Novel bioassay to assess antibiotic effects of fungal endophytes on aphids

Collinson, Nicholas Paul; Mann, Ross; Giri, Khageswor; Malipatil, M. B.; Kaur, Jatinder; Spangenberg, Germán; Valenzuela, Isabel

doi:10.1371/journal.pone.0228813

Cited by 5 publications

(4 citation statements)

References 56 publications

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“…However, a strain without lolitrem B also caused signi cant mortality, indicating this compound must act with others to exert an insecticidal effect. Interestingly, peramine, which does not affect aphids (Collinson et al, 2020), was downregulated during pathogenic development in our study.…”

Section: Protease Gene Expression May Explain the Plasticity Of M Bru...mentioning

confidence: 41%

Transcriptional reprogramming in the entomopathogenic fungus Metarhizium brunneum and its aphid host Myzus persicae during the switch between saprophytic and parasitic lifestyles

Reingold,

Faigenboim,

Matveev

et al. 2024

Preprint

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Background The fungus Metarhizium brunneum has evolved a remarkable ability to switch between different lifestyles. It develops as a saprophyte, an endophyte establishing mutualistic relationships with plants, or a parasite, enabling its use for the control of insect pests such as the aphid Myzus persicae. We tested our hypothesis that switches between lifestyles must be accompanied by fundamental transcriptional reprogramming, reflecting adaptations to different environmental settings. Results We combined high throughput RNA sequencing of M. brunneum in vitro and at different stages of pathogenesis to validate the modulation of genes in the fungus and its host during early infection. In agreement with our hypothesis, we observed transcriptional reprogramming in M. brunneum following conidial attachment, germination on the cuticle, and early-stage growth within the host. This involved the upregulation of genes encoding degrading enzymes and gene clusters involved in synthesis of secondary metabolites that act as virulence factors. The transcriptional response of the aphid host included the upregulation of genes potentially involved in antifungal activity, but antifungal peptides were not induced. We also observed the induction of a host flightin gene, which may be involved in wing formation and flight muscle development. Conclusions The switch from saprophytic to parasitic development in M. brunneum is accompanied by fundamental transcriptional reprogramming during the early phases of infection. The aphid host responds to fungal infection with its own transcriptional reprogramming, reflecting its inability to express antifungal peptides but featuring the induction of genes involved in winged morphs that may enable offspring to avoid the contaminated environment.

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Section: Protease Gene Expression May Explain the Plasticity Of M Bru...mentioning

confidence: 41%

Transcriptional reprogramming in the entomopathogenic fungus Metarhizium brunneum and its aphid host Myzus persicae during the switch between saprophytic and parasitic lifestyles

Reingold,

Faigenboim,

Matveev

et al. 2024

Preprint

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“…This suggested that the presence of B. bassiana decreased M. persicae fecundity. Similarly, Collinson et al [102] reported a significant decrease in fecundity rates for Diuraphis noxia (Mordvilko) and Aploneura lentisci (Passerini) on perennial ryegrass cv. Alto (Lolium perenne L.) endophytically colonized by Epichloë festucae.…”

Section: Discussionmentioning

confidence: 87%

“…Alto (Lolium perenne L.) endophytically colonized by Epichloë festucae. The authors associated these results with the presence of the alkaloids lolitrem B, ergovaline, and peramine identified in colonized plants [102]. Beauveria bassiana produces several molecules in vivo and in vitro with antimicrobial, insecticidal, and cytotoxic activities such as bassianin, tennelin, beauvericin, bassianolide, pyridomacrolidin, and pyridovericin [61,[103][104][105].…”

Section: Discussionmentioning

confidence: 97%

Direct and Indirect Effect via Endophytism of Entomopathogenic Fungi on the Fitness of Myzus persicae and Its Ability to Spread PLRV on Tobacco

