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Review

The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae

by
Maria Michela Salvatore
1,
Anna Andolfi
1,2,* and
Rosario Nicoletti
3,4
1
Department of Chemical Sciences, University of Naples ‘Federico II’, 80126 Naples, Italy
2
BAT Center—Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology, University of Naples ‘Federico II’, 80138 Naples, Italy
3
Council for Agricultural Research and Economics, Research Centre for Olive, Fruit and Citrus Crops, 81100 Caserta, Italy
4
Department of Agricultural Sciences, University of Naples ‘Federico II’, 80055 Portici, Italy
*
Author to whom correspondence should be addressed.
Agriculture 2020, 10(10), 488; https://doi.org/10.3390/agriculture10100488
Submission received: 18 September 2020 / Revised: 13 October 2020 / Accepted: 17 October 2020 / Published: 21 October 2020
(This article belongs to the Special Issue Occurrence and Functions of Endophytic Fungi in Crop Species)
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Abstract

:
Many fungi reported for endophytic occurrence are better known as plant pathogens on different crops, raising questions about their actual relationships with the hosts and other plants in the biocoenosis and about the factors underlying the lifestyle shift. This paper offers an overview of the endophytic occurrence of Lasiodiplodia theobromae (Dothideomycetes, Botryosphaeriaceae), a species known to be able to colonize many plants as both an endophyte and a pathogen. Prevalently spread in tropical and subtropical areas, there are concerns that it may propagate to the temperate region following global warming and the increasing trade of plant materials. The state of the art concerning the biochemical properties of endophytic strains of this species is also examined with reference to a range of biotechnological applications.

1. Introduction

Endophytic fungi are plant-associated microorganisms that colonize the internal tissues of the host without inducing disease symptoms [1]. They represent a poorly understood endosymbiotic group of microbes that ought to be attentively considered by the scientific community, so as to provide comprehensive knowledge regarding their beneficial role and the actual extent of their interactions with plants.
A basic issue hindering studies on the ecological role of these microorganisms is represented by the reported endophytic occurrence of fungal pathogens. In fact, besides the cases where latency is a conspicuous phase of the disease cycle, there are more and more records of renowned pathogens found within asymptomatic hosts, for which an explanation is not immediately available [2,3,4]. Increasing and organizing the current knowledge on conditions associated with the occurrence of these ambiguous species is useful for a more conclusive assessment of their functions and impact on crops. This present paper offers an overview of a fungus which is mainly studied as a pathogen of tropical crops [4,5,6] but that is potentially able to spread as an endophytic associate of plants in the temperate zone.

2. Taxonomic and Phylogenetic Aspects

Lasiodiplodia theobromae (Pat.) Griffon & Maubl. (Dothideomycetes, Botryosphaeriaceae) is the accepted name of the species treated in this paper, prevailing over both the basionym Botryodiplodia theobromae Pat. and the teleomorphic name Botryosphaeria rhodina (Berk & M.A. Curtis) Arx, after the introduction in mycology of the principle “one species—one name” [7]. Isolated and morphologically identified from a wide range of plant hosts [5,8], it represents the type species of Lasiodiplodia which, for many years, was treated as a monotypic genus within the Botryosphaeriaceae [9,10]. However, such a simplified taxonomy was destined to dramatically change with the advent of DNA sequencing. In fact, starting from the year 2004, phylogenetic analyses carried out in the course of studies on L. theobromae in novel pathosystems showed the existence of several clades, even within the pool of strains stored in mycological collections [11,12,13,14]. Evidence of a higher complexity emerged gradually, to such an extent that more than 30 additional species have been described to date, with some of them, such as L. endophytica, L. gonubiensis, L. pseudotheobromae, L. thailandica and L. venezuelensis, reported as endophytes [15,16,17,18,19,20,21,22,23]. Hence, it is likely that several previous findings might be incorrectly classified and that some more recent records are going to be re-examined. The application of high-throughput DNA metabarcoding as a biomonitoring tool is expected to provide a notable contribution in investigations concerning the endophytic occurrence of Lasiodiplodia [24].
To further complicate the issue, the existence of hybrid strains has been ascertained [15,25], which is also considered to have affected species identification. As an example, the taxon L. viticola Úrbez-Torres, Peduto & Gubler [26] has been shown to be a hybrid between L. theobromae and L. mediterranea; both these taxa are known on grapevine (Vitis vinifera), which most likely represented the venue of the hybridization process [15]. An assumption in biology considers as a species an organism whose population is reproductively isolated from other phylogenetically related populations [27]; hence, the existence of hybrids between several Lasiodiplodia spp. may imply that the taxa described so far are not stable. Indeed, further reassessments are to be expected, particularly in consequence of new combinations possibly stimulated by the circulation of plant material hosting genotypes which are potentially capable of hybridizing with autochthonous strains. In order to avoid further misidentifications, the use of multiple genes is recommended when considering the phylogenetic relationships of novel strains, along with direct referencing to the type strains [15,20].
Apart from the variation characterizing the genus Lasiodiplodia, phylogenetic relationships have also been evaluated in the species under discussion. Low genotypic diversity was observed in a study considering three populations from different tree species in Venezuela, South Africa and Mexico. A few predominant genotypes were encountered in the first two countries, without evidence of host specificity and in the presence of a very high gene flow between populations from different hosts. The geographic isolation was substantiated by the finding of unique alleles fixed in the different populations. Moreover, the existence of some genotypes that were widely distributed throughout the three countries, coupled with the evidence that pseudothecia are rarely produced in nature, suggests that reproduction is predominantly clonal [8]. A similar conclusion was reached in another phylogeographic study carried out on coconut palm (Cocos nucifera) in Brazil, where higher genotypic variation was observed in the northeast in connection with the local higher host diversity and a conjectured repeated introduction from Central Africa, regarded as the possible center of radiation of the species. Differences between genotypes were mainly ascribed to mutations [28].
In Cameroon, cocoa (Theobroma cacao) and Terminalia spp. are frequently grown together in a peculiar agri-sylvicultural system. A comparison between strains from these two known hosts of L. theobromae showed high levels of gene diversity and low genotypic differentiation, in the presence of high gene flow between isolates. The absence of a geographic substructure in these populations across the region where the study was carried out is indicative of the symmetrical movement of the fungus between these hosts. Unlike the case documented on grapevine, no evidence of hybridization was found with the closely related L. pseudotheobromae, which also occurs on these plants [29].
Finally, quite a simple genetic structure was once more pointed out in a broader study including strains of more varied origin. In fact, one or two main haplotypes across all genes were identified, and these genotypes were unrelated to both the hosts and the geographic area. Such overall uniformity clearly indicates that large-scale dispersal of L. theobromae is essentially derived from commerce and human activities [4].

3. Endophytic Occurrence of Lasiodiplodia theobromae

After having basically been studied as a plant pathogen responsible for serious damages of crops, particularly in tropical and subtropical regions [5,6], in the last three decades, the literature regarding L. theobromae has been substantially enriched by many reports concerning its endophytic occurrence on plant species which are quite heterogeneous in botanical terms (Table 1).
The total number of 203 findings summarized in Table 1 is indicative of the widespread adaptation of L. theobromae to an endophytic lifestyle. They refer to as many as 189 plant species from 60 families, including representatives of the Pinophyta (seven species) along with the more numerous angiosperms. Among the latter, there are just Annona muricata and two Piper species in the Magnoliids, while Monocots and Eudicots are more common—particularly the families Orchidaceae (21 species) within the former, and Fabaceae (22 species), Combretaceae (12 species), Myrtaceae and Malvaceae (9 species each) within the latter grouping. Most of these plants are trees, which likely depends on both a preference of the fungus for lignified tissues and on the higher number of investigations on endophytes which have been carried out in forests and on woody hosts.
In geographical terms, a greater diffusion of L. theobromae is evident in tropical and subtropical countries (Figure 1), which is related to both the known prevalence of the fungus in this climatic zone and to the more consistent investigational activity in these countries, particularly India and Brazil, with, respectively, 81 and 32 records (ca. 40 and 16% of the total). Some reports are inaccurate and do not allow us to match the endophytic finding of L. theobromae with a definite host [127,128].

