Table of Contents

    Topic review

    Endophytic Fungi

    Subjects: Microbiology
    View times: 10
    Submitted by: Laura Gioia


    An extensive literature search was performed to review current knowledge about endophytic fungi isolated from plants included in the European Food Safety Authority (EFSA) dossier. The selected genera of plants were AcaciaAlbiziaBauhiniaBerberisCaesalpiniaCassiaCornusHamamelisJasminusLigustrumLoniceraNerium, and Robinia. A total of 120 fungal genera have been found in plant tissues originating from several countries. Bauhinia and Cornus showed the highest diversity of endophytes, whereas HamamelisJasminusLonicera, and Robinia exhibited the lowest. The most frequently detected fungi were AspergillusColletotrichumFusariumPenicilliumPhyllosticta, and Alternaria. Plants and plant products represent an inoculum source of several mutualistic or pathogenic fungi, including quarantine pathogens. Thus, the movement of living organisms across continents during international trade represents a serious threat to ecosystems and biosecurity measures should be taken at a global level.

    1. Introduction

    Endophytic fungi are ubiquitous to plants, and are mainly members of Ascomycota or their mitosporic stage, but they also include some taxa of Basidiomycota, Zygomycota, and Oomycota. Endophytes are organisms living within the tissues of plants [1] establishing stable relationships with their host, ranging from non-pathogenic to beneficial [2][3]. The endophytic fungi communities represent an enormous reserve of biodiversity and constitute a rich source of bioactive compounds used in agriculture [4][5]. For these reasons, they have attracted the attention of the scientific community worldwide. By definition, all or at least a significant part of the endophytic fungi life cycle occurs within the plant tissues without causing symptoms to their host [6][7][8]. A wide range of fungi, including pathogens and saprophytes, may be endophytes. Several pathogens live asymptomatically within plant tissues during their latency or quiescent stage, while some saprobes can also be facultative parasites [1][8][9]. Fungal endophytes are influenced by abiotic and biotic factors, occupying different habitats and locations during their life cycle phases. Even if host plants do not show any symptoms, they may represent a source of inoculum for other species [10][11][12][13]. Furthermore, changes in environmental conditions or species hosts may modify the fungal behavior, thus producing disease symptoms [8][11][14]. Large quantities of plants and plant material that are globally traded might contain asymptomatic infections of these fungi. It is generally accepted that the movement of plants and plant products by global trade and human activities is the most common way to introduce exotic pathogens and pests in non-endemic countries. Plant health is increasingly threatened by the introduction of emerging pests and/or pathogens [15][16]. Noticeable examples are represented by the invasion of alien plant pathogens into new areas [17][18][19]. Generally, biological invasions are the main threat to biodiversity [20], causing a decrease in species richness and diversity [20][21] or affecting local biological communities [22], as well as changing ecosystem processes [23][24][25].

    In this scenario, the European Food Safety Authority (EFSA) Panel on Plant Health is responsible for the risk assessment, evaluations of risk reduction options, as well as guidance documents [26] in the domain of plant health for the European Union (EU) [26][27]. Commission Implementing Regulation (EU) [28] prohibits the importation of 35 so-called ‘High-Risk Plants, plant products and other objects’ from all third (non-EU) countries as long as no full risk assessment has been carried out. The EFSA Panel on Plant Health was requested to prepare and deliver risk assessments for these commodities [27][28], to evaluate whether the plant material will remain prohibited or removed from the list, with or without the application of additional measures [27][29]. The Commodity Risk Assessment has to be performed on the basis of technical dossiers provided by National Plant Protection Organizations of third countries. Information required for the preparation and submission of technical dossiers includes data on the pests potentially associated with the plant species or genera and on phytosanitary mitigation measures and inspections [30][31].

    These plants have been identified as ‘High-Risk Plants’ by the EU since they ‘host commonly hosted pests known to have a major impact on plant species which are of major economic, social or environmental importance to the Union’ [28]. However, among these 35 plant genera, within the meaning of Art. 42 of Regulation (EU) 2016/2031, a list of only 13 taxa have been selected by the EFSA as plants mostly traded for ornamental purposes. According to this list, we have reviewed the following genera: Acacia Mill., Albizia Durazz., Bauhinia L., Berberis L., Caesalpinia L., Cassia L., Cornus L., Hamamelis L., Jasminus L., Ligustrum L., Lonicera L., Nerium L., and Robinia L. In this article, as much as possible, we highlight the potential risks associated with the movement of plants or materials among nations. Although other plant species may also have a significant impact, this review is limited to plants included in EU regulation [28] that do not originate within Europe. Thus, given these perspectives for future assessments, the present investigation offers an up-to-date snapshot of endophytic fungi associated with the so-called ‘High-Risk Plants for ornamental purpose’. The aim is to facilitate the information required for technical dossiers, needed by the EFSA to perform the Commodity Risk Assessment of 13 plants mandated on an EU import list.

