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The Ecological Role of Bacterial Seed Endophytes Associated with Wild Cabbage in the United Kingdom

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The Ecological Role of Bacterial Seed Endophytes Associated with Wild Cabbage in the United Kingdom Received: 16 July 2019 | Revised: 25 September 2019 | Accepted: 27 September 2019 DOI: 10.1002/mbo3.954 ORIGINAL ARTICLE The ecological role of bacterial seed endophytes associated with wild cabbage in the United Kingdom Olaf Tyc1,2 | Rocky Putra1,3,4 | Rieta Gols3 | Jeffrey A. Harvey5,6 | Paolina Garbeva1 1Department of Microbial Ecology, Netherlands Institute of Ecology Abstract (NIOO‐KNAW), Wageningen, The Endophytic bacteria are known for their ability in promoting plant growth and de‐ Netherlands fense against biotic and abiotic stress. However, very little is known about the micro‐ 2Department of Internal Medicine I, Goethe University, University Hospital Frankfurt, bial endophytes living in the spermosphere. Here, we isolated bacteria from the seeds Frankfurt, Germany of five different populations of wild cabbage (Brassica oleracea L) that grow within 3Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands 15 km of each other along the Dorset coast in the UK. The seeds of each plant popu‐ 4Hawkesbury Institute for the lation contained a unique microbiome. Sequencing of the 16S rRNA genes revealed Environment, Western Sydney University, that these bacteria belong to three different phyla (Actinobacteria, Firmicutes, and Penrith, Australia Proteobacteria). Isolated endophytic bacteria were grown in monocultures or mix‐ 5Department of Terrestrial Ecology, Netherlands Institute of Ecology, tures and the effects of bacterial volatile organic compounds (VOCs) on the growth Wageningen, The Netherlands and development on B. oleracea and on resistance against a insect herbivore was 6Department of Ecological Sciences, Section Animal Ecology, VU University Amsterdam, evaluated. Our results reveal that the VOCs emitted by the endophytic bacteria had Amsterdam, The Netherlands a profound effect on plant development but only a minor effect on resistance against Correspondence an herbivore of B. oleracea. Plants exposed to bacterial VOCs showed faster seed ger‐ Olaf Tyc, Department of Microbial Ecology, mination and seedling development. Furthermore, seed endophytic bacteria exhib‐ Netherlands Institute of Ecology (NIOO‐ KNAW), PO BOX 50, 6,700 AB Wageningen, ited activity via volatiles against the plant pathogen F. culmorum. Hence, our results The Netherlands. illustrate the ecological importance of the bacterial seed microbiome for host plant Department of Internal Medicine I, Goethe University, University Hospital Frankfurt, health and development. Theodor‐Stern‐Kai 7, 60590 Frankfurt, Germany. KEYWORDS Email: [email protected] bacteria, endophytes, fungal pathogens, insect herbivory, plant growth, plant resistance, Funding information plant‐insect interactions, seed germination Nederlandse Organisatie voor Wetenschappelijk Onderzoek, Grant/Award Number: 864.11.015 1 | INTRODUCTION & Martinez‐Romero, 2006). Endophytic microorganisms live in an intimate relationship with their host throughout many generations Plants are involved in intimate interactions with microbes through‐ (Johnston‐Monje & Raizada, 2011). Many endophytic bacteria are out their entire life cycle, and these interactions are essential for known for their growth‐promoting effect on plants and for prim‐ the growth and health of the plants. Endophytes are nonpatho‐ ing plant immunity by triggering induced systemic resistance (ISR) genic microorganisms that inhabit plants without causing them any and/or induced systemic tolerance (IST) (Hardoim, Overbeek, & harm (Hardoim, Hardoim, Overbeek, & Elsas, 2012; Rosenblueth Elsas JDv., 2008; Nass et al., 2005; Ryu et al., 2004, 2003). Several This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. MicrobiologyOpen. 2019;00:e954. www.MicrobiologyOpen.com | 1 of 15 https://doi.org/10.1002/mbo3.954 2 of 15 | TYC ET AL. studies have shown that endophytes can enhance antagonistic emission with consequences for the host in terms of growth, devel‐ activities of plant pathogens and aid plants against biotic and abi‐ opment, and resistance. otic stresses (Berg et al., 2005; Cosme et al., 2016; Egamberdieva, Here, we aimed to investigate the potential role of volatiles pro‐ Davranov, Wirth, Hashem, & Abd_Allah EF., 2017; Grover, Ali, duced by seed endophytic bacteria associated with wild cabbage Sandhya, Rasul, & Venkateswarlu, 2011). Seed endophytes are (Brassica oleracea L.) on plant growth, development and resistance known to be vertically transmitted from mother plants to their against a leaf chewing insect herbivore and two pathogenic fungi. offspring (Hardoim, Overbeek