Mabola

Bawin

Francis

2021

Insects

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Aphids are major crop pests that transmit more than half of all insect-vectored plant viruses responsible for high yield losses worldwide. Entomopathogenic fungi (EPF) are biological control agents mainly used by foliar application to control herbivores, including sap-sucking pests such as aphids. Their ability to colonize plant tissues and to interact with diverse plant pathogenic microorganisms have been reported. In our study, we evaluated the effectiveness of Beauveria bassiana ((Balsamo-Crivelli) Vuillemin) directly applied by contact or/and indirectly via endophytism in tobacco plants (Nicotiana tabacum L.) against the virus vector Myzus persicae (Sulzer) carrying the Potato leafroll virus (PLRV) or not. We found that both contact treatment and endophytic colonization of leaves significantly increased aphid mortality and decreased the fecundity rate when compared to control plants. In addition, on fungal-colonized leaves, viruliferous aphids were more negatively impacted than virus-free ones and nymph mortality was significantly higher than on fungal-free plants. Furthermore, we assessed PLRV transmission by M. persicae on tobacco plants inoculated with either B. bassiana or Metarhizium acridum ((Driver and Milner) JF Bischoff, Rehner, and Humber) as source or/and recipient plants. Myzus persicae was found to acquire and transmit PLRV regardless of the treatment. Nevertheless, the infection rate of endophytically colonized plants was lower at a seven-day incubation period and had increased to almost 100% after fifteen days. These results suggest that B. bassiana is effective against aphids, both by contact and via endophytism, and both B. bassiana and M. acridum delayed PLRV infection in tobacco.

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“…For example, AR1 produces peramine (a pyrrolopyrazine) and deters Argentine stem weevil, Listronotus bonariensis (Kuschel) (Rowan & Gaynor, 1986;Dymock et al, 1988), and AR37 produces epoxyjanthitrems and has bioactivity against L. bonariensis (Popay & Wyatt, 1995), porina, Wiseana spp. (Jensen & Popay, 2004), African black beetle, Heteronychus arator (Fabricius) (Popay & Thom, 2009), the mealybug Balanococcus poae (Maskell) (Pennell et al, 2005), and the root aphid Aploneura lentisci (Passerini) (Popay & Cox, 2016;Collinson et al, 2020;Popay et al, 2021), but can cause ryegrass staggers in sheep (Fletcher & Sutherland, 2009). As these commercialized strains do not confer protection to L. perenne from all pestiferous insects, identifying new bioactive secondary metabolites from other strains is key to unlocking the full potential of the Epichlo€ e-perennial ryegrass interaction (Johnson et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Two Epichloë festucae var. lolii endophytes in Lolium perenne reduce larval populations of the wheat sheath miner, Cerodontha australis

Jensen

Miller

Cave

et al. 2021

Entomologia Exp Applicata

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The wheat sheath miner, Cerodontha australis Malloch (Diptera: Agromyzidae), is a small leaf-and stem-mining fly that is native to New Zealand and eastern Australia where it feeds on grasses and cereals. Although not considered to be a major insect pest of pastures in New Zealand, it can be abundant during spring and summer in Waikato, New Zealand, and infests tillers of the introduced pasture plant, perennial ryegrass, Lolium perenne L. (Poaceae). Cerodontha australis is not deterred from feeding on L. perenne infected with commercially available strains of the fungal endophyte Epichlo€ e festucae var. lolii, which have been shown to provide protection from a range of other insect pests. In this study, three-pot trials and periodic examination over 18 months of field-collected L. perenne tillers showed that two Epichlo€ e endophyte strains, AR47 and AR48, reduced the survival and feeding damage by C. australis larvae, but there was no evidence of an effect on adult female feeding or oviposition. Compared to other strains of E. festucae var. lolii endophytes tested, plants infected with AR47 and AR48 had fewer and smaller larvae and less larval mining. The number of tillers with mining was reduced in AR47 relative to endophyte-free (Nil) by 57.1% (ranging from 25.0 to 92.5% across trials) and in AR48 by 67.1% (26.3-100%). Larvae in AR47 and AR48 were found further from the base of the tiller where they were less likely to damage the meristem and cause tiller death. The number of larvae and pupae in pseudostems was reduced in AR47 and AR48 compared with Nil by 78.4 and 82.0%, respectively, in the field trial. Very few larvae survived to pupation in AR47 and AR48 plants, with a reduction compared to Nil of over 81.5% in AR47 and over 97% in AR48 in each of the four trials presented here.

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Novel bioassay to assess antibiotic effects of fungal endophytes on aphids

Cited by 5 publications

References 56 publications

Transcriptional reprogramming in the entomopathogenic fungus Metarhizium brunneum and its aphid host Myzus persicae during the switch between saprophytic and parasitic lifestyles

Transcriptional reprogramming in the entomopathogenic fungus Metarhizium brunneum and its aphid host Myzus persicae during the switch between saprophytic and parasitic lifestyles

Direct and Indirect Effect via Endophytism of Entomopathogenic Fungi on the Fitness of Myzus persicae and Its Ability to Spread PLRV on Tobacco

Two Epichloë festucae var. lolii endophytes in Lolium perenne reduce larval populations of the wheat sheath miner, Cerodontha australis

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