PhD position in evolutionary biology of asexual reproduction in poplar rust

This position has been filled!

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Thesis title

Evolutionary and functional studies of reproductive mode polymorphism in the poplar rust fungus, Melampsora larici-populina

Advisors:

Pascal FREY (Senior scientist), main supervisor
Fabien HALKETT (Senior scientist), co-supervisor
Sébastien DUPLESSIS (Senior scientist), co-supervisor

Host laboratory

Tree – Microbe Interactions Department
INRAE / Université de Lorraine
INRAE Grand Est Nancy research centre
54280 Champenoux

https://mycor.iam.inrae.fr/IAM/

Funding : University doctoral contract. Duration 3 years. Monthly net salary about €1600.

Thesis summary

The variability of reproductive modes is a long-standing conundrum in evolutionary biology. Yet, it conditions the evolutionary trajectories of populations and the morphological or physiological characteristics of the individuals that compose them. The phytopathogenic fungus Melampsora larici-populina, causing poplar rust, is particularly interesting for the study of the polymorphism of reproduction modes. Indeed, like most Pucciniales, this species presents a life cycle that alternates between an asexual multiplication phase and a sexual reproduction phase. Besides, we have demonstrated that lineages of the fungus do survive strictly asexually over decades. The thesis proposes to address the issue of variability in reproductive modes along three complementary axes:

  1. An evolutionary ecology approach that will allow us to determine the geographical distribution of the asexual lineages of M. larici-populina using population genetics.
  2. A phenotypic approach that will aim to experimentally demonstrate the level of investment of asexual lineages in sexual reproduction.
  3. A genomic and evolutionary transcriptomic approach that will aim to elucidate the functional basis of the cycle and to find the determinants of the variation of the sexual and asexual reproduction modes.

Application

Send CV, cover letter and contact details of two referees to Pascal Frey (pascal.frey@inra.fr) and Fabien Halkett (fabien.halkett@inrae.fr) before June 28, 2022.

Required skills

The candidate should have a Master degree in ecology, evolutionary biology and/or population biology. He/she should have skills in population genetics and/or genomics and an interest in plant-microorganism interactions. A strong taste for teamwork is essential. Knowledge of French will be an asset but is not mandatory.

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Titre du sujet de thèse :

Études évolutives et fonctionnelles de la variabilité des modes de reproduction chez le champignon responsable de la rouille du peuplier, Melampsora larici-populina.

Encadrants :

Pascal FREY (DR2, HDR), directeur de la thèse

Fabien HALKETT (CRCN), co-encadrant de la thèse

Sébastien Duplessis (DR2, HDR), co-encadrant de la thèse

Laboratoire d’accueil :

UMR Interactions Arbres – Microorganismes

INRAE/Université de Lorraine

Centre INRAE Grand Est Nancy

54280 Champenoux

https://mycor.iam.inrae.fr/IAM/

Université d’inscription de l’étudiant en thèse : Université de Lorraine

Financement : Contrat doctoral universitaire, durée 3 ans, salaire net mensuel environ 1600€.

Résumé de la thèse

La variabilité des modes de reproduction est une énigme de longue date en biologie de l’évolution. Or elle conditionne les trajectoires évolutives des populations et les caractéristiques morphologiques ou physiologiques des individus qui la composent. Le champignon phytopathogène Melampsora larici-populina, agent de la rouille du peuplier, est une espèce particulièrement intéressante pour l’étude du polymorphisme de des modes de reproduction. En effet, comme la plupart des Pucciniales, cette espèce présente un cycle de vie qui alterne entre une phase de multiplication asexuée et une phase de reproduction sexuée. De plus, nous avons mis en évidence l’existence de lignées strictement asexuées du champignon. La thèse propose d’aborder la question de la variabilité des modes de reproduction selon trois axes complémentaires :

  1. Une approche d’écologie évolutive qui permettra de déterminer à l’aide des outils de la génétique des populations la distribution géographique des lignées asexuées de M. larici-populina.
  2. Une approche phénotypique qui visera à démontrer expérimentalement le niveau d’investissement des lignées asexuées dans la reproduction sexuée.
  3. Une approche de génomique et de transcriptomique évolutive qui visera à élucider les bases fonctionnelles de la réalisation du cycle et de trouver les déterminants de la variation des modes de reproduction sexuée et asexuée.

Candidature :

Envoyer un CV, une lettre de motivation et les coordonnées de 2 personnes de référence à Pascal Frey (pascal.frey@inra.fr) et Fabien Halkett (fabien.halkett@inrae.fr) avant le 28 juin 2022.

