Next Article in Journal
Optimal and Robustly Optimal Consumption of Stretch Film Used for Wrapping Cylindrical Baled Silage
Next Article in Special Issue
Endophytism of Lecanicillium and Akanthomyces
Previous Article in Journal
Inherent Reflectance Variability of Vegetation
Previous Article in Special Issue
The Shifting Mycotoxin Profiles of Endophytic Fusarium Strains: A Case Study
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Endophytic Fungi of Citrus Plants

1
Council for Agricultural Research and Economics, Research Centre for Olive, Citrus and Tree Fruit, 81100 Caserta, Italy
2
Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy
Agriculture 2019, 9(12), 247; https://doi.org/10.3390/agriculture9120247
Submission received: 12 October 2019 / Revised: 12 November 2019 / Accepted: 19 November 2019 / Published: 21 November 2019
(This article belongs to the Special Issue Occurrence and Functions of Endophytic Fungi in Crop Species)

Abstract

:
Besides a diffuse research activity on drug discovery and biodiversity carried out in natural contexts, more recently, investigations concerning endophytic fungi have started considering their occurrence in crops based on the major role that these microorganisms have been recognized to play in plant protection and growth promotion. Fruit growing is particularly involved in this new wave, by reason that the pluriannual crop cycle likely implies a higher impact of these symbiotic interactions. Aspects concerning occurrence and effects of endophytic fungi associated with citrus species are revised in the present paper.

1. Introduction

Despite the early pioneering observations dating back to the nineteenth century [1], a settled prejudice that pathogens basically were the only microorganisms able to colonize living plant tissues has long delayed the awareness that endophytic fungi are constantly associated to plants, and remarkably influence their ecological fitness. Overcoming an apparent vagueness of the concept of ‘endophyte’, scientists working in the field have agreed on the opportunity of delimiting what belongs to this functional category. Thus, a series of definitions have been enunciated which are all based on the condition of not causing any immediate overt negative effect to the host [2].
Besides being prompted by the general theoretical intent that all components of biodiversity from natural contexts ought to be exploited for the benefit of humanity, investigations on the endophytic microbiota, or endosphere [3], have also been undertaken with reference to crops. In this respect, it can be said that endophytes are even more relevant in orchards, where the time factor confers higher impact to the establishment of an equilibrium among the species which are part of the tree biocoenosis, and to its possible disruption. Hence, all sorts of contributions have recently been proliferating in the literature, to such an extent that an organization of the available information is now appropriate in order to support the scientific community in achieving further progress. In view of this perspective, the present paper offers a review of the state-of-the-art of research concerning occurrence and effects of endophytic fungi associated with citrus species.

2. Endophytic Occurrence of Citrus Pathogens

The agent of citrus black spot (CBS) Phyllosticta citricarpa, also known under the teleomorph name Guignardia citricarpa (Dothideomycetes, Botryosphaeriaceae), is one of the most noxious pests of these crops in subtropical regions, and it is subject to phytosanitary restrictions by the European Union and the United States. The employment of biomolecular methods has provided substantial support to the distinction between pathogenic isolates, typically slow-growing in axenic cultures and producing a yellow halo on oatmeal agar, and non-pathogenic isolates, which are morphologically similar but fast-growing, and producing conidia embedded within a thicker mucoid sheath [4,5,6,7,8]. The latter, characterized as a different species (Phyllosticta capitalensis), are known to be ubiquitous as endophytes in woody plants, having been reported from at least 70 botanical families [6,9,10]. Guignardia endophyllicola, treated as a separate species in a work also emphasizing its widespread endophytic occurrence [11], is at present recognized as a synonym. Differences between the two sister species also concern their metagenetic cycle. In fact, it has been ascertained that P. citricarpa is heterothallic, while P. capitalensis is homothallic [8]. This consolidated taxonomic distinction supports the exclusion from quarantine measures of plant material harbouring P. capitalensis. To this purpose, several rapid PCR assays have been developed [12,13,14,15,16,17,18,19,20]. The applicative use of these assays has enabled to exclude the presence of the pathogen in New Zealand, unlike what was previously assumed [21], and has supported the hypothesis of the possible endophytic occurrence of P. citricarpa in asymptomatic Citrus spp., as pointed out by several investigations (Table 1). Moreover, the two species have been clearly differentiated on account of their enzymatic profiles, with a higher expression of amylases, endoglucanases, and pectinases in P. citricarpa, suggesting a likely involvement of these enzymes in the pathogenic aptitude of the CBS agent [22]. Differences in terms of pathogenesis-related proteins have been confirmed after the genome sequencing of the two species, disclosing a higher number of coding sequences in P. citricarpa (15,206 versus 14,797). Such a difference has been interpreted considering the presence of growth and developmental genes involved in the expression of pathogenicity [23].
The issue of detection of contaminated material imported from areas where the pathogen is endemic has also prompted investigations concerning the assortment of Phyllosticta spp. able to colonize citrus plants in either symptomatic or latent courses. Several revisions have been published [17,24], and novel species characterized, which consistently enlarge the citrus-associated consortium within this widespread genus. Particularly, the pathogenic P. citriasiana from south-east Asia [25], P. citrichinaensis from China [26], P. citrimaxima from Thailand [24], and P. paracitricarpa from Greece [27], and the non-pathogenic endophytic P. citribraziliensis from Brazil [28] and P. paracapitalensis from New Zealand, Italy, and Spain [27]. The isolation by the latter research group of P. citricarpa from specimen collected in citrus groves in Italy, Malta, and Portugal, following analogue findings in Florida [19,29], is expected to provide impulse for a more thorough assessment of distribution and pathogenicity of this species [30]. A very recent investigation carried out in Australia on several Citrus spp. and growing conditions, has disclosed P. paracapitalensis to be even more widespread than P. capitalensis. Strains of both species were confirmed to be non-pathogenic on fruits under field conditions, and displayed antagonistic effects against the CBS agent, introducing their possible exploitation in the integrated management of this disease [31]. In this respect, it has been speculated that, rather than depending on intrinsic genetic factors, resistance to CBS by C. latifolia could be due to its systematic colonization by P. capitalensis, as disclosed by a dedicated investigation carried out in Brazil [32].
Colletotrichum (Sordariomycetes, Glomerellaceae) is another important ascomycete genus in course of coherent taxonomic revision. Besides Colletotrichum gloeosporioides, the agent of citrus anthracnose, it includes many species known for their endophytic aptitude. A recent investigation carried out in China on several Citrus spp. has shown a high proportion of endophytic strains to belong to C. gloeosporioides sensu stricto, calling for further investigations concerning the asymptomatic occurrence of this pathogen in citrus orchards. Additional identified species are Colletotrichum fructicola from Citrus reticulata cv. Nanfengmiju and Citrus japonica (=Fortunella margarita), and Colletotrichum karstii [33]. A similar widespread occurrence of C. gloeosporioides has been more recently confirmed in Brazil, where just one out of 188 isolates was found to be able to induce post-bloom fruit drop. This syndrome is more frequently associated to the species Colletotrichum abscissum, which, however, does not display an endophytic habit [34]. Endophytic C. gloeosporioides were also previously reported from Citrus limon in Argentina [35] and Cameroon [36].
One more meaningful example of endophytic fungus converting to pathogenic when plants are exposed to stress factors is represented by another member of the Botryosphaeriaceae, Lasiodiplodia theobromae. Characterized by a widespread endophytic occurrence [37,38], this species has been reported to exacerbate pre-harvest fruit drop and post-harvest fruit decay in plants of Citrus sinensis hit by the huanglongbing syndrome [39].
A quite intricate case deserving further investigations with reference to the epidemiological impact by endophytic strains is represented by members of the genus Diaporthe (Sordariomycetes, Diaporthaceae), also known under the anamorph name Phomopsis [40,41], which are widespread in different ecological contexts [41,42]. Besides the longtime known D. citri, more species in this genus have been recently identified as the causal agents of melanose, stem-end rot, and gummosis on Citrus spp., particularly, D. citriasiana and D. citrichinensis in China [43], and D. limonicola, D. melitensis, D. baccae, D. foeniculina, and D. novem in Europe [44]. Even more species have been reported for their endophytic occurrence as a result of a phylogenetic reassessment carried out in China, with eight known (D. arecae species complex, D. citri, D. citriasiana, D. citrichinensis, D. endophytica, D. eres, D. hongkongensis, and D. sojae) and seven new species (D. biconispora, D. biguttulata, D. discoidispora, D. multiguttulata, D. ovalispora, D. subclavata, and D. unshiuensis) [45].
Endophytic occurrence has also been reported for other citrus pathogens, such as the leaf-spot agents Alternaria alternata [35,46,47,48] and Alternaria citri [49], Fusarium oxysporum [48], and Fusarium sarcochroum, known as a possible agent of dieback of twigs on mandarin and lemon [50]. The latter study also introduces new Fusarium spp. (F. citricola, F. salinense, F. siculi), causing cankers on several citrus species. Considering that pathogenic Fusaria often present an early latent stage, this finding claims for further assessments concerning their possible endophytic occurrence. Finally, it is worth mentioning Physoderma citri, a species ascribed to the phylum Blastocladiomycota reported to cause vessel occlusion, but also found in asymptomatic plants of several Citrus spp. [51].

