A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes

Abstract

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 Acacia, Albizia, Bauhinia, Berberis, Caesalpinia, Cassia, Cornus, Hamamelis, Jasminus, Ligustrum, Lonicera, Nerium, 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 Hamamelis, Jasminus, Lonicera, and Robinia exhibited the lowest. The most frequently detected fungi were Aspergillus, Colletotrichum, Fusarium, Penicillium, Phyllosticta, 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.

Full text

agriculture
Review
A Survey of Endophytic Fungi Associated with
High-Risk Plants Imported for Ornamental Purposes
Laura Gioia 1, *, Giada d’Errico 1, * , Martina Sinno 1, Marta Ranesi 1, Sheridan Lois Woo 2,3,4
and Francesco Vinale 4,5
1Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy;
martina.sinno@unina.it (M.S.); marta.ranesi@unina.it (M.R.)
2Department of Pharmacy, University of Naples Federico II, 80131 Naples, Italy; woo@unina.it
3Task Force on Microbiome Studies, University of Naples Federico II, 80128 Naples, Italy
4National Research Council, Institute for Sustainable Plant Protection, 80055 Portici, Italy; frvinale@unina.it
5Department of Veterinary Medicine and Animal Productions, University of Naples Federico II,
80137 Naples, Italy
*Correspondence: laura.gioia@unina.it (L.G.); giada.derrico@unina.it (G.d.); Tel.: +39-2539344 (L.G. & G.d.)
Received: 31 October 2020; Accepted: 11 December 2020; Published: 17 December 2020


Abstract:
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 Acacia,Albizia,Bauhinia,Berberis,Caesalpinia,Cassia,Cornus,Hamamelis,Jasminus,
Ligustrum,Lonicera,Nerium, 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 Hamamelis,Jasminus,Lonicera, and Robinia exhibited the lowest. The most frequently detected
fungi were Aspergillus,Colletotrichum,Fusarium,Penicillium,Phyllosticta, 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.
Keywords:
endophytic fungi; crop protection; Acacia;Albizia;Bauhinia;Berberis;Caesalpinia;Cassia;
Cornus;Hamamelis;Jasminus;Ligustrum;Lonicera;Nerium;Robinia; EFSA; high-risk plants
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
–
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
–
13
]. Furthermore,
changes in environmental conditions or species hosts may modify the fungal behavior, thus producing
Agriculture 2020,10, 643; doi:10.3390/agriculture10120643 www.mdpi.com/journal/agriculture

Agriculture 2020,10, 643 2 of 31
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
–
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 [23–25].
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. Endophytic Fungi Occurring in Selected Plants
Table 1summarizes the abundance of endophytic fungi reported in association with High-Risk
Plants for ornamental purposes. Herein, the number of endophytic species found in association with
the examined plant genera has been taxonomically grouped by fungal genus. There are important
differences in terms of fungi recovered per specific plant genus (SP) as well as in the frequency of
a specific fungal genus (SF). These discrepancies could be explained by the different availability of
literature data on these specific plants.

Agriculture 2020,10, 643 3 of 31
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
AC AL BA BE CP CS CO HA
JA LI
LO NE RO
Tot
SF
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

Agriculture 2020,10, 643 4 of 31
Table 1. Cont.
Fungi Genera Plant Genera
AC AL BA BE CP CS CO HA
JA LI
LO NE RO
Tot
SF
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

Agriculture 2020,10, 643 5 of 31
Table 1. Cont.
Fungi Genera Plant Genera
AC AL BA BE CP CS CO HA
JA LI
LO NE RO
Tot
SF
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
2.1. Acacia
The Acacia, commonly known as wattle, belongs to the family Mimosaceae. The genus comprises
more than 1350 species found throughout the world: almost 1000 are native of Australia, up to
140 species occur in Africa, 89 from Asia, and about 185 species are found in North and South America.
Some Australian wattles are naturalized beyond their native range and have become invasive in
many parts of Europe, South Africa, and Florida, especially in conservation areas [
32
]. Aboriginal
communities use some Acacia species as sources of food and medicine. Australian acacias are widely
used as wood products, ornamental plants, commercial cut flowers, and perfume crops [33].
Endophytic occurrence (Table 2) has been reported for 61 fungal isolates belonging to genera
Lasiodiplodia (7 isolates), Dothiorella (8 isolates), Neofusicoccum (9 isolates), Aspergillus (3 isolates),
Chaetomium (3 isolates), Botryosphaeria (1 isolate), Colletotrichum (2 isolates), Aureobasidium (2 isolates),
Spencermartinsia (2 isolates), Alternaria (1 isolate), Cochliobolus (1 isolate), Diplodia (2 isolates),
Eupenicillium (1 isolate), Fusarium (1 isolate), Moesziomyces (1 isolate), Paraphaeosphaeria (1 isolate),
Penicillium (2 isolates), Eutiarosporella (2 isolates)
,
Pestalotia (1 isolate), Peyronellaea (1 isolate),
Phaeobotryosphaeria (1 isolate), Phoma (2 isolates), Phyllosticta (1 isolate), Wickerhamomyces (1 isolate),
Preussia (1 isolate), Rhizopus (1 isolate), Oblongocollomyces (1 isolate), Trichoderma (1 isolate), and Xylaria
(1 isolate). Plant host tissues were collected in Egypt, China, India, Australia, South Africa, La R
é
union
(France), France, USA, and Hawaii.
Table 2. Endophytic fungi isolated from Acacia species.
Species Host Plant Plant Part Country Reference
Phyllosticta sp. A. amara leaf Masinagudi, India [34]
Xylaria sp. A. amara leaf Masinagudi, India [34]
Aspergillus niger A. arabica leaf Punjab, India [35]
Aspergillus sp. A. auriculaeformis root Guangdong, China [36]
Trichoderma sp. A. auriculaeformis root Guangdong, China [36]
Aureobasidium pullulans A. baileyana phyllode Melbourne, Australia [37]
Alternaria sp. A. decurrens leaf, stem Yunnan, China [38]
Penicillium sp. A. decurrens leaf, stem Yunnan, China [38]
Peyronellaea sp. A. decurrens leaf, stem Yunnan, China [38]