4. Biological and Ecological Traits

As introduced above, endophytes are basically defined by their ability to spread in host tissues without inducing disease symptoms. However, the contraposition with pathogens is not so obvious, considering that many pathogens have a latent stage in their life cycle during which they are characteristically asymptomatic. The duration of this stage is very variable, and the pathogenic shift often depends on changes in the host susceptibility induced by several kinds of stress, which may reduce their tolerance or trigger a more aggressive behavior by the latent pathogen. For instance, plant stress is presented as a fundamental factor stimulating the pathogenic behavior of L. theobromae on dogwoods (Cornus florida), also considering the occasional failure of artificial inoculations during pathogenicity trials [129]. Genetic factors also actively influence the lifestyle shift of plant-associated fungi, as documented in a dedicated study disclosing repeated conversions during the evolutionary history of several species [130].
Members of the Botryosphaeriaceae are renowned as latent pathogens with a wide host range and geographical distribution [50,131]. Confirming this general feature, L. theobromae exerts such an ecological adaptability, particularly in tropical and subtropical regions [4,5]. However, the recent increasing trend in temperature may result in a major range expansion, placing more known and unknown hosts at risk.
Until recently, the incidence of latent pathogens has been underestimated, particularly in the trade of forest and horticulture plants and products; indeed, endophytes have been long disregarded in quarantine measures [131], which has enabled fungi to spread in plant germplasm circulating around the world [2,132]. With specific reference to L. theobromae, it has been conjectured that this fungus might have spread from Mexico to other subtropical countries through the trade of pine seeds [8]. Another hypothesis based on a phylogeographic approach considers the possible spread to South America from Africa to have repeatedly occurred as a consequence of human activities [28]. The availability of molecular techniques for the routine screening of plant material has increased the awareness that this risk has to be monitored [133]. In fact, besides considering pathogenic fungi of crops with an undefined latent stage [134,135], the European Food Safety Agency (EFSA) has recently started to consider the potential presence of disease agents occurring as endophytes in traded ornamental plants [136]. This concern is further supported by data gathered in this review, also considering that several hosts belong to widespread tree genera in boreal forests (e.g., Pinus, Populus, Quercus, Taxus and Zelkova). On the other hand, the accumulation of data on the occurrence of endophytes also provides an indication that some plants could be exempt. As an example, a recent review on the endophytic fungi of olive tree (Olea europaea), gathering all the available data concerning this important crop, has disclosed that, to date, there are no citations concerning L. theobromae, not only in the Mediterranean area but also in several tropical and subtropical countries where the plant has been introduced [3].
Many fungi reported for their endophytic occurrence are better known as plant pathogens. This is to be interpreted not only considering a more or less enduring latent stage within the disease cycle, as introduced above, but also with reference to a variable capacity by plant species to host certain fungal pathogens without showing symptoms of infection. Besides the more established concepts considering an improvement of host fitness in terms of growth promotion and protection against pests and pathogens, in the case of renowned disease agents, it has been conjectured that the capacity of a plant to host and promote their horizontal spread in the biocoenosis reflects a competitive advantage against other susceptible species [137]. This concept is quite appropriate for L. theobromae, which has such a high number of hosts as both a pathogen and an endophyte.
The problematic discernment of the real relationships with the host plant particularly emerged in our overview of the endophytic occurrence of L. theobromae. Indeed, defining this fungus as an endophyte in crops where it is known to cause disease (at least 46 plant species listed in Table 1, underlined) arouses a certain perplexity and raises the question of how to consider observations in the wild. The subject of plant pathology basically consists of diseases affecting crops or forest plants, and thorough assessments concerning fungal diseases of non-crop species are infrequent. In the absence of previous records and symptom descriptions, how can we be sure that a fungus isolated from “asymptomatic” tissues of a plant growing in whatever natural context is not exerting pathogenicity? It is worth observing that most of the plant species listed in Table 1 are not crops, and that for the majority of them, there is just a single finding, which is not at all sufficient for making a decision in this respect. Moreover, rather than being focused on the moment and circumstances of isolation, the issue should be considered with reference to the entire life cycle of the host plant: in this respect, how to consider reports of endophytic occurrence in centuries-old trees such as baobabs? [15,50].
Besides baobabs, there are more plants where it has been clearly demonstrated that the presumed endophytic occurrence is rather considered to refer to isolations carried out during the latent stage of the disease cycle. This is the case of cashew (Anacardium occidentale), where L. theobromae was recovered from healthy tissues at a distance of up to 80 cm from cankers caused by the same, and it was found to transmit through apparently healthy propagation material [92]. In other cases, the issue may be considered to have a “topographical” connotation, basically when the fungus exerts its pathogenic aptitude in some plant parts only. In fact, endophytic asymptomatic colonization of mango (Mangifera indica) shoots and branches has been shown to be prodromal to postharvest fruit rot [93,138]. In the case of Aquilaria spp. used for the production of agarwood, designating L. theobromae as an endophyte seems inappropriate too; in fact, resin formation is promoted as a reaction to an infection process which rather qualifies the fungus as a pathogen [139]. Likewise, internal infections by L. theobromae are reported to cause blue stain of wood after felling in Pinus elliottii [8], as well as in Terminalia spp. [87] and rubberwood (Hevea brasiliensis) [140]. It is worth considering that in similar cases observed on neem (Azadirachta indica) [141] and Ficus insipida [142], the occurrence of the fungus is merely referred to as a pathogenic association.

5. Bioactivities of Endophytic Isolates of Lasiodiplodia theobromae

Endophytes present potential for the exploitation of metabolites and enzymes. The biosynthesis of many secondary metabolites is often a response to environmental factors and fulfils different functions, such as defense, signaling and nutrient acquisition. Moreover, endophytes can influence the metabolism of the host and modify secondary metabolites by enzymatic steps of biochemical transformation [143].
Many studies have shown that endophytic fungi can synthesize bioactive products identical or similar to those produced by plants, representing an alternative source of some drugs and new useful medicinal compounds [144,145]. For this reason, many researchers have focused their attention on endophytes of medicinal plants, and many strains have been isolated which could be used for producing plant-derived drugs through fermentation. Among these fungi, L. theobromae particularly stands out for its ability to synthesize a high number of bioactive compounds [146]. The current panel of products is expected to further increase with reference to the many studies disclosing bioactive properties by endophytic strains of this species. Table 2 refers to investigations concerning endophytic strains of L. theobromae as a possible source of bioactive products, which sometimes are limited to assays carried out with culture filtrates.
Concerning the antibacterial activity, extracts produced by endophytic strains from the medicinal plant Piper hispidum were effective against four human pathogenic bacteria (i.e., Enterococcus hirae, Escherichia coli, Micrococcus luteus and Staphylococcus aureus) and showed good activity against Salmonella tiphy [33]. Antimicrobial activity was again displayed by endophytic strains from Hancornia speciosa, a plant native to Brazil, used to treat various pathologies [106].
Strains isolated from leaves, twigs and bark of Terminalia arjuna showed antimicrobial activity against Bacillus subtilis and Aspergillus niger, along with significant antioxidant properties [84]. The culture extract from an endophytic strain isolated from the mangrove Avicennia lanata in the Philippines was very active against the yeast Saccharomyces cereviseae but inactive against several Gram-negative and Gram-positive bacteria [114].
The culture extracts of endophytic strains from leaf and stem segments of Humboldtia brunonis were inhibitory against Bacillus subtilis, S. aureus, Klebsiella pneumoniae, Proteus volgaris and Candida albicans [62]. The crude extract from another endophytic strain isolated from Madhuca indica in India was found to be active against several common bacteria [102]. A strain isolated from A. sinensis showed low antimicrobial activity against microbial pathogens, particularly Aspergillus famigatus. This strain also displayed cytotoxic activity against some cancer cell lines [81]. Likewise, the culture extract of a strain from Catharanthus roseus exhibited cytotoxicity against the human cervical adenocarcinoma (HeLa) cell line [104].
The anticancer activity was particularly prominent when metal nanoparticles were prepared by exposing the endophytic fungus to metal salt solution. In fact, L. theobromae from leaves of Psidium guajava was used for the biological synthesis of silver nanoparticles, which provided powerful antitumor activity against human breast and lung cancer cells [90]. Silver nanoparticles were also prepared using an endophytic strain of L. theobromae isolated from C. roseus, inducing apoptosis in various types of cancer cells and promoting free radical scavenging [105]. These findings suggest that natural compounds produced by these isolates and incorporated into the nanoparticles have potential as a novel chemotherapeutic agent.
Finally, an endophytic strain of Boswellia ovalifoliolata is capable of growing in the presence of heavy metals (i.e., Co, Cd, Cu and Zn) in concentrations up to 600 ppm, showing that it may be used to remove heavy metals from solid substrates [96].

6. Secondary Metabolites and Enzymes of Endophytic Lasiodiplodia theobromae

As introduced above, the biological properties of culture extracts of endophytic L. theobromae might be linked to the capacity of the fungus to produce bioactive compounds (Figure 2). In fact, L. theobromae is a proficient producer of compounds belonging to different classes of secondary metabolites, such as diketopiperazines, indoles, jasmonates, melleins, lactones and phenols [146].
Biotic and abiotic stimuli influence the capacity of L. theobromae to grow and produce secondary metabolites, with implications for its physiology, lifestyle and pathogenic aptitude [146,147,148]. Studies on fungal genomes have shown that the capability of fungi to produce secondary metabolites has been underestimated, because many secondary metabolite biosynthetic gene clusters are silent under standard cultivation conditions [149,150]. In fact, different metabolomic profiles have been reported for L. theobromae strains according to variation in growth conditions, with reference to temperature [147,148], nutrient availability [151,152], presence of signal molecules [153] and incubation period [122].
Metabolomic investigations of L. theobromae have pointed out that some compounds are produced by endophytic strains only. This is the case of preussomerins and cloropreussomerins, compounds with an unusual structure isolated from the culture extract of a strain from leaves of the mangrove Acanthus ilicifolius and characterized for their cytotoxicity against five human cancer cell lines [112]. Moreover, endophytic strains from Aquilaria sinensis have been reported to produce 2-(2-phenylethyl)chromones, which are among the most abundant constituents of agarwood [154]. The coumarins meranzine and monocerin could be responsible for the antimicrobial activity of the culture extract of an endophytic strain from Dracaena draco, displaying characteristic inhibition zones against Gram-positive and Gram-negative bacteria [36].
Lasiodiplodins were frequently, although not exclusively, reported as products of endophytic strains of L. theobromae [47,69,113]. These macrolides are relevant for a variety of biological properties including cytotoxic, antimicrobial and anti-inflammatory activities [69,155]. Within this class, lasiodiplactone A was obtained from a mangrove endophytic strain showing anti-inflammatory activity [113]. Furthermore, desmethyl-lasiodiplodin was isolated, together with cladospirone B and (-)-mellein, from the crude extract of a strain from leaves of Vitex pinnata. Interestingly, cladospirone B and desmethyl-lasiodiplodin showed good activity against Trypanosoma brucei [122].
An endophytic strain from the medicinal plant Bidens pilosa yielded four depsidones, botryorhodines A-D, and the auxin 3-indolecarboxylic acid, which are not exclusively produced by endophytic strains. Botryorhodines A and B show moderate cytotoxic activity against cervical cancer cells (i.e., HeLa) and antifungal activity against pathogenic fungi, such as Aspergillus terreus and Fusarium oxysporum [126].
The fact that two of the leading natural products, namely camptothecin and taxol, in cancer chemotherapy were originally extracted from plants is quite interesting from an applicative perspective [144]. The first compound has been detected as a secondary metabolite of strains isolated from the leaves and stem of Nothapodytes nimmoniana in the Western Ghats, India [103]. One of these strains (L-6) was investigated in depth with reference to the common phenomenon of attenuation of bioactive metabolite production in axenic cultures. It was found that its re-inoculation in the host promoted higher production of camptothecin, indicating that the fungus receives eliciting signals from the host tissues, or some factors which prevent silencing of the genes responsible for biosynthesis [156].
Taxol, the first billion-dollar natural antitumor product [157], has been reported as a secondary metabolite of several endophytic strains of L. theobromae, from Taxus baccata, Morinda citrifolia, Salacia oblonga and Piper nigrum [32,35,57,110]. Investigational activity carried out on the product extracted from these strains pointed out its ability to counteract the carcinogenic effects of dimethylbenzanthracene [158]. Moreover, valuable studies have disclosed the capacity by non-Taxus endophytic strains to produce the compound through a similar biosynthetic pathway as the one reported from the plant. In fact, the gene encoding 10-deacetylbaccatin-III-O-acetyltransferase, as well as the open reading frame of WRKY1 transcription factor, were cloned and sequenced and found to share high similarity with deposited sequences from Taxus chinensis, T. cuspidata and T. celebica [35].
Of great interest in endophytic L. theobromae is the production of phytohormones, such as indole derivatives and jasmonic acid analogues [146]. It is known that 3-indoleacetic acid and 3-indolecarboxylic acid are the most studied auxins regulating plant growth and development. These compounds have been frequently reported as fungal metabolites [144] and have also been documented as being produced by L. theobromae strains. The biological role of 3-indolecarboxylic acid has not been fully investigated, but some studies address its biosynthesis [159,160,161] and toxicity [147]. Several L. theobromae strains with different lifestyles are in vitro producers of jasmonic acid and analogues. Jasmonic acid is one of the most important signal molecules involved in several plant processes including seed germination, senescence and blooming. Hence, investigations of the bioactive properties of jasmonic acid and related compounds are essentially focused on their role in the interaction between host and pathogen.
The great ability of adaptation to different environments, the capacity to colonize a high number of hosts and the expression of high amounts of extracellular enzymes make L. theobromae a producer of relevant enzymes (Table 2) to be considered for biotechnological applications [162]. The most recognized extracellular enzymes used to penetrate the plant host include cellulases, proteases and lipases. Endophytic strains colonizing C. nucifera, Pongamia pinnata and A. indica exhibited great lipase activity [43]. Moreover, endophytic strains from Terminalia catappa and T. mantaly were found to produce amylases and cellulases [86]. Finally, L. theobromae isolated from Psychotria flavida turned out to be able to degrade irradiated polypropylene thanks to the production of laccases [62].