3. Other Endophytic Fungi and Their Interactions with Pests and Pathogens of Citrus

Besides the above reports, essentially dedicated to pathogenic species/genera upon the aim to assess the epidemiological impact of latent endophytic stages, additional data have been recorded on the overall species assemblage in a few contexts (Table 1). A study carried out on C. limon in Cameroon [36] pointed out that yellowing of leaves affects foliar endophytic communities, and that interactions among endophytes may be a factor driving the yellowing process. In fact, yellow leaves presented a less varied species assortment dominated by C. gloeosporioides in the absence of species belonging to the Mycosphaerellaceae, otherwise common in healthy leaves. In vitro observations in dual cultures showed that the latter were inhibited and overgrown by C. gloeosporioides, even if capable to revert this inhibitory effect when pre-inoculated, which was interpreted as deriving from production of fungitoxic metabolites. This study also demonstrated a low occurrence of species in the Xylariaceae, which are usually quite widespread as tree endophytes [67,68].
The endophytic occurrence of a few yeast species was documented in an investigation carried out on C. sinensis in Brazil [53]. By means of scanning electron microscopy, it was observed that these microorganisms are mostly localized around stomata and in xylem vessels. Isolates of the species Rhodotorula mucilaginosa, Meyerozyma (Pichia) guilliermondii, and Cryptococcus flavescens were inoculated in healthy plants, and re-isolated, without causing any kind of disease symptoms. Quite interestingly, the authors noted that M. guilliermondii primarily occurred in plants colonized by Xylella fastidiosa, the causal agent of citrus variegated chlorosis (CVC), and that the bacterium could thrive on a supernatant separated from cultures of a strain of this species. This finding represents an indication that the presence of the yeast could stimulate the pathogen and could be responsible for more severe disease symptoms. More recently, strains of M. guilliermondii have been recovered, along with strains of Hanseniaspora opuntiae and Pichia kluyveri, from tangerine peel in China. However, it is questionable if this record can actually concern endophytic occurrence considering that authors refer that fruits were purchased on the market rather than being directly collected in the field [59].
Indeed, interactions between endophytic bacteria and fungi are complex, and the assortment of strains which can be recovered is largely influenced by the antagonistic interactions as mediated by the production of antibiotics. In this respect, strains of P. citricarpa isolated from Citrus spp. in Brazil were found to possess inhibitory properties toward several endophytic Bacillus spp. from the same source, while a stimulatory effect was assessed towards the gram-negative Pantoea agglomerans, which can be taken as an indication of the opportunity to investigate possible interference with the development of X. fastidiosa [56].
Antagonistic properties by an isolate of Muscodor sp. from C. sinensis were reported against P. citrocarpa as deriving from the production of volatile organic compounds (VOCs) [61]. Actually, such properties are known for endophytic isolates of Muscodor and other genera of xylariaceous fungi, such as Hypoxylon (=Nodulisporium) and Xylaria, reported from many plant species [69] and also occurring in citrus plants [35,36,49,52].
Endophytic strains belonging to two species of Diaporthe, D. terebinthifolii and the already-mentioned D. endophytica, displayed inhibitory properties against P. citrocarpa in vitro and on detached fruits. Moreover, their transformants expressing the fluorescent protein DsRed proved to be able to actively colonize citrus seedlings, and to remain viable in the plant tissues for one year at least. These evidences support their possible use in the biocontrol of this pathogen [70]. Antifungal properties have also been reported for a strain of another fungus belonging to the Diaporthales (Lasmenia sp.), which was recovered from C. medica var. sarcodactylis [52].
Rather than just concerning agents of cryptogamic diseases, protective effects by endophytic fungi may pertain several kinds of pests [71,72]. Actually, data available in the literature concerning citrus plants are limited but encourage further assessments. For instance, a ustilaginomycetous yeast endophytic in grapefruit (Citrus paradisi), Meira geulakonigae, was found to be able to reduce populations of the citrus rust mite (Phyllocoptruta oleivora) [60]. More recently, two strains of Beauveria bassiana were inoculated in seedlings of C. limon through foliar sprays and proved to be able to colonize the plants endophytically. Besides increasing plant growth, they caused 10%–15% mortality on adults of the Asian citrus psyllid (Diaphorina citri), and the females feeding on the treated plants laid significantly fewer eggs [55]. It is not unlikely that more evidence in this respect can be gathered from targeted investigations concerning naturally occurring endophytes, considering that protective effects have been documented for endophytic strains of F. oxysporum against aphids [73] and nematodes [74].
As a general ecological trait, endophytic fungi seem to be absent in seeds of citrus species [65]. This is to be taken as an indication that these microorganisms are not adapted to a vertical spread, and most likely colonize citrus plants coming from the surrounding environment.