Agriculture 2020,10, 643 6 of 31
Table 2. Cont.
Species Host Plant Plant Part Country Reference
Phoma sp. A. decurrens leaf, stem Yunnan, China [38]
Rhizopus sp. A. decurrens leaf, stem Yunnan, China [38]
Aureobasidium pullulans A. floribunda phyllode Melbourne, Australia [37]
Chaetomium globosum A. floribunda phyllode Melbourne, Australia [37]
Dothiorella heterophyllae A. heterophylla branch La Réunion, France [39]
Dothiorella reunionis A. heterophylla branch La Réunion, France [39]
Lasiodiplodia iranensis A. heterophylla branch La Réunion, France [39]
Lasiodiplodia rubropurpurea A. heterophylla branch La Réunion, France [39]
Neofusicoccum parvum A. heterophylla branch La Réunion, France [39]
Cochliobolus geniculatus A. hindsii leaf Mexico [40]
Colletotrichum gloeosporioides A. hindsii leaf Mexico [40]
Colletotrichum truncatum A. hindsii leaf Mexico [40]
Eupenicillium javanicum A. hindsii leaf Mexico [40]
Fusarium oxysporum A. hindsii leaf Mexico [40]
Moesziomyces bullatus A. hindsii leaf Mexico [40]
Paraphaeosphaeria sp. A. hindsii leaf Mexico [40]
Phoma sp. A. hindsii leaf Mexico [40]
Wickerhamomyces anomalus A. hindsii leaf Mexico [40]
Botryosphaeria dothidea A. karroo branch South Africa [41]
Diplodia allocellula A. karroo branch South Africa [41,42]
Dothiorella brevicollis A. karroo branch South Africa [41,42]
Dothiorella dulcispinae A. karroo branch South Africa [42]
Dothiorella pretoriensis A. karroo branch South Africa [41,42]
Eutiarosporella urbis-rosarum A. karroo branch South Africa [41,42]
Lasiodiplodia pseudotheobromae A. karroo branch South Africa [41]
Lasiodiplodia theobromae A. karroo branch South Africa [41]
Lasiodiplodia gonubiensis A. karroo branch South Africa [41]
Neofusicoccum kwambonambiense A. karroo branch South Africa [41]
Neofusicoccum protearum A. karroo branch South Africa [41]
Neofusicoccum vitifusiforme A. karroo branch South Africa [41,42]
Neofusicoccum australe A. karroo branch South Africa [41]
Neofusicoccum parvum A. karroo branch South Africa [41]
Oblongocollomyces variabilis A. karroo branch South Africa [41]
Phaeobotryosphaeria variabilis A. karroo branch South Africa [42]
Spencermartinsia viticola A. karroo branch South Africa [41,42]
Dothiorella koae A. koa branch Hawaii, USA [39]
Lasiodiplodia theobromae A. koa branch Hawaii, USA [39]
Lasiodiplodia exigua A. koa branch Hawaii, USA [39]
Neofusicoccum occulatum A. koa branch Hawaii, USA [39]
Neofusicoccum parvum A. koa branch Hawaii, USA [39]
Aspergillus ochraceus A. nilotica stem Al-Sharqia, Egypt [43]
Penicillium sp. A. nilotica stem Al-Sharqia, Egypt [43]
Pestalotia sp. A. nilotica stem Al-Sharqia, Egypt [43]
Chaetomium globosum A. podalyriifolia phyllode Melbourne, Australia [37]
Chaetomium sp. A. podalyriifolia phyllode Melbourne, Australia [37]
Preussia sp. A. victoriae leaf Arizona, USA [44]
2.2. Albizia
The genus Albizia (Mimosaceae) comprises almost 150 species, mostly trees and shrubs native
to tropical and subtropical regions of Asia and Africa. They are common components of timber
plantations, cropping, and livestock production systems [
45
]. Albizia synthesizes numerous bioactive
compounds with pharmacological properties such as saponins, alkaloids, flavonoids, and phenolics [
45
].
The species A. lebbeck has been extensively introduced in seasonally dry tropical regions of Africa, Asia,
the Caribbean, and South America, mainly as an ornamental plant, and has become naturalized in
many areas [46].

Agriculture 2020,10, 643 7 of 31
Table 3reports endophytes isolated from Albizia genera. These fungi belong to 14 different
genera, most of them found in leaves and twigs of A. lebbeck originating from Iraq, India, Indonesia,
and Egypt. Isolated fungi included different species of Aspergillus (9 isolates), which are dominant in
comparison to other genera, followed by Fusarium (4 isolates), Penicillium (3 isolates), and Paecilomyces
(2 isolates). One isolate for each of the following genera Neocosmospora, Bipolaris, Colletotrichum,
Diaporthe,Lasiodiplodia,Rosellinia,Acremonium,Trichoderma,Verticillium,Curvularia, and Nigrospora has
been detected.
Table 3. Endophytic fungi isolated from Albizia species.
Species Host Plant Plant Part Country Reference
Acremonium sp. A. lebbeck - Indonesia [47]
Aspergillus fumigatus A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus fumigatus A. lebbeck leaf Al-Sharqia, Egypt [43]
Aspergillus glaucus A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus niger A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus raperi A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus sclerotioniger A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus flavus A. lebbeck leaf and twig Baghdad, Iraq [48]
Aspergillus sp. A. lebbeck - Indonesia [47]
A. lebbeck leaf and twig Baghdad, Iraq [48]
Bipolaris australiensis A. lebbeck leaf and twig Baghdad, Iraq [48]
Colletotrichum sp. A. amara leaf Masinagudi, India [34]
Curvularia cymbopogonis A. lebbeck leaf and twig Baghdad, Iraq [48]
Diaporthe sp. A. amara leaf Masinagudi, India [34]
Fusarium verticilloides A. lebbeck leaf and twig Baghdad, Iraq [48]
Fusarium sp. A. amara leaf Masinagudi, India [34]
A. lebbeck - Indonesia [47]
Fusarium oxysporum A. julibrissin - - [49]
Lasiodiplodia sp. A. amara leaf Masinagudi, India [34]
Neocosmospora solani A. lebbeck leaf and twig Baghdad, Iraq [48]
Paecilomyces variotii A. lebbeck leaf and twig Baghdad, Iraq [48]
Paecilomyces sp. A. lebbeck leaf and twig Baghdad, Iraq [48]
Penicillium sp.
A. lebbeck - Indonesia [47]
A. lebbeck leaf Al-Sharqia, Egypt [43]
A. lebbeck leaf and twig Baghdad, Iraq [48]
Rosellinia sanctae-cruciana A. lebbeck leaf Jammu, India [50]
Trichoderma sp. A. lebbeck - Indonesia [47]
Verticillium sp. A. lebbeck - Indonesia [47]
2.3. Bauhinia
The genus Bauhinia, commonly known as the orchid tree, belongs to the family Fabaceae.
It comprises more than 500 species of shrubs, and small trees mostly native to tropical countries (Africa,
Asia, and South America). Many species are widely used as ornamental plants, forage, human food,
and in folk medicine [51,52].
A total of 107 fungal endophytes have been found in Bauhinia plant tissues (Table 4). The most
common fungi reported were: Aspergillus (13 isolates), Curvularia (8 isolates), Penicillium (7 isolates),
Nigrospora (7 isolates), Fusarium (5 isolates), Phoma (3 isolates), Cladosporium (4 isolates), Acremonium
(3 isolates), Colletotrichum (3 isolates), Phomopsis (3 isolates), Cochliobolus (3 isolates), and Exserohilum
(3 isolates). Furthermore, other genera were found less frequently: Myrothecium (2 isolates), Gibberella
(2 isolates), Lasiodiplodia (2 isolates), Khuskia (1 isolate), Nodulisporium (2 isolates), Pestalotiopsis (2 isolates),
Alternaria (2 isolates), Gibberella (2 isolates), Pithomyces (1 isolate), Diplococcium (2 isolates), Dothiorella
(2 isolates), Ascotricha (2 isolates), Talaromyces (2 isolates), Trichoderma (2 isolates), Spegazzinia (2 isolates),
Kiflimonium (1 isolate), Geotrichum (1 isolate), Corynespora (1 isolate), Diaporthe (1 isolate), Glomerella
(1 isolate), Pestalotia (1 isolate), Scedosporium (1 isolate), Botrytis (1 isolate), Sporormiella (1 isolate),
Phyllosticta (1 isolate), Lasmenia (2 isolates), Albifimbria (1 isolate), Myrmecridium (2 isolates), Sphaeria