7. Conclusions

This overview of the endophytism of L. theobromae based on the literature published in the last three decades has pointed out its widespread occurrence in tropical and subtropical areas and the likeliness of further spread to regions with a temperate climate following the increasing trade of plant material. Hints concerning the biochemical properties are indicative of a certain degree of adaptation to the endophytic lifestyle, particularly deriving from the ability to synthesize bioactive products which may contribute to protection against biological adversities and improve plant fitness. However, the analysis of the available information also raises questions on whether the ability of L. theobromae to colonize such a high number of hosts is rather to be referred to as a fundamental pathogenic aptitude and whether a number of reports are actually referable to its interception during the latency phase of the disease cycle. Finding reasonable answers is clearly dependent on the analysis of additional data resulting from dedicated investigations in both natural and agricultural contexts.

Author Contributions

Conceptualization, R.N. and A.A.; writing—original draft preparation, M.M.S.; writing—review and editing, M.M.S., R.N. and A.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Stone, J.K.; Bacon, C.W.; White, J.F. An overview of endophytic microbes: Endophytism defined. Microb. Endophytes 2000, 3, 29–33. [Google Scholar]
  2. Nicoletti, R. Endophytic Fungi of Citrus Plants. Agriculture 2019, 9, 247. [Google Scholar] [CrossRef] [Green Version]
  3. Nicoletti, R.; Di Vaio, C.; Cirillo, C. Endophytic fungi of olive tree. Microorganisms 2020, 8, 1321. [Google Scholar] [CrossRef]
  4. Mehl, J.; Wingfield, M.J.; Roux, J.; Slippers, B. Invasive everywhere? Phylogeographic analysis of the globally distributed tree pathogen Lasiodiplodia theobromae. Forests 2017, 8, 145. [Google Scholar] [CrossRef] [Green Version]
  5. Punithalingam, E. Plant Diseases Attributed to Botryodiplodia theobromae Pat; J. Cramer: Vaduz, Lichtenstein, 1980; ISBN 9783768212564. [Google Scholar]
  6. Cilliers, A.J.; Swart, W.J.; Wingfield, M.J. A review of Lasiodiplodia theobromae with particular reference to its occurrence on coniferous seeds. S. Afr. For. J. 1993, 166, 47–52. [Google Scholar]
  7. 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, Ö.; Aime, C.; et al. The Amsterdam declaration on fungal nomenclature. IMA Fungus 2011, 2, 105–111. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. 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]
  9. Larignon, P.; Fulchic, R.; Cere, L.; Dubos, B. Observation on black dead arm in French vineyards. Phytopathol. Mediterr. 2001, 40, 336–342. [Google Scholar]
  10. Slippers, B.; Boissin, E.; Phillips, A.J.L.; Groenewald, J.Z.; Lombard, L.; Wingfield, M.J.; Postma, A.; Burgess, T.; Crous, P.W. Phylogenetic lineages in the botryosphaeriales: A systematic and evolutionary framework. Stud. Mycol. 2013, 76, 32–49. [Google Scholar] [CrossRef] [Green Version]
  11. Pavlic, D.; Slippers, B.; Coutinho, T.A.; Gryzenhout, M.; Wingfield, M.J. Lasiodiplodia gonubiensis sp. nov., a new Botryosphaeria anamorph from native Syzygium cordatum in South Africa. Stud. Mycol. 2004, 50, 313–322. [Google Scholar]
  12. Burgess, T.I.; Barber, P.A.; Mohali, S.; Pegg, G.; De Beer, W.; Wingfield, M.J. Three new Lasiodiplodia spp. from the tropics, recognized based on DNA sequence comparisons and morphology. Mycologia 2006, 98, 423–435. [Google Scholar] [CrossRef] [PubMed]
  13. Damm, U.; Crous, P.W.; Fourie, P.H. Botryosphaeriaceae as potential pathogens of Prunus species in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora sp. nov. Mycologia 2007, 99, 664–680. [Google Scholar] [CrossRef] [PubMed]
  14. Alves, A.; Crous, P.W.; Correia, A.; Phillips, A.J.L. Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers. 2008, 28, 1–13. [Google Scholar]
  15. Cruywagen, E.M.; Slippers, B.; Roux, J.; Wingfield, M.J. Phylogenetic species recognition and hybridisation in Lasiodiplodia: A case study on species from baobabs. Fungal Biol. 2017, 121, 420–436. [Google Scholar] [CrossRef] [Green Version]
  16. Coutinho, I.B.L.; Freire, F.C.O.; Lima, C.S.; Lima, J.S.; Gonçalves, F.J.T.; Machado, A.R.; Silva, A.M.S.; Cardoso, J.E. Diversity of genus Lasiodiplodia associated with perennial tropical fruit plants in northeastern Brazil. Plant Pathol. 2017, 66, 90–104. [Google Scholar] [CrossRef]
  17. Netto, M.S.B.; Lima, W.G.; Correia, K.C.; da Silva, C.F.B.; Thon, M.; Martins, R.B.; Miller, R.N.G.; Michereff, S.J.; Câmara, M.P.S. Analysis of phylogeny, distribution, and pathogenicity of Botryosphaeriaceae species associated with gummosis of Anacardium in Brazil, with a new species of Lasiodiplodia. Fungal Biol. 2017, 121, 437–451. [Google Scholar] [CrossRef] [Green Version]
  18. Jiang, N.; Wang, X.W.; Liang, Y.M.; Tian, C.M. Lasiodiplodia cinnamomi sp. nov. from Cinnamomum camphora in China. Mycotaxon 2018, 133, 249–259. [Google Scholar] [CrossRef]
  19. Budiono, B.; Elfita, E.; Muharni, M.; Yohandini, H.; Widjajanti, H. Antioxidant activity of Syzygium samarangense L. and their endophytic fungi. Molekul 2019, 14, 48–55. [Google Scholar] [CrossRef]
  20. de Silva, N.I.; Phillips, A.J.L.; Liu, J.K.; Lumyong, S.; Hyde, K.D. Phylogeny and morphology of Lasiodiplodia species associated with Magnolia forest plants. Sci. Rep. 2019, 9, 14355. [Google Scholar] [CrossRef]
  21. Wang, Y.; Lin, S.; Zhao, L.; Sun, X.; He, W.; Zhang, Y.; Dai, Y.C. Lasiodiplodia spp. associated with Aquilaria crassna in Laos. Mycol. Prog. 2019, 18, 683–701. [Google Scholar] [CrossRef]
  22. Zhao, L.; Wang, Y.; He, W.; Zhang, Y. Stem blight of blueberry caused by Lasiodiplodia vaccinii sp. nov. in China. Plant Dis. 2019, 103, 2041–2050. [Google Scholar] [CrossRef] [PubMed]
  23. Berraf-Tebbal, A.; Mahamedi, A.E.; Aigoun-Mouhous, W.; Špetík, M.; Čechová, J.; Pokluda, R.; Baránek, M.; Eichmeier, A.; Alves, A. Lasiodiplodia mitidjana sp. nov. and other Botryosphaeriaceae species causing branch canker and dieback of Citrus sinensis in Algeria. PLoS ONE 2020, 15, e0232448. [Google Scholar] [CrossRef] [PubMed]
  24. Laurent, B.; Marchand, M.; Chancerel, E.; Saint-Jean, G.; Capdevielle, X.; Poeydebat, C.; Bellée, A.; Comont, G.; Villate, L.; Desprez-Loustau, M.-L. A richer community of Botryosphaeriaceae within a less diverse community of fungal endophytes in grapevines than in adjacent forest trees revealed by a mixed metabarcoding strategy. Phytobiomes J. 2020, 4, 252–267. [Google Scholar] [CrossRef]
  25. Rodríguez-Gálvez, E.; Guerrero, P.; Barradas, C.; Crous, P.W.; Alves, A. Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol. 2017, 121, 452–465. [Google Scholar] [CrossRef]
  26. Úrbez-Torres, J.R. The status of Botryosphaeriaceae species infecting grapevines. Phytopathol. Mediterr. 2011, 50, S5–S45. [Google Scholar]
  27. Taylor, J.W.; Jacobson, D.J.; Kroken, S.; Kasuga, T.; Geiser, D.M.; Hibbett, D.S.; Fisher, M.C. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 2000, 31, 21–32. [Google Scholar] [CrossRef] [Green Version]
  28. Santos, P.H.D.; Carvalho, B.M.; Aguiar, K.P.; Aredes, F.A.S.; Poltronieri, T.P.S.; Vivas, J.M.S.; Mussi Dias, V.; Bezerra, G.A.; Pinho, D.B.; Pereira, M.G.; et al. Phylogeography and population structure analysis reveals diversity by mutations in Lasiodiplodia theobromae with distinct sources of selection. Genet. Mol. Res. 2017, 16. [Google Scholar] [CrossRef]
  29. Boyogueno, A.D.B.; Slippers, B.; Perez, G.; Wingfield, M.J.; Roux, J. High gene flow and outcrossing within populations of two cryptic fungal pathogens on a native and non-native host in Cameroon. Fungal Biol. 2012, 116, 343–353. [Google Scholar] [CrossRef]
  30. Wang, Y.; Guo, L.D.; Hyde, K.D. Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fungal Divers. 2005, 20, 235–260. [Google Scholar]
  31. Ma, Y.M.; Ma, C.C.; Li, T.; Wang, J. A new furan derivative from an endophytic Aspergillus flavus of Cephalotaxus fortunei. Nat. Prod. Res. 2016, 30, 79–84. [Google Scholar] [CrossRef]
  32. Venkatachalam, R.; Subban, K.; Paul, M.J. Taxol from Botryodiplodia theobromae (BT 115)—An endophytic fungus of Taxus baccata. In Proceedings of the 13th International Biotechnology Symposium and Exhibition, Dalian, China, 12–17 October 2008; pp. 189–190. [Google Scholar]
