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An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant

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An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant Report An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant Graphical Abstract Authors Sameh S.M. Soliman, John S. Greenwood, Aureliano Bombarely, ..., Rong Tsao, Dick D. Mosser, Manish N. Raizada Correspondence [email protected] In Brief It has been a mystery why yew trees, which produce the cancer drug Taxol, host fungi that also produce Taxol, which in nature is a fungicide. Soliman et al. show that the fungi store Taxol in hydrophobic bodies, migrate to pathogen entry points, and then release the bodies upon sensing pathogens, to create fungicide-laced barriers for their host. Highlights Accession Numbers d The cancer drug Taxol is a fungicide against wood-decaying JZ896663 fungi (WDF) in yew trees JZ896662 JZ896664 d Inside yew, a fungal endophyte produces Taxol and migrates JZ896665 to pathogen entry points d The endophyte sequesters Taxol in hydrophobic bodies (HBs); WDF induce their release d The HBs can coalesce to form extracellular barriers laced with fungicidal Taxol Soliman et al., 2015, Current Biology 25, 2570–2576 October 5, 2015 ª2015 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2015.08.027 Current Biology Report An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant Sameh S.M. Soliman,1,2 John S. Greenwood,3 Aureliano Bombarely,4 Lukas A. Mueller,5 Rong Tsao,6 Dick D. Mosser,3 and Manish N. Raizada1,* 1Department of Plant Agriculture, University of Guelph, Guelph, ON N1G 2W1, Canada 2David Geffen School of Medicine at UCLA, Los Angeles Biomedical Research Institute, Harbor-UCLA Medical Center, Torrance, CA 90502, USA 3Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON N1G 2W1, Canada 4Department of Horticulture, Virginia Tech, Blacksburg, VA 24071, USA 5SOL Genomic Network, Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA 6The Guelph Food Research Centre, Agriculture and Agri-Food Canada, Guelph, ON N1G 5C9, Canada *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.08.027 SUMMARY hyphae repeated this behavior and grew out from their native habitat, the medullary ray vascular system (Figures 1E and 1F). Surface cracks create sites for pathogen invasion. These hyphae were cultured (Figures S1A and S1B) and identi- Yew trees (Taxus) hyperbranch from long-lived buds fied via 18S rDNA (Figure S1C) as an endophytic fungus that that lie underneath the bark [1], resulting in persistent we previously classified as Paraconiothyrium strain SSM001 bark cracking and deep air pockets, potentially allow- [12]. The fungus was tracked within Taxus by DNA fingerprinting ing pathogens to enter the nutrient-rich vascular (tRFLP) and observed to inhabit only wood (Figures S1E–S1J). system (vertical phloem and inter-connected radial This strain was previously shown to produce Taxol in vitro in the absence of its host [12]. medullary rays [MR]). Yew is famous as the source of the anti-cancer diterpenoid drug Taxol. A mystery Taxol and the Taxol-Producing Endophyte Inhibit has been why both the tree and its resident non-path- Wood-Decaying Fungi In Vitro and in Intact Plants ogenic fungi (endophytes) synthesize Taxol, appar- Based on reports that Taxol is fungicidal in that it can suppress ently redundantly [2–7]. These endophytes, as well fungal mitosis [8–11], we tested whether endophyte SSM001 as pure Taxol, suppress fungal pathogens including could suppress three wood-decaying fungi (WDF): Heterobasi- wood-decaying fungi (WDF) [8–11]. Here we show dion annosum, Phaeolus schweinitzii, and Perenniporia suba- that a Taxol-producing fungal endophyte, Paraconio- cida. These WDF pathogens infect conifers, with P. schweinitzii thyrium SSM001 [12], migrates to pathogen entry known to infect Taxus [13–16]. SSM001 inhibited growth of these points including branch cracks. The fungus seques- WDF in vitro (Figures 1G, S2A, and S2B) similar to their taxane ters Taxol in intracellular hydrophobic bodies that extracts (Figure S2C) and pure Taxol (Figure 1H), but not solvent are induced by WDF for release by exocytosis, after controls (Figure 1I). Pure Taxol did not inhibit SSM001 (Figure 1H) which the bodies can coalesce to form remarkable or regeneration of SSM001 mycelia from protoplasts (Figures S2D and S2E), demonstrating that SSM001 had evolved resis- extracellular barriers, laced with the fungicide. We tance that was not due to its cell wall acting as a barrier. propose that microbial construction of fungicide- To determine whether SSM001 inhibits WDF in planta, Taxus releasing hydrophobic barriers might be a novel plantlets were infected with P. schweinitzii, but only after a prior plant defense mechanism. We further propose that injection