Trichoderma atroviride hyphal regeneration and conidiation depend on cell-signaling processes regulated by a microRNA-like RNA

Villalobos-Escobedo, José Manuel; Martínez-Hernández, J. Pedro; Pelagio‐Flores, Ramón; Rosa, Pablo Gonzalez de la; Carreras-Villaseñor, Nohemí; Abreu‐Goodger, Cei; Herrera‐Estrella, Alfredo

doi:10.1099/mgen.0.000869

Cited by 3 publications

(1 citation statement)

References 64 publications

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“…Individual stressors can also inhibit cells via multiple mechanisms (Alves et al, 2015 ; Benison et al, 2021 ; Cray et al, 2015 ; Hallsworth, 2018 ). Furthermore, stressors may induce so many cellular changes (including secondary stresses such as oxidative damage; Hallsworth et al, 2003 ) that these can mask their primary mode‐of‐action or are misallocated as inducing mechanical injury (e.g., Giannousi et al, 2015 ) albeit that mechanical injury can also act as a source of stress (e.g., Garduño‐Rosales et al, 2022 ; Hallsworth, 2018 ; Villalobos‐Escobedo et al, 2022 ).…”

Section: Simultaneous Inhibition Of Fungi By Multiple Antifungals In ...mentioning

confidence: 99%

Modes‐of‐action of antifungal compounds: Stressors and (target‐site‐specific) toxins, toxicants, or toxin–stressors

Noël

Hallsworth

Gelhaye

et al. 2023

Microbial Biotechnology

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Fungi and antifungal compounds are relevant to the United Nation's Sustainable Development Goals. However, the modes‐of‐action of antifungals—whether they are naturally occurring substances or anthropogenic fungicides—are often unknown or are misallocated in terms of their mechanistic category. Here, we consider the most effective approaches to identifying whether antifungal substances are cellular stressors, toxins/toxicants (that are target‐site‐specific), or have a hybrid mode‐of‐action as toxin–stressors (that induce cellular stress yet are target‐site‐specific). This newly described ‘toxin–stressor’ category includes some photosensitisers that target the cell membrane and, once activated by light or ultraviolet radiation, cause oxidative damage. We provide a glossary of terms and a diagrammatic representation of diverse types of stressors, toxic substances, and toxin–stressors, a classification that is pertinent to inhibitory substances not only for fungi but for all types of cellular life. A decision‐tree approach can also be used to help differentiate toxic substances from cellular stressors (Curr Opin Biotechnol 2015 33: 228–259). For compounds that target specific sites in the cell, we evaluate the relative merits of using metabolite analyses, chemical genetics, chemoproteomics, transcriptomics, and the target‐based drug‐discovery approach (based on that used in pharmaceutical research), focusing on both ascomycete models and the less‐studied basidiomycete fungi. Chemical genetic methods to elucidate modes‐of‐action currently have limited application for fungi where molecular tools are not yet available; we discuss ways to circumvent this bottleneck. We also discuss ecologically commonplace scenarios in which multiple substances act to limit the functionality of the fungal cell and a number of as‐yet‐unresolved questions about the modes‐of‐action of antifungal compounds pertaining to the Sustainable Development Goals.

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Section: Simultaneous Inhibition Of Fungi By Multiple Antifungals In ...mentioning

confidence: 99%

Modes‐of‐action of antifungal compounds: Stressors and (target‐site‐specific) toxins, toxicants, or toxin–stressors

Noël

Hallsworth

Gelhaye

et al. 2023

Microbial Biotechnology

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Trichoderma atroviride hyphal regeneration and conidiation depend on cell-signaling processes regulated by a microRNA-like RNA