  33. Orlandelli, R.C.; Alberto, R.N.; Almeida, T.T.; Azevedo, J.L.; Pamphile, J.A. In vitro antibacterial activity of crude extracts produced by endophytic fungi isolated from Piper hispidum sw. J. Appl. Pharm. Sci. 2012, 2, 137–141. [Google Scholar] [CrossRef]
  34. Orlandelli, R.C.; Alberto, R.N.; Rubin Filho, C.J.; Pamphile, J.A. Diversity of endophytic fungal community associated with Piper hispidum (Piperaceae) leaves. Genet. Mol. Res. 2012, 11, 1575–1585. [Google Scholar] [CrossRef] [PubMed]
  35. Sah, B.; Subban, K.; Chelliah, J. Cloning and sequence analysis of 10-deacetylbaccatin III-10-O-acetyl transferase gene and WRKY1 transcription factor from taxol-producing endophytic fungus Lasiodiplodia theobromea. FEMS Microbiol. Lett. 2017, 364, fnx253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. 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]
  37. Richardson, K.A.; Currah, R.S. The fungal community associated with the roots of some rainforest epiphytes of Costa Rica. Selbyana 1995, 16, 49–73. [Google Scholar]
  38. Duarte dos Santos, C.; Rocha Sousa, E.M.; Leal Candeias, E.; Santos Vitória, N.; Bezerra, J.L.; Newman, M.; Luz, E.D. Lasiodiplodia theobromae as an endophyte on Orchidaceae in Bahia. Agrotrópica 2012, 24, 179–182. [Google Scholar] [CrossRef]
  39. Govinda Rajulu, M. Endophytic fungi of orchids of Arunachal Pradesh, North Eastern India. Curr. Res. Environ. Appl. Mycol. 2016, 6, 293–299. [Google Scholar] [CrossRef]
  40. Sawmya, K.; Vasudevan, T.G.; Murali, T.S. Fungal endophytes from two orchid species—Pointer towards organ specificity. Czech Mycol. 2013, 65, 89–101. [Google Scholar] [CrossRef]
  41. Tibpromma, S.; Hyde, K.D.; Bhat, J.D.; Mortimer, P.E.; Xu, J.; Promputtha, I.; Doilom, M.; Yang, J.-B.; Tang, A.M.C.; Karunarathna, S.C. Identification of endophytic fungi from leaves of Pandanaceae based on their morphotypes and DNA sequence data from southern Thailand. MycoKeys 2018, 33, 25–67. [Google Scholar] [CrossRef]
  42. Dissanayake, R.K.; Ratnaweera, P.B.; Williams, D.E.; Wijayarathne, C.D.; Wijesundera, R.L.C.; Andersen, R.J.; de Silva, E.D. Antimicrobial activities of mycoleptodiscin B isolated from endophytic fungus Mycoleptodiscus sp. of Calamus thwaitesii Becc. J. Appl. Pharm. Sci. 2016, 6, 1–6. [Google Scholar] [CrossRef] [Green Version]
  43. Venkatesagowda, B.; Ponugupaty, E. Diversity of plant oil seed-associated fungi isolated from seven oil-bearing seeds and their potential for the production of lipolytic enzymes. World J. Microbiol. Biotechnol. 2012, 28, 71–80. [Google Scholar] [CrossRef] [PubMed]
  44. Matsumoto, M.; Nago, H. (R)-2-octeno-δ-lactone and other volatiles produced by Lasiodiplodia theobromae. Biosci. Biotechnol. Biochem. 1994, 58, 1262–1266. [Google Scholar] [CrossRef]
  45. Rodrigues, K.F. The foliar fungal endophytes of the Amazonian palm Euterpe oleracea. Mycologia 1994, 86, 376–385. [Google Scholar] [CrossRef]
  46. Aun, E.S.S.; Hui, J.Y.S.; Ming, J.W.W.; Yi, J.C.C.; Wong, C.; Mujahid, A.; Müller, M. Screening of endophytic fungi for biofuel feedstock production using palm oil mill effluent as a carbon source. Malays. J. Microbiol. 2017, 13, 203–209. [Google Scholar]
  47. Sultan, S.; Sun, L.; Blunt, J.W.; Cole, A.L.J.; Munro, M.H.G.; Ramasamy, K.; Weber, J.-F.F. Evolving trends in the dereplication of natural product extracts. 3: Further lasiodiplodins from Lasiodiplodia theobromae, an endophyte from Mapania kurzii. Tetrahedron Lett. 2014, 55, 453–455. [Google Scholar] [CrossRef]
  48. Amirita, A.; Sindhu, P.; Swetha, J.; Vasanthi, N.S.; Kannan, K.P. Enumeration of endophytic fungi from medicinal plants and screeening of extracellular enzymes. World J. Sci. Technol. 2012, 2, 13–19. [Google Scholar]
  49. Zakaria, L.; Nuraini, W.; Aziz, W.; Pisang, D. Molecular identification of endophytic fungi from banana leaves (Musa spp.). Trop. Life Sci. Res. 2018, 29, 201–211. [Google Scholar] [CrossRef]
  50. Sakalidis, M.L.; Hardy, G.E.S.J.; Burgess, T.I. Endophytes as potential pathogens of the baobab species Adansonia gregorii: A focus on the Botryosphaeriaceae. Fungal Ecol. 2011, 4, 1–14. [Google Scholar] [CrossRef] [Green Version]
  51. Mishra, A.; Gond, S.K.; Kumar, A.; Sharma, V.K.; Verma, S.K.; Kharwar, R.N.; Sieber, T.N. Season and tissue type affect fungal endophyte communities of the indian medicinal plant Tinospora cordifolia more strongly than geographic location. Microb. Ecol. 2012, 64, 388–398. [Google Scholar] [CrossRef]
  52. Jin, B.; Jiang, F.; Xu, F.; Ding, Z. An antitumor activity endophytic fungus A33 isolated from Viscum Coloratum of Chinese. In Proceedings of the 2011 International Conference on Remote Sensing, Environment and Transportation Engineering, RSETE 2011, Nanjing, China, 24–26 June 2011; pp. 7368–7371. [Google Scholar]
  53. Duan, X.; Xu, F.; Qin, D.; Gao, T.; Shen, W.; Zuo, S.; Yu, B.; Xu, J.; Peng, Y.; Dong, J. Diversity and bioactivities of fungal endophytes from Distylium chinense, a rare waterlogging tolerant plant endemic to the Three Gorges Reservoir. BMC Microbiol. 2019, 19, 278. [Google Scholar] [CrossRef] [Green Version]
  54. Dissanayake, A.J.; Purahong, W.; Wubet, T.; Hyde, K.D.; Zhang, W.; Xu, H.; Zhang, G.; Fu, C.; Liu, M.; Xing, Q.; et al. Direct comparison of culture-dependent and culture-independent molecular approaches reveal the diversity of fungal endophytic communities in stems of grapevine (Vitis vinifera). Fungal Divers. 2018, 90, 85–107. [Google Scholar] [CrossRef]
  55. Burruano, S.; Alfonzo, A.; Conigliaro, G.; Mondello, V.; Torta, L. First observations on the interaction between Lasiodiplodia theobromae and Epicoccum purpurascens, both endophytes in grapevine buds. In Proceedings of the XV Convegno Nazionale della Società Italiana di Patologia Vegetale (SIPaV), Locorotondo, Italy, 28 September–1 October 2009. [Google Scholar]
  56. Suryanarayanan, T.S.; Murali, T.S.; Venkatesan, G. Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can. J. Bot. 2002, 80, 818–826. [Google Scholar] [CrossRef]
  57. Roopa, G.; Madhusudhan, M.C.; Sunil, K.C.R.; Lisa, N.; Calvin, R.; Poornima, R.; Zeinab, N.; Kini, K.R.; Prakash, H.S.; Geetha, N. Identification of taxol-producing endophytic fungi isolated from Salacia oblonga through genomic mining approach. J. Genet. Eng. Biotechnol. 2015, 13, 119–127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Jami, F.; Slippers, B.; Wingfield, M.J.; Loots, M.T.; Gryzenhout, M. Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecol. 2015, 15, 51–62. [Google Scholar] [CrossRef] [Green Version]
  59. Tejesvi, M.V.; Mahesh, B.; Nalini, M.S.; Prakash, H.S.; Kini, K.R.; Subbiah, V.; Shetty, H.S. Fungal endophyte assemblages from ethnopharmaceutically important medicinal trees. Can. J. Microbiol. 2006, 52, 427–435. [Google Scholar] [CrossRef]
  60. Murali, T.S.; Suryanarayanan, T.S.; Venkatesan, G. Fungal endophyte communities in two tropical forests of southern India: Diversity and host affiliation. Mycol. Prog. 2007, 6, 191–199. [Google Scholar] [CrossRef]
  61. Arora, P.; Wani, Z.A.; Ahmad, T.; Sultan, P.; Gupta, S.; Riyaz-ul-hassan, S. Community structure, spatial distribution, diversity and functional characterization of culturable endophytic fungi associated with Glycyrrhiza glabra L. Fungal Biol. 2019, 123, 373–383. [Google Scholar] [CrossRef]
  62. Sheik, S.; Chandrashekar, K.R. Fungal endophytes of an endemic plant Humboldtia brunonis wall of western Ghats (India) and their antimicrobial and DPPH radical scavenging potentiality. Orient. Pharm. Exp. Med. 2018, 18, 115–125. [Google Scholar] [CrossRef]
  63. Prazeres, I.; Diogo, J.; Bezerra, P.; De Souza, C.M.; Cavalcanti, S.; Lucia, V.; Lima, D.M. Endophytic mycobiota from leaves of Indigofera suffruticosa Miller (Fabaceae): The relationship between seasonal change in Atlantic Coastal Forest and tropical dry forest (Caatinga), Brazil. Afr. J. Microbiol. Res. 2015, 9, 1227–1235. [Google Scholar]
  64. Gonçalves, F.J.T.; Freire, F.D.C.O.; Lima, J.S.; Melo, J.G.M.; Câmara, M.P.S. Patogenicidade de espécies de Botryosphaeriaceae endofíticas de plantas da Caatinga do estado do Ceará em manga e umbu-cajá. Summa Phytopath. 2016, 42, 43–52. [Google Scholar] [CrossRef] [Green Version]