    2. An Overview of Fungal Diversity and Frequency

    Investigations on the mycobiota of plants frequently reported new taxa or new species distribution, and several fungi are still undiscovered or undetected. Numerous higher plants have developed a variety of resistance mechanisms to prevent fungal infections. However, the presence of weakly pathogenic fungi in healthy plant tissues highlights the evolutionary continuum between latent pathogens and symptomless endophytes [15]. Generally, all plants have symbiotic interactions with fungal endophytes which can influence host performance in terms of disease resistance [32][33][34], stress tolerance [35], and biomass accumulation [36]. Fungal endophytes may also change according to plant tissues colonized [37], phenological growth stages, host genotypes [38], and geographical distribution areas [39].

    In this review, a total of 428 endophytic species belonging to 122 fungal genera have been found in association with 13 plant genera (Table 1). The greatest level of fungal diversity was reported in in association with Bauhinia with 43 fungal genera and 94 fungal species, and Cornus with 44 fungal genera and 78 fungal species. The degree of fungal recovery from Acacia (29 genera, 51 species), Albizia (14 genera, 27 species), Berberis (17 genera, 29 species), Caesalpinia (19 genera, 42 species), Cassia (15 genera, 19 species), Ligustrum (20 genera, 29 species), and Nerium (21 genera, 37 species) was nearly half in comparison to the abundance noted in the genera Bauhinia and Cornus. Nonetheless, the lowest diversity showed for Hamamelis (4 species/genera), Jasminus (7 species, 1 genera), Lonicera (3 species/genera), and Robinia (6 species/genera) was also due to the lack of published research about fungal endophytes in these plant genera.

    Table 1. Endophytic fungi isolated from Acacia (AC), Albizia (AL)., Bauhinia (BA), Berberis (BE), Caesalpinia (CP), Cassia (CS), Cornus (CO), Hamamelis (HA), Jasminus (JA), Ligustrum (LI), Lonicera (LO), Nerium (NE), Robinia (RO). Columns report the number of isolated fungal species. The total number of records calculated per fungal genus is indicated as Tot. SF. The total number of records per plant genera is indicated as Tot. SP. Fungal genera are sorted by alphabetic order.

