Endophytism of Lecanicillium and Akanthomyces

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This entry is adapted from the peer-reviewed paper 10.3390/agriculture10060205

The rise of the holobiont concept confers a prominent importance to the endophytic associates of plants, particularly to species known to be able to exert a mutualistic role as defensive or growth-promoting agents. The finding that many entomopathogenic fungi are harbored within plant tissues and possess bioactive properties going beyond a merely anti-insectan effect has recently prompted a widespread investigational activity concerning their occurrence and functions in crops, in the aim of an applicative exploitation conforming to the paradigm of sustainable agriculture.

entomopathogens endophytic fungi crop protection plant growth promotion integrated pest management Cordycipitaceae plant mycobiome

1. Introduction

The great microbial diversity harbored in plants has just started being explored in light of a consolidated awareness that what we manage in the agricultural practice is actually the outcome of the combined expression of plant and microbial genes ^[1]^[2]. The symbiotic relationships between endophytic fungi and their host plants exteriorize in many ways, ranging from opportunistic saprophytism in senescent tissues, to latent pathogenicity disclosing after the impact of various stress factors, to genuine mutualistic interactions deriving from nutritional support and/or increased protection against pests and pathogens. The latter are particularly relevant for the holistic approach making its way in integrated pest management (IPM), considering the crop production system as a whole in the aim to contain rather than eradicate pests.

Within this conceptual rearrangement, the improvement of our knowledge on occurrence and functions of endophytic associates of plants is fundamental in view of their possible exploitation in sustainable agriculture. Endophytic entomopathogens are an important category of the plant microbiome, which is increasingly considered for applicative purposes. So far, the majority of investigations and reports concerning these organisms deal with Beauveria bassiana and Metarhizium anisopliae, with several fine reviews available in the literature ^[3]^[4].

2. Taxonomic Background

Until the early 2000s, these fungi were classified in the section Prostrata of the genus Verticillium, basically with reference to their imperfect stage producing verticillate conidiophores ^[5]. A few species best known for their parasitic behavior against arthropods, nematodes and/or fungi were ascribed to this section, such as V. chlamydosporium, V. lecanii and V. psalliotae. Afterwards, the application of biomolecular techniques enabled to shed light on the phylogenetic relationships within this heterogeneous genus. Particularly, species within the section Prostrata were separated in a few unrelated genera, such as Pochonia, Haptocillium, Simplicillium and Lecanicillium, and their teleomorphs identified within the genera Cordyceps and Torrubiella ^[6]. The species V. fungicola, previously ascribed to the section Albo-erecta in the genus Verticillium, was later aggregated to Lecanicillium ^[7]. As a result of this fundamental revision, about fifteen Lecanicillium species were recognized, a few of which (L. attenuatum, L. longisporum, L. muscarium, L. nodulosum and L. lecanii s.str.) enucleated from the previously collective V. lecanii.

However, as it often happens in fungal taxonomy, such a sound rearrangement was not destined to persist. In fact the genus Lecanicillium was shown to be paraphyletic ^[8], and some species were moved to Akanthomyces, a pre-existing but overlooked genus including entomogenous species ^[9] (Table 1). At the same time, investigations in more or less peculiar ecological contexts brought to the description of novel taxa of both Akanthomyces and Lecanicillium ^[10]^[11], while some species ascribed to the latter genus, such as L. uredinophilum and L. pissodis, were shown to actually fit in the A. lecanii clade ^[12]. Following the dismissal of the dual nomenclature system for pleomorphic fungi, a more comprehensive revision of the whole family of the Cordycipitaceae is in progress. Particularly, rejection has been proposed for the genus name Lecanicillium, while some Akanthomyces species have in turn been moved to another genus (Hevansia) ^[13]. Hence, further adjustments concerning species still classified in Lecanicillium are to be expected.

Table 1. Nomenclatural correspondence of accepted Lecanicillium/Akanthomyces species with sequences of internal transcribed spacers of ribosomal DNA (rDNA-ITS) available in GenBank.