  65. López-González, R.C.; Gómez-Cornelio, S.; Susana, C.; Garrido, E.; Oropeza-Mariano, O.; Heil, M.; Partida-Martínez, L.P. The age of lima bean leaves influences the richness and diversity of the endophytic fungal community, but not the antagonistic effect of endophytes against Colletotrichum lindemuthianum. Fungal Ecol. 2017, 26, 1–10. [Google Scholar] [CrossRef]
  66. Jinu, M.V.; Gini, C.K.; Jayabaskaran, C. In vitro antioxidant activity of cholestanol glucoside from an endophytic fungus Lasiodiplodia theobromae isolated from Saraca asoca. J. Chem. Pharm. Res. 2015, 7, 952–962. [Google Scholar]
  67. Jinu, M.V.; Jayabaskaran, C. Diversity and anticancer activity of endophytic fungi associated with the medicinal plant Saraca asoca. Curr. Res. Environ. Appl. Mycol. 2015, 5, 169–179. [Google Scholar] [CrossRef]
  68. Yao, Y.Q.; Lan, F.; Ming, Y.; Ji, Q.; Wei, G.; Shao, R.; Liang, H.; Li, B. Endophytic fungi harbored in the root of Sophora tonkinensis Gapnep: Diversity and biocontrol potential against phytopathogens. Microbiol. Open 2017, 6, e00437. [Google Scholar] [CrossRef] [PubMed]
  69. Rukachaisirikul, V.; Arunpanichlert, J.; Sukpondma, Y. Metabolites from the endophytic fungi Botryosphaeria rhodina PSU-M35 and PSU-M114. Tetrahedron 2009, 65, 10590–10595. [Google Scholar] [CrossRef]
  70. Gazis, R.; Chaverri, P. Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol. 2010, 3, 240–254. [Google Scholar] [CrossRef]
  71. Samaga, P.V.; Vittal, R.R. Diversity and bioactive potential of endophytic fungi from Nothapodytes foetida, Hypericum mysorense and Hypericum japonicum collected from Western Ghats of India. Ann. Microbiol. 2015, 66, 229–244. [Google Scholar] [CrossRef]
  72. Guerrero, J.J.G.; General, M.A.; Serrano, J.E. Culturable foliar fungal endophytes of mangrove epecies in Bicol region, Philippines. Philipp. J. Sci. 2018, 147, 563–574. [Google Scholar]
  73. Zhou, J.; Li, G.; Deng, Q.; Zheng, D.; Yang, X.; Xu, J. Cytotoxic constituents from the mangrove endophytic Pestalotiopsis sp. induce G 0 /G 1 cell cycle arrest and apoptosis in human cancer cells. Nat. Prod. Res. 2018, 32, 2968–2972. [Google Scholar] [CrossRef]
  74. Li, R.; Yan, D.; Feng, X.; Sun, X. Diversity of Botryosphaeria spp., as endophytes in poplars in Beijing, based on molecular operational taxonomic units. Sci. Silvae Sin. 2014, 50, 109–115. [Google Scholar]
  75. Huang, J.H.; Xiang, M.M.; Jiang, Z.D. Endophytic fungi of bitter melon (Momordica Charantia) in Guangdong province, China. Gt. Lakes Entomol. 2012, 45, 2. [Google Scholar]
  76. Suryanarayanan, T.S.; Venkatachalam, A.; Rajulu, M.G. A comparison of endophyte assemblages in transgenic and non-transgenic cotton plant tissues. Curr. Sci. 2011, 101, 1472–1474. [Google Scholar]
  77. Rubini, M.R.; Silva-ribeiro, R.T.; Pomella, A.W.V.; Maki, C.S. Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int. J. Mol. Sci. 2005, 1, 24–33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Chaithra, M.; Vanitha, S.; Ramanathan, A.; Jegadeeshwari, V.; Rajesh, V. Morphological and molecular characterization of endophytic fungi associated with Cocoa (Theobroma cacao L.) in India. Curr. Appl. Sci. Technol. 2020, 38, 1–8. [Google Scholar] [CrossRef] [Green Version]
  79. Evans, H.C.; Holmes, K.A.; Thomas, S.E. Endophytes and mycoparasites associated with an indigenous forest tree. Mycol. Prog. 2003, 2, 149–160. [Google Scholar] [CrossRef]
  80. Chhipa, H.; Kaushik, N. Fungal and bacterial diversity isolated from Aquilaria malaccensis tree and soil, induces agarospirol formation within 3 months after artificial infection. Front. Microbiol. 2017, 8, 1286. [Google Scholar] [CrossRef]
  81. Cui, J.; Guo, S.; Xiao, P. Antitumor and antimicrobial activities of endophytic fungi from medicinal parts of Aquilaria sinensis. J. Zhejiang Univ. Sci. B 2011, 12, 385–392. [Google Scholar] [CrossRef] [Green Version]
  82. Wang, L.; Zhang, W.M.; Pan, Q.L.; Li, H.H.; Tao, M.H.; Gao, X.X. Isolation and molecular identifcation of endophytic fungi from Aquilaria sinensis. J. Fungal Res. 2009, 7, 37–42. [Google Scholar]
  83. Tejesvi, M.V.; Mahesh, B.; Nalini, M.S.; Prakash, H.S.; Kini, K.R.; Subbiah, V.; Shetty, H.S. Endophytic fungal assemblages from inner bark and twig of Terminalia arjuna W. & A. (Combretaceae). World J. Microbiol. Biotechnol. 2005, 21, 1535–1540. [Google Scholar]
  84. Patil, M.P.; Patil, R.H.; Patil, S.G.; Maheshwari, V.L. Endophytic mycoflora of indian medicinal plant, Terminalia arjuna and their biological activities. Int. J. Biotechnol. Wellness Ind. 2014, 3, 53–61. [Google Scholar]
  85. Begoude, B.A.D.; Slippers, B. Botryosphaeriaceae associated with Terminalia catappa in Cameroon, South Africa and Madagascar. Mycol. Prog. 2010, 9, 101–123. [Google Scholar] [CrossRef] [Green Version]
  86. Toghueo, R.M.K.; Zabalgogeazcoa, I.; De Aldana, B.R.V.; Boyom, F.F. Enzymatic activity of endophytic fungi from the medicinal plants Terminalia catappa, Terminalia mantaly and Cananga odorata. S. Afr. J. Bot. 2017, 109, 146–153. [Google Scholar] [CrossRef]
  87. Begoude, B.A.D.; Slippers, B.; Wingfield, M.J.; Roux, J. The pathogenic potential of endophytic Botryosphaeriaceous fungi on Terminalia species in Cameroon. For. Pathol. 2011, 41, 281–292. [Google Scholar] [CrossRef] [Green Version]
  88. Suryavamshi, G.; Shivanna, M.B. Diversity and antibacterial activity of endophytic fungi in Memecylon umbellatum Burm. F.—A medicinal plant in the Western Ghats of Karnataka, India. Indian J. Ecol. 2020, 47, 171–180. [Google Scholar]
  89. Urdaneta, L.; Araujo, D.; Quirós, M.; Rodríguez, D.; Poleo, N.; Petit, Y. Endophytic mycobiota associated to guava floral buds (Psidium guajava L.) and to flat mite (Brevipalpus phoenicis)(Geijskes)(Acari: Tenuipalpidae). UDO Agríc. 2009, 9, 166–174. [Google Scholar]
  90. Janakiraman, V.; Govindarajan, K.; Magesh, C.R. Biosynthesis of silver nanoparticles from endophytic fungi, and its cytotoxic activity. Bionanoscience 2019, 9, 573–579. [Google Scholar] [CrossRef]
  91. Freire, F.C.; Bezerra, J.L. Foliar endophytic fungi of Ceará State (Brazil): A preliminary study. Summa Phytopath. 2001, 27, 304–308. [Google Scholar]
  92. Cardoso, J.E.; Bezerra, M.A.; Viana, F.M.P.; de Sousa, T.R.M.; Cysne, A.Q.; Farias, F. Endophyte occurrence of Lasiodiplodia theobromae in cashew tissues and its transmission by vegetative propagules. Summa Phytopath. 2009, 35, 262–266. [Google Scholar] [CrossRef]
  93. Johnson, G.I.; Mead, A.J.; Cooke, A.W.; Dean, J.R. Mango stem end rot pathogens—Fruit infection by endophytic colonisation of the inflorescence and pedicel. Ann. Appl. Biol. 1992, 120, 225–234. [Google Scholar] [CrossRef]
  94. Morales, R.V.; Rodríguez, G.M. Micobiota endofítica asociada al cultivo Del mango ’Haden’(Mangifera indica L.) en el oriente de Venezuela. Rev. Cientifìca UDO Agríc. 2009, 9, 393–402. [Google Scholar]
  95. González, E.; Umana, G.; Arauz, L.F. Population fluctuation of Botryodiplodia theobromae Pat. in mango. Agron. Costarric. 1999, 23, 21–29. [Google Scholar]
  96. Aishwarya, S.; Nagam, N.; Vijaya, T.; Netala, R.V. Screening and identification of heavy metal-tolerant endophytic fungi Lasiodiplodia theobromae from Boswellia ovalifoliolata an endemic plant of tirumala hills. Asian J. Pharm. Clin. Res. 2017, 10, 488–491. [Google Scholar]
  97. El-Nagerabi, S.A.F.; Elshafie, A.E.; Alkhanjari, S.S. Endophytic fungi associated with endogenous Boswellia sacra. Biodiversitas 2014, 15, 24–30. [Google Scholar] [CrossRef]
  98. Linnakoski, R.; Puhakka-tarvainen, H.; Pappinen, A. Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecol. 2012, 5, 298–308. [Google Scholar] [CrossRef]
  99. 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]
  100. Senthilkumar, N.; Mohan, V.; Murugesan, S. Studies on endophytic fungi of commercially important tropical tree species in India. Kavaka 2014, 31, 22–31. [Google Scholar]
  101. Osorio, J.A.; Crous, C.J.; de Beer, Z.W.; Wingfield, M.J.; Roux, J. Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol. 2017, 121, 361–393. [Google Scholar] [CrossRef] [Green Version]
  102. Verma, S.K.; Gond, S.K.; Mishra, A.; Sharma, V.K.; Kumar, J.; Singh, D.K.; Kumar, A.; Goutam, J.; Kharwar, R.N. Impact of environmental variables on the isolation, diversity and antibacterial activity of endophytic fungal communities from Madhuca indica Gmel. at different locations in India. Ann. Microbiol. 2014, 64, 721–734. [Google Scholar] [CrossRef]