    Fungi Genera Plant Genera  
    Acremonium   1 3                     4
    Albifimbria     1                     1
    Alternaria 1   1 4 1   3     2   2   14
    Anguillospora       1                   1
    Ascochyta             1             1
    Ascotricha     2                     2
    Aspergillus 3 8 11 1 9 2 3         3   40
    Aureobasidium 2           4             6
    Bacillispora       1                   1
    Beauveria                         1 1
    Bipolaris   1     2             1   4
    Botryosphaeria 1           2             3
    Botrytis     1       1             2
    Campylospora       1                   1
    Cercospora       1                   1
    Chaetomium 2   1                 3   6
    Chrysosporium         1                 1
    Cladosporium     4   1   5     1   3   14
    Clonostachys       1           1     1 3
    Cochliobolus 1   3                 1   5
    Colletotrichum 2 1 3 4 1   2 1 7 3   3   27
    Coprinus           1               1
    Cordyceps             1             1
    Corynespora     1                     1
    Cryptodiaporthe             1             1
    Cryptodiaporthe             1             1
    Curvularia   1 5   2             2   10
    Cylindrocarpon                       1   1
    Cyrptosporiopsis             1             1
    Daldinia           1               1
    Diaporthe   1 1 2     2           1 7
    Didymella             2             2
    Diplococcium     2                     2
    Diplodia 1                 1       2
    Discula             1             1
    Dothiorella 6   2                     8
    Drechslera                       1   1
    Drepanopeziza             1             1
    Elsinoe             1             1
    Epicoccum         1   1             2
    Eupenicillium 1                         1
    Eutiarosporella 1                         1
    Exserohilum     1                     2
    Fusarium 1 4 4 4 4   4     2 1 4 1 29
    Fusidium     1                     1
    Geomyces                       1   1
    Geotrichum     1   1         1       3
    Gibberella     2                     2
    Glomerella     1                     1
    Gloniopsis                         1 1
    Guignardia           1       1 1     3
    Heliscus       1                   1
    Helminthosporium         1   1             2
    Hypoxylon           1               1
    Khuskia     1                     1
    Kiflimonium     1                     1
    Lasiodiplodia 6 1 1   1         2   1   12
    Lasmenia     2                     2
    Lecanicillium             1             1
    Leptosphaerulina             1             1
    Libertella                   1       1
    Lophiostoma             1             1
    Microsphaeropsis       1                   1
    Moesziomyces 1                       1 2
    Myrmecridium     2                     2
    Myrothecium       1                   3
    Nectria         2                 2
    Nemania           1               1
    Neocosmospora   1   1           1       3
    Neofabraea             1             1
    Neofusicoccum 6                         6
    Neonectria             2             2
    Nigrospora     4     1 1 1       1   8
    Nodulisporium     2     2               4
    Oblongocollomyces 1                         1
    Paecilomyces   2                       2
    Papulospora           1               1
    Paraboeremia     1                     1
    Paraphaeosphaeria 1     1                   2
    Penicillium 2 3 7   3 2 8     1   4   30
    Periconia           1               1
    Peroneutypa                   1       1
    Pestalotia 1   1                     2
    Pestalotiopsis     2       4     1       7
    Peyronellaea 1                         1
    Pezicula               1           1
    Phaeobotryosphaeria 1                         1
    Phoma 2   3       1         1   7
    Phomopsis     3 1   2 3     3       12
    Phyllosticta 1   1 1 1   1 1   1 1 1   9
    Phytophthora             1             1
    Pithomyces     1                     1
    Pleuroceras             1             1
    Prathoda       1                   1
    Preussia 1                         1
    Psathyrella           1               1
    Pseudopithomyces     1                     1
    Pseudothielavia                       1   1
    Puccinia       1                   1
    Pycnidiella                   1       1
    Rhizopus 1                 1       2
    Rosellinia   1                       1
    Sarocladium             1             1
    Scedosporium     1                     1
    Sclerotinia             1             1
    Scopulariopsis         1                 1
    Septoria             1             1
    Simplicillium             1             1
    Spegazzinia     2                     2
    Spencermartinsia 1                         1
    Sphaeria     1                     1
    Sporormiella     1                     1
    Stenella             1             1
    Talaromyces     3   2   3             8
    Thelioviopsis           1               1
    Thelonectria             1             1
    Torula                       1   3
    Trichoderma 1 1 2   6   1     2   1   14
    Tubakia             2             2
    Verticillium   1         1             2
    Xylaria 1       2 1 1     2   1   8
    Wickerhamomyces 1                         1
    Tot. SP 51 27 94 29 42 19 78 4 7 29 3 37 6

    The literature evidenced that several fungal endophytes live in association with the investigated plants. The most representative genera in terms of abundance of isolated species were Aspergillus (40 spp.), Penicillium (30), Fusarium (29), Colletotrichum (27), Alternaria (14), and Cladosporium (14). These genera include ubiquitous and generalist fungi as well as several plant pathogens and saprobes [40][41][42].

    It is worth noting the relative homogeneity in distribution of fungi such as ColletotrichumFusarium, and Alternaria among these plant genera. In fact, Colletotrichum was undetected only in Lonicera and RobiniaFusarium in Caesalpinia, and Hamamelis, Jasminus, and Alternaria in Cassia and Lonicera. Although scarcely abundant, the fungal genus Phyllosticta was almost reported for all selected plants except for AlbiziaJasminusRobinia, and Hamamelis. Other endophytic fungi were detected more occasionally. Future surveys may reveal the presence of additional fungal species also from less investigated plants, such as RobiniaJasminum, and Lonicera.

    The presence of pathogenic or saprotrophic fungi has already been discussed by several authors [43][44]Table 1 shows that several of the listed fungi were apparently restricted to a single plant genus or at least exhibit some preference for a particular one. Some common and ubiquitous pathogens have been recovered in more than one plant host. This is the case of F. oxysporum (8 host plant species belonging to 7 different genera), A. alternataA. nigerC. gloeosporioides (7 host plant species), N. oryzae (4 host plant species), B. dothideaC. globosum, C. acutatum (3 host plant species), A. ochraceusA. pullulans, and C. truncatum (3 host plant species).

