Biocontrol Properties of Basidiomycetes: an Overview

Home , Cyptotrama, Heterobasidiomycetes, Lactarius rufus, Meloidogyne arenaria, Neonothopanus nambi, Pleurotus

Journal of Fungi

Review Biocontrol Properties of Basidiomycetes: An Overview

Subramaniyan Sivanandhan 1, Ameer Khusro 2, Michael Gabriel Paulraj 1, Savarimuthu Ignacimuthu 1,3,* and Naif Abdullah AL-Dhabi 4

1 Entomology Research Institute, Loyola College, Nungambakkam, Chennai 600034, Tamil Nadu, India; [email protected] (S.S.); [email protected] (M.G.P.) 2 Department of Plant Biology and Biotechnology, Loyola College, Nungambakkam, Chennai 600034, Tamil Nadu, India; [email protected] 3 The International Scientiﬁc Partnership Program (ISPP), King Saud University, Riyadh 11451, Saudi Arabia 4 Department of Botany and Microbiology, College of Science, King Saud University, P. O. BOX 2454, Riyadh 11451, Saudi Arabia; [email protected] * Correspondence: [email protected]; Tel.: +91-44-2817-8348

Academic Editor: David S. Perlin Received: 27 October 2016; Accepted: 29 December 2016; Published: 10 January 2017

Abstract: In agriculture, there is an urgent need for alternate ecofriendly products to control plant diseases. These alternate products must possess preferable characteristics such as new modes of action, cost effectiveness, biodegradability, and target specificity. In the current scenario, studies on macrofungi have been an area of importance for scientists. Macrofungi grow prolifically and are found in many parts of the world. Basidiomycetes (mushrooms) flourish ubiquitously under warm and humid climates. Basidiomycetes are rich sources of natural antibiotics. The secondary metabolites produced by them possess antimicrobial, antitumor, and antioxidant properties. The present review discusses the potential role of Basidiomycetes as anti-phytofungal, anti-phytobacterial, anti-phytoviral, mosquito larvicidal, and nematicidal agents.

Keywords: biocontrol properties; basidiomycetes; anti-phytofungal activity; anti-phytobacterial activity; anti-phytoviral activity; phytonematicidal activity; mosquito larvicidal activity

1. Introduction Synthetic chemicals are extensively used in all countries for controlling agricultural pests and plant pathogens [1]. Currently 15% of global crop production is lost due to crop pests [2]. To counteract this, agrochemicals are used in excessive quantities/volumes; it has become apparent that these chemicals are responsible for causing environmental pollution. They leave their residues in food [3]. Unrestrained application of synthetic chemicals causes pesticide resistance, toxicity to humans, plants, and animals, and therefore they are regarded as ecologically unacceptable [4]. Mosquitoes are the most well-known vectors of disease causing pathogens which affect millions of people every year [5]. In India, major diseases are caused by mainly three types of mosquitoes [6], namely Aedes aegypti L., Anopheles stephensi (Liston), and Culex quinquefasciatus (Say). Ae. aegypti is a known vector for dengue and chikungunya virus. The malarial parasite is transmitted by An. stephensi and the ﬁlarial nematode is transmitted by Cx. quinquefasciatus. Prevention of mosquito borne diseases is important in order to improve public health, and it is primarily achieved by controlling the vector mosquito population. In recent years, mosquito control programs have encountered failures due to the rapid development of pesticide resistance in mosquitoes [7]. Nematodes have been present for nearly a billion years and are known to cause severe losses to farmers [8]. They feed on many, if not all plants [9]. This pathogen is predominantly part of class

J. Fungi 2017, 3, 2; doi:10.3390/jof3010002 www.mdpi.com/journal/jof J. Fungi 2017, 3, 2 2 of 14

J. Fungi 2017, 3, 2 2 of 14 Chromodorea, order Rhabdihida [10]. Due to chemical contamination of soil caused by commercial Chromodorea, order Rhabdihida [10]. Due to chemical contamination of soil caused by commercial nematicides, newer sources of eco-friendly biomolecules are required in the future. nematicides, newer sources of eco-friendly biomolecules are required in the future. Pest and pathogen diversities are continuously expanding and new strains are continuously Pest and pathogen diversities are continuously expanding and new strains are continuously evolving over time [11]. Scientists are looking for safe and more potent alternate products for evolving over time [11]. Scientists are looking for safe and more potent alternate products for controlling plant pathogens and pests. The use of natural products for pest control is ideal for controlling plant pathogens and pests. The use of natural products for pest control is ideal for sustainable agricultural production with minimum damage to the environment [12]. Basidiomycetes sustainable agricultural production with minimum damage to the environment [12]. Basidiomycetes are the fruiting bodies of higher fungi [13]. Several compounds have been isolated from wild are the fruiting bodies of higher fungi [13]. Several compounds have been isolated from wild Basidiomycetes (Figure1) which showed growth inhibition of bacteria, virus, and fungi (Table1) Basidiomycetes (Figure 1) which showed growth inhibition of bacteria, virus, and fungi (Table 1) and recorded nematicidal and insecticidal properties [14–27]. In the last few years, Basidiomycetes and recorded nematicidal and insecticidal properties [14–27]. In the last few years, Basidiomycetes have received great attention due to their medicinal values, easy availability, and lower side effects have received great attention due to their medicinal values, easy availability, and lower side effects and toxicity on non-target organisms [28]. There are nearly 140,000 Basidiomycetes species reported and toxicity on non-target organisms [28]. There are nearly 140,000 Basidiomycetes species reported among which about 660 species possess medicinal properties [29]. A number of pharmaceutical among which about 660 species possess medicinal properties [29]. A number of pharmaceutical substances with potent and unique characteristics have been extracted from Basidiomycetes [30]. substances with potent and unique characteristics have been extracted from Basidiomycetes [30]. Higher Basidiomycetes contain active polysaccharides in their fruiting bodies, cultured mycelia, Higher Basidiomycetes contain active polysaccharides in their fruiting bodies, cultured mycelia, and and cultured broth [31]. The present review focused on anti-phytofungal, anti-phytobacterial, cultured broth [31]. The present review focused on anti-phytofungal, anti-phytobacterial, anti-phytoviral, phytonematicidal, and mosquito larvicidal activity of Basidiomycetes. anti-phytoviral, phytonematicidal, and mosquito larvicidal activity of Basidiomycetes.

Figure 1. Some of the biocontrol propertiesproperties of Basidiomycetes compounds.

Plant Fungal Diseases Fungi may cause catastrophic plant diseases, because many fungi sporulate prolificallyprolifically and the spores provideprovide copiouscopious inoculums inoculums which which may may infect infect further further plants. plants. The The time time between between infection infection and and the productionthe production of further of further infectious infectious propagules propagules (usually (usually spores) mayspores) be onlymay abe few only days a [32few]. Thedays spores, [32]. ifThe they spores, are wettable, if they are may wettable, be spread may as be high-density spread as high-density inoculums in inoculums surface water in surface or in dropletswater or byin rain-splashdroplets by [33rain-splash]. They may [33]. produce They may phytotoxic produce compounds phytotoxic [34 compounds]. Pathogens [34]. may Pathogens draw nutrients may awaydraw fromnutrients the plantaway by from the production the plant or by induction the producti of growthon regulatorsor induction [32 ].ofColletotrichum growth regulators gloeosporioides [32]. (anamorph)Colletotrichum or gloeosporioidesGlomerella cingulata (anamorph)(teleomorph) or Glomerella causes cingulata anthracnoses (teleomorph) in many tropicalcauses anthracnoses and subtropical in cropsmany [tropical35]. Considerable and subtropical variation crops occurs [35]. inConsiderable culture and hostvariation range, occurs with somein culture strains and able host to range, attack manywith some host speciesstrains whereasable to attack others, many such host as those spec infectingies whereas mango, others, are confinedsuch as those to asingle infecting species mango, [36]. Molecularare confined approaches to a single demonstrated species [36]. that MolecularC. gloeosporioides approachesinfecting demonstratedStylosanthes thatin Australia C. gloeosporioides consisted ofinfecting two clone Stylosanthes populations in Australia that did not consisted combine of readily two clone in the popu fieldlations which that had did resulted not combine from two readily separate in introductionsthe field which into had the resulted country from [37 ].two Some separate strains intr ofoductionsC. gloeosporioides into thepresent country a [37]. considerable Some strains threat of C. to cropsgloeosporioides growing present in countries a considerable where there threat is no to fallow crops period growing corresponding in countries to where the winter there ofis temperateno fallow climatesperiod corresponding [38]. Rice is second to the winter only to of maize temperate in global climat productiones [38]. Rice [39 is]. second It is more only important to maize sincein global it is theproduction staple food [39]. for It aboutis more half important of the world’s since populations. it is the staple It is food attacked for byabout the Ascomycetehalf of the world’s fungus Pyriculariapopulations. oryzae It is(teleomorph), attacked by theMagnaporthe Ascomycete grisea fungus, causing Pyricularia rice blast, oryzae resulting (teleomorph), in 10%–30% Magnaporthe crop loss everygrisea, yearcausing [40 ].rice More blast, than resulting 700 ha in of 10%–30% rice of diverse crop loss genotypes every year with [40]. varying More levels than 700 of resistance ha of rice inof diverse genotypes with varying levels of resistance in Bhutan were affected in 1995 resulting in losses of 1090 tonnes [40]. Other cereals are also affected by P. oryzae or similar species [41]. These