with a commercial fungicide to kill SSM001 (Figure 1J). the endophyte might be evolutionarily analogous to PCR and tRFLP were used to monitor SSM001 (370 bp peak) animal immune cells, in that it might expand plant and WDF (240 bp peak) (Figures S2F–S2T). The commercial immunity by acting as an autonomous, anti-pathogen fungicide caused a 5-fold decrease in SSM001 compared to sentinel that monitors the vascular system. buffer-injected plantlets (Figure 1K). Pre-treated commercial fungicide plants showed significant increases in WDF compared to controls (Figure 1K). Combined with the in vitro and localiza- RESULTS tion data, these observations suggest that SSM001 suppresses WDF in planta (e.g., at branch points). Branching in Taxus Causes Deep Wood Cracks in which a Taxol-Producing Endophytic Fungus Accumulates Taxol Localizes to Hydrophobic Bodies within from Its Vascular Habitat Endophyte SSM001 Surprisingly, at Taxus bark cracks, fungal hyphae hyperaccumu- Electron microscopy revealed unusual hydrophobic bodies lated in air pockets around developing buds (Figure 1D). When (HBs) within cultured hyphae of SSM001 (Figure 2A), an obser- cracking was reproduced artificially by cutting the wood, the vation confirmed using Sudan IV, an orange lipophilic stain 2570 Current Biology 25, 2570–2576, October 5, 2015 ª2015 Elsevier Ltd All rights reserved Figure 1. Persistent Branching of Taxus Plants and Accumulation of the Taxol-Pro- ducing Fungus Paraconiothyrium SSM001 at Wood Medullary Rays and Taxus Branch Points (A) Photographs of persistent Taxus plant branching showing newly formed branch sprout- ing from stem cell populations underlying dead bark. (B) Diagram of a transverse section of a Taxus branch describing the outer and inner layers. (C) Light microscopy of a longitudinal newly formed branch section showing how the outer bark cracks open. (D) Light microscopy of a longitudinal branch section showing the accumulation of Para- coniothyrium SSM001 (stained blue by Trypan blue) surrounding the emerging branch. The branch section was cultured on PDA for 12 hr, fixed, and stained with Trypan blue. (E) Light microscopy of longitudinal wood sections cultured on PDA media for 72 hr, showing the localization and emergence of fungal hyphae in the wood medullary rays (WMR). (F) Confocal microscopy of longitudinal wood sections cultured on PDA media for 18 hr showing localization of Paraconiothyrium SSM001 hyphae within wood medullary rays. See Figure S1 for details of SSM001 taxonomy, phylogenetic relationships, and in planta localization inside Taxus using tRFLP. (G–K) Taxol and Taxol-producing fungus SSM001 are fungicidal against wood-decaying fungi (WDF). Shown are the fungicidal activities (G–I) in vitro and (J, K) in planta. (G) Effect of SSM001 on WDF. Paraconiothyrium (#1) co-cultured alongside (#2) Phaeolus schwei- nitzii WDF showing WDF growth inhibition. (H and I) Effect of pure Taxol standard (H) on WDF and other fungi in comparison to (I) methanol solvent control. Taxol-producing fungi (#1,6), non-Taxol-producing fungal endophytes (#5,7), and three WDF (#2,3,4). Taxol-producing fungi (Paraconiothyrium [#1] and Pestalotipsis [#6]), non-Taxol-producing fungi (Alternaria [#5], Fusarium [#7]), and WDF [#2,3,4]. Numbering is as follows: 1, Paraconiothyrium SSM001; 2, Phaeolus schweinitzii;3,Heterobasidion annosum;4,Perenniporia subacida;5,Alternaria;6,Pestalotiopsis;7,Fusarium graminearum. For supporting data, see Figures S2A–S2E. (J) Three-year-old Taxus plantlets were injected with fungicide (arrow and red color show the injection site). (K) Graph showing quantitative comparisons of WDF (Phaeolus schweinitzii) and Paraconiothyrium SSM001 endophyte between fungicide-injected and non- fungicide-injected plantlets. Error bars represent SEM. Abbreviations are as follows: Pf, Paraconiothyrium SSM001 hyphae; WX, wood xylem; Mr, medullary ray cells. WDF, wood decaying fungus. For the original data concerning the fungicide injections, see Figures S2F–S2T. For the results placed within an ecological model, see Figure S4. (Figure 2B). Because both HBs and Taxol are hydrophobic, Taxol-Containing Hydrophobic Bodies Accumulate we hypothesized that HBs accumulate Taxol, which was Extracellularly at Pathogen Entry Points confirmed by two experiments. First, immunogold labeling Staining with Sudan IV showed that HBs were present in the Taxus using a Taxol monoclonal antibody [17] demonstrated that vascular system (Figure 2I) including the interconnected lateral Taxol accumulated inside HBs within SSM001 hyphae (13/18 medullary rays (Figure 2J) and vertical phloem (Figure 2K). Immu- images, Figure 2C) compared to controls. Second, in a time- nogold labeling using the Taxol monoclonal antibody confirmed course following SSM001 inoculation into liquid
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