4. Biotechnological Implications

The involvement of endophytic fungi in a tripartite relationship with the host plant and its pests and pathogens highlights their basic role in establishing an equilibrium in such a fragile biocoenosis. Indeed, a major biotechnological application of endophytic strains consists in the exploitation of their aptitude to defensive mutualism.
The endophytic habit is conducive for interactions with other microorganisms sharing the same micro-environment. There is strong evidence that these interactions entangle the genetic level, and that interspecific transfer of gene pools regularly occurs. Probably, the best example in this respect is represented by genes encoding for the synthesis of polyketide secondary metabolites, which are usually grouped in clusters and are influenced in their expression by several external factors [75,76]. Horizontal gene transfer from other endophytic microorganisms may eventually explain the ability by a strain of P. citricarpa [77] to produce the blockbuster drug taxol, first extracted from Taxus spp. and afterwards as a secondary metabolite of a high number of endophytic fungi [69,78].
P. citricarpa has been further characterized with reference to production of secondary metabolites. Particularly, it has been reported to produce the new dioxolanone phenguignardic acid butyl ester, along with four previously reported compounds: phenguignardic acid methyl ester, peniisocoumarin G, protocatechuic acid, and tyrosol [79]. Phyllosticta spp. have been reported to have a similar metabolomic profile, including the dioxolanone phytotoxins which are regarded as potential virulence factors. However, one of these products, guignardic acid, has also been reported from P. capitalensis [80]. Biosynthetic abilities by endophytic strains of the latter species also refer to meroterpenes, such as compounds in the guignardone series [81,82,83,84] and the manginoids [85]. Besides a likely implication in the relationships with other citrus-associated microbial species, the bioactive properties of the dioxolanones and the related meroterpene compounds deserve to be further investigated in view of possible pharmaceutical exploitation [79,86].
Protocatechuic acid was again reported from an unidentified fungal strain recovered from leaves of Citrus jambhiri, along with indole-3-acetic acid (IAA) and acropyrone [87]. The latter compound was shown to possess antibiotic properties against Staphylococcus aureus, while the finding of IAA is in line with the many reports of plant hormones produced by endophytic fungi [69], which at least in part unfold the growth-promoting effects exerted on their hosts [88,89]. Production of IAA was also reported from strains of the yeasts Hanseniaspora opuntiae and Meyerozyma guilliermondii from Citrus reticulata, which were able to induce growth-promoting effects on seedlings of Triticum aestivum [59].
The above-mentioned VOCs reported from an endophytic strain of Muscodor sp. from C. sinensis include several sesquiterpenes, namely azulene, cis/trans-α-bergamotene, cedrene, (Z)-β-farnesene, farnesene epoxide, α-himachalene, α-longipinene, thujopsene, 2,4,6-trimethyl-1,3,6-heptatriene, 2-methyl-5,7-dimethylene-1-8-nonadiene, and cis-Z-bisabolene epoxide [61]. Mixtures of these compounds have a possible biotechnological application for the mycofumigation of fruits, proposed for the control of CBS and various post-harvest pathogens [90,91,92]. Concerning VOCs, another possible investigational subject consists in assessing if any endophyte of citrus plants is able to produce compounds occurring in the typical aroma spread by flowers and fruits of these plants, which are exploited by the pharmaceutical and the perfume industries. In this respect, the production of bergapten, a psoralen compound known from bergamot (Citrus bergamia), has already been pointed out by endophytic strains of Penicillium sp. [93] and L. theobromae [94]. Although these findings concern plants other than citrus, it is worth considering that these fungi are also reported as citrus endophytes (Table 1).
Antimicrobial properties of fungi do not just depend on the production of bioactive compounds. In fact, a strain of P. capitalensis (Bios PTK 4) recovered from an unidentified citrus plant was found to be able to synthesize silver nanoparticles extracellularly. These nanoparticles, which were spherical, 5–30 nm in size, well-dispersed, and extremely stable, have been characterized for their antibacterial and antifungal properties [95].

5. Conclusions

Revision of literature in the field shows that a major part of the research activity carried out on endophytic fungi of citrus plants consists in investigations on the occurrence of pathogens, and their discrimination from other ecologically associated taxa. Such a limited approach has, anyway, turned to be useful to disclose an epidemiological relevance of these microorganisms, as related to a modulatory role in the spread of citrus diseases. On that account, possible interactions in conducive contexts with other important pathogens, such as the agent of mal secco Phoma tracheiphila and species of Phytophthora causing foot and root rot, should be attentively considered. Even when there is no apparent direct interaction with disease agents, such as in the cases of CVC incited by X. fastidiosa, tristeza, and other viroses, the possible effect by endophytic fungi in stimulating plant defense reaction, or, more in general, to act as plant disease modifiers [96], should not be disregarded. In this respect, data concerning occasional isolations might well disclose some relevance. Unfortunately, description of the endophytic assemblages in several papers is often approximate or incomplete, such as in a mentioned survey concerning sweet orange (C. sinensis), where just a single strain was characterized out of a sample of over 400 endophytes [61]. It is to be recommended that future investigations in the field be more circumstantial in their approach to describe this component of biodiversity, in the aim of increasing opportunities for its biotechnological exploitation.
Encouraging examples in this direction are represented by two very recent publications from Iran [48,49]. Indeed, the focus on endophytic fungi is gradually evolving from a basically descriptive phase to the analysis of factors influencing the structure and composition of microbiomes, in view of their manipulation for increasing plant protection and productivity. A better comprehension of the already introduced genetic interactions among members of the associated biota and the host tree is crucial for the success of any practical application of endophytic fungi in sustainable agriculture [97]. Moreover, the observed effects of the host genotype [98,99] could be adequately considered in breeding programs, in the aim to select suitable recipient genotypes for fungal inoculants.

Funding

This research received no external funding.

Conflicts of Interest

The author declares no conflict of interest.