  103. Shweta, S.; Gurumurthy, B.R.; Vasanthakumari, M.M.; Ravikanth, G.; Dayanandan, S.; Storms, R.; Shivanna, M.B.; Uma Shaanker, R. Endophyte fungal diversity in Nothapodytes nimmoniana along its distributional gradient in the Western Ghats, India: Are camptothecine (anticancer alkaloid) producing endophytes restricted to specific clades? Curr. Sci. 2015, 109, 127–138. [Google Scholar]
  104. Dhayanithy, G.; Subban, K.; Chelliah, J. Diversity and biological activities of endophytic fungi associated with Catharanthus roseus. BMC Microbiol. 2019, 19, 22. [Google Scholar] [CrossRef]
  105. Akther, T.; Mathipi, V.; Kumar, N.S.; Davoodbasha, M.; Srinivasan, H. Fungal-mediated synthesis of pharmaceutically active silver nanoparticles and anticancer property against A549 cells through apoptosis. Environ. Sci. Pollut. Res. 2019, 26, 13649–13657. [Google Scholar] [CrossRef] [PubMed]
  106. de Oliveira Chagas, M.B.; dos Santos, I.P.; da Silva, L.C.N.; dos Santos Correia, M.T.; de Araújo, J.M.; da Silva Cavalcanti, M.; de Menezes Lima, V.L. Antimicrobial activity of cultivable endophytic fungi associated with Hancornia speciosa gomes bark. Open Microbiol. J. 2017, 11, 179–188. [Google Scholar] [CrossRef]
  107. Suryanarayanan, T.S.; Thennarasan, S. Temporal variation in endophyte assemblages of Plumeria rubra leaves. Fungal Divers. 2004, 15, 197–204. [Google Scholar]
  108. Qadri, M.; Johri, S.; Shah, B.A.; Khajuria, A.; Sidiq, T.; Lattoo, S.K.; Abdin, M.Z.; Riyaz-Ul-Hassan, S. Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. SpringerPlus 2013, 2, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Santamaría, J.; Bayman, P. Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb. Ecol. 2005, 50, 1–8. [Google Scholar] [CrossRef]
  110. Pandi, M.; Kumaran, R.S.; Choi, Y.K.; Kim, H.J.; Muthumary, J. Isolation and detection of taxol, an anticancer drug produced from Lasiodiplodia theobromae, an endophytic fungus of the medicinal plant Morinda citrifolia. Afr. J. Biotechnol. 2011, 10, 1428–1435. [Google Scholar]
  111. Sheik, S.; Chandrashekar, K.R.; Swaroop, K.; Somashekarappa, H.M. Lasiodiplactone A, a novel lactone from the mangrove endophytic fungus Lasiodiplodia theobromae ZJ-HQ1. Int. Biodeterior. Biodegrad. 2015, 105, 21–29. [Google Scholar] [CrossRef]
  112. Chen, S.; Chen, D.; Cai, R.; Cui, H.; Long, Y.; Lu, Y.; Li, C.; She, Z. Cytotoxic and antibacterial preussomerins from the mangrove endophytic fungus Lasiodiplodia theobromae ZJ-HQ1. J. Nat. Prod. 2016, 79, 2397–2402. [Google Scholar] [CrossRef]
  113. Chen, S.; Liu, Z.; Liu, H.; Long, Y.; Chen, D.; Lu, Y.; She, Z. Lasiodiplactone A, a novel lactone from the mangrove endophytic fungus Lasiodiplodia. Org. Biomol. Chem. 2017, 73, 6338–6341. [Google Scholar] [CrossRef]
  114. Moron, L.S.; Lim, Y. Antimicrobial activities of crude culture extracts from mangrove fungal endophytes collected in Luzon Island, Philippines. Philipp. Sci. Lett. 2018, 11, 28–36. [Google Scholar]
  115. Mazlan, N.; Tate, R.; Clements, C.; Edrada-Ebel, R. Metabolomics studies of endophytic metabolites from Malaysian mangrove plant in the search for new potential antibiotics. Planta Med. 2013, 79, PA22. [Google Scholar] [CrossRef]
  116. Cannon, P.F.; Simmons, C.M. Diversity and host preference of leaf endophytic fungi in the Iwokrama forest reserve, Guyana diversity and host preference of leaf endophytic fungi in the. Mycologia 2017, 5514, 210–220. [Google Scholar]
  117. Maheswari, S.; Rajagopal, K. Biodiversity of endophytic fungi in Kigelia pinnata during two different seasons. Curr. Sci. 2013, 515–518. [Google Scholar]
  118. Rajendran, L.; Rajagopal, K.; Subbarayan, K. Efficiency of fungal taxol on human liver carcinoma cell lines. Am. J. Res. Commun. 2013, 1, 112–121. [Google Scholar]
  119. Singh, D.K.; Sharma, V.K.; Kumar, J.; Mishra, A.; Verma, S.K.; Sieber, T.N.; Kharwar, R.N. Diversity of endophytic mycobiota of tropical tree Tectona grandis Linn.f.: Spatiotemporal and tissue type effects. Sci. Rep. 2017, 7, 3745. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Balbool, B.A.; Ahmed, A.A.; Moubasher, M.H.; Helmy, E.A. Production of L-asparaginase (L-ASN) from endophytic Lasiodiplodia theobromae hosted Teucrium polium in Egypt. Microb. Biosyst. 2018, 3, 46–55. [Google Scholar]
  121. Sunayana, N.; Nalini, M.S.; Kumara Sampath, K.K.; Prakash, H.S. Diversity studies on the endophytic fungi of Vitex negundo L. Miycosphere 2014, 5, 578–590. [Google Scholar] [CrossRef]
  122. Kamal, N.; Viegelmann, C.V.; Clements, C.J.; Edrada-Ebel, R.A. Metabolomics-guided isolation of anti-trypanosomal metabolites from the endophytic fungus Lasiodiplodia theobromae. Planta Med. 2017, 83, 565–573. [Google Scholar] [CrossRef] [Green Version]
  123. De Errasti, A.; Carmarán, C.C.; Novas, M.V. Diversity and significance of fungal endophytes from living stems of naturalized trees from Argentina. Fungal Divers. 2010, 41, 29–40. [Google Scholar] [CrossRef]
  124. El-hawary, S.S.; Sayed, A.M.; Rateb, M.E.; Bakeer, W.; Abouzid, S.F.; Mohammed, R.; Sayed, A.M.; Rateb, M.E. Secondary metabolites from fungal endophytes of Solanum nigrum. Nat. Prod. Res. 2017, 31, 2568–2571. [Google Scholar] [CrossRef]
  125. Kannan, K.P.; Muthumary, J. Comparative analysis of endophytic mycobiota in different tissues of medicinal plants. Afr. J. Microbiol. Res. 2012, 6, 4219–4225. [Google Scholar]
  126. Abdou, R.; Scherlach, K.; Dahse, H.; Sattler, I.; Hertweck, C. Phytochemistry Botryorhodines A–D, antifungal and cytotoxic depsidones from Botryosphaeria rhodina, an endophyte of the medicinal plant Bidens pilosa. Phytochemistry 2010, 71, 110–116. [Google Scholar] [CrossRef] [PubMed]
  127. George, T.S.; Samy, K.; Guru, S.; Sankaranarayanan, N. Extraction, purification and characterization of chitosan from endophytic fungi isolated from medicinal plants. World J. Sci. Technol. 2015, 1, 43–48. [Google Scholar]
  128. Vardhana, J.; Kathiravan, G.; Dhivya, R. Biodiversity of endophytic fungi and its seasonal recurrence from some plants. Res. J. Pharm. Technol. 2017, 10, 490–496. [Google Scholar] [CrossRef]
  129. Mullen, J.M.; Gilliam, C.H.; Hagan, A.K.; Morgan-Jones, G. Canker of dogwood caused by Lasiodiplodia theobromae, a disease influenced by drought stress or cultivar selection. Plant Dis. 1991, 75, 886–889. [Google Scholar] [CrossRef]
  130. Delaye, L.; García-guzmán, G.; Heil, M. Endophytes versus biotrophic and necrotrophic pathogens—Are fungal lifestyles evolutionarily stable traits? Fungal Divers. 2013, 1, 125–135. [Google Scholar] [CrossRef]
  131. 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]
  132. Crous, P.W.; Groenewald, J.Z.; Slippers, B.; Wingfield, M.J.; Crous, P.W. Global food and fibre security threatened by current inefficiencies in fungal identification. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2016, 371, 20160024. [Google Scholar] [CrossRef] [Green Version]
  133. Martin, R.R.; Constable, F.; Tzanetakis, I.E. Quarantine regulations and the impact of modern detection methods. Annu. Rev. Phytopathol. 2016, 54, 189–208. [Google Scholar] [CrossRef] [Green Version]
  134. Baker, R.; Bragard, C.; Candresse, T.; Gilioli, G.; Grégoire, J.; Holb, I.; Rafoss, T.; Rossi, V.; Schans, J.; Schrader, G.; et al. Scientific opinion on the pest categorisation of Cryphonectria parasitica (Murrill) Barr. 1. EFSA J. 2014, 12, 3859. [Google Scholar]
  135. Jeger, M.; Bragard, C.; Caf, D.; Candresse, T.; Chatzivassiliou, E.; Dehnen-schmutz, K.; Gilioli, G.; Gregoire, J.; Anton, J.; Miret, J.; et al. Pest categorisation of Gremmeniella abietina. EFSA J. 2017, 15, 5030. [Google Scholar]
  136. EFSA Call for Proposals GP/EFSA/ALPHA/2020/01—Entrusting Support Tasks in the Area of Plant Health Commodity Risk Assessment for High Risk Plants (Plants for Planting for Ornamental Purpose). Available online: http://www.efsa.europa.eu/en/art36grants/article36/gpefsaalpha202001-entrusting-support-tasks-area-plant-health (accessed on 12 September 2020).
  137. Aschehoug, E.T.; Metlen, K.L.; Callaway, R.M.; Newcombe, G. Fungal endophytes directly increase the competitive effects of an invasive forb. Ecology 2012, 93, 3–8. [Google Scholar] [CrossRef]
  138. Lin, Y.; Wang, Y.; Yang, H.; Wang, P. Detection of quiescent infection of mango stem end rot pathogen Lasiodiplodia theobromae in shoot and pre-plucked mango fruit by seminested PCR. Plant Pathol. Bull. 2009, 18, 225–235. [Google Scholar]