Compétences recherchées

Le(la) candidat(e) devra avoir une formation (Master) en écologie, biologie évolutive et/ou biologie des populations. Il(elle) devra avoir des compétences en génétique des populations et/ou en génomique et un intérêt pour les interactions plantes – microorganismes. Un goût prononcé pour le travail en équipe est indispensable.

In memoriam Michel Morelet 1938-2020

It is with great sadness that we inform you that our esteemed colleague Michel Morelet passed away on December 20, 2020 in Nancy in his 83rd year.

Michel Morelet was born on May 20, 1938 in Brazzaville (Congo). After a childhood and education in Congo, Vietnam, and Mali, he was trained at the Agricultural Institute in Yzeure in France from 1956 to 1960, then at the Zootechnical Education Center in Rambouillet. He then did an internship at INRA in Jouy-en-Josas in 1962-1963, then in the phytopathology laboratory of Professor Georges Viennot-Bourgin at INA (now AgroParisTech) in 1963-1964.

He was recruited at INRA in Nancy on January 1, 1965. He was one of the “founding members” of the Forest Pathology Laboratory created in 1964 by Louis Lanier at ENGREF (AgroParisTech Nancy), which moved to Champenoux in 1971, and is now a team of the Department of Tree-Microbe Interactions. Initially recruited as a technician, he quickly became an engineer. For many years, he was in charge of the “Determination Service” of the Forest Pathology Laboratory. In this capacity, he supervised the Master thesis of Pierre Chandelier, who became the first head of the Agricultural and Forest Mycology Unit of the National Plant Protection Laboratory in Nancy (now part of the Anses).

He defended a doctoral thesis in 1983 at the University of Nancy on the “Systematics and biology of Venturia infecting poplars from the Leuce section”. He was an excellent mycologist and taxonomist and was an authority in France and abroad. He named, or renamed, for the first time many pathogenic fungi of trees. He published more than 60 scientific articles, most of them in French. He contributed to Volume I of the seminal book “Mycologie et Pathologie Forestières” by Louis Lanier and co-authors, published in 1978. But his most notable contribution to science was the publication together with Etienne Kiffer of “Deuteromycetes. Mitosporic fungi: classification and generic keys”. This book was first published in French in 1997, and subsequently translated into English in 2000. Throughout his career, Michel Morelet has collected hundreds of fungal specimens (including several type specimens), which constitute the mycological herbarium of the Forest Pathology Lab. This herbarium, which contains nearly 1500 samples, is still kept at the Department of Tree – Microbe Interactions. Michel Morelet retired in 2000, but remained active in the field of fungal taxonomy for many years. Anyone who knew him professionally will remember him as a passionate, jovial man with a very sharp sense of humor.

Our thoughts are with his wife Monique, his children, his grandchildren, and all his loved ones.

Michel Morelet in the Forest Pathology Laboratory at ENGREF in 1970 (party for Gilberte Guinot’s 25th birthday). From left to right: Louis Lanier, MC Langlois, Gilberte Guinot, Michel Morelet.

Michel Morelet at his PhD Thesis defense in 1983. From left to right: Georges Viennot-Bourgin, François Mangenot, Michel Morelet.

Michel Morelet, eternal pipe smoker, at his office in 1988.

Michel Morelet clowning around in his laboratory in 1988.

Michel Morelet (at the top of the hill) during a field trip in Haute-Saône in 1998.

 

Hommage à Michel Morelet (1938-2020)

Nous avons la tristesse de vous faire part du décès de Michel Morelet survenu le 20 décembre 2020 à Nancy dans sa 83e année.

Michel Morelet est né le 20 mai 1938 à Brazzaville. Après une enfance et une scolarité au Congo, au Viêt Nam, puis au Mali, il a été formé à l’Institut Agricole du Centre à Yzeure dans l’Allier de 1956 à 1960, puis au Centre d’Enseignement Zootechnique de Rambouillet. Il a ensuite effectué un stage à l’INRA à Jouy-en-Josas en 1962-1963, puis dans le laboratoire de phytopathologie du Professeur Georges Viennot-Bourgin à l’INA (AgroParisTech) en 1963-1964.

