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New Endemic Fusarium Species Hitch-Hiking with Pathogenic Fusarium Strains Causing Panama Disease in Small-Holder Banana Plots in Indonesia

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New Endemic Fusarium Species Hitch-Hiking with Pathogenic Fusarium Strains Causing Panama Disease in Small-Holder Banana Plots in Indonesia Persoonia 43, 2019: 48–69 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2019.43.02 New endemic Fusarium species hitch-hiking with pathogenic Fusarium strains causing Panama disease in small-holder banana plots in Indonesia N. Maryani1,2,3, M. Sandoval-Denis4,5, L. Lombard4, P.W. Crous2,4,5, G.H.J. Kema1,2 Key words Abstract Fusarium species are well known for their abundance, diversity and cosmopolitan life style. Many members of the genus Fusarium are associated with plant hosts, either as plant pathogens, secondary invaders, saprotrophs, Indonesia and/or endophytes. We previously studied the diversity of Fusarium species in the Fusarium oxysporum species new species complex (FOSC) associated with Fusarium wilt of banana in Indonesia. In that study, several Fusarium species non-pathogenic not belonging to the FOSC were found to be associated with Fusarium wilt of banana. These Fusarium isolates phylogeny belonged to three Fusarium species complexes, which included the Fusarium fujikuroi species complex (FFSC), species complex Fusarium incarnatum-equiseti species complex (FIESC) and the Fusarium sambucinum species complex (FSSC). Using a multi-gene phylogeny that included partial fragments of the beta-tubulin (tub), calmodulin (cmdA), translation elongation factor 1-alpha (tef1), the internal transcribed spacer region of the rDNA (ITS), the large subunit of the rDNA (LSU), plus the RNA polymerase II large subunit (rpb1) and second largest subunit (rpb2) genes, we were able to identify and characterise several of these as new Fusarium species in the respective species complexes identified in this study. Article info Received: 1 August 2018; Accepted: 11 December 2018; Published: 14 March 2019. INTRODUCTION are considered as endophytes and their association with their known host plants is difficult to discern (Kuldau & Yates 2000). Fusarium is one of the most diverse fungal genera that has A complex of Fusarium spp. in the Fusarium oxysporum species been given much attention by mycologists and plant patholo- complex (FOSC) is causing Fusarium wilt on banana (Maryani gists (Snyder & Hansen 1940, Nelson et al. 1983, Geiser et et al. 2019), also known as Panama disease (Stover 1962). al. 2013, Aoki et al. 2014, 2018). Its global distribution, ability The ability of these notorious fungi to infect a wide range of to adapt to manifold climatic conditions, and colonisation of a banana varieties has resulted in substantial economic strain wide number of ecological niches and hosts, makes the diversity in several banana producing regions (Ploetz et al. 2015, http:// and abundance of Fusarium species unparalleled (Booth 1971, fusariumwilt.org/). Several studies acknowledged the diversity Gerlach & Nirenberg 1982, Geiser et al. 2013, Aoki et al. 2014). of Fusarium spp. pathogenic on banana and their worldwide The genus Fusarium includes some of the most devastating distribution, thus recognising the threat to global banana plant pathogens, affecting many agronomical crops. Two of cultivation (Ploetz 2006a, Ordonez et al. 2015, Maryani et al. its species, Fusarium graminearum and F. oxysporum, were 2019). However, to our knowledge, no study has been done included in the top 10 list of fungal plant pathogens regarded to assess which other Fusarium species might be associated as important in terms of scientific and economic impact (Dean with Fusarium wilt on bananas. et al. 2012, Geiser et al. 2013, Aoki et al. 2014). In this study, we report Fusarium species hitch-hiking with Besides their role as plant pathogens, Fusarium species are pathogenic Fusarium spp. causing Panama disease, isolated also known as endophytes or saprophytic colonisers (Leslie from local banana varieties in Indonesia. Therefore, we aim to et al. 1990, Bacon & Yates 2006). Many different Fusarium characterise these non-Fusarium oxysporum isolates, based species are associated with symptomatic and asymptomatic on multi-gene phylogenetic inference, supported by morpho- plants (Leslie et al. 1990, Wang et al. 2004, Pinaria et al. 2010), logical observations. although their role as pathogens can sometimes be difficult to determine via pathogenicity tests. However, many