  139. Chhipa, H.; Chowdhary, K.; Kaushik, N. Artificial production of agarwood oil in Aquilaria sp. by fungi: A review. Phytochem. Rev. 2017, 16, 835–860. [Google Scholar] [CrossRef]
  140. Sajitha, K.L.; Florence, E.J.M.; Arun, S. Screening of bacterial biocontrols against sapstain fungus (Lasiodiplodia theobromae Pat.) of rubberwood (Hevea brasiliensis Muell. Arg.). Res. Microbiol. 2014, 165, 541–548. [Google Scholar] [CrossRef] [PubMed]
  141. Mohali, S.; Encinas, O.; Mora, N. Manchado azul en madera de Pinus oocarpa y Azadirachta indica en Venezuela. Fitopatol. Venez. 2002, 15, 30–32. [Google Scholar]
  142. Mohali, S.R.; Castro-Medina, F.; Úrbez-Torres, J.R.; Gubler, W.D. First report of Lasiodiplodia theobromae and L. venezuelensis associated with blue stain on Ficus insipida wood from the Natural Forest of Venezuela. For. Pathol. 2017, 47, e12355. [Google Scholar] [CrossRef]
  143. Ludwig-Müller, J. Plants and endophytes: Equal partners in secondary metabolite production? Biotechnol. Lett. 2015, 37, 1325–1334. [Google Scholar] [CrossRef] [PubMed]
  144. 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]
  145. Caruso, G.; Abdelhamid, M.; Kalisz, A.; Sekara, A. Linking endophytic fungi to medicinal plants therapeutic activity. A case study on Asteraceae. Agriculture 2020, 10, 286. [Google Scholar] [CrossRef]
  146. Salvatore, M.M.; Alves, A.; Andolfi, A. Secondary metabolites of Lasiodiplodia theobromae: Distribution, chemical diversity, bioactivity, and implications of their occurrence. Toxins 2020, 12, 457. [Google Scholar] [CrossRef] [PubMed]
  147. Félix, C.; Salvatore, M.M.; Dellagreca, M.; Meneses, R.; Duarte, A.S.; Salvatore, F.; Naviglio, D.; Gallo, M.; Jorrín-Novo, J.V.; Alves, A.; et al. Production of toxic metabolites by two strains of Lasiodiplodia theobromae, isolated from a coconut tree and a human patient. Mycologia 2018, 110, 642–653. [Google Scholar] [CrossRef] [PubMed]
  148. Félix, C.; Salvatore, M.M.; DellaGreca, M.; Ferreira, V.; Duarte, A.S.; Salvatore, F.; Naviglio, D.; Gallo, M.; Alves, A.; Esteves, A.C.; et al. Secondary metabolites produced by grapevine strains of Lasiodiplodia theobromae grown at two different temperatures. Mycologia 2019, 111, 466–476. [Google Scholar] [CrossRef] [PubMed]
  149. Keller, N.P.; Turner, G.; Bennett, J.W. Fungal secondary metabolism-from biochemistry to genomics. Nat. Rev. Microbiol. 2005, 3, 937–947. [Google Scholar] [CrossRef]
  150. Salvatore, M.M.; Nicoletti, R.; DellaGreca, M.; Andolfi, A. Occurrence and properties of thiosilvatins. Mar. Drugs 2019, 17, 664. [Google Scholar] [CrossRef] [Green Version]
  151. Uranga, C.C.; Beld, J.; Mrse, A.; Córdova-Guerrero, I.; Burkart, M.D.; Hernández-Martínez, R. Fatty acid esters produced by Lasiodiplodia theobromae function as growth regulators in tobacco seedlings. Biochem. Biophys. Res. Commun. 2016, 472, 339–345. [Google Scholar] [CrossRef]
  152. Jernerén, F.; Eng, F.; Hamberg, M.; Oliw, E.H. Linolenate 9R-dioxygenase and allene oxide synthase activities of Lasiodiplodia theobromae. Lipids 2012, 47, 65–73. [Google Scholar] [CrossRef]
  153. Salvatore, M.M.; Félix, C.; Lima, F.; Ferreira, V.; Duarte, A.S.; Salvatore, F.; Alves, A.; Esteves, A.C.; Andolfi, A. Effect of γ-aminobutyric Acid (GABA) on the metabolome of two strains of Lasiodiplodia theobromae isolated from grapevine. Molecules 2020, 25, 3833. [Google Scholar] [CrossRef]
  154. Zhang, Y.; Liu, H.; Li, W.; Tao, M.; Pan, Q.; Sun, Z.; Ye, W.; Li, H.; Zhang, W. 2-(2-Phenylethyl)chromones from endophytic fungal strain Botryosphaeria rhodina A13 from Aquilaria sinensis. Chin. Herb. Med. 2017, 9, 58–62. [Google Scholar] [CrossRef]
  155. Valayil, M.J.; Kuriakose, G.C.; Jayabaskaran, C. Isolation, purification and characterization of a novel steroidal saponin cholestanol glucoside from Lasiodiplodia theobromae that induces apoptosis in A549 cells. Anticancer Agents Med. Chem. 2016, 16, 865–874. [Google Scholar] [CrossRef]
  156. Vasanthakumari, M.M.; Jadhav, S.S.; Sachin, N.; Vinod, G.; Shweta, S.; Manjunatha, B.L.; Kumara, P.M.; Ravikanth, G.; Nataraja, K.N.; Uma Shaanker, R. Restoration of camptothecine production in attenuated endophytic fungus on re-inoculation into host plant and treatment with DNA methyltransferase inhibitor. World J. Microbiol. Biotechnol. 2015, 31, 1629–1639. [Google Scholar] [CrossRef]
  157. Nicoletti, R. Antitumor and immunomodulatory compounds from fungi. In Reference Module in Life Sciences (Planned for Publication in Encyclopaedia of Mycology); Zaragoza, O., Ed.; Elsevier: Amsterdam, The Netherlands, 2020. [Google Scholar] [CrossRef]
  158. Pandi, M.; Rajapriya, P.; Suresh, G.; Ravichandran, N.; Manikandan, R.; Thiagarajan, R.; Muthumary, J. A fungal taxol from Botryodiplodia theobromae Pat., attenuates 7, 12 dimethyl benz(a)anthracene (DMBA)-induced biochemical changes during mammary gland carcinogenesis. Biomed. Prev. Nutr. 2011, 1, 95–102. [Google Scholar] [CrossRef]
  159. Magnus, V.; Šimaga, Š.; Iskrić, S.; Kveder, S. Metabolism of Tryptophan, Indole-3-acetic acid, and related compounds in parasitic plants from the genus Orobanche. Plant. Physiol. 1982, 69, 853–858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  160. Stahl, E.; Bellwon, P.; Huber, S.; Schlaeppi, K.; Bernsdorff, F.; Vallat-Michel, A.; Mauch, F.; Zeier, J. Regulatory and functional aspects of indolic metabolism in plant systemic acquired resistance. Mol. Plant. 2016, 9, 662–681. [Google Scholar] [CrossRef] [Green Version]
  161. Bartel, B. Auxin biosynthesis. Annu. Rev. Plant. Biol. 1997, 48, 51–66. [Google Scholar] [CrossRef]
  162. Félix, C.; Libório, S.; Nunes, M.; Félix, R.; Duarte, A.S.; Alves, A.; Esteves, A.C. Lasiodiplodia theobromae as a producer of biotechnologically relevant enzymes. Int. J. Mol. Sci. 2018, 19, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Agriculture 10 00488 g001 550
Figure 1. Geographical distribution of endophytic Lasiodiplodia theobromae as resulting from entries of Table 1. The color scale ranging from yellow to red is representative of the number of findings for each country.
Figure 1. Geographical distribution of endophytic Lasiodiplodia theobromae as resulting from entries of Table 1. The color scale ranging from yellow to red is representative of the number of findings for each country.
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Agriculture 10 00488 g002 550
Figure 2. Representative secondary metabolites produced by endophytic Lasiodiplodia theobromae.
Figure 2. Representative secondary metabolites produced by endophytic Lasiodiplodia theobromae.
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Table
Table 1. Plant hosts of endophytic Lasiodiplodia theobromae. Species where the fungus has been also reported as a pathogen are underlined.
Table 1. Plant hosts of endophytic Lasiodiplodia theobromae. Species where the fungus has been also reported as a pathogen are underlined.
SourceOriginRef.
Pinophyta
Pinales, PinaceaePinus elliottiiSouth Africa[8]
Pinus caribaea var. hondurensisVenezuela[8]
Pinus pseudostrobusMexico[8]
Pinus tabulaeformisChina[30]
Pinales, TaxaceaeCephalotaxus hainanensisChina[31]
Taxus baccataIndia[32]
Taxus chinensisChinaGenBank
Magnoliids
Magnoliales, AnnonaceaeAnnona muricataMalaysiaGenBank
Piperales, PiperaceaePiper hispidumBrazil[33,34]
Piper nigrumIndia[35]
Monocots
Asparagales, AsparagaceaeDracaena dracoEgypt[36]
Asparagales, OrchidaceaeCampylocentrum micranthumCosta Rica[37]
Cattleya sp.Brazil[38]
Cymbidium aloifoliumIndia[39]
Dendrobium moschatumIndia[39]
Encyclia fragransCosta Rica[37]
Epidendrum difformeCosta Rica[37]
Epidendrum octomerioidesCosta Rica[37]
Epidendrum radicansIndiaGenBank
Eria flavaIndia[39]
Nidema boothiiCosta Rica[37]
Oncidium sp.Brazil[38]
Paphiopedilum fairrieanumIndia[39]
Phalaenopsis sp.Brazil[38]
Pholidota imbricataIndia[39]
Pholidota pallidaIndia[40]
Pleurothallis guanacastensisCosta Rica[37]
Pleurothallis phyllocardioidesCosta Rica[37]
Sobralia mucronataCosta Rica[37]
Sobralia sp.Costa Rica[37]
Trichosalpinx blasdelliiCosta Rica[37]
Vanilla planifoliaIndia[39]
Pandanales, PandanaceaePandanus sp.Thailand[41]
Arecales, ArecaceaeCalamus thwaitesiiSri Lanka[42]
Cocos nuciferaBrazil[28]
India[43]
Philippines[44]
Euterpe oleraceaBrazil[45]
Nypa fruticansMalaysia[46]
Poales, CyperaceaeMapania kurziiMalaysia[47]
Poales, PoaceaeCynodon dactylonIndiaGenBank
Zingiberales, CostaceaeCostus igneusIndia[48]
