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Endophytic Fungi from the Roots of Horseradish (Armoracia Rusticana)

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Endophytic Fungi from the Roots of Horseradish (Armoracia Rusticana) View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Repository of the Academy's Library Szűcs et al. BMC Plant Biology (2018) 18:85 https://doi.org/10.1186/s12870-018-1295-4 RESEARCH ARTICLE Open Access Endophytic fungi from the roots of horseradish (Armoracia rusticana) and their interactions with the defensive metabolites of the glucosinolate - myrosinase - isothiocyanate system Zsolt Szűcs1, Tamás Plaszkó1, Zoltán Cziáky5, Attila Kiss-Szikszai2, Tamás Emri3, Regina Bertóti4, László Tamás Sinka5, Gábor Vasas1 and Sándor Gonda1* Abstract Background: The health of plants is heavily influenced by the intensively researched plant microbiome. The microbiome has to cope with the plant’s defensive secondary metabolites to survive and develop, but studies that describe this interaction are rare. In the current study, we describe interactions of endophytic fungi with a widely researched chemical defense system, the glucosinolate - myrosinase - isothiocyanate system. The antifungal isothiocyanates are also of special interest because of their beneficial effects on human consumers. Results: Seven endophytic fungi were isolated from horseradish roots (Armoracia rusticana), from the genera Fusarium, Macrophomina, Setophoma, Paraphoma and Oidiodendron. LC-ESI-MS analysis of the horseradish extract incubated with these fungi showed that six of seven strains could decompose different classes of glucosinolates. Aliphatic, aromatic, thiomethylalkyl and indolic glucosinolates were decomposed by different strains at different rates. SPME-GC-MS measurements showed that two strains released significant amounts of allyl isothiocyanate into the surrounding air, but allyl nitrile was not detected. The LC-ESI-MS analysis of many strains’ media showed the presence of allyl isothiocyanate - glutathione conjugate during the decomposition of sinigrin. Four endophytic strains also accepted sinigrin as the sole carbon source. Isothiocyanates inhibited the growth of fungi at various concentrations, phenylethyl isothiocyanate was more potent than allyl isothiocyanate (mean IC50 was 2.30-fold lower). As a control group, ten soil fungi from the same soil were used. They decomposed glucosinolates with lower overall efficiency: six of ten strains had insignificant or weak activities and only three could use sinigrin as a carbon source. The soil fungi also showed lower AITC tolerance in the growth inhibition assay: the median IC50 values were 0.1925 mM for endophytes and 0.0899 mM for soil fungi. Conclusions: The host’s glucosinolates can be used by the tested endophytic fungi as nutrients or to gain competitive advantage over less tolerant species. These activities were much less apparent among the soil fungi. This suggests that the endophytes show adaptation to the host plant’s secondary metabolites and that host metabolite specific activities are enriched in the root microbiome. The results present background mechanisms enabling an understanding of how plants shape their microbiome. Keywords: Myrosinase, Endophytes, Glucosinolate, Isothiocyanate, Fungal enzyme * Correspondence: [email protected]; [email protected] 1Department of Botany, Division of Pharmacognosy, University of Debrecen, Egyetem tér 1, Debrecen H-4010, Hungary Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Szűcs et al. BMC Plant Biology (2018) 18:85 Page 2 of 15 Background Despitealltheabove,theendophytes’ interaction with It is now well established that the plant microbiome the plant defense metabolites is not that studied. affects the health of plants, just as the much more The glucosinolate (GSL) - myrosinase (MYR) - isothio- researched human microbiome influences ours [1]. Of cyanate (ITC) chemical defense system is present in course, the complex groups of microbes also interact Brassicaceae, Capparaceae, Resedaceae and Moringaceae. with the plant metabolites. Some natural products are It is one of the most researched plant defense systems co-products of the endophytes and the plants; several [11]. Myrosinase (EC 3.2.1.147, thioglucoside glucohy- endophytes can selectively transform the plant’ssec- drolase) catalyzes the reaction between a glucosinolate ondary metabolites [2]. Endophytic fungi are an inten- and water to yield glucose and a thiohydroximate. The sively studied subset of the plant microbiome. A huge free thiohydroximate