J. Fungi 2017, 3, 2 3 of 14

J. Fungi 2017, 3, 2 3 of 14 J. Fungi 2017, 3, 2 3 of 14 BhutanJ.J. FungiFungi were 20172017, affected, 33,, 22 in 1995 resulting in losses of 1090 tonnes [40]. Other cereals are also affected33 ofof 1414 by P. oryzae or similar species [41]. These include ﬁnger millet, Eleusine coracana, which, when attacked include finger millet, Eleusine coracana, which, when attacked before grain formation, can suffer beforeincludeinclude grain fingerfinger formation, millet,millet, Eleusine can suffer coracana complete,, which,which, loss whenwhen of yieldattackedattacked [40 ].beforebeforeP. oryzae graingrain causedformatioformatio yieldn, can losses suffer up to complete loss of yield [40]. P. oryzae caused yield losses up to 40% in Tanzania [42]. Several fungi complete loss of yield [40]. P. oryzae caused yield losses up to 40% in Tanzania [42]. Several fungi 40%produce in Tanzania powerful [42 ].mycotoxins. Several fungi For example, produce the powerful Fumonisin mycotoxins. toxins were discovered For example, in the the Transkei Fumonisin produce powerful mycotoxins. For example, the Fumonisin toxins were discovered in the Transkei toxinsregion were of discoveredSouth Africa. in They the Transkeiwere isolated region from of Southcultures Africa. of Gibberella They fujikuroi were isolated (anamorph) from and cultures regionregion ofof SouthSouth Africa.Africa. TheyThey werewere isolatedisolated fromfrom culturescultures ofof Gibberella fujikuroi (anamorph)(anamorph) andand of GibberellaFusarium moniliforme fujikuroi (anamorph) grown on maize, and andFusarium the most moniliforme active compoundgrown was on designated maize, and as thefumonisin most active Fusarium moniliforme growngrown onon maize,maize, andand thethe mostmost activeactive compound was designated as fumonisin B1 (FB1) [43]. FB1 is a sphinganine analogue that, in both plant and animal cells, competitively compoundB1 (FB1) was [43]. designated FB1 is a sphinganine as fumonisin analogue B1 (FB1) that, [ 43in ].both FB1 plant is a sphinganineand animal cells, analogue competitively that, in both inhibits sphingolipid biosynthesis causing sphingoid bases to accumulate [44]. High levels of plantinhibitsinhibits and animal sphingolipidsphingolipid cells,competitively biosynthesisbiosynthesis causingcausing inhibits sphingoidsphingoid sphingolipid basesbases biosynthesis toto accumulateaccumulate causing [44].[44]. HighHigh sphingoid levelslevels basesofof to virulence for maize were always associated with strains of the fungus that produce fumonisins [45]. accumulatevirulence [ 44for]. maize High were levels always of virulence associated for with maize strainsrains were ofof always thethe fungusfungus associated thatthat produce with fumonisins strains of the[45]. fungus that produce fumonisins [45]. 2. Biocontrol Properties of Basidiomycetes 2. Biocontrol Properties of Basidiomycetes Table 1. 2.1. Anti-Phytofungal ActivityActive (Table compounds 1) isolated from different mushroom species. 2.1. Anti-Phytofungal Activity (Table 1)

Active CompoundTable 1. Active Compound compounds Structure isolated from different mushroom Target Pathogen species. Reference Table 1. ActiveActive compoundscompounds isolatedisolated fromfrom differentdifferent mushroommushroom species.species. Ganodermin Active Compound Compound Structure Target Pathogen Reference (GanodermaActive Compound lucidum) CompoundNA StructurePhysalospora Target piricola;Pathogen Botytis cinerea Reference[19] Ganodermin (Ganoderma GanoderminAntifungal protein (Ganoderma NA Physalospora piricola; Botytis cinerea [19] lucidum) Antifungal protein NA Physalospora piricola; Botytis cinerea [19][19] Pleurostrinlucidumlucidum)) ( AntifungalPleurotusAntifungal ostreatus proteinprotein) Pleurostrin (Pleurotus NA Botryosphaeria berengeriana [20] AntifungalPleurostrin protein (Pleurotus NA Botryosphaeria berengeriana [20] ostreatus) Antifungal protein NA Botryosphaeria berengeriana [20] ostreatus) Antifungal protein NA Botryosphaeria berengeriana [20] ErynginostreatusEryngin ())Pleurotus Antifungal(AntifungalPleurotus eryngii eryngii proteinprotein) ) Eryngin (Pleurotus eryngii) NA Mycosphaerella arachidicola [20,23] ErynginAntifungal (Pleurotus protein eryngii)) NA Mycosphaerella arachidicola [20,23] Antifungal protein NA Mycosphaerella arachidicola [20,23][20,23] Antifungal protein AntifungalAntifungal protein protein mLAP mLAP Antifungal protein mLAP NA PhysalosporaPhysalospora piricola piricola [22] [22] (Lyophyllum(Lyophyllum shimeji shimeji) ) NA Physalospora piricola [22][22] ((Lyophyllum shimeji))

Lyophyllin (Lyophyllus Lyophyllin (Lyophyllus Physalospora piricola [22] LyophyllinLyophyllin (Lyophyllus (Lyophyllus shimeji ) PhysalosporaPhysalospora piricola piricola [22] [22] shimeji) Physalospora piricola [22][22] shimejishimeji))

Alternaria alternate; Pyricularia AlternariaAlternaria alternatealternate;;;Pyricularia PyriculariaPyriculariaoryzae ; oryzae; Rhizoctonia solani; Sclerotina Grifoline (Albatrellus oryzaeoryzaeRhizoctonia;; RhizoctoniaRhizoctonia solani; Sclerotinasolanisolani;; SclerotinaSclerotina sclerotiorum ; Grifoline (Albatrellus sclerotiorum; Fusarium graminearum; [46] Grifoline (Albatrellusdispansus dispansus) ) sclerotiorumFusarium graminearum;; Fusarium graminearum; Botytis cinerea; [46] [46] dispansus) sclerotiorumBotytis cinerea;; Fusarium Gaeumannomyces graminearum; [46] dispansus)) BotytisGaeumannomyces cinerea; Gaeumannomyces graminis; Botytis cinerea; Gaeumannomyces graminis; Gloesporium fructigenum graminisGloesporium;; GloesporiumGloesporium fructigenum fructigenumfructigenum Hypsin (Hypsizigus HypsinHypsin (Hypsizigus (Hypsizigus marmoreus ) BotryosphaeriaBotryosphaeria berengeriana berengeriana; ;Botytis Botytis cinerea ; marmoreus) Antifungal NA Botryosphaeria berengeriana;; BotytisBotytis [47] [47] marmoreusAntifungal)) proteinAntifungalAntifungal NA cinerea;Mycosphaerella Mycosphaerella arachidicola arachidicola [47][47] protein cinereacinerea;; MycosphaerellaMycosphaerella arachidicolaarachidicola protein

Alternaria alternata; Fusarium Rufuslactone (Lactarius AlternariaAlternaria alternata alternata; Fusarium;; FusariumFusarium graminearum ; RufuslactoneRufuslactone (Lactarius (Lactarius rufus ) graminearum; Botytis cinerea; [48] [48] rufus) graminearumBotytis cinerea;;; BotytisBotytis Alternaria cinerea;cinerea; brassicae [48][48] rufusrufus)) Alternaria brassicae Alternaria brassicae Cordymin (Cordyceps Rhizoctonia solani; Mycosphaerella CordyminCordymin (Cordyceps (Cordyceps militaris ) NA RhizoctoniaRhizoctonia solani solani; Mycosphaerella; Mycosphaerella [49] Cordymin (Cordyceps NA Rhizoctonia solani;; MycosphaerellaMycosphaerella [49] [49] militarisAntifungal) Antifungal protein protein NA arachidicolaarachidicola; Bipolaris; Bipolaris maydis maydis [49][49] militaris)) AntifungalAntifungal proteinprotein arachidicolaarachidicola;; BipolarisBipolaris maydismaydis

p-Hydroxybenzoic and p-Hydroxybenzoic p-Hydroxybenzoicp-Hydroxybenzoic and and p-Hydroxybenzoic Trichoderma viride; Penicillium Cinnamicp-Hydroxybenzoic acids (Ganoderma and TrichodermaTrichoderma viride viride; Penicillium; Penicillium ochrochloron ; [50] CinnamicCinnamic acids acids (Ganoderma Trichodermaochrochloron viride; P. funiculosum;; PenicilliumPenicillium [50] [50] Cinnamic acids (Ganoderma ochrochloronP. funiculosum; P. funiculosum [50][50] lucidum) ochrochloronochrochloron;; P.P. funiculosumfuniculosum (Ganodermalucidumlucidum lucidum)) )

Cinnamic acids Cinnamic acids

J. Fungi 2017, 3, 2 4 of 14

J. Fungi 2017, 3, 2 4 of 14 J. Fungi 2017, 3, 2 4 of 14 J.J. Fungi Fungi 2017 2017, ,3 3, ,2 2 Table 1. Cont. 44 of of 14 14

J. Fungi 2017, 3, 2 4 of 14 Active Compound Compound Structure Target Pathogen Reference

Chrysotrione A Chrysotrione A Chrysotrione A and B Chrysotrione A Chrysotrione A Fusarium verticillioides [50] Chrysotrione(HygrophorusChrysotrioneChrysotrione A chrysodon A andA andand B BB ) Chrysotrione A Chrysotrione A and B FusariumFusariumFusarium verticillioidesverticillioides verticillioides [50][50] [50] (Hygrophorus(Hygrophorus chrysodon chrysodon) ) Chrysotrione A Fusarium verticillioides [50] ((HygrophorusHygrophorus chrysodon chrysodon)) Chrysotrione A and B Fusarium verticillioides [50] (Hygrophorus chrysodon)