Agriculture 2020,10, 643 8 of 31
(1 isolate), Paraboeremia (1 isolate), Pseudopithomyces (1 isolate), Chaetomium (1 isolate), and Torulomyces
(1 isolate). All host plants, namely B. fortificata,B. brevipes,B. racemosa,B. guianensis,B. monandra,
B. malabarica,B. phoenicea, and B. vahlii, were from Brazil and India.
Table 4. Endophytic fungi isolated with Bauhinia species.
Species Host Plant Plant Part Country Reference
Acremonium sp.
B. brevipes - Brazil [53]
B. forficata - Brazil [53]
B. brevipes leaf Pirapitinga, Brazil [54]
Albifimbriaverrucaria B. fortificata stem Recife, Brazil [55]
Alternaria alternata B. malabarica stem Chennai, India [56]
B. racemosa leaf Mudumalai, India [57]
Ascotricha sp. B. forficata - Brazil [53]
Ascotricha chartarum B. fortificata seed Recife, Brazil [55]
Aspergillus sp.
B. forficata - Brazil [53]
B. monandra leaf Recife, Brazil [58]
B. guianensis - Brazil [53,59,60]
Aspergillus flavus B. malabarica leaf, root Chennai, India [56]
Aspergillus niger
B. fortificata stem Recife, Brazil [55]
B. malabarica leaf, root, stem Chennai, India [56]
B. racemosa leaf Mudumalai, India [57]
Aspergillus ochraceus B. fortificata stem, seed Recife, Brazil [55]
Aspergillus tamarii B. malabarica leaf, stem Chennai, India [56]
Aspergillus terreus B. malabarica leaf, root Chennai, India [56]
Aspergillus versicolor B. vahlii leaf Chilkigarh, India [61]
Botrytis cinerea B. racemosa leaf Mudumalai, India [57]
Chaetomium globosum B. malabarica leaf Chennai, India [56]
Cladosporium sphaerospermum
B. fortificata leaf Recife, Brazil [55]
Cladosporium sp. B. forficata - Brazil [53]
Cladosporium cladosporioides B. racemosa leaf Mudumalai, India [57]
Cladosporium oxysporum B. fortificata sepal Recife, Brazil [55]
Cochliobolus sp. B. forficata - Brazil [53]
Cochliobolus australiensis B. fortificata leaf Recife, Brazil [55]
Cochliobolus lunatus B. fortificata leaf, stem Recife, Brazil [55]
Colletotrichum sp. B. forficata - Brazil [53]
Colletotrichum coccodes B. guianensis stem Belem, Brazil [62]
Colletotrichum gloeosporioides B. racemosa leaf Mudumalai, India [57]
Corynespora cassiicola B. racemosa leaf Mudumalai, India [63]
Curvularia sp. B. monandra leaf Recife, Brazil [58]
Curvularia brachyspora B. malabarica leaf Chennai, India [56]
Curvularia clavata B. guianensis stem Belem, Brazil [62]
B. phoenicea leaf
Kudremukh range, India
[64]
Curvularia lunata
B. malabarica leaf Chennai, India [56]
B. racemosa leaf Mudumalai, India [57]
B. phoenicea bark, leaf
Kudremukh range, India
[64]
Curvularia pallescens B. phoenicea leaf
Kudremukh range, India
[64]
Diaporthe sp. B. brevipes leaf Pirapitinga, Brazil [54]
Diplococcium sp. B. forficata - Brazil [53]
Diplococcium spicatum B. fortificata leaf Recife, Brazil [55]
Dothiorella sp. B. brevipes - Brazil [53]
leaf Pirapitinga, Brazil [54]
Exserohilum rostratum B. racemosa leaf, stem Sathyamangalam, India [65]
B. guianensis stem Belem, Brazil [62,66]
Fusarium culmorum B. malabarica leaf, stem Chennai, India [56]

Agriculture 2020,10, 643 9 of 31
Table 4. Cont.
Species Host Plant Plant Part Country Reference
Fusarium verticillioides B. malabarica root Chennai, India [56]
Fusarium oxysporum B. malabarica leaf, root, stem Chennai, India [56]
B. phoenicea leaf
Kudremukh range, India
[64]
Fusarium sp. B. forficata - Brazil [53]
Fusidium viride B. vahlii petiole Chilkigarh, India [61]
Geotrichum candidum B. vahlii leaf, petiole Chilkigarh, India [61]
Gibberella fujikuroi B. fortificata leaf, stem Recife, Brazil [55]
Gibberella sp. B. forficata - Brazil [53]
Glomerella sp. B. forficata - Brazil [53]
Kiflimonium curvulum B. fortificata sepal, stem Recife, Brazil [55]
Khuskia sp. B. forficata - Brazil [53]
Lasiodiplodia theobromae B. racemosa leaf Mudumalai, India [57,63]
Lasmenia sp. B. forficata - Brazil [53]
Lasmeniabalansae B. fortificata stem Recife, Brazil [55]
Myrmecridium sp. B. forficata - Brazil [53]
Myrmecridium schulzeri B. fortificata sepal Recife, Brazil [55]
Nigrospora oryzae
B. racemosa leaf Mudumalai, India [57]
B. phoenicea stem, leaf
Kudremukh range, India
[64]
B. fortificata sepal Recife, Brazil [55]
Nigrospora sacchari B. phoenicea leaf
Kudremukh range, India
[64]
Nigrospora sp. B. forficata - Brazil [53]
Nigrospora sphaerica B. vahlii stem Chilkigarh, India [61]
B. racemosa leaf, stem Sathyamangalam, India [65]
Nodulisporium sp. B. forficata - Brazil [53]
B. fortificata stem Recife, Brazil [55]
Paraboeremia putaminum B. fortificata sepal Recife, Brazil [55]
Penicillium commune B. fortificata sepal Recife, Brazil [55]
Penicillium corylophilum B. fortificata seed Recife, Brazil [55]
Penicillium glabrum B. fortificata stem, seed Recife, Brazil [55]
Penicillium implicatum B. fortificata stem Recife, Brazil [55]
Penicillium sp. B. forficata - Brazil [53]
B. monandra leaf Recife, Brazil [58]
Penicillium aurantiogriseum B. fortificata seed Recife, Brazil [55]
Pestalotia sp. B. forficata - Brazil [53]
Pestalotiopsis sp. B. brevipes leaf Pirapitinga, Brazil [54]
B. brevipes - Brazil [53]
Phoma sp.
B. forficata - Brazil [53]
B. brevipes - Brazil [53]
leaf Pirapitinga, Brazil [54]
Phomopsis sp. B. brevipes - Brazil [53]
B. forficata - Brazil [53]
Phomopsis diachenii B. fortificata leaf Recife, Brazil [55]
Phyllosticta capitalensis B. racemosa leaf Mudumalai, India [57]
Pithomyces sp. B. forficata - Brazil [53]
Pseudopithomycesatro-olivaceus
B. fortificata seed Recife, Brazil [55]
Scedosporium apiospermum B. guianensis stem Belem, Brazil [62]
Spegazzinia sp. B. forficata - Brazil [53]
Spegazzinia tessarthra B. fortificata leaf Recife, Brazil [55]
Sphaeria baccata B. fortificata sepal Recife, Brazil [55]
Sporormiella minima B. racemosa leaf Mudumalai, India [57]
Talaromyces sp. B. forficata - Brazil [53]
Talaromyces funiculosus B. fortificata leaf Recife, Brazil [55]
Torulomyces lagena B. racemosa leaf Mudumalai, India [57]
Trichoderma piluliferum B. fortificata stem Recife, Brazil [55]
Trichoderma sp. B. forficata - Brazil [53]