References

  1. De Bary, A. Morphologie und Physiologie der Pilze, Flechten und Myxomyceten; Engelmann: Leipzig, Germany, 1866. [Google Scholar]
  2. Hyde, K.D.; Soytong, K. The fungal endophyte dilemma. Fungal Divers. 2008, 33, 163–173. [Google Scholar]
  3. Turner, T.R.; James, E.K.; Poole, P.S. The plant microbiome. Genome Biol. 2013, 14, 209. [Google Scholar] [CrossRef] [PubMed]
  4. McOnie, K.C. The latent occurrence in Citrus and other hosts of a Guignardia easily confused with G. citricarpa, the black spot pathogen. Phytopathology 1964, 54, 64–67. [Google Scholar]
  5. Meyer, L.; Slippers, B.; Korsten, L.; Kotze, J.M.; Wingfield, M.J. Two distinct Guignardia species associated with citrus in South Africa. S. Afr. J. Sci. 2001, 97, 191–194. [Google Scholar]
  6. Baayen, R.P.; Bonants, P.J.M.; Verkley, G.; Carroll, G.C.; van der Aa, H.A.; de Weerdt, M.; van Brouwershaven, I.R.; Schutte, G.C.; Maccheroni, W., Jr.; Glienke de Blanco, C.; et al. Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology 2002, 92, 464–477. [Google Scholar] [CrossRef]
  7. Zavala, M.G.M.; Er, H.L.; Goss, E.M.; Wang, N.Y.; Dewdney, M.; van Bruggen, A.H.C. Genetic variation among Phyllosticta strains isolated from citrus in Florida that are pathogenic or nonpathogenic to citrus. Trop. Plant Pathol. 2014, 39, 119–128. [Google Scholar] [CrossRef]
  8. Guarnaccia, V.; Gehrmann, T.; Silva-Junior, G.J.; Fourie, P.H.; Haridas, S.; Vu, D.; Spatafora, J.; Martin, F.M.; Robert, V.; Grigoriev, I.V.; et al. Phyllosticta citricarpa and sister species of global importance to Citrus. Mol. Plant Pathol. 2019. [Google Scholar] [CrossRef]
  9. Wikee, S.; Udayanga, D.; Crous, P.W.; Chukeatirote, E.; McKenzie, E.H.; Bahkali, A.H.; Dai, D.Q.; Hyde, K.D. Phyllosticta—An overview of current status of species recognition. Fungal Divers. 2011, 51, 43–61. [Google Scholar] [CrossRef]
  10. Wikee, S.; Lombard, L.; Crous, P.W.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Alias, S.A.; McKenzie, E.H.C.; Hyde, K.D. Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers. 2013, 60, 91–105. [Google Scholar] [CrossRef]
  11. Okane, I.; Nakagiri, A.; Ito, T.; Lumyong, S. Extensive host range of an endophytic fungus, Guignardia endophyllicola (anamorph: Phyllosticta capitalensis). Mycoscience 2003, 44, 353–363. [Google Scholar] [CrossRef]
  12. Bonants, P.J.; Carroll, G.C.; De Weerdt, M.; van Brouwershaven, I.R.; Baayen, R.P. Development and validation of a fast PCR-based detection method for pathogenic isolates of the citrus black spot fungus, Guignardia citricarpa. Eur. J. Plant Pathol. 2003, 109, 503–513. [Google Scholar] [CrossRef]
  13. Meyer, L.; Sanders, G.M.; Jacobs, R.; Korsten, L. A one-day sensitive method to detect and distinguish between the citrus black spot pathogen Guignardia citricarpa and the endophyte Guignardia mangiferae. Plant Dis. 2006, 90, 97–101. [Google Scholar] [CrossRef]
  14. Meyer, L.; Jacobs, R.; Kotzé, J.M.; Truter, M.; Korsten, L. Detection and molecular identification protocols for Phyllosticta citricarpa from citrus matter. S. Afr. J. Sci. 2012, 108, 53–59. [Google Scholar] [CrossRef]
  15. Peres, N.A.; Harakava, R.; Carroll, G.C.; Adaskaveg, J.E.; Timmer, L.W. Comparison of molecular procedures for detection and identification of Guignardia citricarpa and G. mangiferae. Plant Dis. 2007, 91, 525–531. [Google Scholar] [CrossRef]
  16. Van Gent-Pelzer, M.P.E.; Van Brouwershaven, I.R.; Kox, L.F.F.; Bonants, P.J.M. A TaqMan PCR method for routine diagnosis of the quarantine fungus Guignardia citricarpa on citrus fruit. J. Phytopathol. 2007, 155, 357–363. [Google Scholar] [CrossRef]
  17. Baldassari, R.B.; Wickert, E.; de Goes, A. Pathogenicity, colony morphology and diversity of isolates of Guignardia citricarpa and G. mangiferae isolated from Citrus spp. Eur. J. Plant Pathol. 2008, 120, 103–110. [Google Scholar] [CrossRef]
  18. Stringari, D.; Glienke, C.; Christo, D.D.; Maccheroni, W., Jr.; Azevedo, J.L.D. High molecular diversity of the fungus Guignardia citricarpa and Guignardia mangiferae and new primers for the diagnosis of the citrus black spot. Braz. Arch. Biol. Technol. 2009, 52, 1063–1073. [Google Scholar] [CrossRef]
  19. Hu, J.; Johnson, E.G.; Wang, N.Y.; Davoglio, T.; Dewdney, M.M. qPCR quantification of pathogenic Guignardia citricarpa and nonpathogenic G. mangiferae in citrus. Plant Dis. 2014, 98, 112–120. [Google Scholar] [CrossRef]
  20. Schirmacher, A.M.; Tomlinson, J.A.; Barnes, A.V.; Barton, V.C. Species-specific real-time PCR for diagnosis of Phyllosticta citricarpa on Citrus species. EPPO Bull. 2019. [Google Scholar] [CrossRef]
  21. Everett, K.R.; Rees-George, J. Reclassification of an isolate of Guignardia citricarpa from New Zealand as Guignardia mangiferae by sequence analysis. Plant Pathol. 2006, 55, 194–199. [Google Scholar] [CrossRef]
  22. Romão, A.S.; Spósito, M.B.; Andreote, F.D.; Azevedo, J.L.D.; Araújo, W.L. Enzymatic differences between the endophyte Guignardia mangiferae (Botryosphaeriaceae) and the citrus pathogen G. citricarpa. Genet. Mol. Res. 2011, 10, 243–252. [Google Scholar] [CrossRef] [PubMed]
  23. Munari Rodrigues, C.; Takita, M.A.; Silva, N.V.; Ribeiro-Alves, M.; Machado, M.A. Comparative genome analysis of Phyllosticta citricarpa and Phyllosticta capitalensis, two fungi species that share the same host. BMC Genom. 2019, 20, 554. [Google Scholar] [CrossRef]
  24. Wikee, S.; Lombard, L.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Cheewangkoon, R.; McKenzie, E.H.C.; Hyde, K.D.; Crous, P.W. A phylogenetic re-evaluation of Phyllosticta (Botryosphaeriales). Stud. Mycol. 2013, 76, 1–29. [Google Scholar] [CrossRef] [PubMed]
  25. Wulandari, N.F.; Toanun, C.; Hyde, K.D.; Duong, L.M.; de Gruyter, J.; Meffert, J.P.; Groenewald, J.Z.; Crous, P.W. Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia. Fungal Divers. 2009, 34, 23–39. [Google Scholar]
  26. Wang, X.; Chen, G.; Huang, F.; Zhang, J.; Hyde, K.D.; Li, H. Phyllosticta species associated with citrus diseases in China. Fungal Divers. 2012, 52, 209–224. [Google Scholar] [CrossRef]