Chrysotrione B Chrysotrione B Chrysotrione B ChrysotrioneChrysotrione B B Agrocybin (Agrocybe Agrocybin (Agrocybe cylindracea) MycosphaerellaMycosphaerella arachidicola arachidicola [51] [51] Agrocybin (Agrocybe Chrysotrione B AgrocybinAgrocybincylindracea ( (AgrocybeAgrocybe) Mycosphaerella arachidicola [51] cylindracea) MycosphaerellaMycosphaerella arachidicola arachidicola [51][51] cylindraceacylindracea)) LentinAgrocybin (Lentinus (Agrocybe edodes ) Lentin (Lentinus edodes) NA Mycosphaerella arachidicola [51][52] Lentin (Lentinus edodes) NA Mycosphaerella arachidicola [52] LentinAntifungalLentinAntifungalcylindracea ( (LentinusLentinus protein protein )edodes edodes )) NA Mycosphaerella arachidicola [52] Antifungal protein NANA MycosphaerellaMycosphaerella arachidicola arachidicola [52][52] AntifungalAntifungal protein protein 1-hydroxypyreneLentin (Lentinus ( Cordycepsedodes) 1-hydroxypyrene1-hydroxypyrene (Cordyceps NA MycosphaerellaFusarium oxysporum arachidicola [52][53] 1-hydroxypyrene1-hydroxypyreneAntifungalmilitaris protein )( (CordycepsCordyceps FusariumFusarium oxysporum oxysporum [53] [53] (Cordycepsmilitaris militaris) ) FusariumFusarium oxysporum oxysporum [53][53] militarismilitaris)) 1-hydroxypyrene (Cordyceps Fusarium oxysporum [53] militaris) Gloeosporium orbiculare; Pyricularia Phellinsin A (Phellinus sp.) Gloeosporium orbiculare; Pyricularia [54] Phellinsin A (Phellinus sp.) GloeosporiumGloeosporium orbiculare orbicularegrisea ; ;Pyricularia Pyricularia [54] PhellinsinPhellinsinPhellinsin A A (APhellinus ( (PhellinusPhellinussp.) sp.) sp.) Gloeosporium orbicularegrisea ; Pyricularia grisea [54][54] [54] griseagrisea Gloeosporium orbiculare; Pyricularia Phellinsin A (Phellinus sp.) [54] Note: NA—not available. grisea Note: NA—not available. Note:Note: NA—not NA—not available. available. The antifungal agent Grifoline isolated from Albatrellus dispansus was effective against several The antifungal agent Grifoline isolated from Albatrellus dispansus was effective against several plantTheThe fungi antifungalantifungal in in vitro agentagent studies GrifolineGrifoline [46]. isolatedPhellinsinisolatedNote: NA—not fromfrom A was AlbatrellusAlbatrellus available. isolated dispansus dispansus from Phellinus waswas effectiveeffective sp. It wasagainstagainst capable severalseveral of 2. Biocontrolplant fungi Properties in in vitro ofstudies Basidiomycetes [46]. Phellinsin A was isolated from Phellinus sp. It was capable of plantinhibitingplant fungifungi the inin ingrowthin vitrovitro studiesstudiesof fungi [46].[46]. such PhellinsinPhellinsin as Gloeosporium AA waswas isolatedisolated orbiculare fromfrom, Pyricularia PhellinusPhellinus sp.sp.grisea ItIt ,was wasThanatephorus capablecapable ofof inhibitingThe antifungal the growth agent of Grifolinefungi such isolated as Gloeosporium from Albatrellus orbiculare dispansus, Pyricularia was effective grisea ,against Thanatephorus several inhibitingcucumerisinhibiting, theAspergillusthe growthgrowth fumigatusofof fungifungi , suchsuchand asTrichophytonas GloeosporiumGloeosporium mentagrophytes orbiculareorbiculare,, PyriculariaPyricularia [54]. A majorgriseagrisea ,, compoundThanatephorusThanatephorus in 2.1. Anti-Phytofungalplantcucumeris fungi, Aspergillusin in vitro Activity fumigatusstudies (Table [46]., 1)and Phellinsin Trichophyton A was mentagrophytes isolated from Phellinus[54]. A majorsp. It wascompound capable ofin cucumerisagriculturalcucumeris,, Aspergillus Aspergilluschemistry wasfumigatusfumigatus derive,, dand andfrom TrichophytonTrichophyton the pine cone mentagrophytesmentagrophytes fungus, Strobilurus [54].[54]. tenacellus AA majormajor [55]. compoundcompound Strobilurins inin inhibitingagricultural the chemistry growth wasof fungiderive suchd from as the Gloeosporium pine cone fungus, orbiculare Strobilurus, Pyricularia tenacellus grisea [55]., Thanatephorus Strobilurins agriculturalareagriculturalThe a antifungalclass chemistrychemistryof fungicidal agent waswas Grifoline derivederivecompounds,dd from isolatedfrom thethewhich pine frompine are coneconeAlbatrellus extracted fungus,fungus, Strobilurus Strobilurus dispansusfrom mycelia tenacellus wastenacellus effectiveof the[55]. [55]. S. StrobilurinsStrobilurins againsttenacellus. several cucumerisare a class, Aspergillus of fungicidal fumigatus compounds,, and Trichophyton which are mentagrophytesextracted from [54].mycelia A majorof the compound S. tenacellus. in plantareStrobilurinsare fungi aa classclass in in Aofof vitro (Figure fungicidalfungicidalstudies 2a) and compounds,compounds, [46 B ].(Figure Phellinsin 2b),whichwhich that A are are was highlyextractedextracted isolated active fromfrom from by inhibitingmyceliamyceliaPhellinus ofof respiration sp.thethe ItS.S. wastenacellus.tenacellus. of capableyeast of agriculturalStrobilurins chemistryA (Figure was2a) and derive B (Figured from the2b), pine that coneare highly fungus, active Strobilurus by inhibiting tenacellus respiration [55]. Strobilurins of yeast inhibitingStrobilurinsandStrobilurins other the filamentous growth AA (Figure(Figure of fungi 2a)fungi2a) andand such[56]. BB (Figure(Figure asTheGloeosporium biochemical 2b),2b), thatthat are areactivities orbiculare highlyhighly of ,activeactivePyricularia strobilurins byby inhibitinginhibiting grisea involve, Thanatephorus respirationrespiration ubihydroquinone ofof yeastyeast cucumeris , areand aother class filamentous of fungicidal fungi compounds, [56]. The biochemical which are activities extracted of strobilurins from mycelia involve of ubihydroquinonethe S. tenacellus. Aspergillusandcytochromeand otherother fumigatus filamentousfilamentous reductase,, and fungifungi whichTrichophyton [56].[56]. plays TheThe biochemicalbiochemicala mentagrophytescrucial role activitiesactivities in respiration[ 54 ofof ]. strobilurinsstrobilurins A major[57]. involveinvolveTheir compound activity, ubihydroquinoneubihydroquinone inhowever, agricultural Strobilurinscytochrome Areductase, (Figure 2a) which and Bplays (Figure a 2b),crucial that role are highlyin respiration active by [57]. inhibiting Their respirationactivity, however, of yeast cytochromedependscytochrome on thereductase,reductase, presence whichwhich of (E)- playsβplays-methoxyacrylate aa crucialcrucial rolerole moiety inin respirationrespiration [58]. Strobilurin [57].[57]. Their Theirfungicides activity,activity, have however,however, become chemistryanddepends other was on filamentous the derived presence fungi from of [56].(E)- theβ The-methoxyacrylate pine biochemical cone fungus, activities moietyStrobilurus [58].of strobilurins Strobilurin tenacellus involve fungicides[55 ubihydroquinone]. Strobilurinshave become are a dependsvaluabledepends ontoolson thethe for presencepresence managing ofof (E)-(E)- plantββ-methoxyacrylate-methoxyacrylate diseases [59]. These moietymoiety strobilurins [58].[58]. StrobilurinStrobilurin are site fungicidesfungicides specific (inhibition havehave becomebecome of classcytochromevaluable of fungicidal tools reductase, for compounds, managing which plant whichplays diseases a are crucial extracted [59]. role These in from respirationstrobilurins mycelia [57].are of thesiteTheir S.specific tenacellusactivity, (inhibition however,. Strobilurins of valuablemitochondrialvaluable toolstools forforrespiration) managingmanaging and plantplant translaminar diseasesdiseases [59].[59]. (systemic) TheseThese strobilurinsstrobilurins compounds areare sitesitethat specific specificprovide (inhibition(inhibition control ofof A (Figuredependsmitochondrial2a) on and the B respiration)presence (Figure of2b), (E)-and thatβ -methoxyacrylatetranslaminar are highly active(systemic) moiety by [58]. inhibitingcompounds Strobilurin respiration that fungicides provide of have yeast control become and of other mitochondrialOomycota,mitochondrial Ascomycota, respiration)respiration) Basidiomycota andand translaminartranslaminar, and Deuteromycota (systemic)(systemic) fungi. compoundscompounds (E)-β-methoxyacrylates thatthat provideprovide of controlstrobilurincontrol ofof ﬁlamentousvaluableOomycota, fungitools Ascomycota, [for56 ].managing The Basidiomycota biochemical plant ,diseases and activities Deuteromycota [59]. ofThese strobilurins fungi.strobilurins (E)- involveβ-methoxyacrylates are site ubihydroquinone specific (inhibitionof strobilurin cytochrome of Oomycota,COomycota, (Figure Ascomycota,Ascomycota,2c) and Oudemansin BasidiomycotaBasidiomycota B,, andand(Figure DeuteromycotaDeuteromycota 2d) from fungi. fungi.cultures (E)-(E)- ββof-methoxyacrylates-methoxyacrylates Xerula pudens inhibit ofof strobilurinstrobilurin many mitochondrialC (Figure 2c) respiration)and Oudemansin and translaminarB (Figure 2d) (systemic) from cultures compounds of Xerula that pudensprovide inhibit control many of reductase,CphytopathogenicC (Figure(Figure which 2c)2c) playsandand fungi. OudemansinOudemansin a Like crucial the rolestrobilurins BB in(Figure(Figure respiration A 2d) 2d)and from fromB, [ 57they ].culturescultures have Their also of activity,of beenXerulaXerula shown however, pudenspudens to inhibitinhibit depends fungalmanymany on the Oomycota,phytopathogenic Ascomycota, fungi. Basidiomycota Like the strobilurins, and Deuteromycota A and B, they fungi. have (E)- alsoβ-methoxyacrylates been shown to inhibitof strobilurin fungal presencephytopathogenicrespirationphytopathogenic of (E)- β[60].-methoxyacrylate fungi. fungi.Strobilurin LikeLike thethe strobilurinsEstrobilurins moiety(Figure [58 AA].2e) andand Strobilurin is B,B, theytheyanother havehave fungicides alsoalsoantifungal beenbeen have shownshown compound become toto inhibitinhibit valuableof fungalfungal the tools Crespiration (Figure 2c)[60]. and StrobilurinOudemansin E B (Figure(Figure 2e)2d) fromis another cultures antifungalof Xerula pudenscompound inhibit of many the for managingrespiration(E)-respirationβ-methoxyacrylate plant[60].[60]. diseasesStrobilurinStrobilurin class [ 59extracted ].EE These (Figure(Figure from strobilurins 2e)mycelial2e) isis areanotheranothercultures site speciﬁcofantifungalantifungal Crepidotus (inhibition compoundcompound fulvotomentosus of mitochondrial ofof . thetheIn phytopathogenic(E)-β-methoxyacrylate fungi. classLike theextracted strobilurins from Amycelial and B, they cultures have alsoof Crepidotus been shown fulvotomentosus to inhibit fungal. In respiration)(E)-addition(E)-ββ-methoxyacrylate-methoxyacrylate andto inhibiting translaminar classfungalclass (systemic)extractedextracted respiration, fromfrom compounds it mycelialhasmycelial been that culturesculturesshown provide toofof induce CrepidotusCrepidotus control cell of fulvotomentosusdeformationsfulvotomentosusOomycota, Ascomycota, [57]... InIn respirationaddition to inhibiting[60]. Strobilurin fungal respiration,E (Figure it 2e)has beenis another shown toantifungal induce cell compound deformations of [57].the BasidiomycotaadditionStrobilurinsaddition to,to and Dinhibitinginhibiting (FigureDeuteromycota 2f) fungalfungal and F respiration,(Figurerespiration,fungi. 2g) (E)- are itit βhasotherhas-methoxyacrylates beenbeen strobilurins, shownshown toextractedto induceinduce of strobilurin from cellcell mycelialdeformationsdeformations C (Figure cultures [57].[57].2 c)of and (E)-Strobilurinsβ-methoxyacrylate D (Figure 2f)class and extractedF (Figure 2g)from are mycelialother strobilurins, cultures extractedof Crepidotus from mycelialfulvotomentosus cultures. Inof StrobilurinstheStrobilurins Basidiomycete D D (Figure(Figure Merismodes 2f)2f) and and FF (Figure(Figureanomala 2g)2g); they areare otherotherhave strobilurins, strobilurins,cytostatic and extractedextracted antifungal fromfrom mycelial mycelialantibiotics culturescultures of the ofof Oudemansinadditionthe Basidiomycete to B inhibiting (Figure Merismodes2 d)fungal from respiration, anomala cultures; they ofit hasXerulahave been cytostatic pudens shown inhibit andto induce antifungal many cell phytopathogenic deformationsantibiotics of [57].thefungi. the the BasidiomyceteBasidiomycete MerismodesMerismodes anomalaanomala;; theythey havehave cytostaticcytostatic andand antifungalantifungal antibioticsantibiotics ofof thethe LikeStrobilurins the strobilurins D (Figure A and 2f) B,and they F (Figure have also2g) are been other shown strobilurins, to inhibit extracted fungal from respiration mycelial [cultures60]. Strobilurin of