Species Names *			ITS Sequence Used in
Lecanicillium	Akanthomyces	Cordyceps/Torrubiella	Phylogenetic Analysis
L. acerosum			NR11268
L. antillanum			AJ292392
L. aphanocladii			LT220701
L. aranearum	A. aranearum	T. alba	AJ292464
L. araneicola			AB378506
L. araneogenum	A. neoaraneogenus		NR161115
L. attenuatum	A. attenuatus		AJ292434
L. cauligalbarum			MH730663
L. coprophilum			MH177615
L. dimorphum			AJ292429
L. flavidum			EF641877
L. fungicola var.aleophilum			NR111064
L. fungicola var.fungicola			NR119653
L. fusisporum			AJ292428
L. kalimantanense			AB360356
L. lecanii	A. lecanii	C. confragosa	AJ292383
L. longisporum	A. dipterigenus		AJ292385
L. muscarium	A. muscarius		NR111096
L. nodulosum	Akanthomyces sp.		EF513012
L. primulinum			NR119418
L. psalliotae			AJ292389
L. restrictum			LT548279
L. sabanense	A. sabanensis		KC633232
L. subprimulinum			MG585314
L. tenuipes			AJ292391
L. testudineum			LT548278
L. uredinophilum	Akanthomyces sp.		MG948305
L. wallacei		T. wallacei	NR111267
Lecanicillium sp.		C. militaris	AF153264
	A. aculeatus		KC519371
	A. coccidioperitheciatus	C. coccidioperitheciata	JN049865
	A. kanyawimiae		MF140751
	A. sphingum	C. sphingum	AY245641
	A. sulphureus	Torrubiella sp.	MF140756
	A. thailandicus	Torrubiella sp.	MF140755
	A. tuberculatus	C. tuberculata	JN049830
	A. waltergamsii		MF140747

* The currently used species names as inferred from the Mycobank database ^[14] are reported in bold.

3. Occurrence

The number of reports concerning endophytic isolates of Lecanicillium and Akanthomyces has increased in recent years. This is due not only to the several taxonomic reassessments introducing new species, but also to the easier access to techniques and databases for DNA sequencing, which in most instances enable one to overcome the intrinsic difficulties of morphological identification. However, more prompts have probably resulted by the awareness of the basic role that endophytic fungi play on plant fitness, introducing applicative perspectives for investigations in the field. For the above genera, literature shows a prevalence of findings concerning natural phytocoenoses (Table 2) over those inherent crops (Table 3); even more so considering that the latter series includes a few cases of endophytic colonization resulting after artificial inoculation in experimental work. Basically connected with the issue of ecosystem simplification characterizing the agricultural contexts, such a difference emphasizes the opportunity to recover the functional role of this component of the plant holobiont in view of improving crop performances.

Table 2. Endophytic occurrence of Lecanicillium/Akanthomyces in wild contexts.

