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Fungal Endophytes of Vanilla Planifolia Across Réunion Island

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Fungal Endophytes of Vanilla Planifolia Across Réunion Island Fungal endophytes of Vanilla planifolia across Réunion Island: isolation, distribution and biotransformation Shahnoo Khoyratty, Joëlle Dupont, Sandrine Lacoste, Tony Palama, Young Choi, Hye Kim, Bertrand Payet, Michel Grisoni, Mireille Fouillaud, Robert Verpoorte, et al. To cite this version: Shahnoo Khoyratty, Joëlle Dupont, Sandrine Lacoste, Tony Palama, Young Choi, et al.. Fungal endophytes of Vanilla planifolia across Réunion Island: isolation, distribution and biotransformation. BMC Plant Biology, BioMed Central, 2015, 10, pp.301 - 301. 10.1186/s12870-015-0522-5. hal- 01397514 HAL Id: hal-01397514 https://hal.archives-ouvertes.fr/hal-01397514 Submitted on 16 Nov 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Khoyratty et al. BMC Plant Biology (2015) 15:142 DOI 10.1186/s12870-015-0522-5 RESEARCH ARTICLE Open Access Fungal endophytes of Vanilla planifolia across Réunion Island: isolation, distribution and biotransformation Shahnoo Khoyratty1,2,3, Joëlle Dupont4, Sandrine Lacoste4, Tony Lionel Palama1,3,5, Young Hae Choi2, Hye Kyong Kim2, Bertrand Payet6, Michel Grisoni7, Mireille Fouillaud6, Robert Verpoorte2 and Hippolyte Kodja1,8* Abstract Background: The objective of the work was to characterize fungal endophytes from aerial parts of Vanilla planifolia. Also, to establish their biotransformation abilities of flavor-related metabolites. This was done in order to find a potential role of endophytes on vanilla flavors. Results: Twenty three MOTUs were obtained, representing 6 fungal classes. Fungi from green pods were cultured on mature green pod based media for 30 days followed by 1H NMR and HPLC-DAD analysis. All fungi from pods consumed metabolized vanilla flavor phenolics. Though Fusarium proliferatum was recovered more often (37.6 % of the isolates), it is Pestalotiopsis microspora (3.0 %) that increased the absolute amounts (quantified by 1HNMR in μmol/g DW green pods) of vanillin (37.0 × 10−3), vanillyl alcohol (100.0 × 10−3), vanillic acid (9.2 × 10−3)and p-hydroxybenzoic acid (87.9 × 10−3) by significant amounts. Conclusions: All plants studied contained endophytic fungi and the isolation of the endophytes was conducted from plant organs at nine sites in Réunion Island including under shade house and undergrowth conditions. Endophytic variation occured between cultivation practices and the type of organ. Given the physical proximity of fungi inside pods, endophytic biotransformation may contribute to the complexity of vanilla flavors. Keywords: Endophytes, Distribution, Diversity, Biotransformation, Vanilla, Interaction Background used as marker compounds to determine quality and The genus Vanilla is a member of the Orchidaceae authenticity of vanilla products. For authentic unadul- family and comprises of approximately 100 species and terated vanilla extracts, the ratios between the four among them, Vanilla planifolia is the most important components are fixed within a certain range [4]. In source of natural vanilla flavor [1]. Natural vanilla flavor Réunion Island, vanilla plants are either cultivated in is the number one flavor tonality in the world as it is the undergrowth or in shade houses. Vanilla pods subtle, but complex [2]. Over 200 compounds have grown in the undergrowth appeared to display substan- already been isolated and identified from vanilla beans. tial qualitative differences of vanillin and vanillic acid These compounds vary in concentration depending on contents in comparison to those grown under shade- the region where the beans are harvested [3]. Four major house conditions. Parameters responsible for such a flavor related components (p-hydroxybenzoic acid, difference have not been identified yet [5]. The major p-hydroxybenzaldehyde, vanillic acid and vanillin) are vanilla flavor constituents are present as glycosides in the pods prior to curing [6]. In order to allow the development of flavor, green pods undergo post-harvest * Correspondence: [email protected] 1Université de La Réunion, UMR PVBMT, 15 avenue René Cassin, CS processing. The exact method for post-harvest 92003-97744Saint Denis Cedex 9, La Réunion, France processing and curing of vanilla pods varies across the 8 UMR PVBMT, Faculté des Sciences et Technologies, Université de La region of the world