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The Banana Root Endophytome: Differences Between Mother Plants and Suckers and Evaluation of Selected Bacteria to Control Fusarium Oxysporum F.Sp

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The Banana Root Endophytome: Differences Between Mother Plants and Suckers and Evaluation of Selected Bacteria to Control Fusarium Oxysporum F.Sp Journal of Fungi Article The Banana Root Endophytome: Differences between Mother Plants and Suckers and Evaluation of Selected Bacteria to Control Fusarium oxysporum f.sp. cubense Carmen Gómez-Lama Cabanás 1 , Antonio J. Fernández-González 2,†, Martina Cardoni 1,† , Antonio Valverde-Corredor 1 , Javier López-Cepero 3, Manuel Fernández-López 2 and Jesús Mercado-Blanco 1,* 1 Departamento de Protección de Cultivos, Instituto de Agricultura Sostenible, Consejo Superior de Investigaciones Científicas (CSIC), Campus ‘Alameda del Obispo’ s/n, Avd. Menéndez Pidal s/n, 14004 Córdoba, Spain; [email protected] (C.G.-L.C.); [email protected] (M.C.); [email protected] (A.V.-C.) 2 Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Calle Profesor Albareda, 18008 Granada, Spain; [email protected] (A.J.F.-G.); [email protected] (M.F.-L.) 3 Departamento Técnico de Coplaca S.C. Organización de Productores de Plátanos, Avd. de Anaga, 11-38001 Santa Cruz de Tenerife, Spain; [email protected] * Correspondence: [email protected]; Tel.: +34-957-499261 Citation: Gómez-Lama Cabanás, C.; † These authors have contributed equally. Fernández-González, A.J.; Cardoni, M.; Valverde-Corredor, A.; Abstract: This study aimed to disentangle the structure, composition, and co-occurrence relationships López-Cepero, J.; Fernández-López, of the banana (cv. Dwarf Cavendish) root endophytome comparing two phenological plant stages: M.; Mercado-Blanco, J. The Banana mother plants and suckers. Moreover, a collection of culturable root endophytes (>1000) was also Root Endophytome: Differences generated from Canary Islands. In vitro antagonism assays against Fusarium oxysporum f.sp. cubense between Mother Plants and Suckers (Foc) races STR4 and TR4 enabled the identification and characterization of potential biocontrol agents and Evaluation of Selected Bacteria to (BCA). Eventually, three of them were selected and evaluated against Fusarium wilt of banana (FWB) Control Fusarium oxysporum f.sp. together with the well-known BCA Pseudomonas simiae PICF7 under controlled conditions. Culturable cubense. J. Fungi 2021, 7, 194. https://doi.org/10.3390/jof7030194 and non-culturable (high-throughput sequencing) approaches provided concordant information and showed low microbial diversity within the banana root endosphere. Pseudomonas appeared as the Academic Editors: Antonieta De Cal, dominant genus and seemed to play an important role in the banana root endophytic microbiome Inmaculada Larena and according to co-occurrence networks. Fungal communities were dominated by the genera Ophioceras, Paloma Melgarejo Cyphellophora, Plecosphaerella, and Fusarium. Overall, significant differences were found between mother plants and suckers, suggesting that the phenological stage determines the recruitment and Received: 3 February 2021 organization of the endophytic microbiome. While selected native banana endophytes showed Accepted: 5 March 2021 clear antagonism against Foc strains, their biocontrol performance against FWB did not improve the Published: 9 March 2021 outcome observed for a non-indigenous reference BCA (strain PICF7). Publisher’s Note: MDPI stays neutral Keywords: biocontrol agents; Canary Islands; Cavendish; co-occurrence networks; endophytes; with regard to jurisdictional claims in Fusarium wilt; Musa acuminata; Pseudomonas chlororaphis; Pseudomonas simiae PICF7 published maps and institutional affil- iations. 1. Introduction Banana (Musa spp.) is one of the most important fruit and cash crop in terms of Copyright: © 2021 by the authors. production volume and trade in the world [1,2]. The global production of bananas is Licensee MDPI, Basel, Switzerland. projected to grow at 1.5% per annum, to reach 135 million tonnes in 2028 [3]. However, a This article is an open access article number of soil-borne pests and diseases are principal limiting factors for banana production distributed under the terms and conditions of the Creative Commons worldwide [1,4]. Among them, Fusarium wilt of banana (FWB) is considered one of the Attribution (CC BY) license (https:// most destructive diseases affecting this crop (estimated affected area of 100,000 ha and creativecommons.org/licenses/by/ around US $2 billion losses according to Ploetz and co-workers [5]. The causal agent 4.0/). is the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc)(Fusarium oxysporum J. Fungi 2021, 7, 194. https://doi.org/10.3390/jof7030194 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 194 2 of 26 Schlechtend: Fr. sp. cubense (E.F. SM) W.C. Snyder & H.N. Hansen), which infects banana roots, progresses into the xylem of the rhizome, induces wilt, and may eventually kill susceptible cultivars [2,5]. There are four recognized races of Foc, which are traditionally identified based on their reaction on different host cultivars [6,7]. Race 1 (R1) isolates attack cultivars Gros Michel (AAA), Silk (AAB), Lady Finger (AAB), Maqueno (Maia Maoli-Popoulu subgroup) (AAB), Pome (AAB), and Pisang Awak (ABB). Race 2 (R2) causes disease in cooking bananas of the Monthan, Bluggoe (ABB) subgroup, other closely related cooking bananas and also affects some bred tetraploids and Enset. Currently, Race 3 is not considered pathogenic in banana, as it only attacks Heliconia spp. (tropical American banana relatives) [8,9]. Finally, Race 4 (R4) affects all cultivars belonging to the Cavendish (AAA) subgroup (the most common cultivar (cv.) in commercial banana plantations) and also those susceptible to R1 and R2 [6,7,10,11]. Race 4 is usually split up into subtropical (STR4) and tropical (TR4) races [12]. Whereas STR4 needs predisposing factors to cause FWB (e.g., plants subjected to cold temperatures and other abiotic stresses), TR4, which has been lately identified as a F. odoratissimum [13], is able to trigger the disease in Cavendish bananas grown under a broad range of conditions, and it is currently considered the most virulent form of the pathogen [6,7,14,15]. In addition, recent surveys in Asia show that TR4 does not only affect Cavendish bananas but also many other cultivars [16,17]. Nowadays, TR4 has been detected in several banana-producing countries, and its steady and alarming spread has raised a huge concern among producers and in the banana industry [18–20]. Thus, research and crop management efforts are currently ongoing to prevent the propagation of the disease, which can seriously compromise the future of this staple food [21–23]. Banana is the main intensive agricultural crop in the Canary Islands, which is a Spanish archipelago located in the Atlantic Ocean. Currently, FWB incidence in these islands ranges from 2 to 12%, although occasional disease incidences affecting up to 30% of the plants have been reported in some areas [14,24]. Fortunately, TR4 has not yet been detected in the archipelago, and only attacks by STR4 have been reported [6,23]. The control of FWB is specially challenging because Foc is (i) a soil-borne pathogen able to persist in the soil for decades, even in the absence of host plants or within alternate hosts that could remain asymptomatic; (ii) a vascular pathogen that is inaccessible to control measures (e.g., non-endophytic biological control agents (BCA), non-systemic fungicides, etc.) once established within the xylem; and (iii) easily spread by banana vegetative propa- gation material, soil, workers, machinery, irrigation water, etc. Moreover, the Cavendish banana monoculture expansion favors the dispersion of the disease, which is a particularly concerning scenario when TR4 is present [12,14,23,25]. Thus, an integrated disease man- agement strategy is the best option to mitigate the impact of FWB on susceptible varieties and to increase the durability of available resistant varieties [2,7]. Conventional measures to control FWB include resistant banana varieties, phytosanitary measures, crop rotation, flood-fallowing, application of organic amendments, soil solarization, and fungicides [6]. Within this integrated management strategy, the use of microbial BCA constitutes a promising and environmentally friendly approach [14]. It is accepted that the plant- associated microbiome, usually an important source of BCA, is crucial for the host’s health, development, and productivity [26]. In this framework, the banana belowground micro- biome is hypothesized to play essential roles, as it has already been studied in different agricultural pathosystems [27,28], including the banana–Foc interaction [1,2,29–32]. Thus, in-depth analyses of the structure, composition, dynamics, and functionality of the root- associated microbiome are useful to improve disease control approaches. Moreover, a comprehensive knowledge on how the plant-associated microbiome is influenced by fac- tors such as the host genotype and its phenological stages, and/or by environmental and pedological parameters is crucial to understand how the plant holobiont cope with a/biotic stresses. In this sense, it is worth mentioning that root endophytic microbial communities may play essential roles such as, for instance, being an important line of defense against vascular pathogens [33,34]. Hence, the manipulation and harnessing of the endophytic mi- J. Fungi 2021, 7, 194 3 of 26 crobiome may help to increase crop production, reduce the incidence of diseases, improve plant resistance, and decrease agrochemicals inputs [2]. Many endophytes are not culturable. For this reason, both culturable-based
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