Species	Host Plant	Country	ITS Sequence ^√	Reference
A. attenuatus	Astrocaryum sciophilum	French Guyana	MK279520	^[15]
	Conifer plant	China	MN908945	GenBank
	Symplocarpus foetidus	Canada	KC916681	^[16]
A. lecanii	Ammophila arenaria	Spain	-	^[17]
	Dactylis glomerata	Spain	AM262369	^[18]
	Deschampsia flexuosa	Finland	KJ529005	^[19]
	Elymus farctus	Spain	AM924163	^[17]
	Laretia acaulis	Chile	-	^[20]
	Pinus sylvestris	Italy	KJ093501	^[21]
	Pinus sylvestris	Poland	-	^[22]
	Shorea thumbuggaia	India	KJ542654	GenBank
	Taxus baccata	Iran	KF573987	^[23]
A. muscarius	Acer campestre	Italy	MT230457	This paper
	Laurus nobilis	Italy	-	^[24]
	Myrtus communis	Italy	MT230435	This paper
	Nypa fruticans	Thailand	MH497223	^[25]
	Quercus robur	Italy	MT230463	This paper
Akanthomyces sp. *	Arctostaphylos uva-ursi	Switzerland	-	^[26]
	Carpinus caroliniana	USA	-	^[27]
L. aphanocladii	Ageratina adenophora	China	MK304090 MK304173 MK304418	^[28]
	Hemidesmus indicus	India	MH594215	^[29]
	Huperzia serrata	China	KP689216 KP689173	^[30]
	Picea mariana	Canada	-	^[31]
L. fungicola	Phragmites australis	Korea	KP017880	^[32]
L. kalimantanense	Zingiber officinale	Indonesia	-	^[33]
L. psalliotae	Cerastium fischerianum	Korea	JX238776	^[34]
	Coix lachryma-jobi	China	KJ572167	GenBank
	Magnolia officinalis	China		GenBank
	Phoradendron perrottettii	Brazil	-	^[35]
	Pinus radiata	New Zealand	-	^[36]
	Sedum oryzifolium	Korea	KU556134	^[37]
	Tapirira guianensis	Brazil	-	^[35]
	Triticum dicoccoides	Israel	-	^[38]
Lecanicillium sp.	Artocarpus lacucha	India	MH700423 MH700428	GenBank
	Bupleurum chinense	China	MG561939	GenBank
	Huperzia serrata	China	KM513600	^[30]
	Liparis japonica	China	KT719186 KT719187 KT719188 KT719189 KT719192	GenBank
	Micrandra spruceana	Peru	MH267985	^[39]
	Microthlaspi perfoliatum	Greece	KT269776	^[40]
	Quassia indica	India	MH910098	GenBank
	Sandwithia guyanensis	French Guyana	MN514023	^[41]
	Theobroma gileri	Ecuador	-	^[42]

^√ Missing ITS accession number implies identification based on morphological characters only, or without depositing the ITS sequence. * These strains were originally identified as Verticillium lecanii.

Table 3. Endophytic occurrence of Lecanicillium/Akanthomyces in crops.

Species	Host Plant	Country	ITS Sequence ^√	Reference
A. attenuatus	Brachiaria sp.	Kenya	KU574698	^[43]
	Salvia miltiorrhiza	China	JX406555	GenBank
A. lecanii	Cucurbita maxima	Australia	-	^[44]
	Gossypium hirsutum	Australia	-	^[45]
	Gossypium hirsutum	Brazil	-	^[46]
	Gossypium hirsutum	Texas, USA	KP407570	^[47]
	Solanum lycopersicum	Australia	-	^[44]
	Phaseolus vulgaris	Australia	-	^[44]
	Phaseolus vulgaris	China	-	^[48]
	Pistacia vera	Iran	MF000354	^[49]
	Triticum aestivum	Australia	-	^[44]
	Vitis vinifera	Spain	-	^[50]
	Zea mays	Australia	-	^[44]
A. muscarius	Brassica oleracea	New Zealand	-	^[51]
	Cucumis sativus	Canada	-	^[52]
	Cucumis sativus	Japan	-	^[53]
	Prunus cerasus	Iran	KY472303	^[54]
L. aphanocladii	Zea mays	Slovenia	-	^[55]
L. dimorphum	Phoenix dactylifera	Spain	-	^[56]
L. psalliotae	Phoenix dactylifera	Spain	-	^[56]
Lecanicillium sp.	Citrus limon	Iran	MN448344	GenBank
	Vitis vinifera	China	MT123107	GenBank
	Zea mays	India	-	^[57]

^√ Missing ITS accession number implies identification based on morphological characters only, or without depositing the ITS sequence.

Overall, Table 2 and Table 3 include 65 citations of endophytic strains belonging to these two genera as a result of a search considering literature in the field and the GenBank database. A widespread capacity to colonize plants from heterogeneous ecological contexts is evident considering that these citations refer to 54 species belonging to 35 botanical families. With 10 species Poaceae is the most represented family, followed by Arecaceae and Pinaceae with three species each, and Anacardiaceae, Apiaceae, Brassicaceae, Cucurbitaceae, Euphorbiaceae and Malvaceae with two species. The rest of the families (Apocynaceae, Araceae, Asteraceae, Betulaceae, Caryophyllaceae, Crassulaceae, Dipterocarpaceae, Ericaceae, Fabaceae, Fagaceae, Lamiaceae, Lauraceae, Lycopodiaceae, Magnoliaceae, Moraceae, Myrtaceae, Orchidaceae, Rosaceae, Rutaceae, Santalaceae, Sapindaceae, Simaroubaceae, Solanaceae, Taxaceae, Vitaceae and Zingiberaceae) are represented by a single species.