  27. Guarnaccia, V.; Groenewald, J.Z.; Li, H.; Glienke, C.; Carstens, E.; Hattingh, V.; Fourie, P.H.; Crous, P.W. First report of Phyllosticta citricarpa and description of two new species, P. paracapitalensis and P. paracitricarpa, from citrus in Europe. Stud. Mycol. 2017, 87, 161–185. [Google Scholar] [CrossRef]
  28. Glienke, C.; Pereira, O.L.; Stringari, D.; Fabris, J.; Kava-Cordeiro, V.; Galli-Terasawa, L.; Cunnington, J.; Shivas, R.G.; Groenewald, J.Z.; Crous, P.W. Endophytic and pathogenic Phyllosticta species, with reference to those associated with citrus black spot. Persoonia 2011, 26, 47–56. [Google Scholar] [CrossRef]
  29. Schubert, T.S.; Dewdney, M.M.; Peres, N.A.; Palm, M.E.; Jeyaprakash, A.; Sutton, B.; Mondal, S.N.; Wang, N.Y.; Rascoe, J.; Picton, D.D. First report of Guignardia citricarpa associated with citrus black spot on sweet orange (Citrus sinensis) in North America. Plant Dis. 2012, 96, 1225. [Google Scholar] [CrossRef]
  30. Jeger, M.; Bragard, C.; Caffier, D.; Candresse, T.; Chatzivassiliou, E.; Dehnen-Schmutz, K.; Gilioli, G.; Gregoire, J.C.; Jaques Miret, J.A.; MacLeod, A.; et al. Evaluation of a paper by Guarnaccia et al. (2017) on the first report of Phyllosticta citricarpa in Europe. EFSA J. 2018, 16, 5114. [Google Scholar]
  31. Tran, N.T.; Miles, A.K.; Dietzgen, R.G.; Drenth, A. Phyllosticta capitalensis and P. paracapitalensis are endophytic fungi that show potential to inhibit pathogenic P. citricarpa on citrus. Australas. Plant Pathol. 2019, 48, 281–296. [Google Scholar] [CrossRef]
  32. Wickert, E.; de Macedo Lemos, E.G.; Kishi, L.T.; de Souza, A.; de Goes, A. Genetic diversity and population differentiation of Guignardia mangiferae from “Tahiti” acid lime. Sci. World J. 2012. [Google Scholar] [CrossRef]
  33. Huang, F.; Chen, G.Q.; Hou, X.; Fu, Y.S.; Cai, L.; Hyde, K.D.; Li, H.Y. Colletotrichum species associated with cultivated citrus in China. Fungal Divers. 2013, 61, 61–74. [Google Scholar] [CrossRef]
  34. Waculicz-Andrade, C.E.; Savi, D.C.; Bini, A.P.; Adamoski, D.; Goulin, E.H.; Silva, G.J., Jr.; Massola, N.S., Jr.; Terasawa, L.G.; Kava, V.; Glienke, C. Colletotrichum gloeosporioides sensu stricto: An endophytic species or citrus pathogen in Brazil? Australas. Plant Pathol. 2017, 46, 191–203. [Google Scholar] [CrossRef]
  35. Durán, E.L.; Ploper, L.D.; Ramallo, J.C.; Piccolo Grandi, R.A.; Hupper Giancoli, Á.C.; Azevedo, J.L. The foliar fungal endophytes of Citrus limon in Argentina. Can. J. Bot. 2005, 83, 350–355. [Google Scholar] [CrossRef]
  36. Douanla-Meli, C.; Langer, E.; Mouafo, F.T. Fungal endophyte diversity and community patterns in healthy and yellowing leaves of Citrus limon. Fungal Ecol. 2013, 6, 212–222. [Google Scholar] [CrossRef]
  37. Mohali, S.; Burgess, T.I.; Wingfield, M.J. Diversity and host association of the tropical tree endophyte Lasiodiplodia theobromae revealed using simple sequence repeat markers. For. Pathol. 2005, 35, 385–396. [Google Scholar] [CrossRef]
  38. Slippers, B.; Wingfield, M.J. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: Diversity, ecology and impact. Fungal Biol. Rev. 2007, 21, 90–106. [Google Scholar] [CrossRef]
  39. Zhao, W.; Bai, J.; McCollum, G.; Baldwin, E. High incidence of preharvest colonization of huanglongbing-symptomatic Citrus sinensis fruit by Lasiodiplodia theobromae (Diplodia natalensis) and exacerbation of postharvest fruit decay by that fungus. Appl. Environ. Microbiol. 2015, 81, 364–372. [Google Scholar] [CrossRef] [Green Version]
  40. Udayanga, D.; Liu, X.; McKenzie, E.H.C.; Chukeatirote, E.; Bahkali, A.H.A.; Hyde, K.D. The genus Phomopsis: Biology, applications, species concepts and names of common phytopathogens. Fungal Divers. 2011, 50, 189–225. [Google Scholar] [CrossRef]
  41. Gomes, R.R.; Glienke, C.; Videira, S.I.R.; Lombard, L.; Groenewald, J.Z.; Crous, P.W. Diaporthe: A genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 2013, 31, 1–41. [Google Scholar] [CrossRef] [Green Version]
  42. Savi, D.C.; Aluizio, R.; Glienke, C. Brazilian plants: An unexplored source of endophytes as producers of active metabolites. Planta Med. 2019, 85, 619–636. [Google Scholar]
  43. Huang, F.; Hou, X.; Dewdney, M.M.; Fu, Y.; Chen, G.; Hyde, K.D.; Li, H. Diaporthe species occurring on citrus in China. Fungal Divers. 2013, 61, 237–250. [Google Scholar] [CrossRef]
  44. Guarnaccia, V.; Crous, P.W. Emerging citrus diseases in Europe caused by species of Diaporthe. IMA Fungus 2017, 8, 317–334. [Google Scholar] [CrossRef] [Green Version]
  45. Huang, F.; Udayanga, D.; Wang, X.; Hou, X.; Mei, X.; Fu, Y.; Hyde, K.D.; Li, H. Endophytic Diaporthe associated with Citrus: A phylogenetic reassessment with seven new species from China. Fungal Biol. 2015, 119, 331–347. [Google Scholar] [CrossRef]
  46. Peever, T.L.; Canihos, Y.; Olsen, L.; Ibáñez, A.; Liu, Y.C.; Timmer, L.W. Population genetic structure and host specificity of Alternaria spp. causing brown spot of Minneola tangelo and rough lemon in Florida. Phytopathology 1999, 89, 851–860. [Google Scholar] [CrossRef] [Green Version]
  47. Akimitsu, K.; Peever, T.L.; Timmer, L.W. Molecular, ecological and evolutionary approaches to understanding Alternaria diseases of citrus. Mol. Plant Pathol. 2003, 4, 435–446. [Google Scholar] [CrossRef]
  48. Sadeghi, F.; Samsampour, D.; Seyahooei, M.A.; Bagheri, A.; Soltani, J. Diversity and spatiotemporal distribution of fungal endophytes associated with Citrus reticulata cv. Siyahoo. Curr. Microbiol. 2019, 76, 279–289. [Google Scholar] [CrossRef]
  49. Juybari, H.Z.; Tajick Ghanbary, M.A.; Rahimian, H.; Karimi, K.; Arzanlou, M. Seasonal, tissue and age influences on frequency and biodiversity of endophytic fungi of Citrus sinensis in Iran. For. Pathol. 2019, e12559. [Google Scholar] [CrossRef]
  50. Sandoval-Denis, M.; Guarnaccia, V.; Polizzi, G.; Crous, P.W. Symptomatic Citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia 2018, 40, 1–25. [Google Scholar] [CrossRef] [Green Version]
  51. Childs, J.F.L.; Kopp, L.E.; Johnson, R.E. A species of Physoderma present in Citrus and related species. Phytopathology 1965, 55, 681–687. [Google Scholar]
  52. Ho, M.Y.; Chung, W.C.; Huang, H.C.; Chung, W.H.; Chung, W.H. Identification of endophytic fungi of medicinal herbs of Lauraceae and Rutaceae with antimicrobial property. Taiwania 2012, 57, 229–241. [Google Scholar]