where vanilla is produced. Réunion, 15, Avenue René Cassin, BP 7151Saint-Denis Cédex 09, Ile de la Réunion, France Full list of author information is available at the end of the article © 2015 Khoyratty et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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. Khoyratty et al. BMC Plant Biology (2015) 15:142 Page 2 of 19 Endophytic fungi are defined functionally by their by de novo synthesis of a precursor where the organism occurrence within asymptomatic tissues of plants [7]. In produces an intermediate in vanillin biosynthesis. Biotrans- spite of the ubiquitous features, the scale of their diver- formation of vanillin precursors is not limited to vanilla sity, their host range, and geographic distributions much plants, but can also be achieved with microorganisms about endophytes is still unknown for many plants (Fig. 1), e.g. fungi. including vanilla. Endophytic fungi can either be trans- For instance, p-coumaric acid is converted in vitro to mitted vertically or horizontally. Vertical transmission p-hydroxybenzaldehyde by the fungus Paecilomyces var- occurs when fungi are transferred from the host to the iotii grown on minimal medium containing basal inor- offspring via host tissues. Horizontal transmission occurs ganic salts with p-coumaric acid as a sole carbon source when fungi are transferred to the host via spores e.g. [13]. Vanillic acid is formed from vanillin by Hormoden- through aerial means. Endophytes can be involved in drum sp. grown in vitro on basal medium [14]. Vanillyl biomass production and nutrient cycling in the plant [7]. alcohol is made by Pestalotia palmarum from ferulic Previously Porras-Alfaro and Bayman [8] isolated non- acid grown in vitro on synthetic medium supplied with pathogenic fungi from inside asymptomatic roots of van- glucose [15]. Furthermore, the simplicity of vanillin illa plants. Mycorrhizal fungi interact symbiotically with structure has led to the use of various precursors in the roots through an association of the mycelium (typically microbial or enzymatic process of vanillin production: basidiomycete) while the hyphae form a mass around lignin, curcumin, siam benzoin resin, phenolic stilbenes, the rootlets or penetrate root cells. They are absent from isoeugenol, eugenol, ferulic acid, aromatic amino acids, the outer root cortex and hence differ from endophytes and glucose via de novo biosynthesis while several fungi that are present deeper inside plant tissues. The mycor- have the capacity to metabolize the aforementioned pre- rhizal fungi Ceratobasidium spp., Thanatephorus spp. and cursors. A similarity can thus be seen between biotrans- Tulasnella spp. were found to be associated to different formations in vanilla cells with regards to metabolites species of vanilla Porras-Alfaro and Bayman [8]. Morpho- related to vanilla flavor, and fungal biotransformations of logical identification followed by elongation factor gene these compounds. Given such similarities in the biosyn- sequence analysis showed that several Fusarium spp. thetic pathways of polyphenols in vanilla plants and arepresentinvanillaplantsinIndonesia[9]. fungi, it is not surprising that a possible role of microor- Metabolomics is defined as both the qualitative and ganisms in vanilla has been investigated before. Roling quantitative analysis of all primary and secondary me- et al. [16] and Dunphy and Bala [2, 17], for example, tabolites of an organism [10]. Two chemical analysis studied a possible involvement of microorganisms dur- techniques used in metabolic profiling include 1H ing the curing of the pods all pointing principally to the nuclear magnetic resonance (NMR) spectroscopy and occurrence of bacteria and actinomycetes. The current high-performance liquid chromatography (HPLC). For study concerns another aspect though: the possible role instance, high-performance liquid chromatography - diode of fungal endophytes in the vanilla plant and the green array detector (HPLC-DAD) analysis showed the presence pods in the formation of vanilla flavor related com- of 3,4-O-(Z)-dicaffeoylquinic acid and quercetin-7-O-glu- pounds. So far no fungal endophytes have been isolated coside as the main components from in vitro microplants from aerial parts of the plant. of Hyptis marrubioides Epling inoculated with bacterial In this work, endophytes were isolated from organs, and fungal endophytic isolates [11]. Similarly
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