Agriculture 2020,10, 643 10 of 31
2.4. Berberis
The genus Berberis (Berberidaceae) comprises almost 500 species of deciduous or evergreen shrubs,
which occur in the temperate and subtropical regions of Europe, Asia, Africa, and America [
67
].
This genus has remarkable pharmacological properties [
68
]. Berberine and Berbamine are the main
compounds produced by these plants, together with alkaloids, tannins, phenolic compounds, sterols,
and triterpenes [69].
Numerous endophytic fungi belonging to 19 genera have been isolated from tissues of Berberis
from India, China, Kenya, and the USA (Table 5). Isolated fungi included different species of Fusarium
(4 isolates) and Colletotrichum (4 isolates), followed by Alternaria (4 isolates), Anguillospora (1 isolate),
Phomopsis (1 isolate), Campylospora (1 isolate), Cercospora (1 isolate), Clonostachys (1 isolate), Heliscus
(1 isolate), Diaporthe (2 isolates), Microsphaeropsis (1 isolate), Phyllosticta (1 isolate), Paraphalosphaera
(1 isolate), Prathoda (1 isolate), Bacillispora (1 isolate), Neocosmospora (1 isolate), Aspergillus (1 isolate),
Myrothecium (1 isolate), and Puccinia (1 isolate).
Table 5. Endophytic fungi isolated from Berberis species.
Species Host Plant Plant Part Country Reference
Alternaria alternata B. poiretii leaf, twig Beijing, China [70]
B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Alternaria macrospora B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Alternaria solani B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Anguillospora crassa Berberis sp. root Western Himalaya [71]
Aspergillus flavus B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Campylospora parvula Berberis sp. root Western Himalaya [71]
Cercospora citrullina B. aristata stem Sial Sui, District Rajouri, J&K, India [68]
Clonostachys rosea B. aristata root Sial Sui, District Rajouri, J&K, India [68]
Colletotrichum coccodes B. aristata root Sial Sui, District Rajouri, J&K, India [68]
Colletotrichum coffeanum B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Colletotrichum gloeosporioides B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Colletotrichum kahawae B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Bacillispora aquatica Berberis sp. root Western Himalaya [71]
Diaporthe sp. B. vulgaris leaf, stem Kenya [72]
Neocosmospora falciformis B. aristata root Sial Sui, District Rajouri, J&K, India [68]
Fusarium lateritium B. aristata stem Sial Sui, District Rajouri, J&K, India [68]
Fusarium nematophilum B. aristata root Sial Sui, District Rajouri, J&K, India [68]
Fusarium oxysporum B. aristata stem Sial Sui, District Rajouri, J&K, India [68]
Fusarium solani B. aristata root Sial Sui, District Rajouri, J&K, India [68]
Heliscus lugdunensis Berberis sp. root Western Himalaya [71]
Microsphaeropsis conielloides B. poiretii twig Beijing, China [70]
Myrothecium inundatum B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Paraphaeosphaeria sp.
B. thunbergii
stem China [73]
Phomopsis sp. B. poiretii twig Beijing, China [70]
Diaporthe tersa B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Phyllosticta capitalensis B. aristata leaf Sial Sui, District Rajouri, J&K, India [68]
Prathoda longissima Berberis sp. root Western Himalaya [71]
Puccinia graminis f. sp. tritici B. vulgaris - Pacific Northwest USA [74]
2.5. Caesalpinia
The genus Caesalpinia (Fabaceae) includes approximately 200 species, mainly arboreal and shrubby
species, distributed in seasonally dry tropical forests, as well as in tropical and warm temperate
savannas, tropical wet forests, and tropical coastal habitats [
75
]. Several classes of compounds,
mainly flavonoids, diterpenes, and steroids, have been isolated from Caesalpinia species, which have
shown various medicinal properties [
75
]. The most common species cultivated as ornamental plants
are C. pulcherrima and C. echinata.

Agriculture 2020,10, 643 11 of 31
A total of 44 fungal endophytes were isolated from leaves, stems, and bark of plants collected
from India, Brazil, and Indonesia (Table 6). Fungal genera associated with different species of
Caesalpinia were: Aspergillus (10 isolates), followed by Trichoderma (6 isolates) and Fusarium (4 isolates).
Other isolated endophytes have been identified as Penicillum (3 isolates), Curvularia (2 isolates),
Nectria (2 isolates), Bipolaris (2 isolates), Xylaria (2 isolates), and one isolate for the genera Alternaria,
Chrysosporium,Cladosporium,Colletotrichum,Epicoccum,Geotrichum,Helminthosporium,Lasiodiplodia,
Talaromyces,Scopulariopsis, and Phyllosticta, respectively.
Table 6. Endophytic fungi isolated from Caesalpinia species.
Species Host Plant Plant Part Country Reference
Alternaria alternata C. pulcherrima leaf India [76]
Aspergillus flavus C. pulcherrima leaf India [76]
Aspergillus fumigatus C. pulcherrima leaf India [76]
Aspergillus niger C. pulcherrima leaf India [76]
Aspergillus flavus var. oryzae C. pulcherrima leaf India [76]
Aspergillus rugulosus C. pulcherrima leaf India [76]
Aspergillus terreus C. pulcherrima leaf India [76]
Aspergillus sp.
C. pyramidalis leaf Brazil [53]
C. echinata leaf Brazil [53]
C. echinata stem, bark Brazil [77]
Aspergillus nidulans C. pulcherrima leaf India [76]
Bipolaris oryzae C. pulcherrima leaf India [76]
Bipolaris sp. C. pulcherrima leaf India [76]
Chrysosporium sp. C. sappan stem Indonesia [78]
Cladosporium cladosporioides C. echinata leaf Brazil [79]
Colletotrichum gloeosporioides C. echinata leaf Brazil [79]
Curvularia lunata C. sappan stem Indonesia [78]
Curvularia pallescens C. echinata leaf Brazil [79]
Epicoccum sp. C. echinata Brazil [53]
Fusarium sp. C. echinata
leaf Brazil [53]
stem Brazil [77]
stem, bark Brazil [77]
C. pulcherrima leaf India [76]
Geotrichum candidum C. sappan stem Indonesia [78]
Helminthosporium sp. C. pulcherrima leaf India [76]
Lasiodiplodia theobromae C. echinata leaf Brazil [79]
Nectria sp. C. echinata - Brazil [53]
Nectria pseudotrichia C. echinata stem, bark Brazil [77]
stem [80]
Penicillium citrinum C. pulcherrima leaf India [76]
Penicillium chrysogenum C. pulcherrima leaf India [76]
Penicillium sp. C. sappan stem Indonesia [78]
Phyllosticta sorghina C. echinata stem, bark Brazil [77]
Scopulariopsis coprophila C. echinata leaf Brazil [79]
Talaromyces sp. C. echinata stem, bark Brazil [77]
leaf Brazil [53]
Trichoderma atroviride C. pyramidalis stem, bark Brazil [81]
Trichoderma harzianum C. pyramidalis stem, bark Brazil [81]
Trichoderma koningiopsis C. pyramidalis stem, bark Brazil [81]
Trichoderma longibrachiatum C. pyramidalis stem, bark Brazil [81]
Trichoderma virens C. pyramidalis stem, bark Brazil [81]
Trichoderma sp. C. sappan stem Indonesia [78]
Xylaria sp. C. echinata leaf Brazil [53]
Xylaria berteri C. echinata stem, bark Brazil [77]