subsequently spontaneously rear- amount of scientific literature is gathering on this ranges to isothiocyanates and byproducts (Fig. 1)[12, group, which is not that straightforward to define [3, 13]. Most isothiocyanates are extremely pungent and 4]. Various definitions exist, but they are usually con- exert various bioactivities due to their reactive -NCS sidered non-pathogenic strains that live inside plants groups, which results in strong antimicrobial, insecti- without causing apparent symptoms [3, 4]. Endo- cidal and other effects [12]. This chemical defense sys- phytes are very good subjects for drug discovery. The tem is present in vegetables of the Brassicaceae with possibility of finding new natural products is a signifi- various glucosinolates. Interestingly, the isothiocyanates cant driving force of the research of these fungi [5]. have beneficial effects on humans, making the Brassica- Endophytes are also well studied for production of ceae crops healthy functional foods. Regular consump- different enzymes that operate under special condi- tion of low amounts of isothiocyanates can prevent tions, for example, endophytes isolated from plants different human diseases [12]. living in saline habitats, harbor enzymes that can op- Glucosinolates are chemically stable and are sepa- erate at high salt concentrations [6]. Their beneficial rated from their activating enzyme – MYR – by interaction with plants also has potential uses in crop compartmentalization. They typically come in contact protection and plant health promotion (e.g. biocon- in planta when the plant tissue is damaged. There is trol, salt tolerance [7, 8]).However,thenon- a considerable variability of the actual separation pathogenic lifestyle can not be considered stable [3, strategy that depends on species, organ, developmen- 4]. “True” endophytes sometimes become latent path- tal stage and many other factors [11]. Myrosinase and ogens, and this has severe agricultural impact [9, 10]. the GSLs are usually stored in separate cells, but this Fig. 1 The glucosinolate – myrosinase – isothiocyanate system and its interactions with fungi and members of the ecosystem. Known sources of enzymes are color coded: Plants: black, fungi or bacteria: red, insects: blue. Abbreviations: ESP, epithionitrile specifier protein, NSP, nitrile specifier protein, TFP, thiocyanate-forming protein. References: [13, 56, 61, 62] Szűcs et al. BMC Plant Biology (2018) 18:85 Page 3 of 15 is not always the case. The GSL - ITC system is this activity would make this system more complex. therefore considered a “chemical bomb” that is trig- Also, in such an approach, a direct comparison with gered by the attack of pathogens and herbivores [11]. some control group of fungi would be desirable so that The isothiocyanates were shown to have potent anti- the specificity of the phenomenon can be assessed. fungal activity in many papers (e.g. [14–16]). It is an The aim of the current study was to test the hypoth- interesting question how endophytes tolerate the iso- esis that endophytes interfere with the GSL - MYR - thiocyanates of the plants. Actually, myrosinase activ- ITC chemical defense system of plants. The main ques- ity can benefit microorganisms, as it enables them to tions are: 1., Do endophytes tolerate the ITCs of the host obtain glucose from the thioglucoside. For endo- better than non-endophytic fungi? 2., Can endophytes phytes, there would be an additional benefit as it decompose GSLs? Can they use them as a carbon would give them the option to disarm the “chemical source? 3., How specific is the activity of the endo- bomb” of the host. Of course, they have to cope with phytes? To answer the above questions, we used isolated the toxicity of the released ITCs or prevent its release fungal root endophytes from Armoracia rusticana (as shown for an Aspergillus sp. strain [17]). MYR (horseradish), a Brassicaceae crop with a very high abun- activity was shown to be present in many microbial dance of ITCs. The strains were grown on horseradish organisms including Aspergillus sp., Fusarium sp. [18], extract to test their glucosinolate decomposing capacity Citrobacter [19], Enterobacter [20]aswellasmany and their ability to produce various decomposition prod- other species. Strains capable of metabolizing ucts. Their ITC tolerance and ability to use GSLs as a glucosinolates are part of the human gut microbial sole carbon source was also examined. As a reference community [21–23]. group, a set of soil fungi from the same soil was used. Regarding
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