Il fut recruté à l’INRA à Nancy le 1er janvier 1965. Il fit partie des « membres fondateurs » du Laboratoire de Pathologie Forestière créé en 1964 par Louis Lanier à l’ENGREF (AgroParisTech Nancy), laboratoire qui déménagea à Champenoux en 1971 et qui constitue aujourd’hui une équipe de l’UMR Interactions Arbres – Microorganismes. Recruté initialement comme technicien, il devint rapidement Ingénieur d’Etude. Il fut pendant de nombreuses années responsable du « Service de détermination » du Laboratoire de Pathologie Forestière. A ce titre, il encadra le DEA de Pierre Chandelier, qui devint le premier responsable de l’Unité de Mycologie Agricole et Forestière du Laboratoire National de la Protection des Végétaux à Nancy (aujourd’hui intégrée à l’Anses).

Michel Morelet soutint une thèse de doctorat en 1983 à l’Université de Nancy sur la « Systématique et biologie des Venturia inféodés aux peupliers de la section Leuce ». Il était un excellent mycologue et systématicien et faisait autorité en France comme à l’étranger. Il nomma, ou renomma, pour la première fois de nombreux de champignons pathogènes des arbres. Il a publié plus de 60 articles scientifiques, la plupart en langue française. Il contribua au tome I de l’ouvrage de référence « Mycologie et pathologie forestières » de Louis Lanier et co-auteurs, publié en 1978. Mais sa contribution la plus notable fut la publication en 1997 avec Etienne Kiffer de l’ouvrage « Les Deutéromycètes : Classification et clés d’identification générique » aux éditions INRA (aujourd’hui QUAE). Cet ouvrage fut traduit en anglais en 2000 aux éditions Taylor & Francis. Tout au long de sa carrière, Michel Morelet réunit des échantillons (dont des échantillons-type) qui constituent l’herbier mycologique de Pathologie forestière. Cet herbier, qui compte près de 1500 échantillons, est toujours conservé au sein de l’UMR Interactions Arbres – Microorganismes. Michel Morelet prit sa retraite en 2000, mais resta encore actif dans le domaine de la taxonomie fongique pendant de nombreuses années. Tous ceux qui l’ont connu professionnellement se souviendront d’un homme passionné, jovial et doté d’un sens de l’humour très acéré.

Nos pensées vont à son épouse Monique, ses enfants, ses petits enfants, et à tous ses proches.

Au Laboratoire de Pathologie Forestière à l’ENGREF (rue Girardet à Nancy) en 1970 : pot à l’occasion des 25 ans de Gilberte Guinot. De gauche à droite : Louis Lanier, M.C. Langlois, Gilberte Guinot, Michel Morelet.

Michel Morelet à l’issue de sa soutenance de thèse le 25 novembre 1983. De gauche à droite : Georges Viennot-Bourgin, François Mangenot, Michel Morelet.

Michel Morelet, éternel fumeur de pipe, à son bureau en 1988.

Michel Morelet faisant le pitre dans son laboratoire en 1988.

Michel Morelet (au sommet de la butte) lors d’une sortie de terrain en Haute-Saône en 1998.

Texte rédigé par J. Pinon et P. Frey

Offre de CDD Technicien(ne) gestionnaire de la tiquothèque du programme de recherche participative CiTIQUE

Vous serez accueilli(e) au Laboratoire Tous Chercheurs, au sein de l’UMR IAM, sur le Centre INRAE Grand Est Nancy situé sur la commune de Champenoux. Vous viendrez en appui au programme national CiTIQUE lancé en 2017, qui vise à faire travailler ensemble des chercheurs et des acteurs de la société civile intéressés par les tiques et les maladies qu’elles transmettent, notamment la maladie de Lyme. Vous aurez en charge l’ensemble du processus de gestion des tiques envoyées par les citoyens contributeurs du programme CiTIQUE en vue de leur utilisation par les scientifiques partenaires du programme et/ou par les stagiaires (élèves, citoyens) lors des stages de recherche Tous Chercheurs.

Formation recommandée : Baccalauréat général ou technologique

Connaissances souhaitées : Connaissances en biologie et en techniques de laboratoire

Expérience appréciée en gestion de ressources biologiques (manipulations au laboratoire et utilisation d’outils numériques)

Type de contrat : CDD

Durée du contrat : 3 mois temps-plein (prolongation possible jusqu’à 2 ans)

Date d’entrée en fonction : 01/10/2020

Modalités pour postuler : Transmettre un CV, une lettre de motivation et les coordonnées (email et téléphone) de deux personnes de référence à Mme Annick Brun-Jacob (annick.brun@univ-lorraine.fr), responsable du laboratoire Tous Chercheurs de Nancy.