Such a variety of hosts seems to contrast any hypothesis of host specialization, and is rather indicative of a possible tendency to spread horizontally within the phytocoenoses. In this respect, the recovery of A. muscarius from four woody species (Acer campestre, Laurus nobilis, Quercus robur and Myrtus communis in two separate stands) at the Astroni Nature Reserve near Napoli, Italy (^[24] and in this paper), appears to support this ability, which may as well imply a permanent functional role in natural ecosystems. On the other hand, indications of a constant association with crop species could be favorable for possible applications in IPM. The limited available data only support preliminary clues in the case of cotton (Gossypium hirsutum) where, considering the economic impact of insect pests, the endophytic occurrence of strains of A. lecanii reported from distant countries such as Australia, Brazil and the United States might deserve further attention.

Phylogenetic Relationships of Endophytic Strains

In the evolving taxonomic scheme outlined above, the endophytic isolates provisionally classified as Lecanicillium sp. are to be further considered for a more definite taxonomic assignment. In this perspective, we propose a phylogenetic analysis (Figure 1) considering strains whose sequences of internal transcribed spacers of ribosomal DNA (rDNA-ITS) are deposited in GenBank (Table 2 and Table 3), along with official reference strains for the currently accepted species of Lecanicillium and Akanthomyces (Table 1).

Figure 1. Phylogenetic tree based on maximum likelihood (ML) analysis of the rDNA-ITS sequences deposited in GenBank for the known species (Table 1) and the endophytic strains of Lecanicillium and Akanthomyces (in bold, Table 2 and Table 3). Multiple sequence alignment comprised 592 nucleotide positions, including gaps. The analysis was carried out using RAxML software (version 8.2.12; https://cme.h-its.org/exelixis/web/software/raxml) for ML, PAUP (version 4.0a166; https://paup.phylosolutions.com) for maximum parsimony (MP), and MrBayes (version 3.2.7a; https://nbisweden.github.io/MrBayes/download.html) for Bayesian analysis. Phylogenetic tree was drawn using FigTree software (version 1.4.4; http://tree.bio.ed.ac.uk/software/figtree). Details and complete references are specified in a recent paper ^[58]. Bootstrap support values ≥60% for ML and MP are presented above branches as follows: ML/MP, bootstrap support values <50% are marked with ‘-’. Branches in bold are supported by Bayesian analysis (posterior probability ≥95%). Simplicillium lanosoniveum CBS 704.86 (GenBank: AJ292396) was used as outgroup reference. Main clades are indicated by colored boxes A, B, C, D, E and F.

Although more DNA sequences, such as the translation elongation factor 1 alpha (TEF) and RNA polymerase II largest subunits 1 (RPB1) and 2 (RPB2), are considered in taxonomic assessments concerning genera in the Cordycipitaceae ^[12]^[13]^[25]^[59], provisional identification of isolates recovered in the course of biodiversity studies is routinely done on account of ITS. Therefore only these kinds of sequences are usually deposited in GenBank for such strains, representing the only possible marker available for phylogenetic reconstructions.

In the absence of opportunities for a direct examination of these isolates, the phylogenetic tree proposed in Figure 1 provides an indication for their provisional assimilation to any of the accepted taxa in the genera Lecanicillium and Akanthomyces. A major cluster in the upper part of the tree includes the type strains of the species of Cordyceps, Akanthomyces (except A. aranearum), and of L. nodulosum and L. uredinophilum, which are also credited for ascription to Akanthomyces, along with all the endophytic strains ascribed to the species A. lecanii, A. muscarius and A. attenuatus (clades A, B and C, respectively). However, just two out of seven endophytic isolates ascribed to A. lecanii are next to the type strain of this species, while five more isolates rather group with A. muscarius. Confirming evidence from previous phylogenetic analyses ^[25]^[59], A. attenuatus is very close to A. muscarius, but an isolate from the palm Astrocaryum sciophilum is displaced in clade B. Another isolate from Brachiaria sp. reported as A. attenuatus is more distant, having L. uredinophilum as the closest relative. While these remarks cannot be taken as an evidence of a more common endophytic occurrence of A. muscarius, they represent an indication that at least some isolates of this species might have been misidentified as A. lecanii. This is not surprising, considering that a previous study pointed out the difficulty of resolving species ascription of strains previously ascribed to V. lecanii by using ITS sequences only ^[60].