E (Figurethe Basidiomycete2e) is another Merismodes antifungal anomala compound; they have of the cytostatic (E)- β-methoxyacrylate and antifungal antibiotics class extracted of the from

J. Fungi 2017, 3, 2 5 of 14 mycelial cultures of Crepidotus fulvotomentosus. In addition to inhibiting fungal respiration, it has beenJ. Fungi shown 2017, 3, 2 to induce cell deformations [57]. Strobilurins D (Figure2f) and F (Figure2g) are other5 of 14 strobilurins, extracted from mycelial cultures of the Basidiomycete Merismodes anomala; they have cytostatic(E)-β-methoxyacrylate and antifungal class. antibiotics These st ofrobilurins the (E)-β inhibit-methoxyacrylate many fungi, class. and like These strobilurins strobilurins A inhibitand B, manythey also fungi, are andpotent like inhibitors strobilurins of respiration A and B, they [57,61]. also Strobilurin are potent M inhibitors which was of respirationisolated from [57 ,61the]. StrobilurinMycena sp.M showed which wasantifungal isolated and from cytostatic the Mycena activitiessp. showed [61]. antifungal Other strobilurins and cytostatic F (Figure activities 2g), [61 G]. Other(Figure strobilurins 2h), and H F (Figure (Figure 22i)g), ex Gtracted (Figure from2h),and culture H (Figure fluids2 i)of extractedBolinea lutea from inhibited culture ﬂuidsAspergillus of Bolineafumigatus lutea, Botrytisinhibited cinereaAspergillus, Microsporum fumigatus canis,, Botrytis and cinereaSporothrix, Microsporum schenckii. canisThese, and compoundsSporothrix schenckiireduced. Thesefungal compoundsrespiration. reducedHowever, fungal they respiration.might be different However, from they the might analogs be differentpreviously from described the analogs [58]. previouslyWang et al. describedreported that [58]. 15 WangkDa antifungal et al. reported protein thatdesignated 15 kDa as antifungal Ganodermin, protein was designated isolated from as Ganodermin,Ganoderma lucidum was isolated. It inhibited from Ganoderma mycelial lucidumgrowth. Itof inhibited Botrytis mycelialcinerea, growthFusarium of oxyporumBotrytis cinerea, and, FusariumBotryosphaeria oxyporum berengeriana, and Botryosphaeria. The IC50 (concentration berengeriana. which The IC 50inhibits(concentration 50% growth) which values inhibits of 50%the growth)ganodermin values against of the B. ganodermin cinerea, Fusarium against oxysporumB. cinerea, ,andFusarium B. berengeriana oxysporum were, and 15.2–0.7B. berengeriana µM, 12.4–0.3were 15.2–0.7µM, andµ M,18.1–0.5 12.4–0.3 µM,µM, respectively. and 18.1–0.5 Pleurostrin,µM, respectively. an antifungal Pleurostrin, peptide an antifungal with about peptide half withthe size about of halfganodermin, the size ofhas ganodermin, been isolated has fr beenom the isolated oyster from Basidiomycetes the oyster Basidiomycetes Pleurotus ostreatusPleurotus. Ganodermin ostreatus. Ganodermininhibited mycelial inhibited growth mycelial in the growth phytopathogenic in the phytopathogenic fungi Botrytis fungi cinereaBotrytis, F. oxyporum cinerea,, F.and oxyporum Peyronellaea, and Peyronellaeaarachidicolla. arachidicollaVery few bioactive. Very few proteins, bioactive such proteins, as a lectin such and as a a ribonuclease, lectin and a ribonuclease,have been isolated have beenfrom isolatedG. lucidum from [19].G. The lucidum antifungal[19]. The activity antifungal of culture activity filt ofrates, culture methanol, ﬁltrates, and methanol, water extracts and water of extractsStereum ofostrea,Stereum an inedible ostrea, an Basidiomycetes, inedible Basidiomycetes, was tested was against tested three against plant three fungal plant pathogens fungal pathogens namely namelyBotrytis Botrytiscinerea, Colletotrichum cinerea, Colletotrichum miyabeanus miyabeanus, and Colletotrichum, and Colletotrichum gloeosporioides gloeosporioides [61]. [61].

(a) (b)(c)

(d) (e) (f)

(g) (h)(i)

Figure 2. Strobilurin A (a); Strobilurin B (b); Strobilurin C (c); Oudemansin B (d); Strobilurin E (e); Figure 2. Strobilurin A (a); Strobilurin B (b); Strobilurin C (c); Oudemansin B (d); Strobilurin E (e); Strobilurin D (f); Strobilurin F (g); (h); Strobilurin H (i). Strobilurin D (f); Strobilurin F (g); (h); Strobilurin H (i). 2.2. Anti-Phytobacterial Activities Secondary metabolites isolated from various Basidiomycetes have been known to show antibacterial properties [62–65]. Basidiomycetes provide effective and low-cost products for human and plant disease control. Members of Ganodermatales, Poriales, Agaricales, and Stereales show potential antibacterial activity and these may become substitutes for developing new antibiotics [66].

J. Fungi 2017, 3, 2 6 of 14

The effect of secondary metabolites of Basidiomycetes has been investigated mainly on human and animal pathogens. Erjave et al. reported that 15 Basidiomycetes extracts showed moderate to high antibacterial activities and three extracts regressed the disease as well as reduced the severity in vitro and in vivo against bacterial wilt disease caused by Ralstonia solanacearum [67]. Extracts from Clytocybe geotropa showed broad range of inhibition against R. solanacearum, Erwinia carotovora subsp. carotovora, P. syringae pv. syringae, X. campestris pv. Vesicatoria, and Clavibacter michiganensis subsp. sepedonicus. Purified protein, Clitocypin, from C. geotropa showed effective inhibition against C. michiganensis subsp. Sepedonicus [68]. The fungicide strobilurin F 500 enhanced resistance of tobacco to the wild fire pathogen Pseudomonas syringae pv. tabaci [69]. Coprinol (Figure 3), isolated from Coprinus sp., showed inhibitory activity against most of the plant pathogens [70].

2.3. Anti-Phytoviral Activity Brandt and Piraino (2000) divided the antiviral compounds from fungi into two major classes: (i)J. Fungi biological2017, 3, 2 response modifiers and (ii) viral inhibitors [71]. The effect of Basidiomycete6 of 14 polysaccharides has been investigated using human and animal virus models [72]. Ganoderma lucidum2.2. Anti-Phytobacterial and G. applanatum Activities strains were able to inhibit the tobacco mosaic virus (TMV) at a concentration of 1000 µg/mL [73]. The filtrate from cultured biomass of the polypore Fomes fomentariusSecondary was effective metabolites against isolated the mechanical from various transmission Basidiomycetes of TMV have [74].been A new known lectin, to named show AALantibacterial (Agrocybe properties aegerita [ 62lectin),–65]. Basidiomycetes had been purified provide from effective the andfruiting low-cost bodies products of the for humanedible Basidiomycetesand plant disease A. control.aegerita Members[26]. Aqueous of Ganodermatales, extracts from Agaricus Poriales, brasiliensis Agaricales, and and Lentinula Stereales edodes show fruitingpotential bodies antibacterial showed activity antiviral and activity these mayagainst become the aphid-borne substitutes formosaic developing virus [75]. new The antibiotics neutral and [66]. acidThe effectpolysaccharides of secondary metaboliteshave different of Basidiomycetes characteristics has been of investigated anti-phytoviral mainly onactivity. human Glucuronoxylomannanand animal pathogens. (GXM) Erjave etwas al. considerably reported that less 15 Basidiomycetesactive; in this case, extracts the showedtotal preparation moderate occupiedto high antibacterial an intermediate activities position, and three revealing extracts evidence regressed that the activity disease of as the well total as preparation reduced the severityrelative toin vitrothe infectivityand in vivo ofagainst TMV was bacterial induced wilt to disease a grea causedter extent by Ralstonia [76]. The solanacearum effect of Basidiomycete[67]. Extracts metabolitesfrom Clytocybe on geotropaplant pathogenicshowed broad viruses range has ofbeen inhibition poorly againststudied R.[75]. solanacearum A pink quinone,, Erwinia tentatively carotovora identifiedsubsp. carotovora as β-L-glutaminyl-3,4-benzoquinone,, P. syringae pv. syringae, X. campestris presentpv. inVesicatoria sporophores, and ofClavibacter Agaricus michiganensisbisporus is a potentsubsp. inhibitorsepedonicus of. plant Puriﬁed virus protein, infections Clitocypin, [77]. It fromshowedC. geotropa inhibitoryshowed activity effective to infection inhibition of TMV against on NicotianaC. michiganensis glutinosasubsp.. In particular,Sepedonicus the[68 ].acid The polysacchar fungicide strobilurinide of GXM F 500 (Figure enhanced 4) produced resistance by of Tremella tobacco mesentericato the wild consisted ﬁre pathogen of a linearPseudomonas backbone syringae of β-(1pv.→2)tabaci (1→4)-linked[69]. Coprinol oligosaccharides (Figure3), isolatedof xylose from and glucuronicCoprinus sp., acid showed [78–80]. inhibitory activity against most of the plant pathogens [70].

FigureFigure 3. Coprinol.Coprinol.