Date limite pour postuler : 07 septembre 2020

Plus d’informations : Offre emploi Tiquothécaire INRAE

Articles

Mediation of plant–mycorrhizal interaction by a lectin receptor-like kinase J Labbé, W Muchero, O Czarnecki, J Wang, X Wang, AC Bryan, K Zheng, … Nature plants 5 (7), 676-680

Abstract

The molecular mechanisms underlying mycorrhizal symbioses, the most ubiquitous and impactful mutualistic plant–microbial interaction in nature, are largely unknown. Through genetic mapping, resequencing and molecular validation, we demonstrate that a G-type lectin receptor-like kinase (lecRLK) mediates the symbiotic interaction between Populus and the ectomycorrhizal fungus Laccaria bicolor. This finding uncovers an important molecular step in the establishment of symbiotic plant–fungal associations and provides a molecular target for engineering beneficial mycorrhizal relationships.

SlZRT2 encodes a ZIP family Zn transporter with dual localization in the ectomycorrhizal fungus Suillus luteusL Coninx, N Smisdom, A Kohler, N Arnauts, M Ameloot, F Rineau, … Frontiers in microbiology 10

Ectomycorrhizal (ECM) fungi are important root symbionts of trees, as they can have significant effects on the nutrient status of plants. In polluted environments, particular ECM fungi can protect their host tree from Zn toxicity by restricting the transfer of Zn while securing supply of essential nutrients. However, mechanisms and regulation of cellular Zn homeostasis in ECM fungi are largely unknown, and it remains unclear how ECM fungi affect the Zn status of their host plants. This study focuses on the characterization of a ZIP (Zrt/IrtT-like protein) transporter, SlZRT2, in the ECM fungus Suillus luteus, a common root symbiont of young pine trees. SlZRT2 is predicted to encode a plasma membrane-located Zn importer. Heterologous expression of SlZRT2 in yeast mutants with impaired Zn uptake resulted in a minor impact on cellular Zn accumulation and growth. The SlZRT2 gene product showed a dual localization and was detected at the plasma membrane and perinuclear region. S. luteus ZIP-family Zn uptake transporters did not show the potential to induce trehalase activity in yeast and to function as Zn sensors. In response to excess environmental Zn, gene expression analysis demonstrated a rapid but minor and transient decrease in SlZRT2 transcript level. In ECM root tips, the gene is upregulated. Whether this regulation is due to limited Zn availability at the fungal–plant interface or to developmental processes is unclear. Altogether, our results suggest a function for SlZRT2 in cellular Zn redistribution from the ER next to a putative role in Zn uptake in S. luteus.

Plant Glutathione Transferases: Diverse, Multi-Tasking Enzymes with Yet-to-Be Discovered Functions J Csiszár, A Hecker, NE Labrou, P Schröder, DE Riechers Frontiers in plant science 10, 1304

Comparative transcriptomics of Gymnosporangium spp. teliospores reveals a conserved genetic program at this specific stage of the rust fungal life cycle SQ Tao, B Cao, E Morin, YM Liang, S Duplessis BMC genomics 20 (1), 723

Abstract

Background

Gymnosporangium spp. are fungal plant pathogens causing rust disease and most of them are known to infect two different host plants (heteroecious) with four spore stages (demicyclic). In the present study, we sequenced the transcriptome of G. japonicum teliospores on its host plant Juniperus chinensis and we performed comparison to the transcriptomes of G. yamadae and G. asiaticum at the same life stage, that happens in the same host but on different organs.

Results

Functional annotation for the three Gymnosporangium species showed the expression of a conserved genetic program with the top abundant cellular categories corresponding to energy, translation and signal transduction processes, indicating that this life stage is particularly active. Moreover, the survey of predicted secretomes in the three Gymnosporangiumtranscriptomes revealed shared and specific genes encoding carbohydrate active enzymes and secreted proteins of unknown function that could represent candidate pathogenesis effectors. A transcript encoding a hemicellulase of the glycoside hydrolase 26 family, previously identified in other rust fungi, was particularly highly expressed suggesting a general role in rust fungi. The comparison between the transcriptomes of the three Gymnosporangium spp. and selected Pucciniales species in different taxonomical families allowed to identify lineage-specific protein families that may relate to the biology of teliospores in rust fungi. Among clustered gene families, 205, 200 and 152 proteins were specifically identified in G. japonicumG. yamadaeand G. asiaticum, respectively, including candidate effectors expressed in teliospores.

Conclusions

This comprehensive comparative transcriptomics study of three Gymnosporangium spp. identified gene functions and metabolic pathways particularly expressed in teliospores, a stage of the life cycle that is mostly overlooked in rust fungi. Secreted protein encoding transcripts expressed in teliospores may reveal new candidate effectors related to pathogenesis. Although this spore stage is not involved in host plant infection but in the production of basidiospores infecting plants in the Amygdaloideae, we speculate that candidate effectors may be expressed as early as the teliospore stage for preparing further infection by basidiospores.

At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margaritaprovides insights into plant, endobacterial and fungal interactions F Venice, S Ghignone, A Salvioli di Fossalunga, J Amselem, M Novero, … Environmental Microbiology

Summary

As members of the plant microbiota, arbuscular mycorrhizal fungi (AMF, Glomeromycotina) symbiotically colonize plant roots. AMF also possess their own microbiota, hosting some uncultivable endobacteria. Ongoing research has revealed the genetics underlying plant responses to colonization by AMF, but the fungal side of the relationship remains in the dark. Here, we sequenced the genome of Gigaspora margarita, a member of the Gigasporaceae in an early diverging group of the Glomeromycotina. In contrast to other AMF, Gmargarita may host distinct endobacterial populations and possesses the largest fungal genome so far annotated (773.104 Mbp), with more than 64% transposable elements. Other unique traits of the Gmargaritagenome include the expansion of genes for inorganic phosphate metabolism, the presence of genes for production of secondary metabolites and a considerable number of potential horizontal gene transfer events. The sequencing of Gmargarita genome reveals the importance of its immune system, shedding light on the evolutionary pathways that allowed early diverging fungi to interact with both plants and bacteria.

Article: Scientific reports

Soil temperature and hydric potential influences the monthly variations of soil Tuber aestivum DNA in a highly productive orchard F Todesco, S Belmondo, Y Guignet, L Laurent, S Fizzala, F Le Tacon, … Scientific Reports 9 (1), 1-10

Abstract

Tuber aestivum, also known as the summer or Burgundy truffle, is an ectomycorrhizal Ascomycete associated with numerous trees and shrubs. Its life cycle occurs in the soil, and thus soil parameters such as temperature and water availability could influence it. Taestivumcultivation has started in several countries, but ecological and agronomic requirements for the establishment and management of orchards are largely unknown. The aims of this work were: 1) to design a specific qPCR protocol using genomic data to trace and quantify Taestivum DNA in the soil; and 2) to assess the monthly soil DNA dynamic according to soil parameters (i.e. soil hydric potential and temperature) in this orchard. The study was conducted in a highly productive Taestivum orchard (hazels, oaks, pines, lime and hornbeam). The production started five years after the plantation and then increased exponentially to reach a maximum of 320 kg/ha in 2017. The soil hydric potential and temperature partially explained the monthly Taestivum soil DNA variability. The data presented here offer new insights into Taestivum ecology and cultivation.

Seminar: Guillaume Bilodeau

le 27 septembre, l’unité de mycologie accueillera Guillaume Bilodeau, un collègue scientifique du Canadian Food Inspection Agency qui travaille principalement sur l’identification et la caractérisation des champignons phytopathogènes (https://www.researchgate.net/profile/Guillaume_Bilodeau).

Guillaume proposera un séminaire : “Détection / identification d’agents phytopathogènes réglementés utilisant des données de génomes et métagénomique ”

Le séminaire aura lieu en nos locaux de Pixérécourt, Malzéville, le 27 à 14h00.

BMC Genomics

The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata D Armaleo, O Müller, F Lutzoni, ÓS Andrésson, G Blanc, HB Bode, … BMC genomics 20 (1), 60

Abstract

Background

Lichens, encompassing 20,000 known species, are symbioses between specialized fungi (mycobionts), mostly ascomycetes, and unicellular green algae or cyanobacteria (photobionts). Here we describe the first parallel genomic analysis of the mycobiont Cladonia grayi and of its green algal photobiont Asterochloris glomerata. We focus on genes/predicted proteins of potential symbiotic significance, sought by surveying proteins differentially activated during early stages of mycobiont and photobiont interaction in coculture, expanded or contracted protein families, and proteins with differential rates of evolution.