  53. Santos Gai, C.; Teixeira Lacava, P.; Maccheroni, W., Jr.; Glienke, C.; Araújo, W.L.; Miller, T.A.; Azevedo, J.L. Diversity of endophytic yeasts from sweet orange and their localization by scanning electron microscopy. J. Basic Microbiol. 2009, 49, 441–451. [Google Scholar]
  54. Rodríguez, P.; Reyes, B.; Barton, M.; Coronel, C.; Menéndez, P.; Gonzalez, D.; Rodríguez, S. Stereoselective biotransformation of α-alkyl-β-keto esters by endophytic bacteria and yeast. J. Mol. Catal. B Enzym. 2011, 71, 90–94. [Google Scholar] [CrossRef]
  55. Bamisile, B.S.; Dash, C.K.; Akutse, K.S.; Qasim, M.; Ramos Aguila, L.C.; Wang, F.; Keppanan, R.; Wang, L. Endophytic Beauveria bassiana in foliar-treated Citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects 2019, 10, 176. [Google Scholar] [CrossRef] [Green Version]
  56. Araújo, W.L.; Maccheroni, W., Jr.; Aguilar-Vildoso, C.I.; Barroso, P.A.; Saridakis, H.O.; Azevedo, J.L. Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can. J. Microbiol. 2001, 47, 229–236. [Google Scholar] [CrossRef]
  57. Glienke-Blanco, C.; Aguilar-Vildoso, C.I.; Vieira, M.L.C.; Barroso, P.A.V.; Azevedo, J.L. Genetic variability in the endophytic fungus Guignardia citricarpa isolated from citrus plants. Genet. Mol. Biol. 2002, 25, 251–255. [Google Scholar] [CrossRef]
  58. Manoharan, G.; Sairam, T.; Thangamani, R.; Ramakrishnan, D.; Tiwari, M.K.; Lee, J.K.; Marimuthu, J. Identification and characterization of type III polyketide synthase genes from culturable endophytes of ethnomedicinal plants. Enzyme Microb. Technol. 2019, 131, 109396. [Google Scholar] [CrossRef]
  59. Ling, L.; Li, Z.; Jiao, Z.; Zhang, X.; Ma, W.; Feng, J.; Zhang, J.; Lu, L. Identification of novel endophytic yeast strains from tangerine peel. Curr. Microbiol. 2019, 76, 1066–1072. [Google Scholar] [CrossRef]
  60. Paz, Z.; Burdman, S.; Gerson, U.; Sztejnberg, A. Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora. J. Appl. Microbiol. 2007, 103, 2570–2579. [Google Scholar] [CrossRef]
  61. Pena, L.C.; Jung, L.F.; Savi, D.C.; Servienski, A.; Aluizio, R.; Goulin, E.H.; Galli-Terasawa, L.V.; Lameiro de Noronha Sales Maia, B.H.; Annies, V.; Cavichiolo Franco, C.R.; et al. A Muscodor strain isolated from Citrus sinensis and its production of volatile organic compounds inhibiting Phyllosticta citricarpa growth. J. Plant Dis. Prot. 2017, 124, 349–360. [Google Scholar] [CrossRef]
  62. Rodrigues, K.F.; Sieber, T.N.; Grünig, C.R.; Holdenrieder, O. Characterization of Guignardia mangiferae isolated from tropical plants based on morphology, ISSR-PCR amplifications and ITS1-5.8 S-ITS2 sequences. Mycol. Res. 2004, 108, 45–52. [Google Scholar] [CrossRef]
  63. Miles, A.K.; Tan, Y.P.; Tan, M.K.; Donovan, N.J.; Ghalayini, A.; Drenth, A. Phyllosticta spp. on cultivated citrus in Australia. Australas. Plant Pathol. 2013, 42, 461–467. [Google Scholar] [CrossRef]
  64. Schüepp, H. Untersuchungen über Guignardia citricarpa Kiely, den Erreger der Schwarzfleckenkrankheit auf Citrus. J. Phytopathol. 1960, 40, 258–271. [Google Scholar] [CrossRef]
  65. Azevedo, J.L.; Maccheroni, W., Jr.; Pereira, J.O.; de Araújo, W.L. Endophytic microorganisms: A review on insect control and recent advances on tropical plants. Electron. J. Biotechnol. 2000, 3, 15–16. [Google Scholar] [CrossRef]
  66. Hawksworth, D.L.; Crous, P.W.; Redhead, S.A.; Reynolds, D.R.; Samson, R.A.; Seifert, K.A.; Taylor, J.W.; Wingfield, M.J.; Abaci, O.; Aime, C.; et al. The Amsterdam declaration on fungal nomenclature. IMA Fungus 2011, 2, 105–112. [Google Scholar] [CrossRef] [Green Version]
  67. 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. [Google Scholar] [CrossRef]
  68. U’Ren, J.M.; Miadlikowska, J.; Zimmerman, N.B.; Lutzoni, F.; Stajich, J.E.; Arnold, A.E. Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota). Mol. Phylogenet. Evol. 2016, 98, 210–232. [Google Scholar] [CrossRef] [Green Version]
  69. Nicoletti, R.; Fiorentino, A. Plant bioactive metabolites and drugs produced by endophytic fungi of Spermatophyta. Agriculture 2015, 5, 918–970. [Google Scholar] [CrossRef] [Green Version]
  70. Camargo Dos Santos, P.J.; Savi, D.C.; Rodrigues Gomes, R.; Goulin, E.H.; Da Costa Senkiv, C.; Ossamu Tanaka, F.A.; Rodrigues Almeida, A.M.; Galli-Terasawa, L.; Kava, V.; Glienke, C. Diaporthe endophytica and D. terebinthifolii from medicinal plants for biological control of Phyllosticta citricarpa. Microbiol. Res. 2016, 186, 153–160. [Google Scholar] [CrossRef]
  71. Hartley, S.E.; Gange, A.C. Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Ann. Rev. Entomol. 2009, 54, 323–342. [Google Scholar] [CrossRef]
  72. Eberl, F.; Uhe, C.; Unsicker, S.B. Friend or foe? The role of leaf-inhabiting fungal pathogens and endophytes in tree-insect interactions. Fungal Ecol. 2019, 38, 104–112. [Google Scholar] [CrossRef]
  73. Martinuz, A.; Schouten, A.; Menjivar, R.D.; Sikora, R.A. Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol. Control 2012, 62, 206–212. [Google Scholar] [CrossRef]
  74. Bogner, C.W.; Kamdem, R.S.; Sichtermann, G.; Matthäus, C.; Hölscher, D.; Popp, J.; Proksch, P.; Grundler, F.M.; Schouten, A. Bioactive secondary metabolites with multiple activities from a fungal endophyte. Microb. Biotechnol. 2017, 10, 175–188. [Google Scholar] [CrossRef] [PubMed]
  75. Brakhage, A.A.; Schroeckh, V. Fungal secondary metabolites–strategies to activate silent gene clusters. Fungal Genet. Biol. 2011, 48, 15–22. [Google Scholar] [CrossRef] [PubMed]
  76. Deepika, V.B.; Murali, T.S.; Satyamoorthy, K. Modulation of genetic clusters for synthesis of bioactive molecules in fungal endophytes: A review. Microbiol. Res. 2016, 182, 125–140. [Google Scholar] [CrossRef] [PubMed]
  77. Kumaran, R.S.; Muthumary, J.; Hur, B.K. Taxol from Phyllosticta citricarpa, a leaf spot fungus of the angiosperm Citrus medica. J. Biosci. Bioeng. 2008, 106, 103–106. [Google Scholar] [CrossRef] [PubMed]
  78. Nicoletti, R.; Fiorentino, A. Antitumor metabolites of fungi. Curr. Bioact. Comp. 2014, 10, 207–244. [Google Scholar] [CrossRef]
  79. Savi, D.C.; Shaaban, K.A.; Mitra, P.; Ponomareva, L.V.; Thorson, J.S.; Glienke, C.; Rohr, J. Secondary metabolites produced by the citrus phytopathogen Phyllosticta citricarpa. J. Antibiot. 2019, 72, 306–310. [Google Scholar] [CrossRef]