2.3. Anti-Phytoviral Activity Brandt and Piraino (2000) divided the antiviral compounds from fungi into two major classes: (i) biological response modifiers and (ii) viral inhibitors [71]. The effect of Basidiomycete polysaccharides has been investigated using human and animal virus models [72]. Ganoderma lucidum and G. applanatum strains were able to inhibit the tobacco mosaic virus (TMV) at a concentration of 1000 µg/mL [73]. The filtrate from cultured biomass of the polypore Fomes fomentarius was effective against the mechanical transmission of TMV [74]. A new lectin, named AAL (Agrocybe aegerita lectin), had been purified fromFigure the fruiting 4. Polysaccharide bodies of theglucur edibleonoxylomannan Basidiomycetes (GXM).A. aegerita [26]. Aqueous extracts from Agaricus brasiliensis and Lentinula edodes fruiting bodies showed antiviral activity against the aphid-borne mosaic virus [75]. The neutral and acid polysaccharides have different characteristics of anti-phytoviral activity. Glucuronoxylomannan (GXM) was considerably less active; in this case, the total preparation occupied an intermediate position, revealing evidence that activity of the total preparation relative to the infectivity of TMV was induced to a greater extent [76]. The effect of Basidiomycete metabolites on plant pathogenic viruses has been poorly studied [75]. A pink quinone, tentatively identified as β-L-glutaminyl-3,4-benzoquinone, present in sporophores of Agaricus bisporus is a potent inhibitor of plant virus infections [77]. It showed inhibitory activity to infection of TMV on Nicotiana glutinosa. In particular, the acid polysaccharide of GXM (Figure4) produced by Tremella mesenterica consisted of a linear backbone of β-(1→2) (1→4)-linked oligosaccharides of xylose and glucuronic acid [78–80]. J. Fungi 2017, 3, 2 6 of 14

2.3. Anti-Phytoviral Activity Brandt and Piraino (2000) divided the antiviral compounds from fungi into two major classes: (i) biological response modifiers and (ii) viral inhibitors [71]. The effect of Basidiomycete polysaccharides has been investigated using human and animal virus models [72]. Ganoderma lucidum and G. applanatum strains were able to inhibit the tobacco mosaic virus (TMV) at a concentration of 1000 µg/mL [73]. The filtrate from cultured biomass of the polypore Fomes fomentarius was effective against the mechanical transmission of TMV [74]. A new lectin, named AAL (Agrocybe aegerita lectin), had been purified from the fruiting bodies of the edible Basidiomycetes A. aegerita [26]. Aqueous extracts from Agaricus brasiliensis and Lentinula edodes fruiting bodies showed antiviral activity against the aphid-borne mosaic virus [75]. The neutral and acid polysaccharides have different characteristics of anti-phytoviral activity. Glucuronoxylomannan (GXM) was considerably less active; in this case, the total preparation occupied an intermediate position, revealing evidence that activity of the total preparation relative to the infectivity of TMV was induced to a greater extent [76]. The effect of Basidiomycete metabolites on plant pathogenic viruses has been poorly studied [75]. A pink quinone, tentatively identified as β-L-glutaminyl-3,4-benzoquinone, present in sporophores of Agaricus bisporus is a potent inhibitor of plant virus infections [77]. It showed inhibitory activity to infection of TMV on Nicotiana glutinosa. In particular, the acid polysaccharide of GXM (Figure 4) produced by Tremella mesenterica consisted of a linear backbone of β-(1→2) (1→4)-linked oligosaccharides of xylose and glucuronic acid [78–80].

J. Fungi 2017, 3, 2 7 of 14 Figure 3. Coprinol.

Figure 4. Figure 4. Polysaccharide glucur glucuronoxylomannanonoxylomannan (GXM).

2.4. Phytonematicidal Activity Researchers throughout the world have become increasingly interested in diminishing the use of chemical strategies against parasites [81–83]. A recent study has demonstrated that some species of edible Basidiomycetes such as Pleurotus species possess nematicidal activity through the production of a nematode-toxin, which is able to inhibit the nematode movement, allowing hyphal penetration, and finally digesting the body by enzymatic action [84]. Such biological activity could be the result of a self-defense mechanism in Basidiomycetes which acts against the attack of myceliophagous nematodes [85]. Other studies have shown that P. ostreatus produces a nematode-toxin similar to peroxides which inhibits the movement of nematodes and subsequently degrades them, reaching a mortality of 95% in the free-living nematode Panagrellus redivivus (adults) and the phytopathogenic nematode Bursaphelenchus xylophilus [86]. Another study conducted by Palizi et al. showed that P. eryngii caused 50% mortality against the phytopathogenic nematode Heterodera schantii which caused wilting in sugarcane and other crops. In general, nematicidal activity shown by the different strains of P. eryngii ranged between 4.8%–99.6%. The nematicidal effect of specific edible Basidiomycetes could be influenced by a number of factors like temperature, incubation time of the confrontation, inner genetic characteristics of each of the strains, and differences between nematode species used [87]. Some dead larvae observed with mycelium inside their bodies suggested that the larval death was a consequence of body rupture and invasion by fungal mycelia [87]. Mamiy reported that a strain of Coprinus comatus immobilized, killed, and consumed the free-living nematode Panagrellus redivivus and the root-knot nematode Meloidogyne arenaria [88]. The author reported mechanical damage in the free-living nematode P. redivivus, 8 h post-confrontation with C. comatus mycelia, resulting in 90% nematode immobilization and subsequent degradation, at 24 ◦C incubation. The strains of the edible Pleurotus ostreatus ECS-1123 and ECS-0152, P. eryngii ECS-1290 and ECS -1291, P. cornucopiae ECS-1328 and ECS-1330, and Lentinula edodes ECS-0401 displayed high nematicidal activity with a range of 82% to 99% mortality [84]. Bua-art et al. reported the potential use of bioactive compounds from luminescent Basidiomycete (Neonothopanus nambi) for control of plant parasitic root-knot nematode Meloidogyne incognita. The results revealed that concentrations of 500 mg/L were highly toxic to M. incognita causing 100% mortality within 30 min [89]. Anisaldehyde, 3-chloro-anisaldehyde, and (4-methoxyphenyl)-1,2-propandiol were isolated from several common wood and forest-litter degrading fungi (e.g., Pleurotus pulmonarius, Bjerkandera adusta, Hypholoma fasciculare, and Pholiota squarrosa)[90]. Weak antifungal and nematicidal properties have been described for p-anisaldehyde (Figure5a) and (4-methoxyphenyl)-1,2-propandiol. Fatty acids like S-coriolic acid or linoleic acid (Figure5b) isolated from P. pulmonarius exhibited nematicidal effects against the saprophytic nematode Caenorhabditis elegans, with LD50 (Median lethal dosage) values of 10 and 5 µg/mL, respectively [91]. These nematicidal effects depended on the degree of unsaturation and the length of the fatty acid. A nematicidal monoterpene, 1,2-dihydroxymintlactone, was isolated from Cheimonophyllum candidissimum. It recorded LD50 value of 25 µg/mL against C. elegans and herbicidal effects against Setaria italica and Lepidium sativum at concentrations starting from 50 µg/mL [92]. Cheimonophyllons and cheimonophyllal were isolated from the wood-inhabiting Basidiomycete Cheimonophyllum candidissimum and they exhibited nematicidal activities against nematode C. elegans [92]. The Furaldehydes, 5-pentyl-2-furaldehyde (Figure5c) J. Fungi 2017, 3, 2 8 of 14 and 5(4-penteny)-2-furaldehyde (Figure5d) isolated from Irpex lacteus, exhibited nematicidal activity against Aphelencoides besseyi [93]. A nematicidal cyclic peptide omphalotin (Figure5e) was isolated from biomass after fermentation of Omphalotus olearius [94]. 1-Hydroxypyrene (Figure5f) derived from Crinipellis stipitaria showed very strong nematicidal activity against C. elegans [53]. The cultural filtrates from Amauroderma macer, Laccaria tortilis, and Tylopilus striatulus showed high nematicidal activityJ. Fungi against2017, 3, 2 the pine wood nematode Bursaphelenchus xylophilus [95]. 8 of 14

(a) (b)(c)(d)

(e) (f)

FigureFigure 5. p-anisaldehyde5. p-anisaldehyde (a); Linoleic ( acida); (b);Linoleic 5-pentyl-2-furaldehyde acid (b); (c);5-pentyl-2-furaldehyde 5(4-penteny)-2-furaldehyde (c); (d5(4-penteny)-2-furaldehyde); Omphalotin (e); 1-Hydroxypyrene (d); Omphalotin (f). (e); 1-Hydroxypyrene (f).

2.5. Mosquito Larvicidal Activity 2.5. Mosquito Larvicidal Activity Few studies have been done to find out the mosquito larvicidal activity of Basidiomycetes Few studies have been done to ﬁnd out the mosquito larvicidal activity of Basidiomycetes extracts. extracts. The (Oxiran-2-yl) methylpentanoate (Figure 6a) isolated from submerged culture of The (Oxiran-2-yl) methylpentanoate (Figure6a) isolated from submerged culture of Cyptotrama asprata Cyptotrama asprata showed 100% larvicidal activity at 1.25 ppm (parts per million) concentration showed 100% larvicidal activity at 1.25 ppm (parts per million) concentration against Aedes aegypti after against Aedes aegypti after 8 h [96]. High larvicidal activities against Ae. aegypti and Anopheles 8 h [96]. High larvicidal activities against Ae. aegypti and Anopheles nuneztovari were observed using nuneztovari were observed using the crude extracts of Pycnoporus sanguineus and Pestalotiopsis the crude extracts of Pycnoporus sanguineus and Pestalotiopsis virgulata [97]. Crude ethanolic extract of virgulata [97]. Crude ethanolic extract of Lactarius gymnocarpoides showed maximum larvicidal Lactarius gymnocarpoides showed maximum larvicidal activity against Ae. aegypti [98]. Ethanol extracts activity against Ae. aegypti [98]. Ethanol extracts of Amanita phalloides, Russula cellulata, Lactarius of Amanita phalloides, Russula cellulata, Lactarius gymnocarpoides, and L. densifolius exhibited weak gymnocarpoides, and L. densifolius exhibited weak activity against Cx. quinquefasciatus and Ae. aegypti activity against Cx. quinquefasciatus and Ae. aegypti [99]. The larvicidal activity of methanolic extract [99]. The larvicidal activity of methanolic extract of G. lucidum against fourth instar larvae of Cx. of G. lucidum against fourth instar larvae of Cx. pipiens was tested post 24 h exposure and it ranged pipiens was tested post 24 h exposure and it ranged from 18.25% at 0.5 mg·L−1 concentration to 100% from 18.25% at 0.5 mg·L−1 concentration to 100% at 5 mg·L−1 concentration [100]. 4-(2-hydroxyethyl) at 5 mg·L−1 concentration [100]. 4-(2-hydroxyethyl) phenol (Figure 6b) and phenol (Figure6b) and 3-methoxy-5-methyl-1,2-benzenediol (Figure6c) with LC 50 values of 231 and 3-methoxy-5-methyl-1,2-benzenediol (Figure 6c) with LC50 values of 231 and 237 ppm, respectively, 237 ppm, respectively, were isolated from Basidiomycete JO5289, and were found to be active against were isolated from Basidiomycete JO5289, and were found to be active against Ae. aegypti larvae Ae. aegypti larvae after 24 h [101]. Thaeogyroporus porentosus, Xylaria nigripes, Chlorophyllum sp., and after 24 h [101]. Thaeogyroporus porentosus, Xylaria nigripes, Chlorophyllum sp., and Steccherinum species had good larvicidal activities against Ae. aegypti with mortality ranging from 10%–70% and 18%–90% for 24 and 48 h exposure times, respectively [102].