Results

A) In coculture, the fungus upregulated small secreted proteins, membrane transport proteins, signal transduction components, extracellular hydrolases and, notably, a ribitol transporter and an ammonium transporter, and the alga activated DNA metabolism, signal transduction, and expression of flagellar components. B) Expanded fungal protein families include heterokaryon incompatibility proteins, polyketide synthases, and a unique set of G-protein α subunit paralogs. Expanded algal protein families include carbohydrate active enzymes and a specific subclass of cytoplasmic carbonic anhydrases. The alga also appears to have acquired by horizontal gene transfer from prokaryotes novel archaeal ATPases and Desiccation-Related Proteins. Expanded in both symbionts are signal transduction components, ankyrin domain proteins and transcription factors involved in chromatin remodeling and stress responses. The fungal transportome is contracted, as are algal nitrate assimilation genes. C) In the mycobiont, slow-evolving proteins were enriched for components involved in protein translation, translocation and sorting.

Conclusions

The surveyed genes affect stress resistance, signaling, genome reprogramming, nutritional and structural interactions. The alga carries many genes likely transferred horizontally through viruses, yet we found no evidence of inter-symbiont gene transfer. The presence in the photobiont of meiosis-specific genes supports the notion that sexual reproduction occurs in Asterochloriswhile they are free-living, a phenomenon with implications for the adaptability of lichens and the persistent autonomy of the symbionts. The diversity of the genes affecting the symbiosis suggests that lichens evolved by accretion of many scattered regulatory and structural changes rather than through introduction of a few key innovations. This predicts that paths to lichenization were variable in different phyla, which is consistent with the emerging consensus that ascolichens could have had a few independent origins.

Article: Environmental Microbiology

Ascoma genotyping and mating type analyses of mycorrhizas and soil mycelia of Tuber borchii in a truffle orchard established by mycelial inoculated plants P Leonardi, C Murat, F Puliga, M Iotti, A Zambonelli Environmental Microbiology

Summary

Tuber borchii (the Bianchetto truffle) is a heterothallic Ascomycete living in symbiotic association with trees and shrubs. Maternal and paternal genotype dynamics have already been studied for the black truffles Tuber melanosporumand Tuber aestivum but not yet for T. borchii. In this study, we analysed maternal and paternal genotypes in the first truffle orchard realized with plants inoculated with five different T. borchii mycelia. Our aims were to test the persistence of the inoculated mycelia, if maternal and/or paternal genotypes correspond to inoculated mycelia and to assess the hermaphroditism of T. borchii. The mating type of each isolate as well as those of mycorrhizas, ascomata and extraradical soil mycelia was determined. Moreover, simple sequence repeat (SSR) profiles of maternal and paternal genotypes were assessed in 18 fruiting bodies to investigate the sexual behaviour of this truffle. The maternal genotypes of the fruiting bodies corresponded to those of the inoculated mycelia with only two exceptions. This confirmed that the inoculated mycelia persisted 9 years after plantation. As regards paternal partner, only two had the same genotype as those of the inoculated mycelia, suggesting hermaphroditism. Most of the new paternal genotypes originated from a recombination of those of inoculated mycelia.

Article: Environmental Microbiology

Multi‐omic analyses of exogenous nutrient bag decomposition by the black morel Morchella importuna reveal sustained carbon acquisition and transferring H Tan, A Kohler, R Miao, T Liu, Q Zhang, B Zhang, L Jiang, Y Wang, L Xie, … Environmental microbiology

Summary

The black morel (Morchella importuna Kuo, O’Donnell and Volk) was once an uncultivable wild mushroom, until the development of exogenous nutrient bag (ENB), making its agricultural production quite feasible and stable. To date, how the nutritional acquisition of the morel mycelium is fulfilled to trigger its fruiting remains unknown. To investigate the mechanisms involved in ENB decomposition, the genome of a cultivable morel strain (MimportunaSCYDJ1‐A1) was sequenced and the genes coding for the decay apparatus were identified. Expression of the encoded carbohydrate‐active enzymes (CAZymes) was then analyzed by metatranscriptomics and metaproteomics in combination with biochemical assays. The results show that a diverse set of hydrolytic and redox CAZymes secreted by the morel mycelium is the main force driving the substrate decomposition. Plant polysaccharides such as starch and cellulose present in ENB substrate (wheat grains plus rice husks) were rapidly degraded, whereas triglycerides were accumulated initially and consumed later. ENB decomposition led to a rapid increase in the organic carbon content in the surface soil of the mushroom bed, which was thereafter consumed during morel fruiting. In contrast to the high carbon consumption, no significant acquisition of nitrogen was observed. Our findings contribute to an increasingly detailed portrait of molecular features triggering morel fruiting.