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Secondary Metabolites Produced by Neofusicoccum Species Associated with Plants: a Review

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Secondary Metabolites Produced by Neofusicoccum Species Associated with Plants: a Review agriculture Review Secondary Metabolites Produced by Neofusicoccum Species Associated with Plants: A Review Maria Michela Salvatore 1 , Artur Alves 2 and Anna Andolfi 1,3,* 1 Department of Chemical Sciences, University of Naples Federico II, 80126 Naples, Italy; [email protected] 2 CESAM-Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal; [email protected] 3 BAT Center-Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples Federico II, 80055 Portici, Italy * Correspondence: andolfi@unina.it; Tel.: +39-081-2539179 Abstract: The genus Neofusicoccum is comprised of approximately 50 species with a worldwide distribution and is typically associated with plants. Neofusicoccum is well-known for the diseases it causes on economically and ecologically relevant host plants. In particular, members of this genus are responsible for grapevine diseases, such as leaf spots, fruit rots, shoot dieback, bud necrosis, vascular discoloration of the wood, and perennial cankers. Many secondary metabolites, including (−)-botryoisocoumarin A, botryosphaerones, cyclobotryoxide and isosclerone, were identified from species of Neofusicoccum and their structural variability and bioactivities might be associated with the role of these compounds in the fungal pathogenicity and virulence. In this review, we summarize the secondary metabolites from Neofusicoccum species focusing on the role of these compounds in the interaction between the fungus and host plant. Keywords: Botryosphaeria; Botryosphaeriaceae; phytopathogens; plant–fungus interaction; Botryosphaeria dieback Citation: Salvatore, M.M.; Alves, A.; Andolfi, A. Secondary Metabolites Produced by Neofusicoccum Species Associated with Plants: A Review. 1. Introduction Agriculture 2021, 11, 149. https:/// doi.org10.3390/agriculture11020149 The genus Neofusicoccum (Dothideomycetes, Botryosphaeriales, Botryosphaeriaceae) was introduced in 2006 to reassign species that were previously included in the genus Academic Editor: David Guest Fusicoccum and its sexual morph Botryosphaeria [1]. Initially, the genus included 13 species Received: 14 January 2021 but it has grown considerably, due mainly to the description of a large number of cryptic Accepted: 8 February 2021 species, and currently contains about 50 distinct species listed in MycoBank [2] and Index Published: 11 February 2021 Fungorum [3]. Species in the genus Neofusicoccum are typically associated with plants, being com- Publisher’s Note: MDPI stays neutral mon in a wide range of woody hosts, from forest trees to crops and ornamentals [4,5]. with regard to jurisdictional claims in The majority of these species have a worldwide distribution, a plurivorous nature, and published maps and institutional affil- exhibit an endophytic or latent pathogen lifestyle. Some Neofusicoccum species are plant iations. pathogens of increasing relevance, causing diseases, most commonly dieback and canker, on economically and ecologically relevant host plants, such as grapevine, olive, eucalypts, among many others [4,5]. Grapevine is a particularly relevant crop worldwide, and sev- eral species of Neofusicoccum have been reported to be pathogens of this host. In fact, N. Copyright: © 2021 by the authors. parvum is regarded as one of the most aggressive causal agents of Botryosphaeria dieback Licensee MDPI, Basel, Switzerland. of grapevine [6]. This article is an open access article In the last decade, literature concerning metabolites produced by Neofusicoccum species distributed under the terms and has been significantly enriched by many reports dealing with the biosynthetic potential of conditions of the Creative Commons this fungal genus. Attribution (CC BY) license (https:// This review is intended as a reference guide to secondary metabolites produced creativecommons.org/licenses/by/ by Neofusicoccum species, emphasizing their role in the fungal association with plants. 4.0/). Agriculture 2021, 11, 149. https://doi.org/10.3390/agriculture11020149 https://www.mdpi.com/journal/agriculture Agriculture 2021, 11, 149 2 of 19 The main part of this paper comprises over 90 compounds identified as products of Neofusicoccum species and collected in 10 classes on the basis of their chemical structures. Furthermore, some aspects relating to the biosynthesis of these metabolites and related compounds, as well as their bioactivities, are also discussed in dedicated subparagraphs. A final section includes information on the relevance of phytotoxic secondary metabolites produced by Neofusicoccum species associated to grapevine trunk diseases. 2. Secondary Metabolites Fungi from the genus Neofusicoccum are a promising source of secondary metabolites which can be classified according to their chemical structures. As can be seen from Table1, compounds produced by Neofusicoccum species belong to different classes of natural prod- ucts, including 5,6-dihydro-2-pyrones, melleins, myrtucommulones and naphthalenones, which have peculiar biological and chemical features. Table 1. List of secondary metabolites produced by Neofusicoccum species. Code Compound Formula Nominal Mass (U) Cyclohexenones 1 Cyclobotryoxide C8H10O4 170 2 (−)-Terremutin C7H8O4 156 3 (+)-Terremutin hydrate C7H10O5 174 4 (−)-4-Chloro-terremutin hydrate C7H9ClO4 192 5 (+)-4-Hydroxysuccinate-terremutin hydrate C11H14O8 274 6 (+)-epi-Sphaeropsidone C7H8O4 156 5,6-Dihydro-2-pyrones 7 Asperlin C10H12O5 212 8 (6R,7S)-Dia-asperlin C10H12O5 212 9 Luteopyroxin C9H12O4 184 Fatty acids 10 Elaidic acid C18H34O2 282 11 Ethyl elaidate C20H38O2 310 12 Linoleic acid C18H32O2 280 13 Ethyl linoleate C20H36O2 308 14 Methyl linoleate C19H34O2 294 15 9,12,15-Octadecatrienoate ethyl ester C20H34O2 306 16 Ethyl oleate C20H38O2 310 17 Methyl oleate C19H36O2 296 18 Palmitic acid C16H32O2 256 19 Methyl palmitate C17H34O2 270 20 Palmitoleic acid C16H30O2 254 21 Stearic acid C18H36O2 284 22 Ethyl stearate C20H40O2 312 23 Undecan-2-one C11H22O 170 Melleins 24 (R)-(−)-Mellein C10H10O3 178 25 (R)-(−)-3-Hydroxymellein C10H10O4 194 26 (3R,4R)-(−)-4-Hydroxymellein C10H10O4 194 27 (3R,4S)-(−)-4-Hydroxymellein C10H10O4 194 28 (3R)-5-Hydroxymellein C10H10O4 194 29 7-Hydroxymellein C10H10O4 194 30 (±)-Botryoisocoumarin A C11H12O4 208 31 (+)-Neoisocoumarin C10H10O5 210 Agriculture 2021, 11, 149 3 of 19 Table 1. Cont. Code Compound Formula Nominal Mass (U) Myrtucommulones 32 Myrtucommulone A C38H52O10 668 33 Myrtocommulone B C24H30O6 414 34 Myrtucommulone D C38H50O9 650 Naphthalenones 35 Botryosphaerone A C13H16O6 268 36 Botryosphaerone B C13H16O6 268 37 Botryosphaerone C C14H18O6 282 38 Botryosphaerone D C13H16O5 252 39 Isosclerone C11H12O2 176 40 O-Methylasparvenone C13H16O4 236 41 O-Methylaspmenone C10H10O3 178 42 (3R,4R)-3-Methoxyl-botryosphaerone D C14H18O5 266 43 3,4,5-Trihydroxy-1-tetralone C10H10O4 194 (3S,4S)-3,4,8-Trihydroxy-6-methoxy-3,4- 44 C H O 224 dihydro-1(2H)-naphthalenone 11 12 5 Naphthoquinones 45 Botryosphaenin C15H16O6 292 46 Neofusnaphthoquinone A C27H24O10 508 47 6-Ethyl-2,7-dimethoxyyjuglone C14H14O5 262 48 6-(1-Hydroxyethyl)-2,7-Dimethoxyjuglone C14H14O6 278 49 6-(1-Methoxylethyl)-2,7-dimethoxyjuglone C15H16O6 292 6-(1-Hydroxyethyl)-2,7-dimethoxyjuglone 50 C H O 320 monoacetate 16 16 7 5-Hydroxy-2,7-dimethoxynaphthalene-1,4- 51 C H O 234 dione 12 10 5 Phenols and alcohols 52 2-Ethyldecan-1-ol C12H26O 186 53 2-Hydroxypropyl salicylic acid C10H12O4 196 54 2-Methylbutan-1-ol C5H12O 88 55 3-Methylcatechol C7H8O2 124 56 6-Methyl-salicylic acid C8H8O3 152 57 Isobutanol C4H10O 74 58 Isopentyl alcohol C5H12O 88 59 p-Cresol C7H8O 108 60 Phenylethyl alcohol C8H10O 122 61 Tyrosol C8H10O2 138 Sesquiterpenes 62 Aristolene C15H24 204 63 Aristolochene C15H24 204 64 δ-Amorphene C15H24 204 65 Botryosterpene C16H22O3 262 66 Calarene C15H24 204 67 α-Cadinol C15H26O 222 68 α-Cedrene epoxide C15H24O 220 69 β-Cedren-9-one C15H24 204 70 α-Copaene C15H24 204 71 5-Neo-cedranol C14H24O 208 72 γ-Cadinene C15H24 204 73 δ-Cadinene C15H24 204 74 β-Elemene C15H24 204 Agriculture 2021, 11, 149 4 of 19 Table 1. Cont. Code Compound Formula Nominal Mass (U) 75 Ermophylene C15H24 204 76 Germacrene D C15H24 204 77 Globulol C15H26O 222 78 Guaiol acetate C17H28O2 264 79 Juniper camphor C15H26O 222 80 α-Selinene C15H24 204 81 Trans-cadina-1(2)-4-diene C15H24 204 82 Valecene C15H24 204 83 Zonarene C15H24 204 Miscellaneous 84 Azelaic acid C9H16O4 188 5-(Carboxymethyl)-7-hydroxy-1,4a- 85 dimethyl-6-methylene decahydron C16H24O5 296 aphthalene-1-carboxylic acid 86 (−)-Terpestacin C25H38O4 402 87 Luteoxepinone C9H12O4 184 88 Luteoethanone A C11H15NO3 209 89 Luteoethanone B C10H13NO3 195 90 Neoanthraquinone C18H16O4 296 91 (±)-Nigrosporione C8H10O4 170 Members of the genus Neofusicoccum are often symbiotically associated with differ- ent plant species. Symbiotic association between a fungus and a plant is a widespread phenomenon in nature and several symbiotic lifestyles have been defined considering the benefits to or impacts on host and symbiont [7]. Recent studies have indicated that botryosphaeriaceous fungi may express different symbiotic lifestyles in response to host internal signals or environmental factors which also influence the secondary metabolites production [8–12]. In fact, secondary metabolites may have a crucial role in the fungal lifestyles because these compounds have a broad number of biological functions, including mediating communication, nutrient acquisition and acting as virulence factors [13,14]. Neofusicoccum species found as endophytes
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