Zingiberales, MusaceaeMusa spp.Malaysia[49]
Eudicots
Proteales, ProteaceaeGrevillea agrifoliaAustralia[50]
Ranunculales, MenispermaceaeTinospora cordifoliaIndia[51]
Santalales, SantalaceaeViscum coloratumChina[52]
Saxifragales, HamamelidaceaeDistilium chinenseChina[53]
Vitales, VitaceaeVitis viniferaChina[54]
Italy[55]
Celastrales, CelastraceaeElaeodendrum glaucumIndia[56]
Salacia oblongaIndia[57]
Fabales, FabaceaeAcacia karrooSouth Africa[58]
Acacia mangiumVenezuela[8]
Acacia synchroniciaAustralia[50]
Albizzia lebbeckIndiaGenbank
Arachis hypogaeaIndia[56]
Bauhinia racemosaIndia[56]
Butea monospermaIndia[59,60]
Cassia fistulaIndia[56]
Crotalaria medicagineaAustralia[50]
Dalbergia lanceolariaIndia[60]
Dalbergia latifoliaIndia[56]
Glycyrrhiza glabraIndia[61]
Humboldtia brunonisIndia[62]
Indigofera suffruticosaBrazil[63]
Libidibia (Caesalpinia) ferreaBrazil[64]
Lysiphyllum cunninghamiiAustralia[50]
Mimosa caesalpinifoliaBrazil[64]
Ougeinia oojeinensisIndia[60]
Phaseolus lunatusMexico[65]
Pongamia pinnataIndia[43]
Saraca asocaIndia[66,67]
Sophora tonkinensisChina[68]
Malpighiales, ChrysobalanaceaeLicania rigidaBrazil[64]
Malpighiales, ClusiaceaeGarcinia mangostanaThailand[69]
Malpighiales, EuphorbiaceaeCroton campestrisBrazil[64]
Croton sonderianusBrazil[64]
Givotia rottleriformisIndia[60]
Hevea brasiliensisMalaysiaGenBank
Peru[70]
Malpighiales, HypericaceaeHypericum mysorenseIndia[71]
Malpighiales, RhizophoraceaeBruguiera cylindricaPhilippines[72]
Ceriops tagalChinaGenBank
Rhizophora mucronataChina[73]
Malpighiales, SalicaceaePopulus sp.China[74]
Oxalidales, ElaeocarpaceaeElaeocarpus ganitrusIndiaGenBank
Elaeocarpus tuberculatusIndia[56]
Rosales, MoraceaeArtocarpus altilisEcuadorGenbank
Ficus oppositaAustralia[50]
Ficus racemosaIndiaGenBank
Ficus trigonaEcuadorGenBank
Rosales, RhamnaceaeZiziphus xylopyrusIndia[60]
Rosales, UlmaceaeZelkova carpinifoliaIranGenBank
Cucurbitales, CucurbitaceaeMomordica charantiaChina[75]
Fagales, FagaceaeQuercus castaneifoliaIranGenBank
Fagales, JuglandaceaePterocarya fraxinifoliaIranGenBank
Brassicales, MoringaceaeMoringa oleiferaBrazil[64]
Malvales, MalvaceaeAdansonia digitataAustralia[50]
Cameroon[15]
Adansonia gregoriiAustralia[50]
Adansonia zaAustralia[50]
Gossypium hirsutumIndia[76]
Grewia tiliaefoliaIndia[56]
Helicteres isoraIndia[60]
Kydia calycinaIndia[60]
Theobroma cacaoBrazil[77]
India[78]
Theobroma gileriEcuador[79]
Malvales, ThymelaeaceaeAquilaria malaccensisIndia[80]
Aquilaria sinensisChina[81,82]
TaiwanGenBank
Myrtales, CombretaceaeAnogeissus latifoliaIndia[60]
Combretum leprosumBrazil[64]
Lumnitzera littoreaPhilippines[72]
Terminalia arjunaIndia[83,84]
Terminalia bellericaIndia[56]
Terminalia catappaCameroon[85,86]
Terminalia crenulataIndia[60]
Terminalia ivorensisCameroon[87]
Terminalia mantalyCameroon[86,87]
Terminalia pterocaryaAustralia[50]
Terminalia superbaCameroon[87]
Terminalia tomentosaIndia[56]
Myrtales, LythraceaeLagerstroemia microcarpaIndia[60]
Lagerstroemia parvifloraIndia[60]
Myrtales, MelastomataceaeMemecylon umbellatumIndia[88]
Myrtales, MyrtaceaeCalytrix sp.Australia[50]
Corymbia sp.Australia[50]
Eucalyptus sp.Australia[50]
Eucalyptus urophyllaVenezuela[8]
Eugenia unifloraBrazil[64]
Psidium guajavaVenezuela[89]
Brazil[64]
India[90]
NigeriaGenBank
Psidium rufumBrazil[64]
Syzygium cordatumSouth Africa[11]
Syzygium cuminiIndia[60]
Sapindales, AnacardiaceaeAnacardium occidentaleBrazil[91,92]
Astronium fraxinifoliumBrazil[64]
Mangifera indicaAustralia[93]
Brazil[91]
Venezuela[94]
Costa Rica[95]
Myracrodruon urundeuvaBrazil[64]
Spondias mombinBrazil[64]
Spondias sp.Brazil[64]
Sapindales, BurseraceaeBoswellia ovalifoliataIndia[96]
Boswellia sacraOman[97]
Protium heptaphyllumBrazil[64]
Sapindales, MeliaceaeAzadirachta indicaIndia[43]
Khaya anthothecaGhana[98]
Sapindales, RutaceaeCitrus sinensisUSA[99]
Sapindales, SapindaceaeNephelium lappaceumMalaysiaGenBank
Paullinia cupanaBrazilGenBank
Sapindales, SimaroubaceaeAilanthus excelsaIndia[100]
Simarouba amaraBrazil[64]
Ericales, EbenaceaeDiospyros montanaIndia[60]
Ericales, LecythidaceaeBarringtonia racemosaSouth Africa[101]
Careya arboreaIndia[60]
Ericales, SapotaceaeMadhuca indicaIndia[102]
Icacinales, IcacinaceaeNothapodytes nimmonianaIndia[103]
Pyrenacantha sp.IndiaGenBank
Boraginales, BoraginaceaeAuxemma oncocalyxBrazil[64]
Cordia obliquaIndia[60]
Cordia trichotomaBrazil[64]
Cordia wallichiIndia[60]
Gentianales, ApocynaceaeAlstonia scholarisIndia[56]
Catharanthus roseusIndia[90,104,105]
Hancornia speciosaBrazil[106]
Holarrhena antidysentericaIndia[59]
Plumeria rubraIndia[107]
Rauwolfia serpentinaIndia[108]
Gentianales, LoganiaceaeStrychnos potatorumIndia[60]
Gentianales, RubiaceaeCoffea arabicaPuerto Rico[109]
Ixora nigricansIndia[60]
Morinda citrifoliaIndia[110]
Psychotria flavidaIndia[62,111]
Psychotria sp.Brazil[64]
Lamiales, AcanthaceaeAcanthus ilicifoliusChina[112,113]
Avicennia lanataPhilippines[114]
Malaysia[115]
Lamiales, BignoniaceaeJacaranda sp.Guyana[116]
Kigelia pinnataIndia[117]
Radermachera xylocarpaIndia[56]
Stereospermum angustifoliumIndia[60]
Lamiales, LamiaceaeGmelina arboreaIndia[60]
Plectranthus amboinicusIndia[118]
Pogostemon cablinChinaGenBank
Premna tomentosaIndia[60]
Tectona grandisIndia[60,119]
Teucrium poliumEgypt[120]
Vitex negundoIndia[121]
Vitex pinnataMalaysia[122]
Lamiales, OleaceaeLigustrum lucidumArgentina[123]
Olea dioicaIndia[56]
Solanales, SolanaceaeSolanum melongenaBrazilGenBank
Solanum nigrumEgypt[124]
Solanum surratenseIndia[125]
Solanum torvumIndia[125]
Withania somniferaIndia[125]
Apiales, AraliaceaeDendropanax laurifoliusMalaysiaGenBank
Asterales, AsteraceaeBidens pilosaEgypt[126]
Table
Table 2. Bioactivities of endophytic isolates of Lasiodiplodia theobromae.
Table 2. Bioactivities of endophytic isolates of Lasiodiplodia theobromae.
BioactivitySourceSample testedRef.
AntibacterialAcanthus ilicifoliusSecondary metabolites[112]
Aquilaria sinensisCulture filtrate extract[81]
Calamus thwaitesiiCulture filtrate extract[42]
Dracaena dracoCulture filtrate extract[36]
Garcinia mangostanaSecondary metabolites[69]
Hancornia speciosaCulture filtrate extract[106]
Humboldtia brunonisCulture filtrate extract[62]
Madhuca indicaCulture filtrate extract[102]
Piper hispidumCulture filtrate extract[33]
Terminalia arjunaCulture filtrate extract[84]
AntifungalA. sinensisCulture filtrate extract[81]
Avicennia lanataCulture filtrate extract[114]
Bidens pilosaCulture filtrate extract and secondary metabolites[126]
H. speciosaCulture filtrate extract[106]
H. brunonisCulture filtrate extract[62]
T. arjunaCulture filtrate extract[84]
Anti-inflammatoryAcanthus ilicifoliusSecondary metabolites[113]
AntioxidantCatharanthus roseusCulture filtrate and mycelial extracts[104]
C. roseusSilver nanoparticles[105]
T. arjunaCulture filtrate extract[84]
AntiprotozoalA. lanataCulture filtrate extract and chromatographic fraction[115]
Vitex pinnataSecondary metabolites[122]
CytotoxicAcanthus ilicifoliusSecondary metabolites[112]
A. sinensisCulture filtrate extract[81]
B. pilosaCulture filtrate extract and secondary metabolites[126]
C. roseusSilver nanoparticles[90]
C. roseusCulture filtrate and mycelial extracts[104]
Morinda citrifoliaSecondary metabolite[110]
Plectranthus amboinicusSecondary metabolite[118]
EnzymaticAzadirachta indicaIsolate[43]
Cocos nuciferaIsolate[43]
Pongamia pinnataIsolate[43]
Psychotria flavidaIsolate[111]
Terminalia catappaIsolate[86]
Terminalia mantalyIsolate[86]
Heavy metal toleranceBoswellia ovalifoliataIsolate[96]
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Salvatore, M.M.; Andolfi, A.; Nicoletti, R. The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae. Agriculture 2020, 10, 488. https://doi.org/10.3390/agriculture10100488

AMA Style

Salvatore MM, Andolfi A, Nicoletti R. The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae. Agriculture. 2020; 10(10):488. https://doi.org/10.3390/agriculture10100488

Chicago/Turabian Style

Salvatore, Maria Michela, Anna Andolfi, and Rosario Nicoletti. 2020. "The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae" Agriculture 10, no. 10: 488. https://doi.org/10.3390/agriculture10100488

APA Style

Salvatore, M. M., Andolfi, A., & Nicoletti, R. (2020). The Thin Line between Pathogenicity and Endophytism: The Case of Lasiodiplodia theobromae. Agriculture, 10(10), 488. https://doi.org/10.3390/agriculture10100488

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