytic fungi and host plants have similar pathways for synthesizing secondary metabolites due to horizontal gene transfer (Wang and Dai 2011;Soliman et al 2013), and that endophytic fungi could become an important source of novel bioactive secondary metabolites. Many bioactive substances are potentially useful to modern medicine, including cryptocin, gentiopicrin, spiroquinazoline alkaloids, taxol, vinblastine, vincristine, and so on (Stierle et al 1993;Li et al 2000;Barros and Rodrigues-Filho 2005;Yin et al 2009;Soliman et al 2013). Several recently reported novel bioactive secondary metabolites produced by fungal endophytes (Asai et al 2013;Xu et al 2013;Akay et al 2014;Xiao et al 2014;Zhang et al 2014a, b;Zhou et al 2014a, b) are presented in Fig.…”

Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

“…In tropical trees, within-species variation in plant secondary chemistry (including variation among young and old leaves [Brenes-Arguedas et al, 2006]) is usually small compared to among-species differences (Sedio et al, 2017). However, it is unclear which chemicals are produced by hosts or by endophytes (Soliman et al, 2013;Vallet et al, 2018) and which are inducible from interactions between the two (Mejía et al, 2008;Hartley et al, 2015). These chemicals have the potential to exhibit a range of ecologically important effects, and while they could have either beneficial or detrimental effects on hosts, they are most often investigated in the context of mounting defensive responses.…”

New Approach To Improve Taxol Biosynthetic

“…[61,62]. The fungal endophyte stimulates its host to produce a fungicide to which it is resistant, perhaps to remove rivals [63]. Taxol is a fungicide, and the endophyte is resistant to Taxol.…”

“…Fungal endophyte induces transcription of ratelimiting genes in the plant Taxol biosynthetic pathway. therefore fungicides by reduction of fungal endophyte lead to decrease Taxol content and transcript and/or protein levels corresponding to two critical genes required for plant Taxol biosynthesis [63].…”