Agriculture 2020,10, 643 12 of 31
2.6. Cassia
The genus Cassia (Fabaceae) comprises about 600 species native to tropical and subtropical regions
of Southeast Asia, Africa, Northern Australia, and Latin America [
82
,
83
]. In particular, C. fistula and
C. alata are distributed worldwide and used as ornamental and medicinal plants for their biological and
pharmacological properties [
82
–
84
]. Some investigations on phytochemicals of Cassia revealed that
it comprises compounds like anthraquinones, alkaloids, catechols, flavonoids, phenolic compounds,
saponins, steroids, tannins, and triterpenoids [83–86].
Nineteen endophytic fungi have been isolated from different tissues of Cassia species from
Thailand, India, Malaysia, and Brazil (Table 7): Aspergillus (2 isolates), Nodulisporium (2 isolates),
Penicillium (2 isolates), Phomopsis (2 isolates), Daldinia (1 isolate), Coprinus (1 isolate), Guignardia
(1 isolate), Hypoxylon (1 isolate), Nemania (1 isolate), Nigrospora (1 isolate), Papulospora (1 isolate),
Periconia (1 isolate), Xylaria (1 isolate), Psathyrella (1 isolate), and Thielaoviopsis (1 isolate).
Table 7. Endophytic fungi isolated from Cassia species.
Species Host Plant Plant Part Country Reference
Aspergillus flavus C. siamea leaf Malaysia [87]
Aspergillus sp. C. fistula leaf, stem, fruit India [88]
Coprinus sp. C. fistula leaf Bangkok, Thailand [89]
Daldinia sp. C. fistula leaf Bangkok, Thailand [89]
Guignardia sp. C. occidentalis leaf Brazil [53]
Hypoxylon sp. C. fistula leaf Bangkok, Thailand [89]
Nemania sp. C. fistula leaf Bangkok, Thailand [89]
Nigrospora sp. C. fistula leaf Bangkok, Thailand [89]
Nodulisporium sp. C. fistula leaf Bangkok, Thailand [89]
- - [90]
Papulospora sp. C. fistula bark India [91]
Penicillium
sclerotiorum C. fistula - India [92]
Penicillium sp. C. fistula leaf Bangkok, Thailand [89]
Periconia sp. C. fistula bark India [91]
Phomopsis cassiae C. spectabilis - Brazil [52]
Phomopsis sp. C. fistula leaf Bangkok, Thailand [89]
Psathyrella sp. C. fistula leaf Bangkok, Thailand [89]
Thelioviopsis sp. C. fistula leaf India [91]
Xylaria sp. C. fistula leaf Bangkok, Thailand [89]
2.7. Cornus
The genus Cornus (Cornaceae) consists of over 50 species of woody plants, many of which are
cultivated as ornamental and medicinal trees [
93
]. The most widespread ornamental plants of the
genus are C. florida and C. stolonifera, called the flowering dogwood, native to northern and central
America [
93
]. The species C. officinalis is widely distributed in China, Korea, and Japan, and used for
its several pharmacological activities. Among bioactive compounds, iridoids, tannins, and flavonoids
are the major components [94].
About 90 fungal endophytes have been isolated and identified from C. alba,C. alternifolia,
C. stolonifera, C. controversa, and C. officinalis collected in Canada, USA, Japan, China, and Korea
(Table 8): Penicillium (8 isolates), Fusarium (4 isolates), Cladosporium (5 isolates), Colletotrichum
(5 isolates), Alternaria (6 isolates), Pestalotiopsis (5 isolates), Aureobasidium (4 isolates), Botryosphaeria
(3 isolates), Cryptodiaporthe (2 isolates), Phomopsis (3 isolates), Talaromyces (4 isolates), Aspergillus
(3 isolates), Discula (4 isolates), Diaporthe (3 isolates), Neonectria (2 isolates), Trichoderma (2 isolates),
Tubakia (2 isolates), and Didymella (3 isolates). Only one isolate of the following genera has been
reported: Ascochyta,Botrytis,Cyrptosporiopsis,Elsinoe,Epicoccum,Helminthosporium,Lecanicillium,
Leptosphaerulina,Lophiostoma,Drepanopeziza,Nigrospora, Sarocladium, Cordyceps,Phyllosticta,Phytophthora,

Agriculture 2020,10, 643 13 of 31
Phoma,Pleuroceras,Thelonectria,Sclerotinia,Neofabraea,Septoria,Simplicillium,Stenella,Verticillium,
and Xylaria.
Table 8. Endophytic fungi isolated from Cornus species.
Species Host Plant Plant Part Country Reference
Alternaria alternata Cornus spp. leaf Japan, USA [95]
Alternaria sp. C. stolonifera leaf Canada [96]
Alternaria tenuissima C. officinalis twig, leaf China [97]
Cornus spp. leaf Japan [95]
Ascochyta medicaginicola C. officinalis twig China [97]
Aspergillus flavus var. oryzae C. alba leaf - [98]
Aspergillus sp. Cornus spp. leaf Japan, USA [95]
Aureobasidium pullulans Cornus spp. leaf USA [95]
Aureobasidium sp. C. stolonifera leaf Canada [96]
Cornus spp. leaf Japan, USA [95]
Botryosphaeria dothidea C. officinalis twig, leaf China [97]
Cornus spp. leaf Japan [95]
Botryosphaeria sp. Cornus spp. leaf Japan [95]
Botrytis sp. C. stolonifera leaf Canada [96]
Cladosporium cladosporioides C. stolonifera leaf Canada [96]
Cladosporium herbarum C. stolonifera leaf Canada [96]
Cladosporium sp. C. stolonifera leaf Canada [96]
Cornus spp. leaf Japan [95]
Cladosporium sphaerospermum
C. stolonifera leaf Canada [96]
Colletotrichum acutatum Cornus spp. leaf USA, Japan [95]
Colletotrichum gloeosporioides C. officinalis twig, leaf China [97]
C. stolonifera leaf Canada [96]
Colletotrichum sp. Cornus spp. leaf Japan [95]
Cordycepsfarinose C. stolonifera leaf Canada [96]
Cryptodiaporthe corni C. alternifolia stem USA [99]
bark, phloem USA [100]
Cyrptosporiopsis sp. Cornus spp. leaf USA [95]
Diaporthe amygdali Cornus spp. leaf USA, Japan [95]
Diaporthe lagerstroemiae Cornus spp. leaf Japan [95]
Didymellapinodella C. officinalis twig China [97]
Didymella glomerata Cornus spp. leaf USA, Japan [95]
Discula destructiva
Cornus spp. leaf USA [101]
leaf USA [95]
C. florida leaf Germany [102]
leaf Italy [103]
Drepanopeziza populi C. officinalis twig China [97]
Elsinoe fawcettii Cornus spp. leaf USA [95]
Epicoccum nigrum C. stolonifera leaf Canada [96]
Fusarium lateritium C. controversa stem Korea [104]
Fusarium oxysporum C. officinalis root China [97]
Fusarium sp. Cornus spp. leaf Japan [95]
C. stolonifera leaf Canada [96]
Helminthosporium velutinum C. officinalis twig China [97]
Lecanicillium psalliotae C. stolonifera leaf Canada [96]
Leptosphaerulina australis C. officinalis twig China [97]
Lophiostoma sp. Cornus spp. leaf USA [95]
Neofabraea sp. Cornus spp. leaf USA [95]
Neonectria sp. Cornus spp. leaf USA, Japan [95]
Nigrospora sphaerica C. florida stem
Tennessee, USA
[105]
Penicillium brevicompactum C. stolonifera leaf Canada [96]
Penicillium chrysogenum Cornus spp. leaf USA [95]
Penicillium citrinum C. stolonifera leaf Canada [96]
Penicillium miczynskii C. stolonifera leaf Canada [96]
Penicillium simplicissimum Cornus spp. leaf USA [95]
Penicillium sp. C. stolonifera leaf Canada [96]