Interestingly, no endophytic isolates provisionally identified as Lecanicillium sp. belong to the above major Akanthomyces cluster. Three of them are part of clade D, corresponding to the species L. aphanocladii, which also includes two strains identified as L. psalliotae. This is acceptable since these species and L. dimorphum have been reported in a close phylogenetic relationship in previous analyses ^[6]^[59]. However, L. psalliotae seems somehow problematic with reference to the resolution power of ITS, considering that it was reported as the closest relative (99.65% sequence identity at 100% query cover) of another isolate from Microthlaspi perfoliatum ^[40], which is in a quite distant position in our phylogenetic tree.

As many as seven unidentified strains cluster with L. fungicola, prevalently with the type strain of var. aleophilum (clade E), indicating a relevant endophytic occurrence of this species, which was not recognized so far. Another isolate reported as L. fungicola ^[32], deserves a more careful consideration with reference to its basal placement. In fact, BLAST search in GenBank indicated a 100% identity with ten strains of this species and several strains of the unrelated Simplicillium aogashimaense. The latter was characterized in 2013 with the support of a phylogenetic analysis based on ITS only, which anyway showed a consistent distance from L. fungicola ^[61]. Quite meaningfully, in our analysis the isolate in question was placed in proximity to the outgroup (Simplicillium lanosoniveum) on which our tree was rooted. Considering that sequences of six out of this group of ten L. fungicola strains were deposited in GenBank before 2013, it is quite possible that original misidentification of those that might rather have been Simplicillium strains could have determined the incorrect assignment of the more recent isolates.

Finally, three isolates (two Indian from Artocarpus lacucha and one Chinese from Vitis vinifera) are grouped in clade F together with the type strains of the recently described L. coprophilum ^[11], L. restrictum and L. testudineum ^[62]. A BLAST search in the GenBank database shows the first species as the closest relative, with 100% and 99.81% ITS sequence identity for the Chinese and the Indian isolates, respectively.

4. Implications in Crop Protection

As introduced above, so far there are few observations concerning the effects of endophytic strains of Lecanicillium and Akanthomyces in crops. Within the limited data available so far, cotton stands out for remarks on the endophytic occurrence of A. lecanii from independent cropping areas. In Australia an endophytic isolate was shown to be able to colonize cotton plants ensuring protection against the cotton aphid (Aphis gossypii) after artificial inoculation. Besides evidence from direct microscopic examination, the ability to colonize plant tissues was confirmed by re-isolation from leaves of the treated plants, which was successful up to 35 days after inoculation. This persistence can be taken as an indication of an endophytic life strategy, considering that endophytic colonization enables the fungus to become resident in a stable and nutritious insect-attracting environment. High humidity enhanced colonization of both plants and aphids; this expected effect is relevant for the management of the cotton aphid, which is most commonly found in the lower canopy, where humidity is high and the fungus is more protected against the adverse effects of UV radiation from sun ^[63]. Moreover, contact with conidia of A. lecanii significantly reduced the rate and period of reproduction of A. gossypii. The culture filtrate of the fungus significantly increased mortality and reduced reproduction, while feeding-choice experiments indicated that the aphids might be able to detect the fungal metabolites. The ethyl acetate and methanolic fractions of culture filtrate and mycelia also caused significant mortality and reduced fecundity ^[64]. Besides cotton, the same strain displayed the ability to colonize plants of wheat, corn, tomato, bean and pumpkin after artificial inoculation of leaves, while soil inoculation was ineffective ^[44].