    3. The Most Common Plant Pathogens

    The most frequent endophytes detected from the investigated plants are cosmopolitan and ubiquitous pathogens that may cause severe yield losses. In detail, F. oxysporum is responsible for the wilt of vascular tissues on numerous crops that may result in plant death, even if several strains have proved to be non-pathogenic [45]. It has been isolated from 8 different plant species belonging to 7 genera, namely A. hindsiiA. julibrissinB. malabaricaB. phoeniceaB. aristata, C. officinalisL. lucidum, and N. oleander. The fungus A. alternata may infect over 380 host plant species causing leaf spots, rots, and blights. It includes opportunistic forms in developing field crops as well as saprophytic strains that may cause harvest and post-harvest spoilage of harvested products. One of the major concerns represented by its infection is related to the production of mycotoxins that may be introduced in the food chain [46]. In this review, A. alternata has been found in association with 3 genera, in 7 plant species (B. malabaricaB. racemosaB. poiretiiB. aristataCornus sp., L. lucidum, and C. pulcherrima). The saprophytic pathogen A. niger is responsible for the spoilage of a wide range of fruit, vegetable, and food products. It is also the causal agent of the black rot of onion bulbs, the kernel rot of maize, and the black mold rot of cherry [47][48]. It has been found within plant tissues of A. arabicaA. lebbeckB. fortificataB. malabaricaB. racemosaC. pulcherrima, and N. oleander (7 plant species or 4 genera). Furthermore, three different species of Colletotrichum have been isolated from reviewed plants. C. gloeosporioides has been isolated from 7 plant species (3 genera), namely A. hindsiiB. racemosaB. aristataC. echinataC. officinalisC. stolonifera, and L. lucidum, whereas C. acutatum has been found in Cornus spp., Hamamelis sp., and H. virginiana (3 species; 2 genera). Both Colletotrichum species may cause severe fruit rot mainly occurring in pre- and post-harvest [49]. Moreover, C. truncatum, the causal agent of anthracnose disease affecting several leguminous crops [49], has been collected from 2 plant genera, namely A. hindsii and J. sambac. Furthermore, C. lunata, was isolated from the tissues of 4 plant species (2 genera), including B. malabarica, B. racemosa, B. phoenicea, and C. sappan, is the causal agent of seed and seedling blight in several crops, such as rice, millet, sugarcane, and rice, and of maize leaf spot [50]. Besides, B. dothidea reported in association with A. karrooCornus sp., and C. officinalis may cause cankers, dieback, fruit rot, and blue stain in woody plants, including Acacia, Eucalyptus, Vitis, and Pistachio [12]. Concerning the species F. lateritium, it has been extensively investigated as the causal agent of chlorotic leaf distortion on sweet potato (Ipomoea batatas) in the USA [51]. This fungus has been isolated from three different plant species and genera (B. aristata, C. controversa, and L. lucidum). Moreover, the common soil-borne fungus G. candidum, found in association with B. vahlii, C. sappan, and L. lucidum, is the causal agent of sour-rot of tomatoes and citrus fruits, and it is also one of the most economically important post-harvest diseases of citrus [52]. Also, C. cladosporioides, detected in B. racemosa, C. echinata, and C. stolonifera, is the causal agent of blossom blight in strawberries [53]. Other pathogenic fungi associated with these selected plants are less widespread and some of them are subjected to containment measures in some countries. This is the case of N. parvum, N. oryzae, L. theobromae, and D. destructiva. In particular, N. parvum, isolated as an endophyte in three Acacia species (A. heterophylla, A. karroo, and A. koa), is one of the most aggressive causal agent of Botryosphaeria dieback on the grapevine and it is known as an aggressive polyphagous pathogen attacking more than 100 plant hosts [54]. Also, N. oryzae, reported from H. mollis, B. phoenicea, B. racemosa, and B. fortificata, may reduce plant growth and seed quality of rice plants as well as Brassica spp., maize, and cotton [55]. Moreover, L. theobromae, found in association with six different plant species (A. karroo, A. koa, B. racemosa, C. echinata, L. lucidum, and N. oleander), is the causal agent of dieback, root rot, and blights for a wide range of plant hosts, mainly located in tropical and subtropical regions [56]. Finally, D. desctructiva, recovered from three different species of Cornus, is the causal agent of the dogwood anthracnose, a devastating disease that was firstly documented in the USA and then introduced into Europe [57].

    Generally, closely related organisms, including pathogenic fungi as well as those non-pathogenic, may share similar ecological niches and may potentially interact among themselves. Their co-occurrence could be due to phylogenetic evolution or some unclear biological benefits gained [58][59]. The effects of this interaction may lead to a definition of spaces for development and survival. Nevertheless, it is widely known that non-indigenous species represent one of the greatest threats to native biodiversity [11][23][24][25]. In fact, a fungal invasion into a new ecosystem may change the native endophytic community structure, leading to the extinction of host-specialized fungi [60]. This antagonistic phenomenon is regulated by the production of antifungal compounds, mycoparasitism, or competition for space and resources [58], as well as a synergy of these interactions [59]. Biological invasions may set in motion a long-lasting cascade of effects on the plant host and associated species in unpredictable ways. Generally, the ecological importance of native species prior to the invasion may not be quantified because of the lack of information on fungal communities, especially for non-pathogenic fungal species. As a consequence of global trade and climatic or environmental changes, studies about the impact of new organisms on the ecosystem represent innovative challenges worldwide. In view of these considerations, even if fungal pathogens found in association with investigated plants are widely distributed in the EU [60][61][62][63][64][65][66][67][68], the risk posed by the introduction of potentially noxious species may be very high. Thus, our results suggest the importance of monitoring imported material to avoid the introduction of such alien species.

