Predicting functions of putative fungal sesquiterpene synthase genes based on multiomics data analysis

Nosenko, Tetyana; Zimmer, Ina; Ghirardo, Andrea; Köllner, Tobias G.; Weber, Baris; Polle, Andrea; Rosenkranz, Maaria; Schnitzler, Jörg‐Peter

doi:10.1016/j.fgb.2023.103779

Cited by 7 publications

(7 citation statements)

References 56 publications

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“…Even though fungi, like bacteria, are increasingly recognized as valuable sources for TS activity, far fewer have been characterized compared to plants, providing insufficient data to perform ML studies. Using an alternative multiomics approach, Nosenko and co-workers predicted the product profiles for 116 out of 146 putative sTS genes from 30 different fungal species . The prediction method is based on the assumption that closely related sTS genes likely share the same initial steps in the reaction cascade, even though the final products may be quite divergent, a feature that was also observed for plant sTSs .…”

Section: Predictive and High-throughput Engineering Of Tssmentioning

confidence: 99%

“…Using an alternative multiomics approach, Nosenko and co-workers predicted the product profiles for 116 out of 146 putative sTS genes from 30 different fungal species. 201 The prediction method is based on the assumption that closely related sTS genes likely share the same initial steps in the reaction cascade, even though the final products may be quite divergent, a feature that was also observed for plant sTSs. 61 Combined with gene expression information and patterns of volatile compound emission, this allowed the authors to assign function to the putative fungal sTSs.…”

Section: Predictive and High-throughput Engineering Of Tssmentioning

confidence: 99%

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Decoding Catalysis by Terpene Synthases

Whitehead,

Leferink,

Johannissen

et al. 2023

ACS Catal.

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The review by Christianson, published in 2017 on the twentieth anniversary of the emergence of the field, summarizes the foundational discoveries and key advances in terpene synthase/cyclase (TS) biocatalysis (Christianson, D. W. Chem Rev 2017, 117 (17), 11570–11648. DOI: 10.1021/acs.chemrev.7b00287). Here, we review the TS literature published since then, bringing the field up to date and looking forward to what could be the near future of TS rational design. Many revealing discoveries have been made in recent years, building on the knowledge and fundamental principles uncovered during those initial two decades of study. We use these to explore TS reaction chemistry and see how a combined experimental and computational approach helps to decipher the complexities of TS catalysis. Revealed are a suite of catalytic motifs which control product outcome in TSs, some obvious, some more subtle. We examine each in detail, using the most recent papers and insights to illustrate how exactly this fascinating class of enzymes takes a single acyclic substrate and turns it into the many thousands of complex terpenoids found in Nature. We then explore some of the recent strategies for TS engineering, including machine learning and other data-driven approaches. From this, rational and predictive engineering of TSs, “designer terpene synthases”, will begin to emerge as a realistic goal.

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Section: Predictive and High-throughput Engineering Of Tssmentioning

confidence: 99%

Section: Predictive and High-throughput Engineering Of Tssmentioning

confidence: 99%

Decoding Catalysis by Terpene Synthases

Whitehead,

Leferink,

Johannissen

et al. 2023

ACS Catal.

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“…Fungal VOCs are organic chemicals with low molecular weight that originate from metabolic processes within the fungus, evaporate easily at moderate temperature (Macías-Rodríguez et al, 2015) and participate in the communication between fungal species (Guo et al, 2019; Guo et al, 2020; Weikl et al, 2016; Wonglom et al, 2020). Several studies suggest that fungal VOC profiles are similar for fungi with comparable lifestyles (El Jaddaoui et al, 2023; Farh & Jeon, 2020; Guo et al, 2020; Guo et al, 2021; Müller, Faubert et al, 2013; Razo-Belmán et al, 2023) and also Trichoderma species have been demonstrated to produce several volatiles (many being sesquiterpenes), as well as receive, and respond to VOCs (Guo et al, 2019; Guo et al, 2020; Huang et al, 2022; Macías-Rodríguez et al, 2020; Nosenko et al, 2023; Rajani et al, 2021; Ruangwong et al, 2021). It is already well-known that VOCs are pivotal in orchestrating inter-species and inter-kingdom signaling within the rhizosphere, a dynamic environment, where various organisms interact (Faure et al, 2009; Werner et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Lifestyle-specific responses ofTrichodermaspp. in mycoparasitic confrontations and implications for biocontrol ofPopulusxcanescens