  80. Buckel, I.; Andernach, L.; Schüffler, A.; Piepenbring, M.; Opatz, T.; Thines, E. Phytotoxic dioxolanones are potential virulence factors in the infection process of Guignardia bidwellii. Sci. Rep. 2017, 7, 8926. [Google Scholar] [CrossRef] [Green Version]
  81. Yuan, W.H.; Liu, M.; Jiang, N.; Guo, Z.K.; Ma, J.; Zhang, J.; Song, Y.C.; Tan, R.X. Guignardones A–C: Three meroterpenes from Guignardia mangiferae. Eur. J. Org. Chem. 2010, 33, 6348–6353. [Google Scholar] [CrossRef]
  82. Guimarães, D.O.; Lopes, N.P.; Pupo, M.T. Meroterpenes isolated from the endophytic fungus Guignardia mangiferae. Phytochem. Lett. 2012, 5, 519–523. [Google Scholar] [CrossRef]
  83. Han, W.B.; Dou, H.; Yuan, W.H.; Gong, W.; Hou, Y.Y.; Ng, S.W.; Tan, R.X. Meroterpenes with toll-like receptor 3 regulating activity from the endophytic fungus Guignardia mangiferae. Planta Med. 2015, 81, 145–151. [Google Scholar] [CrossRef] [Green Version]
  84. Sun, Z.H.; Liang, F.L.; Wu, W.; Chen, Y.C.; Pan, Q.L.; Li, H.H.; Ye, W.; Liu, H.X.; Li, S.N.; Tan, G.H.; et al. Guignardones P–S, new meroterpenoids from the endophytic fungus Guignardia mangiferae A348 derived from the medicinal plant smilax glabra. Molecules 2015, 20, 22900–22907. [Google Scholar] [CrossRef] [Green Version]
  85. Chen, K.; Zhang, X.; Sun, W.; Liu, J.; Yang, J.; Chen, C.; Liu, X.; Gao, L.; Wang, J.; Li, H.; et al. Manginoids A–G: Seven monoterpene–shikimate-conjugated meroterpenoids with a spiro ring system from Guignardia mangiferae. Org. Lett. 2017, 19, 5956–5959. [Google Scholar] [CrossRef]
  86. Li, T.X.; Yang, M.H.; Wang, X.B.; Wang, Y.; Kong, L.Y. Synergistic antifungal meroterpenes and dioxolanone derivatives from the endophytic fungus Guignardia sp. J. Nat. Prod. 2015, 78, 2511–2520. [Google Scholar] [CrossRef]
  87. Eze, P.M.; Ojimba, N.K.; Abonyi, D.O.; Chukwunwejim, C.R.; Abba, C.C.; Okoye, F.B.C.; Esimone, C.O. Antimicrobial activity of metabolites of an endophytic fungus isolated from the leaves of Citrus jambhiri (Rutaceae). Trop. J. Nat. Prod. Res. 2018, 2, 145–149. [Google Scholar] [CrossRef]
  88. Doty, S.L. Growth-promoting endophytic fungi of forest trees. In Endophytes of Forest Trees; Pirttilä, A., Frank, A., Eds.; Springer: Berlin, Germany, 2011; pp. 151–156. [Google Scholar]
  89. Waqas, M.; Khan, A.L.; Kamran, M.; Hamayun, M.; Kang, S.M.; Kim, Y.H.; Lee, I.J. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 2012, 17, 10754–10773. [Google Scholar] [CrossRef]
  90. Suwannarach, N.; Kumla, J.; Bussaban, B.; Nuangmek, W.; Matsui, K.; Lumyong, S. Biofumigation with the endophytic fungus Nodulisporium spp. CMU-UPE34 to control postharvest decay of citrus fruit. Crop Prot. 2013, 45, 63–70. [Google Scholar] [CrossRef]
  91. Gomes, A.A.M.; Queiroz, M.V.; Pereira, O.L. Mycofumigation for the biological control of post-harvest diseases in fruits and vegetables: A review. Austin J. Biotechnol. Bioeng. 2015, 2, 1051. [Google Scholar]
  92. Kaddes, A.; Fauconnier, M.L.; Sassi, K.; Nasraoui, B.; Jijakli, M.H. Endophytic fungal volatile compounds as solution for sustainable agriculture. Molecules 2019, 24, 1065. [Google Scholar] [CrossRef] [Green Version]
  93. Huang, Z.; Yang, J.; Cai, X.; She, Z.; Lin, Y. A new furanocoumarin from the mangrove endophytic fungus Penicillium sp. (ZH16). Nat. Prod. Res. 2012, 26, 1291–1295. [Google Scholar] [CrossRef]
  94. Zaher, A.M.; Moharram, A.M.; Davis, R.; Panizzi, P.; Makboul, M.A.; Calderón, A.I. Characterisation of the metabolites of an antibacterial endophyte Botryodiplodia theobromae Pat. of Dracaena draco L. by LC–MS/MS. Nat. Prod. Res. 2015, 29, 2275–2281. [Google Scholar] [CrossRef]
  95. Balakumaran, M.D.; Ramachandran, R.; Kalaichelvan, P.T. Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiol. Res. 2015, 178, 9–17. [Google Scholar] [CrossRef]
  96. Busby, P.E.; Ridout, M.; Newcombe, G. Fungal endophytes: Modifiers of plant disease. Plant Mol. Biol. 2016, 90, 645–655. [Google Scholar] [CrossRef]
  97. Schlaeppi, K.; Bulgarelli, D. The plant microbiome at work. Mol. Plant Microbe Interact. 2015, 28, 212–217. [Google Scholar] [CrossRef]
  98. Ahlholm, J.U.; Helander, M.; Henriksson, J.; Metzler, M.; Saikkonen, K. Environmental conditions and host genotype direct genetic diversity of Venturia ditricha, a fungal endophyte of birch trees. Evolution 2002, 56, 1566–1573. [Google Scholar] [CrossRef]
  99. Balint, M.; Tiffin, P.; Hallstrom, B.; O’Hara, R.B.; Olson, M.S.; Fankhauser, J.D.; Piepenbring, M.; Schmitt, I. Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS ONE 2013, 8, e53987. [Google Scholar] [CrossRef] [Green Version]
Table 1. Endophytic fungi reported from Citrus species.
Table 1. Endophytic fungi reported from Citrus species.
Endophyte 1Plant SpeciesCountryReference
Alternaria alternataC. limon, C. tangeloFlorida[46]
Citrus spp.Japan[47]
C. limonArgentina[35]
C. reticulataIran[48]
Alternaria brassicicolaC. reticulataIran[48]
Alternaria carthamiC. reticulataIran[48]
Alternaria citriC. sinensisIran[49]
Alternaria infectoriaC. sinensisIran[49]
Alternaria rosaeC. sinensisIran[49]
Alternaria sp.C. kotokanTaiwan[52]
C. sinensisIran[49]
Annulohypoxylon stygiumC. sinensisIran[49]
Arthrinium sp.C. japonicaTaiwan[52]
Ascochyta medicaginicolaC. reticulataIran[48]
Aspergillus nidulansC. sinensisIran[49]
Aspergillus nigerC. reticulataIran[48]
Aspergillus pallidofulvusC. reticulataIran[48]
Aspergillus terreusC. sinensisIran[49]
Aureobasidium iranianumC. reticulataIran[48]
Aureobasidium melanogenumC. reticulataIran[48]
Aureobasidium pullulansC. sinensisBrazil[53]
C. japonicaUruguay[54]
C. reticulataIran[48]
Beauveria bassianaC. limonChina[55]
Biscogniauxia mediterraneaC. sinensisIran[49]
Biscogniauxia nummulariaC. sinensisIran[49]
Bjerkandera adustaC. sinensisIran[49]
Botryosphaeria sp.C. aurantiumTaiwan[52]
Camarosporium sp.C. aurantium, C. medica var. sarcodactylisTaiwan[52]
Candida parapsilosisC. sinensisBrazil[53]
Cercospora sp.C. limonCameroon[36]
C. sinensisIran[49]
Chaetomium globosumC. sinensisIran[49]
Chaetomium sp.C. sinensisTaiwan[52]
Cladosporium cladosporioidesC. reticulataIran[48]