    The entry is from 10.3390/agriculture10120643


    1. Andrews, J.H.; Hirano, S.S. Microbial Ecology of Leaves; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 1991; pp. 467–479.
    2. Ragozzino, A.; d’Errico, G. Interactions between nematodes and fungi: A concise review. Redia 2011, 94, 123–125.
    3. d’Errico, G.; Mormile, P.; Malinconico, M.; Bolletti Censi, S.; Lanzuise, S.; Crasto, A.; Woo, S.L.; Marra, R.; Lorito, M.; Vinale, F. Trichoderma spp. and a carob (Ceratonia siliqua) galactomannan to control the root-knot nematode Meloidogyne incognita on tomato plants. Can. J. Plant. Pathol. 2020, 1–8.
    4. Vinale, F.; Nicoletti, R.; Lacatena, F.; Marra, R.; Sacco, A.; Lombardi, N.; d’Errico, G.; Digilio, M.C.; Lorito, M.; Woo, S.L. Secondary metabolites from the endophytic fungus Talaromyces pinophilus. Nat. Prod. Res. 2017, 31, 1778–1785.
    5. d’Errico, G.; Aloj, V.; Flematti, G.R.; Sivasithamparam, K.; Worth, C.M.; Lombardi, N.; Ritini, A.; Marra, R.; Lorito, M.; Vinale, F. Metabolites of a Drechslera sp. endophyte with potential as biocontrol and bioremediation agent. Nat. Prod. Res. 2020, 1–9.
    6. Stone, J.K.; Bacon, C.W.; White, J.F. An overview of endophytic microbes: Endophytism defined. Microb. Endophytes. 2000, 3, 29–33.
    7. Wilson, D. Fungal endophytes which invade insect galls: Insect pathogens, benign saprophytes, or fungal inquilines? Oecologia 1995, 103, 255–260.
    8. Petrini, O. Fungal endophytes of tree leaves. In Microbial Ecology of Leaves; Andrews, J.H., Hirano, S.S., Eds.; Springer: New York, NY, USA, 1991; pp. 179–197.
    9. Osono, T. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can. J. Microbiol. 2006, 52, 701–716.
    10. Redman, R.S.; Dunigan, D.D.; Rodriguez, R.J. Fungal symbiosis from mutualism to parasitism: Who controls the outcome, host or invader? New Phytol. 2001, 151, 705–716.
    11. Dunn, A.M.; Hatcher, M.J. Parasites and biological invasions: Parallels, interactions, and control. Trends Parasit. 2015, 31, 189–199.
    12. Marsberg, A.; Kemler, M.; Jami, F.; Nagel, J.H.; Postma-Smidt, A.; Naidoo, S.; Wingfield, M.J.; Crous, P.W.; Spatafora, J.W.; Hesse, C.N.; et al. Botryosphaeria dothidea: A latent pathogen of global importance to woody plant health. Mol. Plant. Pathol. 2017, 18, 477–488.
    13. Slippers, B.; Smit, W.A.; Crous, P.W.; Coutinho, T.A.; Wingfield, B.D.; Wingfield, M.J. Taxonomy, phylogeny and identification of Botryosphaeriaceae associated with pome and stone fruit trees in South Africa and other regions of the world. Plant. Pathol. 2007, 56, 128–139.
    14. Facon, B.; Genton, B.J.; Shykoff, J.; Jarne, P.; Estoup, A.; David, P. A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol. Evol. 2006, 21, 130–135.
    15. Saul, W.C.; Jeschke, J.; Heger, T. The role of eco-evolutionary experience in invasion success. NeoBiota 2013, 17, 57.
    16. Pautasso, M.; Schlegel, M.; Holdenrieder, O. Forest health in a changing world. Microb. Ecol. 2015, 69, 826–842.
    17. Grünwald, N.J. Genome sequences of Phytophthora enable translational plant disease management and accelerate research. Can. J. Plant Pathol. 2012, 34, 13–19.
    18. Cleary, M.; Nguyen, D.; Marčiulynienė, D.; Berlin, A.; Vasaitis, R.; Stenlid, J. Friend or foe? Biological and ecological traits of the European ash dieback pathogen Hymenoscyphus fraxineus in its native environment. Sci. Rep. 2016, 6, 21895.
    19. Dickie, I.A.; Bolstridge, N.; Cooper, J.A.; Peltzer, D.A. Co-invasion by Pinus and its mycorrhizal fungi. New Phytol. 2010, 187, 475–484.
    20. McNeely, J.A. An introduction of human dimensions of invasive alien species. In The Great Reshuffling: Human Dimensions of Invasive Alien Species; McNeely, J.A., Ed.; IUCN: Cambridge, UK, 2001; pp. 5–20.
    21. Hejda, M.; Pyšek, P.; Jarošík, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 2009, 97, 393–403.
    22. Olden, J.D.; Rooney, T.P. On defining and quantifying biotic homogenization. Glob. Ecol. Biogeog. 2006, 15, 113–120.
    23. Ehrenfeld, J.G. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol. Syst. 2010, 41, 59–80.
    24. Vilà, M.; Espinar, J.L.; Hejda, M.; Hulme, P.E.; Jarošík, V.; Maron, J.L.; Pyšek, P. Ecological impacts of invasive alien plants: A meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 2011, 14, 702–708.
    25. Lazzaro, L.; Mazza, G.; d’Errico, G.; Fabiani, A.; Giuliani, C.; Inghilesi, A.F.; Lagomarsino, A.; Landi, S.; Lastrucci, L.; Pastorelli, R.; et al. How ecosystems change following invasion by Robinia pseudoacacia: Insights from soil chemical properties and soil microbial, nematode, microarthropod and plant communities. Sci. Total Environ. 2018, 622, 1509–1518.