J. Fungi 2017, 3, 2 9 of 14

Steccherinum species had good larvicidal activities against Ae. aegypti with mortality ranging from 10%–70%J. Fungi 2017 and, 3, 2 18%–90% for 24 and 48 h exposure times, respectively [102]. 9 of 14

(a) (b)(c)

Figure 6. (Oxiran-2-yl)6. (Oxiran-2-yl) methylpentanoate methylpentanoate (a); 4-(2-hydroxyethyl) (a); 4-(2-hydroxyethyl) phenol (b); 3-methoxy-5-methyl-1,2- phenol (b); benzenediol3-methoxy-5-methyl-1,2-benzenediol (c). (c).

3. Conclusions 3. Conclusions Basidiomycetes occupy a prominent position in medical and biological research fields because Basidiomycetes occupy a prominent position in medical and biological research fields because of of their antimicrobial, insecticidal, and nematicidal properties. They are easily available or cultivable their antimicrobial, insecticidal, and nematicidal properties. They are easily available or cultivable and and economic. As such, their secondary metabolites with active principles can be produced economic. As such, their secondary metabolites with active principles can be produced cost-effectively. cost-effectively. The present review clearly shows the various biological properties of The present review clearly shows the various biological properties of Basidiomycetes compounds Basidiomycetes compounds against plant pathogenic microbes, vector mosquitoes, and nematodes. against plant pathogenic microbes, vector mosquitoes, and nematodes. Discovery of more novel Discovery of more novel natural products from Basidiomycetes for the control of plant diseases, natural products from Basidiomycetes for the control of plant diseases, vector mosquitoes, and vector mosquitoes, and nematodes will lead to ecofriendly crop protection methods. The nematodes will lead to ecofriendly crop protection methods. The interactions between the bioactive interactions between the bioactive metabolites of Basidiomycetes and host cells should be studied to metabolites of Basidiomycetes and host cells should be studied to understand the mechanisms behind understand the mechanisms behind their antibacterial, larvicidal, nematicidal, and other activities. their antibacterial, larvicidal, nematicidal, and other activities. The potential bioactive metabolites The potential bioactive metabolites obtained from Basidiomycetes should be urgently obtained from Basidiomycetes should be urgently commercialized to reduce the unwanted effects of commercialized to reduce the unwanted effects of synthetic chemicals. synthetic chemicals. Acknowledgments: The authors are thankful to Entomology Research Institute, Loyola College, Chennai for Acknowledgments:financial assistance Theand authorsfacilities. are This thankful was also to Entomology partially financially Research Institute,supported Loyola by King College, Saud Chennai University for financial assistance and facilities. This was also partially financially supported by King Saud University through through vice Deanship of Research Chairs. We thank Stephen Nehru, G. for reading through the manuscript. vice Deanship of Research Chairs. We thank Stephen Nehru, G. for reading through the manuscript. Author Contributions:Contributions: TheThe authorsauthors SubramaniyanSubramaniyan Sivanandhan,Sivanandhan, Ameer Khusro and MichaelMichael GabrielGabriel PaulrajPaulraj collected thethe data data and and wrote wrote the manuscript.the manuscript. The authorsThe authors Savarimuthu Savarimuth Ignacimuthu,u Ignacimuthu, and Naif and Abdullah Naif AL-DhabiAbdullah designedAL-Dhabi the designed outline the and outline assisted and in assisted manuscript in manuscript preparation preparation and correction. and correction.

ConﬂictsConflicts ofof Interest:Interest: TheThe authorsauthors declaredeclare nono conﬂictconflict ofof interest.interest.

ReferencesReference

1. Whipps, J.M.; Lumsden, R.D. Commercial use of fungifungi asas plantplant diseasedisease biologicalbiological controlcontrol agents:agents: StatusStatus and prospects. In Fungal Biocontrol Agents: Progress, Progress, Problems Problems and and Potential Potential; ;Butt, Butt, T.M., T.M., Jackson, Jackson, C., C., Eds.; CABI Publishing: Oxfordshire, UK, 2001; Volume 9,9, pp.pp. 9–22.9–22. 2. Maxmen, A. Crop pests: Under attack. Nature 2013, 501, S15–S17.S15–S17. [CrossRef][PubMed] 3. Montesinos, E.E. Development, Development, registration registration and commercializationand commercialization of microbial of microbial pesticides pesticides for plant protection.for plant Int.protection. Microbiol. Int.2003 Microbiol, 6, 245–252.. 2003, 6 [CrossRef, 245–252.][ PubMed] 4. Bhattacharjee, R.; Dey, Dey, U. An overview of fungalfungal and bacterial biopesticides to control plantplant pathogens/diseases. Afr.Afr. J. J. Microbiol. Microbiol. Res. Res. 20142014, ,88, ,1749–1762. 1749–1762. 5. Reegan, A.D.; Gandhi, Gandhi, M.R.; M.R.; Paulraj, Paulraj, M.G.; M.G.; Ignacimuthu, Ignacimuthu, S. S. Ovicidal Ovicidal and and oviposition oviposition deterrent deterrent activities activities of ofmedicinal medicinal plant plant extracts extracts against against AedesAedes aegypti aegypti L.L. and and CulexCulex quinquefasciatus quinquefasciatus SaySay mosquitoes (Diptera: Culicidae). Osong Public Health Res. Perspect Perspect.. 2015,, 6,, 64–69. 64–69. [CrossRef][PubMed] 6. Dhiman, R.C.; Pahwa, S.; Dhillon, G.P.; Dash, A.P. Climate change and threat of vector-borne diseases in India: Are we prepared? Parasitol. Res. 2010, 106, 763–773. 7. Benelli, G. Research in mosquito control: Current challenges for a brighter future. Parasitol. Res. 2015, 114, 2801–2805. 8. Williamson, V.M.; Gleason, C.A. Plant-nematode interactions. Curr. Opin. Plant Biol. 2003, 6, 327–333.

J. Fungi 2017, 3, 2 10 of 14

6. Dhiman, R.C.; Pahwa, S.; Dhillon, G.P.; Dash, A.P. Climate change and threat of vector-borne diseases in India: Are we prepared? Parasitol. Res. 2010, 106, 763–773. [CrossRef][PubMed] 7. Benelli, G. Research in mosquito control: Current challenges for a brighter future. Parasitol. Res. 2015, 114, 2801–2805. [CrossRef][PubMed] 8. Williamson, V.M.; Gleason, C.A. Plant-nematode interactions. Curr. Opin. Plant Biol. 2003, 6, 327–333. [CrossRef] 9. Dropkin, V.H. Introduction to Plant Nematology, 2nd ed.; John Wiley and Sons Inc.: Columbia, SC, USA, 1989; pp. 1–304. 10. Campbell, J.F.; Kaya, H.K. How and why a parasitic nematode jumps. Nature 1999, 397, 485–486. [CrossRef] 11. Spread of Crop Pest Threatens Global Food Security as Earth Warms. Available online: http://www. exeter.ac.uk/research/inspiring/keythemes/science/news/archive/title_316965_en.html (accessed on 1 September 2013). 12. Gillespie, A. Conservation, Biodiversity and International Law; Edward Elgar Publishing: Chelteham, New Zealand, 2013; pp. 1–579. 13. Wasser, S.P.; Weis, A.L. Medicinal properties of substances occurring in higher basidiomycetes mushrooms: Current perspectives (review). Int. J. Med. Mushrooms 1999, 1, 31–62. [CrossRef] 14. Anke, T. Basidiomycetes: A source for new bioactive secondary metabolites. Prog. Ind. Microbiol. 1989, 27, 51–66. 15. Gowrie, S.U.; Chathurdevi, G.; Rani, K. Evaluation of bioactive potential of basidiocarp extracts of Ganoderma lucidum. Int. J. Pharm. Res. Allied Sci. 2014, 3, 36–46. 16. Kolundžić,M.; Grozdanić,N.Ð.; Dodevska, M.; Milenković,M.; Sisto, F.; Miani, A.; Farronato, G.; Kundaković, T. Antibacterial and cytotoxic activities of wild mushroom Fomes fomentarius (L.) Fr., Polyporaceae. Ind. Crops. Prod. 2016, 79, 110–115. 17. Ren, L.; Hemar, Y.; Perera, C.O.; Lewis, G.; Krissansen, G.W.; Buchanan, P.K. Antibacterial and antioxidant activities of aqueous extracts of eight edible mushrooms. Bioact. Carbohydr. Diet. Fibre 2014, 3, 41–51. [CrossRef] 18. Santos, D.N.; de Souza, L.L.; de Oliveira, C.A.; Silva, E.R.; de Oliveira, A.L. Arginase inhibition, antibacterial and antioxidant activities of Pitanga seed (Eugenia uniflora L.) extracts from sustainable technologies of high pressure extraction. Food Biosci. 2015, 12, 93–99. [CrossRef] 19. Wang, H.; Ng, T. Ganodermin, an antifungal protein from fruiting bodies of the medicinal mushroom Ganoderma lucidum. Peptides 2006, 27, 27–30. [CrossRef][PubMed] 20. Chu, K.; Xia, L.; Ng, T. Pleurostrin, an antifungal peptide from the oyster mushroom. Peptides 2005, 26, 2098–2103. [CrossRef][PubMed] 21. Sajeena, A.; Marimuthu, T. Efficacy, stability and persistence of Ganosol, a Ganoderma based fungicide against plant pathogens. J. Plant Prot. Sci. 2013, 5, 17–25. 22. Lam, S.; Ng, T. First simultaneous isolation of a ribosome inactivating protein and an antifungal protein from a mushroom (Lyophyllum shimeji) together with evidence for synergism of their antifungal effects. Arch. Biochem. Biophys. 2001, 393, 271–280. [CrossRef][PubMed] 23. Wang, H.; Ng, T. Eryngin, a novel antifungal peptide from fruiting bodies of the edible mushroom Pleurotus eryngii. Peptides 2004, 25, 1–5. [CrossRef][PubMed] 24. Wasser, S.P.; Weis, A.L. Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: A modern perspective. Crit. Rev. Immunol. 1999, 19, 65–96. [PubMed] 25. Faccin, L.C.; Benati, F.; Rincão, V.P.; Mantovani, M.S.; Soares, S.A.; Gonzaga, M.L.; Nozawa, C.; Carvalho, L.R. Antiviral activity of aqueous and ethanol extracts and of an isolated polysaccharide from Agaricus brasiliensis against poliovirus type 1. Lett. Appl. Microbiol. 2007, 45, 24–28. [CrossRef][PubMed] 26. Sun, H.; Zhao, C.G.; Tong, X.; Qi, Y.P. A lectin with mycelia differentiation and antiphytovirus activities from the edible mushroom Agrocybe aegerita. J. Biochem. Mol. Biol. 2003, 36, 214–222. [CrossRef][PubMed] 27. Wang, M.; Triguéros, V.; Paquereau, L.; Chavant, L.; Fournier, D. Proteins as active compounds involved in insecticidal activity of mushroom fruitbodies. J. Econ. Entomol. 2002, 95, 603–607. [CrossRef][PubMed] 28. Jo, W.S.; Hossain, M.A.; Park, S.C. Toxicological profiles of poisonous, edible, and medicinal mushrooms. Mycobiology 2014, 42, 215–220. [CrossRef][PubMed] J. Fungi 2017, 3, 2 11 of 14