and Elsas, 2008; Frank, Saldierna These wild cabbage populations are considered to be the ancestors Guzmán and Shay, 2017; Nelson, 2018), suggesting that the role of of current cultivated cabbage. Seeds originated from five popula‐ seed endophytes is highly crucial, especially at the early stage of tions growing along the rugged coastline of Dorset, United Kingdom host plant development (Berg & Raaijmakers, 2018; Nelson, 2018; (Gols, Dam, Raaijmakers, Dicke, & Harvey, 2009; Van Geem, Harvey, Truyens, Weyens, Cuypers, & Vangronsveld, 2015). However, little Cortesero, Raaijmakers, & Gols, 2015; Wichmann, Alexander, Hails, is known so far about the ecological role of the seed endophytes & Bullock, 2008). Previous work has shown that there is consider‐ and seed microbiome. able population‐related variation in the expression of primary and Essential for plant–microbe interactions and communication are secondary metabolites (glucosinolates) in British populations of wild secondary (or specialized) metabolites produced by either partners. cabbage. These differences have an effect on the behavior and de‐ Both plants and microorganisms produce a wide variety of second‐ velopment of several species of insect herbivores and their natural ary metabolites including volatile and nonvolatile compounds. Only enemies associated with these plants both in the laboratory and in in the past few decades, the functional role of microbial volatiles the field (Gols, Bullock, Dicke, Bukovinszky, & Harvey, 2011; Gols et has been increasingly acknowledged and investigated (Sharifi & Ryu, al., 2008; Harvey, Dam, Raaijmakers, Bullock, & Gols, 2011; Moyes, 2018). Plant‐associated microorganisms produce an vast array of Collin, Britton, & Raybould, 2000; Newton, Bullock, & Hodgson, volatiles ranging from inorganic compounds, such as CO2, NH3, and 2009; Van Geem et al., 2015). However, this previous research ig‐ HCN to a plethora of organic compounds, such as terpenes, ketones, nored the possibly important role played by the plant microbiome on alcohols, alkenes, alkanes, esters, and sulfur‐derived compounds plant traits that affect growth, fitness, and defense. We hypothesize (Kanchiswamy, Malnoy, & Maffei, 2015; Schulz & Dickschat, 2007). that seeds of wild cabbage contain cultivable endophytic bacteria Volatile organic compounds (VOCs) are compounds with a small whose volatiles are beneficial for the host plant. Here, we aim to molecular weight (<300 da). They can easily evaporate and travel isolate endophytic bacteria from five different populations of wild through air and water‐filled pores in the soil (Penuelas et al., 2014; cabbage plant populations. We hypothesize that the five different Schulz & Dickschat, 2007). So far, the most well studied VOCs emit‐ plant populations harbor different endophytic bacterial strains, each ted by soil microorganisms are terpenes, nitrogen‐based compounds producing its specific volatile blend, which in turn differentially af‐ like indole and sulfur‐containing compounds like dimethyl disulfide fect their interaction with the host plant. (Tyc, Song, Dickschat, Vos, & Garbeva, 2017). Soil microorganisms can employ volatiles as info chemicals, growth stimulants, growth 2 | MATERIALS AND METHODS inhibitors, and inhibitors of quorum sensing (Chernin et al., 2011; Effmert, Kalderas, Warnke, & Piechulla, 2012; Kai et al., 2009; Kim, 2.1 | Seeds and extraction of endophytic bacteria Lee, & Ryu, 2013). Moreover, interspecific interactions of phyloge‐ netically different bacteria can also alter the volatile blend compo‐ Seeds of five different populations of wild cabbage Brassica oleracea sition, affecting the activity of volatiles (Garbeva, Hordijk, Gerards, collected from the Dorset coast in the UK were used in this study: A: & Boer, 2014; Tyc et al., 2015). The effects of the emitted micro‐ Durdle Door (DD; 50˚62’N, 2˚27’W), B: Kimmeridge (KIM; 50˚35’N, bial VOCs on the host plants and their antagonists can vary from 2˚03’W), C: Old Harry (OH; 50˚38’N, 1˚55’W), D: St. Aldhelms Head negative, positive to neutral (van Dam, Weinhold, & Garbeva, 2016). (SAH; 50˚69’N, 2˚05’W), and E: Winspit (WIN; 50˚34’N, 2˚02’W) For instance, plant‐growth promoting effects were reported for vol‐ (Van Geem et al., 2015) (Figure 1a; Figure A1). Seeds were surface‐ atiles emitted by bacteria (Park, Dutta, Ann, Raaijmakers, & Park, sterilized by a modified protocol by Araujo et al. (2002). To this end, 2015; Ryu et al., 2003) and fungi (Cordovez et al., 2017). In addition, seeds (1 g) of each plant population were subsequently incubated volatiles from an endophyte of maize (Zea mays), Enterobacter aero‐ for 3 min in 2% NaOCl, 3 min in 80% ethanol, and rinsed five times genes have been shown to alter the host plant's resistance to a fungal with
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