    26. Jeger, M.; Schans, J.; Lövei, G.L.; van Lenteren, J.; Navajas, M.; Makowski, D.B.; Ceglarska, E. Risk assessment in support of plant health. Efsa J. 2012, 10, s1012.
    27. European Union. Regulation (EU) 2016/2031 of the European Parliament of the Council of 26 October 2016 on protective measures against pests of plants, amending Regulations (EU) No 228/2013,(EU) No 652/2014 and (EU) No 1143/2014 of the European Parliament and of the Council and repealing Council Directives 69/464/EEC, 74/647/EEC, 93/85/EEC, 98/57/EC, 2000/29/EC, 2006/91/EC and 2007/33/EC. Off. J. Eur. Union 2016, 317, 4–104.
    28. European Union. Commission Implementing Regulation (EU) 2018/2019 of 18 December 2018 establishing a provisional list of high risk plants, plant products or other objects, within the meaning of Article 42 of Regulation (EU) 2016/2031 and a list of plants for which phytosanitary certificates are not required for introduction into the Union, within the meaning of Article 73 of that Regulation. Off. J. Eur. Union 2018, 323, 10–15.
    29. Directive, C. Council Directive 2000/29/EC of 8 May 2000 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community (Annex II). Off. J. Eur. Union. 2000, 169, 60.
    30. European Food Safety Authority, (EFSA); Dehnen-Schmutz, K.; Jaques Miret, J.A.; Jeger, M.; Potting, R.; Corini, A.; Simone, G.; Kozelska, S.; Munoz Guajardo, I.; Stancanelli, G.; et al. Information required for dossiers to support demands for import of high risk plants, plant products and other objects as foreseen in Article 42 of Regulation (EU) 2016/2031. EFSA Support Publ 2018, 15, 1492E.
    31. European Food Safety Authority, (EFSA); Panel on Plant Health (PLH); Bragard, C.; Dehnen-Schmutz, K.; Di Serio, F.; Gonthier, P.; Jacques, M.A.; Miret, J.A.J.; Justesen, A.F.; MacLeod., A.; et al. Guidance on commodity risk assessment for the evaluation of high risk plants dossiers. Efsa J 2019, 17, e05668.
    32. Saikkonen, K.; Faeth, S.H.; Helander, M.; Sullivan, T.J. Fungal endophytes: A continuum of interactions with host plants Annu. Rev. Ecol. Evol. Syst. 1998, 29, 319–343.
    33. Stone, J.K.; Polishook, J.D.; White, J.F. Endophytic fungi. In Biodiversity of 25 Fungi. Inventory and Monitoring Methods; Mueller, G.M., Bills, G.F., Foster, M.S., Eds.; Elsevier Academic Press: San Diego, CA, USA, 2004; pp. 241–270.
    34. Busby, P.E.; Ridout, M.; Newcombe, G. Fungal endophytes: Modifiers of plant disease. Plant Mol. Biol. 2016, 90, 645–655.
    35. Rodriguez, R.J.; White, J.F., Jr.; Arnold, A.E.; Redman, A.R.A. Fungal endophytes: Diversity and functional roles. New Phytol. 2009, 182, 314–330.
    36. Mucciarelli, M.; Scannerini, S.; Bertea, C.; Maffei, M. In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol. 2003, 158, 579–591.
    37. Wearn, J.A.; Sutton, B.C.; Morley, N.J.; Gange, A.C. Species and organ specificity of fungal endophytes in herbaceous grassland plants. J. Ecol. 2012, 100, 1085–1092.
    38. Cheplick, G.P.; Cho, R. Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytol. 2003, 158, 183–191.
    39. Geisen, S.; Kostenko, O.; Cnossen, M.C.; ten Hooven, F.C.; Vreš, B.; van Der Putten, W.H. Seed and root endophytic fungi in a range expanding and a related plant species. Front. Microbiol. 2017, 8, 1645.
    40. Arnold, A.E. Understanding the diversity of foliar endophytic fungi: Progress, challenges, and frontiers. Fungal Biol. Rev. 2007, 21, 51–66.
    41. Hoffman, M.T.; Arnold, A.E. Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol. Res. 2008, 112, 331–344.
    42. Davis, E.C.; Franklin, J.B.; Shaw, A.J.; Vilgalys, R. Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: Phylogenetics, distribution, and symbiosis. Am. J. Bot. 2003, 90, 1661–1667.
    43. Kowalski, T.; Kehr, R. Fungal endophytes of living branch bases in several European tree species. In Endophytic Fungi in Grasses an Woody Plants; Redlin, S.C., Carris, L.M., Eds.; American Phytopathological Society (APS): St Paul, MN, USA, 1996; pp. 67–86.
    44. Peláez, F.; Collado, J.; Arenal, F.; Basilio, A.; Cabello, A.; Matas, M.D.; Garcia, J.B.; Del Val, A.G.; González, V.; Gorrochategui, J.; et al. Endophytic fungi from plants living on gypsum soils as a source of secondary metabolites with antimicrobial activity. Mycol. Res. 1998, 102, 755–761.
    45. Michielse, C.B.; Rep, M. Pathogen profile update: Fusarium oxysporum. Mol. Plant. Pathol. 2009, 10, 311.
    46. Logrieco, A.; Moretti, A.; Solfrizzo, M. Alternaria toxins and plant diseases: An overview of origin, occurrence and risks. World Mycotoxin J. 2009, 2, 129–140.