Fusarium species have not been associated with any disease symptoms MATERIALS AND METHODS on plants (Wang et al. 2004, Pinaria et al. 2010). Therefore, they Isolates Isolates were obtained from the pseudostems of local banana 1 Wageningen Plant Research, Wageningen, The Netherlands. plants clearly displaying symptoms of Fusarium wilt, which were 2 Wageningen University and Research, Laboratory of Phytopathology, Wageningen, The Netherlands; sampled in small-holder backyard plantations across Indonesia corresponding author e-mail: [email protected]. in 2014–2015 (Maryani et al. 2019). The dried pseudo stem 3 Biology Education, Universitas Sultan Ageng Tirtayasa (UNTIRTA), Banten, samples were cut into pieces of 2 × 3 cm and plated on Komada Indonesia. medium (Komada 1975). Single-spore isolates were derived 4 Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands. from resulting fungal colonies, and transferred to potato dex- 5 Faculty of Natural and Agricultural Sciences, Department of Plant Sciences, trose agar (PDA), on which they were maintained as working University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa. cultures, or stored in 20 % (v/v) glycerol at -80 °C for long term © 2019 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. N. Maryani et al.: New endemic fusaria on banana 49 preservation. All isolates were deposited in the Indonesian Culture Collection (InaCC) Cibinong, Indonesia. LS479437 LS479436 LS479435 – – – tub Morphological characterisation – – – – – – – – – Morphological characterisations of the Fusarium species were performed on PDA for colony growth rates, pigmentation and beta-tubulin. : tef1 production of aerial conidia; carnation leaf agar (CLA; Fisher et tub al. 1982) for formation of sporodochia and sporodochial conidia, – – – – – and synthetic low-nutrient agar (SNA; Nirenberg 1981) for chla- 3 numbers. mydospores. To induce sporulation, cultures were incubated under continuous white light (Osram L18W/840 Cool White) LS479868 LS479453 LS479439 LS479851 LS479442 LS479434 LS479850 LS479441 LS479433 LS479861 LS479862 – LS479447 LS479855 LS479443 rpb2 LS479856 LS479444 number for 7 d at 25 °C. Growth rates of all isolates were determined on PDA after 7 d incubation at 25 °C in the dark. Colony colour accession notation followed the mycological colour charts of Rayner accession (1970). Morphological characters were examined after mount- LS479872 LS479854 LS479882 LS479869 LS479454 LS479440 LS479871 LS479853 – LS479870 LS479852 – LS479880 LS479866 LS479451 – LS479881 LS479867 LS479452 LS479438 rpb1 ing fungal structures in sterile water and observed using light – – – – microscopy (Nikon Eclipse 80i microscope) with Differential GenBank/ENA Interference Contrast (DIC) optics and a Nikon AZ100 ster- : translation elongation factor 1-alpha gene; eomicroscope, both equipped with Nikon DS-Ri2 high definition tef1 and GenBank/ENA – – – – – – – – – colour digital cameras. Photographs and measurements were taken using the Nikon software NIS-elements D software v. 4.50. The length and width of at least 30 conidiogenous collection of cells and 50 conidia were measured, and the mean values, – – – – – – – – ITS LSU standard deviation (SD) with maximum-minimum values were year – calculated. All descriptions, illustrations and nomenclatural data were deposited in MycoBank (Crous et al. 2004). strain. origin, on cal DNA isolation, amplification and analyses ex-type : T – Genomic DNA was isolated using the DNA Wizard Magnetic DNA Purification System for Food kit (Promega, USA). Partial : RNA polymerase second largest subunit gene; : RNA information Maryani; collected gene sequences were determined for the RNA polymerase N. 2 rpb2 largest subunit gene (rpb1) using primers RPB1-Fa and RPB1- of 2015 – 2015 – 2014 – 2014 – 2014 – 2014 – 2014 – details G2R (O’Donnell et al. 2010), RNA polymerase second largest ABB ABB ABB 2015 LS479429 LS479417 LS479890 ABB LS479875 ABB LS479859 ABB 2015 ABB 2014 LS479445 LS479424 2014 LS479425 2014 LS479412 LS479426 LS479413 LS479885 LS479427 LS479414 LS479886 LS479874 LS479415 LS479887 LS479876 LS479888 LS479858 LS479878 LS479860 LS479879 LS479864 LS479446 LS479865 LS479449 LS479450 ABB 2015 ABB ABB 2014 2014 LS479421 LS479430 LS479418 LS479891 ABB subunit gene (rpb2) using primers RPB2-5f2 and RPB2-7cr with Host genotype Year Collection (O’Donnell et al. 2010), the translation elongation factor 1-alpha Indo: gene (tef1) using primers EF1 and EF2 (O’Donnell et al. 1998a), Kirana AA Kirana
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