Cladosporium sp.C. limon, C. reshni, C. sinensis, C. sunki,
C. trifoliata, C. volkameriana
Brazil[56]
Cladosporium xanthochromaticumC. reticulataIran[48]
Colletotrichum boninenseC. limonCameroon[36]
C. sinensisIran[49]
Colletotrichum fructicolaC. japonica, C. reticulataChina[43]
Colletotrichum gloeosporioidesC. limon, C. reshni, C. sinensis, C. sunki,
C. trifoliata, C. volkameriana
Brazil[56]
C. limonArgentina[35]
Cameroon[36]
C. grandis, C. reticulata, C. sinensis, C. unshiuChina[43]
C. sinensisIran[49]
Colletotrichum karstiiC. grandis, C. limonChina[43]
Colletotrichum sp.C. aurantium, C. medica var. sarcodactylis,
C. sinensis
Taiwan[52]
C. deliciosa, C. reticulataBrazil[57]
C, aurantifoliaIndia[58]
Coprinellus radiansC. sinensisIran[49]
Coprinopsis sp.C. medicaTaiwan[52]
Cryptococcus flavescensC. sinensisBrazil[53]
Cryptococcus laurentiiC. sinensisBrazil[53]
Cyanodermella sp.C. medica var. sarcodactylis, Citrus sp.Taiwan[52]
Diaporthe arecae s.c. 2C. grandis, C. limon, C. reticulata, C. sinensis, Citrus sp., C. unshiuChina[45]
Diaporthe biconispora2,*C. grandis, C. japonica, C. sinensisChina[45]
Diaporthe biguttulata2,*C. limonChina[45]
Diaporthe citri2C. reticulata, C. unshiuChina[43,45]
Diaporthe citriasiana2C. unshiuChina[43]
Diaporthe citrichinensis2C. grandis, C. japonicaChina[45]
Diaporthe discoidispora2,*C. sinensis, C. unshiuChina[45]
Diaporthe endophytica2C. limonChina[45]
Diaporthe eres2C. japonica, Citrus sp., C. unshiuChina[45]
Diaporthe eucalyptorum2C. limonCameroon[36]
Diaporthe foeniculina2C. sinensisIran[49]
Diaporthe hongkongensis2C. grandis, C. reticulata, C. sinensis, C. unshiuChina[45]
Diaporthe multiguttulata2,*C. grandisChina[45]
Diaporthe ovalispora2,*C. limonChina[45]
Diaporthe phaseolorum2C. limonCameroon[36]
Diaporthe sojae2C. limon, C. reticulata, C. unshiuChina[45]
Diaporthe sp. 2C. limonCameroon[36]
C. aurantium, C. medica, C. sinensisTaiwan[52]
C. japonicaChina[45]
C. reticulataIran[48]
Diaporthe unshiuensis2,*C. japonicaChina[45]
Didymella microchlamydosporaC. reticulataIran[48]
Discostroma sp.C. medicaTaiwan[52]
Epicoccum nigrumC. sinensisIran[49]
Eutypella sp.C. medica var. sarcodactylisTaiwan[52]
Fusarium culmorumC. sinensisIran[49]
Fusarium incarnatumC. sinensisIran[49]
Fusarium oxysporumC. reticulataIran[48]
Fusarium proliferatumC. sinensisIran[49]
Fusarium sarcochroumC. limon, C. reticulataItaly, Spain[50]
Fusarium sp.C. sinensisTaiwan[52]
C. reticulataIran[48]
Hanseniaspora opuntiaeC. reticulataChina[59]
Hypholoma fasciculareC. sinensisIran[49]
Hypoxylon investiensC. sinensisIran[49]
Lasiodiplodia theobromaeC. sinensisChina[39]
Lasmenia sp.C. medica var. sarcodactylisTaiwan[52]
Meira geulakonigaeC. paradisiIsrael[60]
Meyerozyma caribbicaC. reticulataIran[48]
Meyerozyma guilliermondiiC. sinensisBrazil[53]
C. reticulataChina[58]
Muscodor sp.C. sinensisBrazil[61]
Mycoleptodiscus sp.C. aurantiumTaiwan[52]
Mycosphaerella sp.C. limonCameroon[36]
Myrothecium sp.C. reticulataIran[48]
Neocosmospora solaniC. reticulataIran[48]
Neosetophoma sp.C. reticulataIran[48]
Nigrospora oryzaeC. sinensisIran[49]
Nigrospora sphaericaC. limonArgentina[35]
Nodulisporium sp.C. limonArgentina[35]
Passalora loranthiC. limonCameroon[36]
Penicillium citrinumC. reticulataIran[48]
Pestalotiopsis mangiferaeC. limonCameroon[36]
Pestalotiopsis microsporaC. limonCameroon[36]
Pestalotiopsis sp.C. limonCameroon[36]
Phaeoacremonium parasiticumC. reticulataIran[48]
Phialophora sp.C. sinensisBrazil[53]
Phoma sp.C. limonCameroon[36]
Phyllosticta capitalensis2Citrus spp.South Africa[4]
C. deliciosa, C. reticulataBrazil[57]
C. aurantium, C. natsudaidai, C. trifoliataJapan[11]
C. aurantiumBrazil[62]
C. latifoliaBrazil[17]
C. limonia, C. sinensis, Citrus sp.Brazil[28]
C. aurantium, C. australasicaAustralia[63]
C. limonCameroon[36]
Italy, Malta, Spain Greece, Portugal[27]
C. aurantifoliaItaly
C. sinensisIran[49]
Phyllosticta citribraziliensis2,*Citrus sp.Brazil[28]
Phyllosticta citricarpa2Citrus sp.South Africa[64]
C. reshni, C. sinensis, C. sunki, C. trifoliata,
C. volkameriana
Brazil[56]
C. deliciosa, C. reticulataBrazil[65]
C. limonArgentina[35]
C. latifoliaBrazil[17]
C. sinensisFlorida[29]
Phyllosticta paracapitalensis2,*C. aurantifolia
C. floridana
C. limon
New Zealand
Italy
Spain
[27]
C. aurantium, C. australasica, C. hystrix, C. japonica, C. maxima, C. reticulata, C. wintersiiAustralia[31]
Phyllosticta sp. 2C. medica var. sarcodactylisTaiwan[52]
Physoderma citriCitrus spp.Florida[51]
Pichia kluyveriC. reticulataChina[59]
Pseudocercospora sp.C. japonicaTaiwan[52]
Pseudopestalotiopsis theaeC. limonCameroon[36]
Pseudozyma flocculosaC. reticulataIran[48]
Rhodotorula dairenensisC. sinensisBrazil[53]
Rhodotorula mucilaginosaC. sinensisBrazil[53]
Rosellinia sp.C. sinensisIran[49]
Sarocladium subulatumC. sinensisIran[49]
Scedosporium apiospermumC. reticulataIran[48]
Sordaria fimicolaC. sinensisIran[49]
Sporobolomyces sp.C. sinensisBrazil[53]
Sporormiella minimaC. limonArgentina[35]
C. sinensisIran[49]
Stemphylium sp.C. aurantium, C. japonicaTaiwan[52]
Stenella sp.C. limonCameroon[36]
Talaromyces purpurogenusC. reticulataIran[48]
Talaromyces trachyspermusC. reticulataIran[48]
Xylaria cubensisC. sinensisIran[49]
Xylaria sp.C. limonCameroon[36]
C. japonicaTaiwan[52]
Zasmidium sp.C. limonCameroon[36]
1 Species are reported according to the latest accepted name, which might not correspond to the one used in the corresponding reference. 2 Conforming to the principle ‘one fungus—one name’ [66], the older genus names Diaporthe and Phyllosticta have been considered to deserve priority over Phomopsis and Guignardia, respectively. * Novel species described for the first time from this plant source.

Share and Cite

MDPI and ACS Style

Nicoletti, R. Endophytic Fungi of Citrus Plants. Agriculture 2019, 9, 247. https://doi.org/10.3390/agriculture9120247

AMA Style

Nicoletti R. Endophytic Fungi of Citrus Plants. Agriculture. 2019; 9(12):247. https://doi.org/10.3390/agriculture9120247

Chicago/Turabian Style

Nicoletti, Rosario. 2019. "Endophytic Fungi of Citrus Plants" Agriculture 9, no. 12: 247. https://doi.org/10.3390/agriculture9120247

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop