Inter- and intra-specific variation in destruxin production by insect pathogenic Metarhizium spp., and its significance to pathogenesis

Amiri-Besheli, Behnam; Khambay, B. P. S.; Cameron, Stuart; Deadman, M. L.; Butt, Tariq M.

doi:10.1017/s095375629900146x

Cited by 96 publications

(61 citation statements)

References 12 publications

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“…As reported previously (17,22), our preliminary analysis confirmed that the M. robertsii strain ARSEF 23 produced dtxs in Czapek Dox (CD) broth, whereas the M. acridum strain CQMa 102 did not. Comparative genomic analysis indicated that the genome structures of M. robertsii and M. acridum are largely syntenic (15).…”

Section: Resultssupporting

confidence: 87%

“…3A) would support the hypothesis that they are the intermediate products of DtxS2 metabolism. These assumptions are consistent with the negatively correlated relationships of dtx production levels, e.g., the decrease of dtx A is paralleled with the increase of dtx E in media (17). The steroselectivity and sterochemistry of DtxS2 have yet to be determined.…”

Section: Discussionsupporting

confidence: 68%

“…The Metarhizium genus contains a dozen species (14), including M. anisopliae and M. robertsii, which can kill hundreds of insect species, and M. acridum, which can only kill locusts and grasshoppers (15,16). It has frequently been observed that dtx production correlates with host specificity (12,17). Besides their insecticidal activity, dtxs have also been explored as potential pharmaceuticals to treat cancer, osteoporosis, Alzheimer's disease, and hepatitis B (18)(19)(20).…”

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confidence: 99%

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Unveiling the biosynthetic puzzle of destruxins in Metarhizium species

Wang

Kang

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

212

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The authors note that Fig. 2 and its corresponding legend appeared incorrectly. The corrected figure and its corrected legend appear below.As a result of this correction, the authors note that on page 1288, right column, first full paragraph, lines 6-7, "the first substrate" should instead appear as "the second substrate"; that in the subsequent paragraph, line 2, "the A3 domain" should instead appear as "the A4 domain"; that in the same paragraph, lines 5-6, "A3 (for Val/Ile) and A4 (Val)" should instead appear as "A5 (for Val) and A6 (Ala)"; that on page 1290, right column, first full paragraph, line 10, "the A3 domain" should instead appear as "the A4 domain"; and that in the same paragraph, line 15, "A2 domain" should instead appear as "A3 domain."Also as a result of this correction, Fig. S1 appeared incorrectly. Please see separate SI Correction. These errors do not affect the conclusions of the article.

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Section: Resultssupporting

confidence: 87%

Section: Discussionsupporting

confidence: 68%

mentioning

confidence: 99%

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Unveiling the biosynthetic puzzle of destruxins in Metarhizium species

Wang

Kang

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

212

192

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“…Evidence that most specialists arose from generalists includes the following: (i) the vast majority of isolates found in nature belong to the genetically very diverse M. anisopliae var. anisopliae and typically demonstrate wide host ranges; (ii) specialist strains are scattered among generalists in phylogenies and have independently adapted to different insects; (iii) specialization is associated with conditions that are assumed to be derived, including reduced diet breadth (2,35,40). Specialist and generalist strains are often closely linked in phylogenies, indicating that there are genetic mechanisms allowing rapid adaptation (40).…”

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confidence: 99%

Comparative Genomics Using Microarrays Reveals Divergence and Loss of Virulence-Associated Genes in Host-Specific Strains of the Insect PathogenMetarhizium anisopliae

et al. 2009

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Many strains of Metarhizium anisopliae have broad host ranges, but others are specialists and adapted to particular hosts. Patterns of gene duplication, divergence, and deletion in three generalist and three specialist strains were investigated by heterologous hybridization of genomic DNA to genes from the generalist strain Ma2575. As expected, major life processes are highly conserved, presumably due to purifying selection. However, up to 7% of Ma2575 genes were highly divergent or absent in specialist strains. Many of these sequences are conserved in other fungal species, suggesting that there has been rapid evolution and loss in specialist Metarhizium genomes. Some poorly hybridizing genes in specialists were functionally coordinated, indicative of reductive evolution. These included several involved in toxin biosynthesis and sugar metabolism in root exudates, suggesting that specialists are losing genes required to live in alternative hosts or as saprophytes. Several components of mobile genetic elements were also highly divergent or lost in specialists. Exceptionally, the genome of the specialist cricket pathogen Ma443 contained extra insertion elements that might play a role in generating evolutionary novelty. This study throws light on the abundance of orphans in genomes, as 15% of orphan sequences were found to be rapidly evolving in the Ma2575 lineage.It is difficult to trace and reconstruct the evolutionary processes of diversification and radiation of species. In particular, genes that contribute to ecological diversification and the nature of the evolutionary forces acting during this process are poorly understood, partly because genes directly involved in ecological attributes are hard to identify (13). This is not the case with fungi, as they have genes encoding secreted products with specific environmental adaptations, e.g., scavenging nutrients and penetrating host barriers. During its pathogenic life cycle the ubiquitous insect pathogen Metarhizium anisopliae secretes a formidable array of hydrolytic enzymes, antimicrobial compounds, and toxins. These properties, plus its experimental tractability, have made M. anisopliae a common research subject and model system for studying pathogenicity and for developing useful products for medicine, agriculture, and biotechnology (33).The phylogeny of the Metarhizium genus has been well characterized (12). It is a largely clonal organism (4), containing subtypes with wide host ranges (e.g., M. anisopliae var. anisopliae Ma2575) and subtypes that, like M. anisopliae var. acridum Ma324 (used for locust control), show specificity for certain locusts, beetles, crickets, homopterans, etc., and are unable to infect other insects (5). While some specialized lineages, such as M. anisopliae var. acridum, are phylogenetically distant from generalist strains, implying evolutionarily conserved host use patterns, closely related strains can also differ greatly in host range and requirements for germination (16,40,42). Evidence that most specialists arose from generalis...

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“…Generally, in vitro production of destruxins by M. anisopliae is positively correlated with virulence of the fungus against its hosts, i.e., strains that produce relatively high levels of destruxin in vitro tend to exhibit greater virulence against in-sects, although exceptions to this trend exist (3,20,42,69). Furthermore, in vitro assays utilizing purified destruxins have demonstrated a wide range of biological activities against insects, including immunosuppression, activation of calcium channels in muscle, antifeedant activity, and acute toxicity (28,57,60,66,67,75,81).…”

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confidence: 99%

Agrobacterium -Mediated Disruption of a Nonribosomal Peptide Synthetase Gene in the Invertebrate Pathogen Metarhizium anisopliae Reveals a Peptide Spore Factor

Moon

Donzelli

Krasnoff

et al. 2008

Appl Environ Microbiol

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Numerous secondary metabolites have been isolated from the insect pathogenic fungus Metarhizium anisopliae, but the roles of these compounds as virulence factors in disease development are poorly understood. We targeted for disruption by Agrobacterium tumefaciens-mediated transformation a putative nonribosomal peptide synthetase (NPS) gene, MaNPS1. Four of six gene disruption mutants identified were examined further. Chemical analyses showed the presence of serinocyclins, cyclic heptapeptides, in the extracts of conidia of control strains, whereas the compounds were undetectable in ⌬Manps1 mutants treated identically or in other developmental stages, suggesting that MaNPS1 encodes a serinocyclin synthetase. Production of the cyclic depsipeptide destruxins, M. anisopliae metabolites also predicted to be synthesized by an NPS, was similar in ⌬Manps1 mutant and control strains, indicating that MaNPS1 does not contribute to destruxin biosynthesis. Surprisingly, a MaNPS1 fragment detected DNA polymorphisms that correlated with relative destruxin levels produced in vitro, and MaNPS1 was expressed concurrently with in vitro destruxin production. ⌬Manps1 mutants exhibited in vitro development and responses to external stresses comparable to control strains. No detectable differences in pathogenicity of the ⌬Manps1 mutants were observed in bioassays against beet armyworm and Colorado potato beetle in comparison to control strains. This is the first report of targeted disruption of a secondary metabolite gene in M. anisopliae, which revealed a novel cyclic peptide spore factor.

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Inter- and intra-specific variation in destruxin production by insect pathogenic Metarhizium spp., and its significance to pathogenesis

Cited by 96 publications

References 12 publications

Unveiling the biosynthetic puzzle of destruxins in Metarhizium species

Unveiling the biosynthetic puzzle of destruxins in Metarhizium species

Comparative Genomics Using Microarrays Reveals Divergence and Loss of Virulence-Associated Genes in Host-Specific Strains of the Insect PathogenMetarhizium anisopliae

Agrobacterium -Mediated Disruption of a Nonribosomal Peptide Synthetase Gene in the Invertebrate Pathogen Metarhizium anisopliae Reveals a Peptide Spore Factor

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