Agriculture 2020,10, 643 14 of 31
Table 8. Cont.
Species Host Plant Plant Part Country Reference
Penicillium spinulosum Cornus spp. leaf Japan [95]
Penicillium thomii C. stolonifera leaf Canada [96]
Phytophthora palmivora C. florida leaf, shoot USA [106]
Pestalotiopsis mangiferae Cornus spp. leaf Japan [95]
Pestalotiopsis microspora Cornus spp. leaf USA, Japan [95]
Pestalotiopsis monochaeta Cornus spp. leaf Japan [95]
Pestalotiopsis sp. Cornus spp. leaf Japan [95]
Phoma moricola C. officinalis twig China [97]
Phomopsis sp. C. stolonifera leaf Canada [96]
Cornus spp. leaf USA, Japan [95]
Phyllosticta fallopiae C. officinalis leaf China [97]
Phytophthora nicotianae C. florida leaf, shoot USA [106]
Pleuroceras tenellum Cornus spp. leaf USA [95]
Sarocladiumkiliense C. stolonifera leaf Canada [96]
Sclerotinia sclerotiorum C. stolonifera leaf Canada [96]
Septoria sp. C. stolonifera leaf Canada [96]
Simplicillium lanosoniveum C. officinalis fruit China [97]
Stenella sp. C. stolonifera leaf Canada [96]
Talaromyces assiutensis C. officinalis root China [97]
Talaromycescecidicola Cornus spp. leaf USA, Japan [95]
Talaromyces trachyspermus C. officinalis root China [97]
Thelonectriadiscophora Cornus spp. leaf Japan [95]
Trichoderma lixii Cornus spp. leaf USA, Japan [95]
Tubakia sp. Cornus spp. leaf USA, Japan [95]
Verticillium dahliae Cornus spp. leaf USA [95]
Xylaria sp. Cornus spp. leaf USA [95]
2.8. Hamamelis
Hamamelis (Hamamelidaceae), commonly known as witch hazel, comprises six species of
ornamental shrubs. This genus is distributed across North America and eastern Asia. Bark extracts
contain proanthocyanidins and polyphenolic fractions, with medicinal properties [107,108].
Fungal endophytes belonging to genera Colletotrichum,Nigrospora,Pezicula, and Phyllosticta have
been isolated from Hamamelis plant tissues in the USA, China, Netherlands, Canada, and Japan
(Table 9).
Table 9. Endophytic fungi isolated from Hamamelis species.
Species Host Plant Plant Part Country Reference
Colletotrichum acutatum H. virginiana leaf Dutchess Co., USA [109]
Hamamelis sp. leaf Litchfield, USA [109]
Nigrospora oryzae H. mollis leaf China [110]
Pezicula sporulosa H. mollis - Netherlands [111]
H. virginiana - Canada [112]
Phyllosticta hamamelidis H. japonica leaf Japan [113,114]
2.9. Jasminum
The genus Jasminum (Oleaceae) includes more than 200 species distributed in China, Africa,
Asia, Australia, South Pacific Islands, and Europe. Jasmines are widely cultivated for ornamental,
medical, and cosmetical uses. The species J. sambac, commonly known as Arabian Jasmine, is cultivated
throughout India and tropical regions. This genus has been reported for several uses due to the following
pharmaceutical activities: antimicrobial [
115
], antioxidant [
116
], antidiabetic [
117
], antiviral [
118
],
and antitumor [
119
]. Seven species of endophytic fungi of the genus Colletotrichum have been reported
from J. sambac in India and Vietnam (Table 10).

Agriculture 2020,10, 643 15 of 31
Table 10. Endophytic fungi isolated from Jasminum species.
Species Host Plant Plant Part Country Reference
Colletotrichum dematium J. sambac leaf India [120]
Colletotrichum truncatum J. sambac leaf Vietnam [121]
Colletotrichum jasminicola J. sambac leaf, shoot India [120]
Colletotrichum
jasminigenum J. sambac leaf Vietnam [121]
Colletotrichum
jasmini-sambac J. sambac leaf Vietnam [121]
Colletotrichum siamense J. sambac leaf Vietnam [121]
Colletotrichum sp. J. sambac leaf Vietnam [121]
2.10. Ligustrum
Ligustrum (Family Oleaceae) is a genus of about 50 species of shrubs and trees from warm areas of
Europe to Asia [
122
]. Several species of the genus have been cultivated in many areas of the world as
urban ornamental hedge and street trees. In particular, the most widespread species L. lucidum compete
with and inhibit the regeneration of native flora, becoming invasive in many areas with a subtropical
and temperate climate, such as North America, South America, Europe, Asia, Africa, and Oceania [
123
].
Due to its active constituents such as glycosides, flavonoids, phenylpropanoids, phenylethanoid,
and terpenoids, Ligustrum spp. have been widely used as a health remedy in European, Chinese,
and Japanese communities [124,125].
Collected data showed that 29 species of endophytes belonging to 20 genera have been found in
plant tissues of L. lucidum, L. compactum, L. quihoui,L. obsusifoilium, and L. vulgare (Table 11): Guignardia
(3 isolates), Alternaria (2 isolates), Colletotrichum (3 isolates), Fusarium (2 isolates), Xylaria (2 isolates),
Pestalotiopsis (1 isolate), Trichoderma (2 isolates), Lasiodiplodia (2 isolates), Phomopsis (3 isolates),
and one isolate of Diplodia, Geotrichum, Libertella,Neocosmospora,Cladosporium, Peroneutypa,Penicillium,
Phyllosticta,Pycnidiella, and Rhizopus, respectively.
Table 11. Endophytic fungi isolated from Ligustrum species.
Species Host Plant Plant Part Country Reference
Alternaria alternata L. lucidum leaf, petiole Buenos Aires, Argentina [126]
Alternaria cheiranthi L. lucidum leaf Buenos Aires, Argentina [126]
Cladosporium oxysporum L. lucidum leaf Buenos Aires, Argentina [126]
Colletotrichum crassipes L. lucidum leaf Buenos Aires, Argentina [126]
Colletotrichum sp. L. roxburghii leaf Bhavani, India [34]
Colletotrichum gloeosporioides L. lucidum leaf Buenos Aires, Argentina [126]
Diplodia mutila L. lucidum stem Buenos Aires, Argentina [127]
Fusarium oxysporum L. lucidum - Jiangsu, China [128]
Fusarium lateritium L. lucidum stem Buenos Aires, Argentina [127]
Geotrichum candidum L. lucidum leaf Buenos Aires, Argentina [126]
Guignardia mangiferae
L. compactum var. tschonski leaf Kyoto, Japan [129]
L. quihoui leaf Kyoto, Japan [129]
L. obsusifoilium leaf Kyoto, Japan [129]
Lasiodiplodia theobromae L. lucidum stem Buenos Aires, Argentina [127]
Lasiodiplodia sp. L. roxburghii leaf Bhavani, India [34]
Libertella sp. L. lucidum branches Argentina [130]
Neocosmospora solani L. lucidum - Jiangsu, China [128]
Peroneutypa scoparia L. lucidum branches Argentina [130]
Penicillum sp. L. lucidum leaf China [131]
Pestalotiopsis sp. L. roxburghii leaf India [132]
Bhavani, India [34]
Phomopsis ligustri-vulgaris L. lucidum leaf Buenos Aires, Argentina [126]
Phomopsis sp. L. vulgare leaf
Braunschweig, Germany
[133]
L. roxburghii leaf Bhavani, India [34]
Phyllosticta sp. L. roxburghii leaf Bhavani, India [34]