29. Wasser, S.P. A Book Review: The Fungal Pharmacy: Medicinal Mushrooms of Western Canada (Robert Rogers, 2006, Prairie Deva Press, Edmonton Alberta, 234 pp., $39.95 CDN). Int. J. Med. Mushrooms. 2008, 10, 97–100. [CrossRef] 30. Valverde, M.E.; Hernández-Pérez, T.; Paredes-López, O. Edible mushrooms: Improving human health and promoting quality life. Int. J. Microbiol. 2015, 2015.[CrossRef][PubMed] 31. Wasser, S.P. Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Antimicrob. Agents Chemother. 2011, 89, 1323–1332. [CrossRef][PubMed] 32. Richard, N.S. Introduction to Plant Pathology; John Wiley & Sons: New York, NY, USA, 2006; pp. 1–50. 33. Knogge, W. Fungal infection of plants. Plant Cell 1996, 8, 1711–1722. [CrossRef][PubMed] 34. Bronson, C.R. The genetics of phytotoxin production by plant pathogenic fungi. Experientia 1991, 47, 771–776. [CrossRef] 35. Than, P.P.; Prihastuti, H.; Phoulivong, S.; Taylor, P.W.; Hyde, K.D. Chilli anthracnose disease caused by Colletotrichum species. J. Zhejiang Univ. Sci. B 2008, 9, 764–778. [CrossRef][PubMed] 36. Hayden, H.P.K.; Aitken, E.; Irwin, J. Genetic-relationships as assessed by molecular markers and cross-infection among strains of Colletotrichum gloeosporioides. Aust. J. Bot. 1994, 42, 9–18. [CrossRef] 37. Braithwaite, K.S.; Irwin, J.A.; Manners, J.M. Restriction fragment length polymorphisms in Colletotrichum gloeosporioides infecting Stylosanthes spp. in Australia. Mycol. Res. 1990, 94, 1129–1137. [CrossRef] 38. Talbot, N.J. On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 2003, 57, 177–202. [CrossRef][PubMed] 39. Hafner, S. Trends in maize, rice, and wheat yields for 188 nations over the past 40 years: A prevalence of linear growth. Agric. Ecosyst. Environ. 2003, 97, 275–283. [CrossRef] 40. Thinlay, X.; Finckh, M.R.; Bordeos, A.C.; Zeigler, R.S. Effects and possible causes of an unprecedented rice blast epidemic on the traditional farming system of Bhutan. Agric. Ecosyst. Environ. 2000, 78, 237–248. [CrossRef] 41. Prabhu, A.S.; Filippi, M.C.; Castro, N. Pathogenic variation among isolates of Pyricularia oryzae affecting rice, wheat, and grasses in Brazil. Int. J. Pest Manag. 1992, 38, 367–371. 42. Hubert, J.; Mabagala, R.B.; Mamiro, D.P. Efficacy of selected plant extracts against Pyricularia grisea, causal agent of rice blast disease. Am. J. Plant Sci. 2015, 6, 602–611. [CrossRef] 43. Gelderblom, W.C.; Jaskiewicz, K.; Marasas, W.F.; Thiel, P.G.; Horak, R.M.; Vleggaar, R.; Kriek, N.P. Fumonisins—Novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbiol. 1988, 54, 1806–1811. [PubMed] 44. Madden, L.; Nutter, J.F. Modeling crop losses at the field scale. Can. J. Plant Pathol. 1995, 17, 124–137. [CrossRef] 45. Desjardins, A.E.; Plattner, R.D.; Nelsen, T.C.; Leslie, J.F. Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl. Environ. Microbiol. 1995, 61, 79–86. [PubMed] 46. Luo, D.Q.; Shao, H.J.; Zhu, H.J.; Liu, J.K. Activity in vitro and in vivo against plant pathogenic fungi of grifolin isolated from the basidiomycete Albatrellus dispansus. Z. Naturforsch. C J. Biosci. 2005, 60, 50–56. [CrossRef] 47. Lam, S.; Ng, T. Hypsin, a novel thermostable ribosome-inactivating protein with antifungal and antiproliferative activities from fruiting bodies of the edible mushroom Hypsizigus marmoreus. Biochem. Biophys. Res. Commun. 2001, 285, 1071–1075. [CrossRef][PubMed] 48. Luo, D.Q.; Wang, F.; Bian, X.Y.; Liu, J.K. Rufuslactone, a new antifungal sesquiterpene from the fruiting bodies of the basidiomycete Lactarius rufus. J. Antibiot. 2005, 58, 456–459. [CrossRef][PubMed] 49. Wong, J.H.; Ng, T.B.; Wang, H.; Sze, S.C.; Zhang, K.Y.; Li, Q.; Lu, X. Cordymin, an antifungal peptide from the medicinal fungus Cordyceps militaris. Phytomedicine 2011, 18, 387–392. [CrossRef][PubMed] 50. Heleno, S.A.; Ferreira, I.C.; Esteves, A.P.; Cirić,A.;´ Glamoˇclija,J.; Martins, A.; Soković,M.; Queiroz, M.J. Antimicrobial and demelanizing activity of Ganoderma lucidum extract, p-hydroxybenzoic and cinnamic acids and their synthetic acetylated glucuronide methyl esters. Food Chem. Toxicol. 2013, 58, 95–100. [CrossRef] [PubMed] 51. Ngai, P.H.; Zhao, Z.; Ng, T. Agrocybin, an antifungal peptide from the edible mushroom Agrocybe cylindracea. Peptides 2005, 26, 191–196. [CrossRef][PubMed] J. Fungi 2017, 3, 2 12 of 14

52. Ngai, P.H.; Ng, T. Lentin, a novel and potent antifungal protein from shitake mushroom with inhibitory effects on activity of human immunodeﬁciency virus-1 reverse transcriptase and proliferation of leukemia cells. Life Sci. 2003, 73, 3363–3374. [CrossRef][PubMed] 53. Lambert, M.; Kremer, S.; Anke, H. Antimicrobial, phytotoxic, nematicidal, cytotoxic, and mutagenic activities of 1-hydroxypyrene, the initial metabolite in pyrene metabolism by the basidiomycete Crinipellis stipitaria. Bull. Environ. Contam. Toxicol. 1995, 55, 251–257. [CrossRef][PubMed] 54. Hwang, E.I.; Yun, B.S.; Kim, Y.K.; Kwon, B.M.; Kim, H.G.; Lee, H.B.; Jeong, W.J.; Kim, S.U. Phellinsin A, a novel chitin synthases inhibitor produced by Phellinus sp. PL3. J. Antibiot. 2000, 53, 903–911. [CrossRef] [PubMed] 55. Robles-Hernández, L.; Gonzalez-Franco, A.C.; Soto-Parra, J.M.; Montes-Domínguez, F. Review of agricultural and medicinal applications of basidiomycete mushrooms. Tecnociencia Chihuah. 2008, 2, 95–107. 56. Anke, T.; Oberwinkler, F.; Steglich, W.; Schramm, G. The strobilurins-new antifungal antibiotics from the basidiomycete Strobilurus tenacellus. J. Antibiot. 1977, 30, 806–810. [CrossRef][PubMed] 57. Weber, W.; Anke, T.; Steffan, B.; Steglich, W. Antibiotics from basidiomycetes. XXXII. Strobilurin E: A new cytostatic and antifungal (E)-BETA-methoxyacrylate antibiotic from Crepidotus fulvotomentosus Peck. J. Antibiot. 1990, 43, 207–212. [CrossRef][PubMed] 58. Fredenhagen, A.; Kuhn, A.; Peter, H.H.; Cuomo, V.; Giuliano, U. Strobilurins F, G and H, three new antifungal metabolites from Bolinea lutea. I. Fermentation, isolation and biological activity. J. Antibiot. 1990, 43, 655–660. [CrossRef][PubMed] 59. Gullino, M.L.; Leroux, P.; Smith, C.M. Uses and challenges of novel compounds for plant disease control. Crop Prot. 2000, 19, 1–11. [CrossRef] 60. Anke, T.; Besl, H.; Mocek, U.; Steglich, W. Antibiotics from basidiomycetes. XVIII. Strobilurin C and Oudemansin B, two new antifungal metabolites from Xerula species (Agaricales). J. Antibiot. 1983, 36, 661–666. [CrossRef][PubMed] 61. Imtiaj, A.; Jayasinghe, C.; Lee, G.W.; Lee, T.S. Antibacterial and antifungal activities of Stereum ostrea, an inedible wild mushroom. Mycobiology 2007, 35, 210–214. [CrossRef][PubMed] 62. Wang, Y.; Bao, L.; Yang, X.; Li, L.; Li, S.; Gao, H.; Yao, X.S.; Wen, H.; Liu, H.W. Bioactive sesquiterpenoids from the solid culture of the edible mushroom Flammulina velutipes growing on cooked rice. Food Chem. 2012, 132, 1346–1353. [CrossRef] 63. Fu, L.Q.; Guo, X.S.; Liu, X.; He, H.L.; Wang, Y.L.; Yang, Y.S. Synthesis and antibacterial activity of C-2 (S)-substituted pleuromutilin derivatives. Chin. Chem. Lett. 2010, 21, 507–510. [CrossRef] 64. Saddiqe, Z.; Naeem, I.; Maimoona, A. A review of the antibacterial activity of Hypericum perforatum L. J. Ethnopharmacol. 2010, 131, 511–521. [CrossRef][PubMed] 65. Barros, L.; Baptista, P.; Estevinho, L.M.; Ferreira, I.C. Effect of fruiting body maturity stage on chemical composition and antimicrobial activity of Lactarius sp. mushrooms. J. Agric. Food. Chem. 2007, 55, 8766–8771. [CrossRef][PubMed] 66. Alves, M.J.; Ferreira, I.C.; Dias, J.; Teixeira, V.; Martins, A.; Pintado, M. A review on antimicrobial activity of mushroom (Basidiomycetes) extracts and isolated compounds. Planta Med. 2012, 78, 1707–1718. [CrossRef] [PubMed] 67. Erjavec, J.; Ravnikar, M.; Brzin, J.; Grebenc, T.; Blejec, A.; Gosak, M.Ž.; Sabotiˇc,J.; Kos, J.; Dreo, T. Antibacterial activity of wild mushroom extracts on bacterial wilt pathogen Ralstonia solanacearum. Plant Dis. 2016, 100, 453–464. [CrossRef] 68. Dreo, T.; Zelko, M.; Skubic, J.; Brzin, J.; Ravnikar, M. Antibacterial activity of proteinaceous extracts of higher basidiomycetes mushrooms against plant pathogenic bacteria. Int. J. Med. Mushrooms 2007, 9, 226–237. 69. Herms, S.; Seehaus, K.; Koehle, H.; Conrath, U. A strobilurin fungicide enhances the resistance of tobacco against tobacco mosaic virus and Pseudomonas syringae pvtabaci. Plant Physiol. 2002, 130, 120–127. [CrossRef] [PubMed] 70. Johansson, M.; Sterner, O.; Labischinski, H.; Anke, T. Coprinol, a new antibiotic cuparane from a Coprinus species. Z. Naturforsch. C J. Biosci. 2001, 56, 31–34. [CrossRef] 71. Brandt, C.R.; Piraino, F. Mushroom antivirals. Recent Res. Dev. Antimicrob. Agents Chemother. 2000, 4, 11–26. 72. Gao, Y.; Zhou, S.; Huang, M.; Xu, A. Antibacterial and antiviral value of the genus Ganoderma P. Karst. species (Aphyllophoromycetideae): A review. Int. J. Med. Mushrooms 2003, 5.[CrossRef] J. Fungi 2017, 3, 2 13 of 14