    47. Samson, A.R.; Hoekstra, E.S.; Frisvad, J.C.; Filtenborg, O. Introduction to Food and Airborne Fungi, 6th ed.; The Dutch Centraalbureau Voor Schimmelcultures: Utrecht, The Netherlands, 2000; pp. 64–97.
    48. Gautam, A.K.; Sharma, S.; Avasthi, S.; Bhadauria, R. Diversity, Pathogenicity and Toxicology of A. niger: An important spoilage fungi. Res. J. Microbiol. 2011, 6, 270–280.
    49. Phoulivong, S.; Cai, L.; Chen, H.; McKenzie, E.H.C.; Abdelsalam, K.; Chukeatirote, E.; Hyde, K.D. Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Divers. 2010, 44, 33–43.
    50. Bisht, S.; Kumar, P.; Purohit, J. In Vitro Management of Curvularia Leaf Spot of Maize Using Botanicals, Essential Oils and Bio-Control Agents. Bioscan 2013, 8, 731–733.
    51. Vitale, S.; Santori, A.; Wajnberg, E.; Castagnone-Sereno, P.; Luongo, L.; Belisario, A. Morphological and molecular analysis of Fusarium lateritium, the cause of gray necrosis of hazelnut fruit in Italy. Phytopathology 2011, 101, 679–686.
    52. Yaghmour, M.A.; Bostock, R.M.; Adaskaveg, J.E.; Michailides, T.J. Propiconazole sensitivity in populations of Geotrichum candidum, the cause of sour rot of peach and nectarine, in California. Plant. Dis. 2012, 96, 752–758.
    53. Nam, M.H.; Park, M.S.; Kim, H.S.; Kim, T.I.; Kim, H.G. Cladosporium cladosporioides and C. tenuissimum cause blossom blight in strawberry in Korea. Mycobiology 2015, 43, 354–359.
    54. Manca, D.; Bregant, C.; Maddau, L.; Pinna, C.; Montecchio, L.; Linaldeddu, B.T. First report of canker and dieback caused by Neofusicoccum parvum and Diplodia olivarum on oleaster in Italy. Ital. J. Mycol. 2020, 49, 85–91.
    55. Sharma, P.; Meena, P.D.; Chauhan, J.S. First Report of Nigrospora oryzae (Berk. & Broome) Petch Causing Stem Blight on Brassica juncea in India. J. Phytopathol. 2013, 161, 439–441.
    56. Salvatore, M.M.; Andolfi, A.; Nicoletti, R. The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae. Agriculture 2020, 10, 488.
    57. Mantooth, K.; Hadziabdic, D.; Boggess, S.; Windham, M.; Miller, S.; Cai, G.; Spatafora, J.; Zhang, N.; Staton, M.; Ownley, B.; et al. Confirmation of independent introductions of an exotic plant pathogen of Cornus species, Discula destructiva, on the east and west coasts of North America. PLoS ONE 2017, 12, 1–26.
    58. Saunders, M.; Glenn, A.E.; Kohn, L.M. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: Using functional traits to reveal mechanisms in community processes. Evol. Appl. 2010, 3, 525–537.
    59. Maciá-Vicente, J.G.; Ferraro, V.; Burruano, S.; Lopez-Llorca, L.V. Fungal assemblages associated with roots of halophytic and non-halophytic plant species vary differentially along a salinity gradient. Microb. Ecol. 2012, 64, 668–679.
    60. McKinney, L.V.; Thomsen, I.M.; Kjær, E.D.; Bengtsson, S.B.K.; Nielsen, L.R. Rapid invasion by an aggressive pathogenic fungus (Hymenoscyphus pseudoalbidus) replaces a native decomposer (Hymenoscyphus albidus): A case of local cryptic extinction? Fungal Ecol. 2012, 5, 663–669.
    61. Ragazzi, A.; Moricca, S.; Capretti, P.; Dellavalle, I.; Turco, E. Differences in composition of endophytic mycobiota in twigs and leaves of healthy and declining Quercus species in Italy. For. Pathol. 2003, 33, 31–38.
    62. Moricca, S.; Ginetti, B.; Ragazzi, A. Species-and organ-specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol. Mediterr. 2012, 51, 587–598.
    63. Collado, J.; Platas, G.; González, I.; Peláez, F. Geographical and seasonal influences on the distribution of fungal endophytes in Quercus ilex. New Phytol. 1999, 144, 525–532.
    64. Peršoh, D. Factors shaping community structure of endophytic fungi–evidence from the Pinus-Viscum-system. Fungal Divers. 2013, 60, 55–69.
    65. Martins, F.; Pereira, J.A.; Bota, P.; Bento, A.; Baptista, P. Fungal endophyte communities in above-and belowground olive tree organs and the effect of season and geographic location on their structures. Fungal Ecol. 2016, 20, 193–201.
    66. Fisher, P.J.; Petrini, O.; Petrini, L.E.; Sutton, B.C. Fungal endophytes from the leaves and twigs of Quercus ilex L. from England, Majorca and Switzerland. New Phytol 1994, 127, 133–137.
    67. Zamora, P.; Martínez-Ruiz, C.; Diez, J.J. Fungi in needles and twigs of pine plantations from northern Spain. Fungal Divers. 2008, 30, 171–184.
    68. Glynou, K.; Ali, T.; Buch, A.K.; Haghi Kia, S.; Ploch, S.; Xia, X.; Ali Çelik, A.; Thines, M.; Maciá-Vicente, J.G. The local environment determines the assembly of root endophytic fungi at a continental scale. Environ. Microbiol. 2016, 18, 2418–2434.