Agriculture 2020,10, 643 16 of 31
Table 11. Cont.
Species Host Plant Plant Part Country Reference
Pycnidiella resinae L. lucidum leaf Buenos Aires, Argentina [126]
Rhizopus microsporus L. lucidum stem Buenos Aires, Argentina [127]
Trichoderma harzianum L. lucidum leaf Buenos Aires, Argentina [126]
Trichoderma koningii L. lucidum stem Buenos Aires, Argentina [127]
Xylaria sp. L. roxburghii leaf Bhavani, India [34]
L. lucidum leaf Buenos Aires, Argentina [126]
2.11. Lonicera
Lonicera (Caprifoliaceae) is a genus that comprises more than 150 species of shrubs and twining
climbers, occurring in North America, South Europe, North Africa, Philippines, and Malaysia [
134
].
L. japonica and L. morrowii, which are native to Asia, are ornamental species distributed in many areas
of the world. In the USA, they are considered invasive plants [
135
]. Only 3 fungal species have
been found to grow as endophytes in Lonicera plant tissues (Table 12): Fusarium sp., Phyllosticta sp.,
and Guignarda mangiferae.
Table 12. Endophytic fungi isolated from Lonicera species.
Species Host Plant Plant Part Country Reference
Fusarium sp. L. japonica leaf
Henan, China
[136]
Guignardia mangiferae L. morrowii leaf Kyoto, Japan [129]
Phyllosticta sp. L. morrowii leaf Kyoto, Japan [129]
2.12. Nerium
N. oleander, commonly called oleander, is the only species currently classified in the genus
Nerium (Family Apocynaceae). This evergreen shrub is native or naturalized to a wide area, from the
Mediterranean region to the Arabian Peninsula and Asia [
137
]. Several biologically active compounds
have been reported in the bark (cardenolides, triterpenoidal saponins, oleanderol, rutin, dambonitol
in leaves, odorosides), roots (triterpene, steroidal cardenolide, volatile oil, stearic acid, oleic acid),
and flowers (gitoxigenin, uzarigenin, strospeside, odoroside H) [137–140].
Collected data showed that 38 fungi were isolated from leaves, stems, flowers, and roots of plants
collected in India and China (Table 13). These isolates belong to the genera, Fusarium (4 isolates),
Penicillium (4 isolates), Cladosporium (3 isolates), Chaetomium (3 isolates), Colletotrichum (3 isolates),
Aspergillus (3 isolates), Curvularia (2 isolates), Alternaria (2 isolates), Cylindrocephalum (1 isolate),
Lasiodiplodia (1 isolate), Torula (1 isolate), Phyllosticta (1 isolate), Phoma (1), Rhizopus (1 isolate), Geomyces
(1 isolate), Pseudothielavia (1 isolate), Trichoderma (1 isolate), Xylaria (1 isolate), Bipolaris (1 isolate),
Cochliobolus (1 isolate), and Drechslera (1 isolate).
Table 13. Endophytic fungi isolated from Nerium species.
Species Host Plant Plant Part Country Reference
Alternaria brassicicola N. oleander stem, flower India [141]
Alternaria sp. N. oleander leaf Southern India [142]
Aspergillus flavus N. oleander flower Chennai, India [143]
Aspergillus niger N. oleander flower Chennai, India [143]
Aspergillus sp. N. oleander stem, root China [144]
Bipolaris sp. N. oleander stem, flower India [141]
Chaetomium sp.
N. oleander stem, flower India [141]
N. oleander stem Hong Kong, China [145]
N. oleander leaf Southern India [142]
Cladosporium sp.
N. oleander stem Hong Kong, China [145]
N. oleander stem India [141]
N. oleander leaf Southern India [142]

Agriculture 2020,10, 643 17 of 31
Table 13. Cont.
Species Host Plant Plant Part Country Reference
Cochliobolus sp. N. oleander stem, flower India [141]
Colletotrichum sp.
N. oleander stem Hong Kong, China [145]
N. oleander flower Chennai, India [143]
N. oleander leaf Southern India [142]
Curvularia brachyspora N. oleander stem, flower India [141]
Curvularia sp. N. oleander stem, flower India [141]
Cylindrocephalum sp. N. oleander stem, flower India [141]
Drechslera sp. N. oleander stem India [141]
Fusarium oxysporum N. oleander flower Chennai, India [143]
Fusarium semitectum N. oleander stem, flower India [141]
Fusarium sp. N. oleander stem, flower India [141]
N. oleander leaf Southern India [142]
Geomyces sp. N. oleander stem China [144]
Lasiodiplodia theobromae N. oleander flower Chennai, India [143]
Nigrospora sp. N. oleander root China [144]
Penicillium sp.
N. oleander stem China [144]
N. oleander stem, flower India [141]
N. oleander root China [146]
N. oleander leaf Southern India [142]
Phoma sp. N. oleander stem Hong Kong, China [145]
Phyllosticta sp. N. oleander leaf Southern India [142]
Rhizopus stolonifera N. oleander flower Chennai, India [143]
Pseudothielavia terricola N. oleander stem India [141]
Torula sp. N. oleander stem Hong Kong, China [145]
Trichoderma sp. N. oleander stem, root China [144]
Xylaria sp. N. oleander leaf Southern India [142]
2.13. Robinia
Robinia is a genus of flowering plants of the family Fabaceae. R. pseudoacacia, called black locust,
grows naturally on a wide range of sites. It is considered to be one of the 40 most invasive woody
species all over the world [
147
] and it is included in the invasive alien species list of the EU [
148
,
149
].
It is used for many purposes, such as ornamental plant, for shelterbelts, land reclamation, fuelwood,
and pulp production [
147
]. Six species of endophytic fungi were isolated from R. pseudoacacia in
Germany, Slovakia, Hungary, and China (Table 14).
Table 14. Endophytic fungi isolated from Robinia species.
Species Host Plant Plant Part Country Reference
Beauveria bassiana R. pseudoacacia - Mly ˇnany, Slovakia [150]
Diaporthe oncostoma
R. pseudoacacia stem Hungary [151]
Monodictys fluctuata
R. pseudoacacia - Germany [152]
Fusarium sp. R. pseudoacacia - Huaxi district, China [153]
Gloniopsis sp. R. pseudoacacia - Huaxi district, China [153]
Clonostachys sp. R. pseudoacacia - Huaxi district, China [153]
3. 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 [
154
–
156
],
stress tolerance [
157
], and biomass accumulation [
158
]. Fungal endophytes may also change according

Agriculture 2020,10, 643 18 of 31
to plant tissues colonized [
159
], phenological growth stages, host genotypes [
160
], and geographical
distribution areas [161].
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.
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 [162–164].
It is worth noting the relative homogeneity in distribution of fungi such as Colletotrichum,Fusarium,
and Alternaria among these plant genera. In fact, Colletotrichum was undetected only in Lonicera
and Robinia,Fusarium 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 Albizia,Jasminus,Robinia, 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 Robinia,Jasminum, and Lonicera.
The presence of pathogenic or saprotrophic fungi has already been discussed by several
authors [
165
,
166
]. Table 1shows 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. alternata,A. niger,C. gloeosporioides (7 host
plant species), N. oryzae (4 host plant species), B. dothidea,C. globosum, C. acutatum (3 host plant species),
A. ochraceus,A. pullulans, and C. truncatum (3 host plant species).
4. 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 [
167
]. It has been isolated from 8 different plant species belonging to
7 genera, namely A. hindsii,A. julibrissin,B. malabarica,B. phoenicea,B. aristata, C. officinalis,L. 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 [
168
]. In this review, A. alternata has been found in association with 3 genera, in 7 plant
species (B. malabarica,B. racemosa,B. poiretii,B. aristata,Cornus 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 [
169
,
170
]. It has been found within plant tissues of A. arabica,
A. lebbeck,B. fortificata,B. malabarica,B. racemosa,C. 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. hindsii,B. racemosa,

Agriculture 2020,10, 643 19 of 31
B. aristata,C. echinata,C. officinalis,C. 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 [
171
]. Moreover, C. truncatum,
the causal agent of anthracnose disease affecting several leguminous crops [
171
], 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 [
172
]. Besides, B. dothidea reported in association with A. karroo,Cornus 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 [
173
]. 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 [
174
].
Also, C. cladosporioides, detected in B. racemosa, C. echinata, and C. stolonifera, is the causal agent of
blossom blight in strawberries [
175
]. 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 [
176
]. 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 [177]. 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 [
178
]. 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 [179].
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 [
180
,
181
].
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 [11,23–25]
. In fact, a fungal invasion into a new ecosystem may change
the native endophytic community structure, leading to the extinction of host-specialized fungi [
182
].
This antagonistic phenomenon is regulated by the production of antifungal compounds, mycoparasitism,
or competition for space and resources [
180
], as well as a synergy of these interactions [
181
]. 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 [
182
–
190
], 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.