Stange,

Kersting,

Sivaprakasam Padmanaban

et al. 2024

Preprint

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Trichodermaspp. are gaining popularity in agriculture and forestry due to their multifaceted roles in promoting plant growth through e.g. nutrient translocation, hormone production, induction of plant systemic resistance, but also direct antagonism of other fungi. However, the mycotrophic nature of the genus bears the risk of possible interference with other native plant-beneficial fungi, such as ectomycorrhiza, in the rhizosphere. Such interference could yield unpredictable consequences for the host plants of these ecosystems. We investigated whetherTrichodermaspp. can differentiate between beneficial ectomycorrhizal fungi (represented byLaccaria bicolorandHebeloma cylindrosporum) and pathogenic fungi (represented byFusarium graminearumandAlternaria alternata) in different confrontation scenarios, including a newly developed olfactometer 'race tube'-like system. Using two independent species,T. harzianum, andT. atrobrunneum, with plant-growth-promoting and immune-stimulating properties towardsPopulus x canescens, our study revealed robustly accelerated growth towards phytopathogens, while showing a contrary response to ectomycorrhizal fungi. Transcriptomic analyses identified distinct genetic programs during interaction corresponding to the lifestyles, emphasizing the expression of mycoparasitism-related genes only in the presence of phytopathogens. The findings reveal a critical mode of fungal community interactions belowground and suggest thatTrichodermaspp. can distinguish between fungal partners of different lifestyles already at a distance.

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“…The majority of studies focusing on identifying and characterizing volatile terpenes in ECM fungi have looked at the headspace above fungal hyphae (Abdulsalam et al 2021 ; Ditengou et al 2015 ; Ezediokpu et al 2022 ). More recently, one study was published using an ECM fungus where the authors heterologously expressed individual terpene synthases to determine their soluble products (Nosenko et al 2023 ). Phylogenetically, the two fungal models considered here had protein orthologs that fell across the majority of the five major clades.…”

Section: Discussionmentioning

confidence: 99%

“…Within mutualistic ECM fungi, the majority of our knowledge concerning potential roles for terpenes in communicating with plant hosts comes from transcriptomic and comparative genomic studies (Chot et al 2023 ; Lebreton et al 2022 ; Nosenko et al 2023 ; Ruytinx et al 2021 ). For example, terpene synthesis in the ECM fungus Piloderma croceum was found to be significantly regulated (Liao et al 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Sesquiterpenes of the ectomycorrhizal fungus Pisolithus microcarpus alter root growth and promote host colonization

Plett,

Wojtalewicz,

Plett

et al. 2024

Mycorrhiza

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Trees form symbioses with ectomycorrhizal (ECM) fungi, maintained in part through mutual benefit to both organisms. Our understanding of the signaling events leading to the successful interaction between the two partners requires further study. This is especially true for understanding the role of volatile signals produced by ECM fungi. Terpenoids are a predominant class of volatiles produced by ECM fungi. While several ECM genomes are enriched in the enzymes responsible for the production of these volatiles (i.e., terpene synthases (TPSs)) when compared to other fungi, we have limited understanding of the biochemical products associated with each enzyme and the physiological impact of specific terpenes on plant growth. Using a combination of phylogenetic analyses, RNA sequencing, and functional characterization of five TPSs from two distantly related ECM fungi (Laccaria bicolor and Pisolithus microcarpus), we investigated the role of these secondary metabolites during the establishment of symbiosis. We found that despite phylogenetic divergence, these TPSs produced very similar terpene profiles. We focused on the role of P. microcarpus terpenes and found that the fungus expressed a diverse array of mono-, di-, and sesquiterpenes prior to contact with the host. However, these metabolites were repressed following physical contact with the host Eucalyptus grandis. Exposure of E. grandis to heterologously produced terpenes (enriched primarily in $$\gamma$$ γ -cadinene) led to a reduction in the root growth rate and an increase in P. microcarpus–colonized root tips. These results support a very early putative role of fungal-produced terpenes in the establishment of symbiosis between mycorrhizal fungi and their hosts.

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Predicting functions of putative fungal sesquiterpene synthase genes based on multiomics data analysis

Cited by 7 publications

References 56 publications

Decoding Catalysis by Terpene Synthases

Decoding Catalysis by Terpene Synthases

Lifestyle-specific responses ofTrichodermaspp. in mycoparasitic confrontations and implications for biocontrol ofPopulusxcanescens

Sesquiterpenes of the ectomycorrhizal fungus Pisolithus microcarpus alter root growth and promote host colonization

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