73. Kovalenko, O.; Polishchuk, O.; Krupodorova, T. Screening of metabolites produced by strains of Ganoderma lucidum [Curt.: Fr] P. Karst and Ganoderma applanatum [Pirs.: Waller] Pat. for their activity against tobacco mosaic virus. Bull. Tara Shevchenko Nat. Univ. Kyiv. Ser. Biol. 2008, 51, 32–34. 74. Zjawiony, J.K. Biologically Active Compounds from Aphyllophorales (Polypore) Fungi. J. Nat. Prod. 2004, 67, 300–310. [CrossRef][PubMed] 75. Di Piero, R.M.; Novaes, Q.S.; Pascholati, S.F. Effect of Agaricus brasiliensis and Lentinula edodes mushrooms on the infection of passionﬂower with Cowpea aphid-borne mosaic virus. Braz. Arch. Biol. Technol. 2010, 53, 269–278. [CrossRef] 76. Kovalenko, O.G.; Polishchuk, O.N.; Wasser, S.P. Virus Resistance induced by glucuronoxylomannan isolated from submerged cultivated yeast-like cell biomass of medicinal yellow brain mushroom Tremella mesenterica Ritz.: Fr.(Heterobasidiomycetes) in hypersensitive host plants. Int. J. Med. Mushrooms 2009, 11, 199–205. [CrossRef] 77. Tavantzis, S.; Smith, S. Isolation and evaluation of a plant-virus-inhibiting quinone from sporophores of Agaricus bisporus. Phytopathology 1982, 72, 619–621. [CrossRef] 78. Kakuta, M.; Sone, Y.; Umeda, T.; Misaki, A. Comparative structural studies on acidic heteropolysaccharides isolated from “Shirokikurage” fruit body of Tremella fuciformis Berk, and the growing culture of its yeast-like cells. Agric. Biol. Chem. 1979, 43, 1659–1668. [CrossRef] 79. Kovalenko, A. Protein-carbohydrate interactions in the realization of plant resistance to viruses. Mikrobiol. Zhurnal 1993, 55, 74–91. 80. Vinogradov, E.; Petersen, B.O.; Duus, J.Ø.; Wasser, S. The structure of the glucuronoxylomannan produced by culinary-medicinal yellow brain mushroom (Tremella mesenterica Ritz.: Fr., Heterobasidiomycetes) grown as one cell biomass in submerged culture. Carbohydr. Res. 2004, 339, 1483–1489. [CrossRef][PubMed] 81. Haydock, P.P.; Woods, S.R.; Grove, I.G.; Hare, M.C.; Perry, R.N.; Moens, M. Chemical control of nematodes. In Plant Nematology; CABI Publishing: Oxfordshire, UK, 2006; pp. 392–410. 82. Haydock, P.P.; Woods, S.R.; Grove, I.G.; Hare, M.C.; Perry, R.N.; Moens, M. Chemical control of nematodes. In Plant Nematology, 2nd ed.; CABI Publishing: Oxfordshire, UK, 2013; pp. 459–479. 83. Soltani, T.; Nejad, R.F.; Ahmadi, A.R.; Fayazi, F. Chemical control of root-knot nematode (Meloidogyne javanica) on olive in the greenhouse conditions. J. Plant Pathol. Microbiol. 2013, 2013.[CrossRef] 84. Comans-Pérez, R.; Aguilar-Marcelino, L.; Mendoza de Gives, P.; Sánchez, J.; López-Arellano, M.; Singh, M. In vitro lethal capability of ten strains of edible mushrooms against Haemonchus contortus (Nematoda) infective larvae [conference poster]. In Proceedings of the 8th International Conference on Mushroom Biology and Mushroom Products (ICMBMP8), New Delhi, India, 19–22 November 2014; Volume I & II, pp. 557–562. 85. Luo, H.; Li, X.; Li, G.; Pan, Y.; Zhang, K. Acanthocytes of Stropharia rugosoannulata function as a nematode-attacking device. Appl. Environ. Microbiol. 2006, 72, 2982–2987. [CrossRef][PubMed] 86. Kwok, O.; Plattner, R.; Weisleder, D.; Wicklow, D. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J. Chem. Ecol. 1992, 18, 127–136. [CrossRef][PubMed] 87. Palizi, P.; Goltapeh, E.; Pourjam, E.; Safaie, N. Potential of oyster mushrooms for the biocontrol of sugar beet nematode (Heterodera schachtii). J. Plant Prot. Res. 2009, 49, 27–34. [CrossRef] 88. Mamiy, Y. Attraction of the pinewood nematode to mycelium of some wood-decay fungi. Jpn. J. Nematol. 2006, 36, 1–9. [CrossRef] 89. Bua-art, S.; Saksirirat, W.; Hiransalee, A.; Kanokmedhaku, S.; Lekphrom, R. Effect of bioactive compound from luminescent mushroom (Neonothopanus nambi Speg.) on root-knot nematode (Meloidogyne incognita Chitwood) and non-target organisms. KKU Res. J. 2011, 16, 331–341. 90. De Jong, E.; Cazemier, A.E.; Field, J.A.; de Bont, J.A. Physiological role of chlorinated aryl alcohols biosynthesized de novo by the white rot fungus Bjerkandera sp. strain BOS55. Appl. Environ. Microbiol. 1994, 60, 271–277. [PubMed] 91. Stadler, M.; Mayer, A.; Anke, H.; Sterner, O. Fatty acids and other compounds with nematicidal activity from cultures of Basidiomycetes. Planta Med. 1994, 60, 128–132. [CrossRef][PubMed] 92. Lorenzen, K.; Anke, T. Basidiomycetes as source for new bioactive natural products. Curr. Org. Chem. 1998, 2, 329–364. 93. Hayashi, M.; Wada, K.; Munakata, K. New nematicidal metabolites from a fungus, Irpex lacteus. Agric. Biol. Chem. 1981, 45, 1527–1529. J. Fungi 2017, 3, 2 14 of 14

94. Mayer, A.; Anke, H.; Sterner, O. Omphalotin, a new cyclic peptide with potent nematicidal activity from Omphalotus olearius I. Fermentation and biological activity. Nat. Prod. Lett. 1997, 10, 25–32. [CrossRef] 95. Dong, J.Y.; Li, X.P.; Li, L.; Li, G.H.; Liu, Y.J.; Zhang, K.Q. Preliminary results on nematicidal activity from culture filtrates of Basidiomycetes against the pine wood nematode, Bursaphelenchus xylophilus (Aphelenchoididae). Ann. Microbiol. 2006, 56, 163–166. [CrossRef] 96. Njogu, E.M.; Njue, A.; Omolo, J.O.; Cheplogoi, P.K. Larvicidal activity of (oxiran-2-yl) methylpentanoate extracted from mushroom Cyptotrama asprata against mosquito Aedes aegypti. Int. J. Biol. Chem. Sci. 2009, 3. [CrossRef] 97. Bucker, A.; Bucker, N.C.; Souza, A.Q.; Gama, A.M.; Rodrigues-Filho, E.; Costa, F.M.; Tadei, W.P. Larvicidal effects of endophytic and basidiomycete fungus extracts on Aedes and Anopheles larvae (Diptera, Culicidae). Rev. Soc. Bras. Med. Trop. 2013, 46, 411–419. [CrossRef][PubMed] 98. Chelela, B.L.; Chacha, M.; Matemu, A. Larvicidal potential of wild mushroom extracts against Culex quinquefasciatus. Am. J. Res. Commun. 2014, 2, 105–114. 99. Baraza, L.; Joseph, C.; Moshi, M.; Nkunya, M. Chemical constituents and biological activity of three Tanzanian wild mushroom species. Tanzan. J. Sci. 2007, 33.[CrossRef] 100. Olayemi, I.K. Evaluation of Larvicidal efficacy of extract of the fungus Ganoderma lucidum, for the control of the filarial vector mosquito, Culex pipiens pipiens (Diptera: Culicidae). Am. J. Drug Discov. Dev. 2013, 3, 130–139. [CrossRef] 101. Chirchir, D.K. Isolation and Purification of Mosquito Larvicidal Compounds from Extracts of a Basidiomycete jo5289. Master’s Thesis, Egerton University, Njoro, Kenya, February 2010. 102. Thongwat, D.; Pimolsri, U.; Somboon, P. Screening for mosquito larvicidal activity of thai mushroom extracts with special reference to Steccherinum sp against Aedes aegypti (L.)(Diptera: Culicidae). Southeast Asian J. Trop. Med. Public Health 2015, 46, 586–595. [PubMed]

© 2017 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).