Additional reports from cotton come from Texas ^[47] and Brazil, where the endophytic occurrence of A. lecanii was detected in leaves and roots of both normal and Bt-transgenic plants ^[46]. Although no aspects concerning interactions with pests were evaluated in these cases, it is meaningful that several strains of A. lecanii were recovered in each of these three contexts, indicating a possible common association of this species with cotton, which deserves to be more thoroughly verified.

The adaptation of A. lecanii to exert entomopathogenicity in association with plants is well attested by the finding that the fungus responds to volatile compounds produced by the plant during insect feeding. Particularly, in a model based on thale cress (Arabidopsis thaliana) and the mustard aphid (Lipaphis erysimi), compounds such as methyl salicylate and menthol were found to promote spore germination and pathogenicity of the fungus ^[65]^[66].

Besides aphids, protective effects after systemic colonization have been demonstrated against the red spider mite (Tetranychus urticae) in bean plants. In this case a strain of A. lecanii was reported to spread within the plant tissues after artificial inoculation of seeds, promoting growth and impairing survival and fecundity of the mites. These effects were even carried over the following generation of mites fed on fresh plants ^[48].

Pathogenicity of A. lecanii against a wide array of noxious arthropods is integrated by antagonism towards plant pathogenic fungi. In addition to a general antifungal activity demonstrated in vitro against polyphagous species such as Sclerotinia sclerotiorum, Rhizoctonia solani and Aspergillus flavus ^[49], possible exploitation of this double functionality has been conceived on several crops, such as coffee where A. lecanii behaves as both a parasite of the leaf rust (Hemileia vastatrix) and a pathogen of the green scale (Coccus viridis) ^[67]. The same role can be considered in crops where powdery mildews can represent a major phytosanitary problem, such as cucurbits ^[68]^[69].

Moreover, antifungal effects could derive from stimulation of the plant defense response, as reported for an endophytic strain able to promote such reaction against Pythium ultimum in transformed cucumber plants ^[52]. Additional experimental evidence in this regard is provided by observations carried out on the date palm (Phoenix dactylifera) where the inoculation of endophytic strains of L. dimorphum and L. cf. psalliotae, previously reported for entomopathogenicity against the red palm scale (Phoenicococcus marlatti) ^[56], induced proteins involved in plant defense or stress response. Proteins related with photosynthesis and energy metabolism were also upregulated, along with accumulation of a heavy chain myosin-like protein ^[70].

The concurrent role against plant pests and pathogens is known to operate for other Lecanicillium and Akanthomyces species, and for non-endophytic strains of various origin, as more in detail discussed in dedicated papers ^[71]^[72]. The need to combat multiple adversities has also prompted the evaluation of a possible combined use of these fungi with chemical pesticides. In this respect, it has been observed that the spread of A. lecanii in plant tissues is not affected by treatments with insecticides belonging to several classes ^[73]. Moreover, substantial safety of insecticides has been reported in in vitro assays carried out on A. muscarius, while several herbicides and fungicides were responsible for negative effects or even suppression of mycelial growth ^[74]. For the latter species, in vivo observations on the sweet potato whitefly (Bemisia tabaci) demonstrated the positive effects of association with chemical insecticides in view of reducing their use, particularly in the greenhouse ^[75]. Again with reference to application of A. muscarius for the control of B. tabaci, it is worth mentioning the synergistic effects resulting in combined treatments with matrine, a plant-derived quinolizidine alkaloid ^[76].

In addition to the indirect side effects deriving from protection against biotic and abiotic adversities, many endophytes have been reported to promote plant growth through essentially two mechanisms; that is the release of plant hormones, or the improvement of nutritional conditions. Of course, strains possessing both properties are likely to contribute in an additive manner, as observed for an isolate of L. psalliotae from cardamom (Elettaria cardamomum). Besides producing indole-3-acetic acid, this strain enhanced chlorophyll content of leaves as a likely result of release of siderophores, and increased availability of zinc and inorganic phosphate by promoting their solubilization ^[77]. Release of siderophore has also been reported for an endophytic isolate of A. lecanii from Pistacia vera ^[49].

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