Villalobos-Escobedo¹,

Martínez-Hernández²,

Pelagio‐Flores

et al. 2022

Microbial Genomics

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The ability to respond to injury is essential for the survival of an organism and involves analogous mechanisms in animals and plants. Such mechanisms integrate coordinated genetic and metabolic reprogramming events requiring regulation by small RNAs for adequate healing of the wounded area. We have previously reported that the response to injury of the filamentous fungus Trichoderma atroviride involves molecular mechanisms closely resembling those of plants and animals that lead to the formation of new hyphae (regeneration) and the development of asexual reproduction structures (conidiophores). However, the involvement of microRNAs in this process has not been investigated in fungi. In this work, we explore the participation of microRNA-like RNAs (milRNAs) molecules by sequencing messenger and small RNAs during the injury response of the WT strain and RNAi mutants. We found that Dcr2 appears to play an important role in hyphal regeneration and is required to produce the majority of sRNAs in T. atroviride. We also determined that the three main milRNAs produced via Dcr2 are induced during the damage-triggered developmental process. Importantly, elimination of a single milRNA phenocopied the main defects observed in the dcr2 mutant. Our results demonstrate the essential role of milRNAs in hyphal regeneration and asexual development by post-transcriptionally regulating cellular signalling processes involving phosphorylation events. These observations allow us to conclude that fungi, like plants and animals, in response to damage activate fine-tuning regulatory mechanisms.

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Argonaute and Dicer are essential for communication between Trichoderma atroviride and fungal hosts during mycoparasitism

Enriquez-Felix,

Pérez-Salazar,

Rico-Ruiz

et al. 2024

Microbiol Spectr

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Trichoderma species are known for their mycoparasitic activity against phytopathogenic fungi that cause significant economic losses in agriculture. During mycoparasitism, Trichoderma spp. recognize molecules produced by the host fungus and release secondary metabolites and hydrolytic enzymes to kill and degrade the host’s cell wall. Here, we explored the participation of the Trichoderma atroviride RNAi machinery in the interaction with six phytopathogenic fungi of economic importance. We determined that both Argonaute-3 and Dicer-2 play an essential role during mycoparasitism. Using an RNA-Seq approach, we identified that perception, detox, and cell wall degradation depend on the T. atroviride -RNAi when interacting with Alternaria alternata, Rhizoctonia solani AG2 , and R. solani AG5. Furthermore, we constructed a gene co-expression network that provides evidence of two gene modules regulated by RNAi, which play crucial roles in essential processes during mycoparasitism. In addition, based on small RNA-seq, we conclude that siRNAs regulate amino acid and carbon metabolism and communication during the Trichoderma -host interaction. Interestingly, our data suggest that siRNAs might regulate allorecognition ( het ) and transport genes in a cross-species manner. Thus, these results reveal a fine-tuned regulation in T. atroviride dependent on siRNAs that is essential during the biocontrol of phytopathogenic fungi, showing a greater complexity of this process than previously established. IMPORTANCE There is an increasing need for plant disease control without chemical pesticides to avoid environmental pollution and resistance, and the health risks associated with the application of pesticides are increasing. Employing Trichoderma species in agriculture to control fungal diseases is an alternative plant protection strategy that overcomes these issues without utilizing chemical fungicides. Therefore, understanding the biocontrol mechanisms used by Trichoderma species to antagonize other fungi is critical. Although there has been extensive research about the mechanisms involved in the mycoparasitic capability of Trichoderma species, there are still unsolved questions related to how Trichoderma regulates recognition, attack, and defense mechanisms during interaction with a fungal host. In this work, we report that the Argonaute and Dicer components of the RNAi machinery and the small RNAs they process are essential for gene regulation during mycoparasitism by Trichoderma atroviride .

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Trichoderma atroviride hyphal regeneration and conidiation depend on cell-signaling processes regulated by a microRNA-like RNA

Cited by 3 publications

References 64 publications

Modes‐of‐action of antifungal compounds: Stressors and (target‐site‐specific) toxins, toxicants, or toxin–stressors

Modes‐of‐action of antifungal compounds: Stressors and (target‐site‐specific) toxins, toxicants, or toxin–stressors

Trichoderma atroviride hyphal regeneration and conidiation depend on cell-signaling processes regulated by a microRNA-like RNA

Argonaute and Dicer are essential for communication between Trichoderma atroviride and fungal hosts during mycoparasitism

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