Agriculture 2020,10, 643 20 of 31
5. Emerging and Potential Threats Due to Commercial Trade
Several species reported in this review are Quarantine Pests (QP) or Regulated as Non-Quarantine
Pests (RNQP), as defined by containment measures within the importing country [
191
]. Among the
fungal pathogens found in Cornus species, Elsinoe fawcettii is listed as a QP in the EU, Tunisia, and Israel.
This fungus is the causal agent of Citrus scab and it is one of the most important pathogens in
many areas of citrus production [
192
]. E. fawcettii is common in South America and its presence
has been detected in other areas such as Central and South Africa, India and South-Eastern Asia,
and Australia [192].
Furthermore, the following pathogens are RNQP in the EU: F. verticilloides (isolated from
B. malabarica and A. lebbeck), C. acutatum (isolated from Cornus spp., H. virginiana, and Hamamelis sp.),
S. sclerotiorum (isolated from C. stolonifera), and V. dahliae (isolated from Cornus sp.). Outside the EU,
the following species are listed as QP: L. theobromae and P. palmivora (in Morocco), A. nidulans,
A. macrospora, C. kahawae,C. citrullina,C. herbarum,C. pallescens,A. brassicicola,F. semitectum,
F. verticillioides,N. oryzae, and P. longissima (in Mexico), P. graminis (Canada and USA), Diaporthe tersa
(in Israel), C.acutatum (in Tunisia and Israel), and C. gloeosporioides and P. capitalensis (in Egypt) [192].
Organisms that move across continents may or may not become dangerous depending on several
factors, and unexpected consequences may occur [
193
,
194
]. The current knowledge about the fungal
community associated with ornamental plants and their interaction with the environment is fragmentary.
Fungi species generally well known as pathogens, are not necessarily pathogenic when isolated as
endophytes [
6
–
8
]. Genetic mutation can occur in virulent pathogens, transforming the original pathogen
into a nonpathogenic strain [
9
]. Likewise, even though some endophytes are mutualistic, this does not
imply that they will not have negative impacts if introduced in a new ecosystem [
6
,
9
]. Alien pathogens
can often encounter more susceptible host plants and different microbial and abiotic environments
without their own ‘natural enemies’. The so-called ‘risk pathway’ defined by international protocols
tend to assume that the pathogen will attack a plant host taxonomically similar to that of the susceptibile
plant species in its native countries. However, an invasive pathogen may spread to new target hosts,
when introduced in a new ecosystem, and novel pathogen combinations can occur [
11
]. The disease
outcomes of these combinations may be extremely complex and the invasive pathogen populations
can reach explosive distribution levels that are usually difficult to eradicate once established [
23
–
25
].
Beyond the damage which may occur on the host plant species and local microbial communities,
biological invasions may affect entire ecosystems and the connected ecosystem processes and services,
such as soil fertility, fire control, hydrology, and recreation and tourism amenities [
23
–
25
]. In response
to expanding global trade, several EU regulations [
27
–
29
] and international protocols [
195
,
196
] are
aimed at regulating over-dissemination and accidental introduction of plant diseases. However, despite
existing laws and efforts to prevent the introduction of potential pathogens at ports of entry, many
of them will evade detection and establish alien populations [
197
,
198
]. Many pathogenic fungi may
be undetected, transported in the form of inocula as endophytes, propagules, mycelium, or spores
of vegetative material. In addition, large import volumes often permit the inspection of only a small
proportion of the introduced plants. According to the precautionary principle, all imported plant
species should be considered as a potential threat (vectors of fungi), therefore the presence and
establishment may not depend on the number of arrivals. As a consequence, even a reduced amount
of infected plants, which can easily escape phytosanitary inspections, may cause the introduction
and the spread of diseases with devastating outcomes [
199
]. The development of tools, such as new
molecular diagnosistics [
200
] and volatile compounds detection devices [
201
], that allow the rapid
and on-site identification of potentially invasive species and the screening of large volumes of plants,
clearly appears to be essential [
202
]. Despite increasing trade, targeted investment in biosecurity may
be effective to reduce pathogen introduction and limit the establishment of alien microorganisms. Thus,
we highlight the importance of surveillance due to the potential risk of accidental introductions in the
absence of effective biosecurity measures.

Agriculture 2020,10, 643 21 of 31
6. Conclusions
Globalization has led to intensified movement of people, plants, and plant products, and an increase
in the unintentional introduction of non-native fungal species into new ecosystems. Many plant
pathogens are biological opportunistic invaders causing several billion dollars in losses to crops,
pastures, and forests annually, worldwide. Consideration needs to be given to building resilience in
the new environments, from the perspective of pathogen introductions. In particular, the monitoring of
plants and plant products, plus early identification-detection of pathogen risks are key steps towards
ensuring successful regulation to exclude potential disorders caused by pathogens. This review
demonstrated the broad fungal diversity recovered from a small group of ornamental plants that have
been relatively unexplored as fungal hosts. Even if the reviewed plant genera are not recognized
as sources of significant forest diseases, that have had an ecosystemic impact on a continental scale
in the past, we highlight the risk represented by plants as inoculum sources of potentially harmful
organisms. Overall, many other species not listed by the EU have represented or may cause important
impact in many ecosystemic, environmental, and ecological issues. Our literature search revealed that
fungal species may also be introduced through a few hundred plants and invade new ecosystems.
In this context, it is important to underline that the amount of imported plant material may not be
related to a specific risk, but needs to be considered and evaluated to estimate the negative impacts on
agriculture, forestry, and public health, associated with non-indigenous species in European ecosystems.
For example, little is known about the effects of invasive species on ecosystem services, although some
historic pest invasions (e.g., chestnut blight from North America to Europe) have destroyed host tree
species in their locations. The true challenge lies in preventing further damage to natural and managed
ecosystems. For this reason, preventative policies need to take into account the means through which
pathogens gain access to the EU. The accidental introduction of potentially harmful pathogens also links
to other issues of major policy concern (i.e., biotechnology, human health, climate change, etc.) that
should be addressed through improved international cooperation and a holistic approach. We should
expect that some strategies should be continued or further established to prevent or monitor future
introductions, especially at airports, seaports, and other ports of entry, to reduce risks to an acceptable
level and preserve natural and agricultural ecosystems.
Author Contributions:
Conceptualization, L.G., G.d., F.V. and S.L.W.; literature investigation L.G., G.d., M.S. and
M.R.; writing—original draft preparation, L.G. and G.d.; writing—review and editing, project administration, F.V.
and S.L.W.; funding acquisition, F.V. and S.L.W. All authors have read and agreed to the published version of
the manuscript.
Funding:
This research was funded by the following projects: MIURPON (Grant number Linfa 03PE_00026_1;
Grant number Marea 03PE_00106); POR FESR CAMPANIA 2014/2020-O.S. 1.1 (Grant number Bioagro 559);
MISE CRESO (Grant number Protection n. F/050421/01-03/X32); PSR Veneto 16.1.1 (Grant number Divine n.
3589659); PSR Campania 2014/2020 Misura 16-Tipologia di intervento 16.1–Azione 2 ‘Sostegno ai Progetti Operativi
di Innovazione (POI)’—Progetto ‘DI.O.N.IS.O.’, C.U.P. B98H19005010009; European Union Horizon 2020 Research
and Innovation Program, ECOSTACK (Grant agreement no. 773554); PRIN 2017 (Grant number PROSPECT
2017JLN833).
Conflicts of Interest: The authors declare no conflict of interest.
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