Populus MYC2 orchestrates root transcriptional reprogramming of defence pathway to impair Laccaria bicolor ectomycorrhizal development.
Laccaria bicolor
MYC2 transcription factor
ectomycorrhiza
plant defence
plant–microbe interactions
poplar
symbiosis
terpenes
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
received:
12
12
2023
accepted:
30
01
2024
pubmed:
20
2
2024
medline:
20
2
2024
entrez:
20
2
2024
Statut:
ppublish
Résumé
The jasmonic acid (JA) signalling pathway plays an important role in the establishment of the ectomycorrhizal symbiosis. The Laccaria bicolor effector MiSSP7 stabilizes JA corepressor JAZ6, thereby inhibiting the activity of Populus MYC2 transcription factors. Although the role of MYC2 in orchestrating plant defences against pathogens is well established, its exact contribution to ECM symbiosis remains unclear. This information is crucial for understanding the balance between plant immunity and symbiotic relationships. Transgenic poplars overexpressing or silencing for the two paralogues of MYC2 transcription factor (MYC2s) were produced, and their ability to establish ectomycorrhiza was assessed. Transcriptomics and DNA affinity purification sequencing were performed. MYC2s overexpression led to a decrease in fungal colonization, whereas its silencing increased it. The enrichment of terpene synthase genes in the MYC2-regulated gene set suggests a complex interplay between the host monoterpenes and fungal growth. Several root monoterpenes have been identified as inhibitors of fungal growth and ECM symbiosis. Our results highlight the significance of poplar MYC2s and terpenes in mutualistic symbiosis by controlling root fungal colonization. We identified poplar genes which direct or indirect control by MYC2 is required for ECM establishment. These findings deepen our understanding of the molecular mechanisms underlying ECM symbiosis.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
658-674Subventions
Organisme : Biological and Environmental Research
ID : DE-AC05-589 00OR22725
Organisme : Recherches Avancees sur la Biologie de l'Arbre et les Ecosystemes Forestiers
ID : ANR-11-LABX-0002-01
Organisme : Joint Genome Institute
Informations de copyright
© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
Références
Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, Li Z, Toshinori K, Ecker JR, Schroeder JI. 2016. An ABA‐increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Scientific Reports 6: 28941.
Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. [WWW document] URL http://www.bioinformatics.babraham.ac.uk/projects/fastqc [accessed 30 November 2021].
Bailey TL, Johnson J, Grant CE, Noble WS. 2015. The Meme suite. Nucleic Acids Research 43: W39–W49.
Bartlett A, O'Malley RC, Huang SSC, Galli M, Nery JR, Gallavotti A, Ecker JR. 2017. Mapping genome‐wide transcription‐factor binding sites using DAP‐seq. Nature Protocols 12: 1659–1672.
Basso V, Kohler A, Miyauchi S, Singan V, Guinet F, Šimura J, Novák O, Barry KW, Amirebrahimi M, Block J et al. 2020. An ectomycorrhizal fungus alters sensitivity to jasmonate salicylate gibberellin and ethylene in host roots. Plant, Cell and Environment 43: 1047–1068.
Basso V, Veneault‐Fourrey C. 2020. Role of jasmonates in beneficial microbe–root interactions. In: Champion A, Laplaze L, eds. Jasmonate in plant biology: methods in molecular biology. New York, NY, USA: Humana, 43–67.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120.
Bonito G, Hameed K, Ventura R, Krishnan J, Schadt CW, Vilgalys R. 2016. Isolating a functionally relevant guild of fungi from the root microbiome of Populus. Fungal Ecology 22: 35–42.
Breen J, Bellgard M. 2010. Germin‐like proteins (GLPs) in cereal genomes: gene clustering and dynamic roles in plant defence. Functional and Integrative Genomics 10: 463–476.
Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: a mid‐size family of genes for specialized metabolism that is highly diversified throughout the kingdom. The Plant Journal 66: 212–229.
Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D. 2011. The bHLH transcription factor MYC3 interacts with the jasmonate ZIM‐domain proteins to mediate jasmonate response in Arabidopsis. Molecular Plant 4: 279–288.
Chini A, Fonseca SGDC, Fernandez G, Adie B, Chico JM, Lorenzo O, García‐Casado G, López‐Vidriero I, Lozano FM, Ponce MR et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666–671.
Conrath U, Beckers GJ, Flors V, García‐Agustín P, Jakab G, Mauch F, Newman M, Pieterse CMJ, Poinssot B, Pozo MJ et al. 2006. Priming: getting ready for battle, molecular plant–microbe. Interactions 19: 1062–1071.
Cope KR, Bascaules A, Irving TB, Venkateshwaran M, Maeda J, Garcia K, Rush TA, Ma C, Labbé J, Jawdy S et al. 2019. The ectomycorrhizal fungus Laccaria bicolor produces lipochitooligosaccharides and uses the common symbiosis pathway to colonize Populus roots. Plant Cell 31: 2386–2410.
Daguerre Y, Basso V, Hartmann‐Wittulski S, Schellenberger R, Meyer L, Bailly J, Kohler A, Plett JM, Martin F, Veneault‐Fourrey C. 2020. The mutualism effector MiSSP7 of Laccaria bicolor alters the interactions between the poplar JAZ6 protein and its associated proteins. Scientific Reports 10: 20362.
Danner H, Boeckler GA, Irmisch S, Yuan JS, Chen F, Gershenzon J, Unsicker AB, Köllner TG. 2011. Four terpene synthases produce major compounds of the gypsy moth feeding‐induced volatile blend of Populus trichocarpa. Phytochemistry 72: 897–908.
Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey‐Klett P. 2007. The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytologist 175: 743–755.
Diévart A, Clark SE. 2004. LRR‐containing receptors regulating plant development and defense. Development 131: 251–261.
Ditengou FA, Müller A, Rosenkranz M, Felten J, Lasok H, Van Doorn MM, Legué V, Palme K, Schnitzler J, Polle A. 2015. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nature Communications 6: 6279.
Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners J et al. 2007. MYC2 differentially modulates diverse jasmonate‐dependent functions in Arabidopsis. Plant Cell 19: 2225–2245.
Du M, Zhao J, Tzeng DT, Liu Y, Deng L, Yang T, Zhai Q, Wu F, Huang Z, Zhou M et al. 2017. MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate‐mediated plant immunity in tomato. Plant Cell 29: 1883–1906.
Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annual Reviews in Plant Biology 70: 527–557.
Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V. 2009. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiology 151: 1991–2005.
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R. 2009. (+)‐7‐iso‐jasmonoyl‐L‐isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344–350.
Fracchia F, Basso V, Guinet F, Veneault‐Fourrey C, Deveau A. 2022. Confocal laser scanning microscopy approach to investigate plant–fungal interactions. In: Martin F, Uroz S, eds. Microbial environmental genomics: methods in molecular biology. New York, NY, USA: Humana, 325–335.
Grover A. 2012. Plant chitinases: genetic diversity and physiological roles. Critical Reviews in Plant Sciences 31: 57–73.
Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. 2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635–2648.
Ho‐Plágaro T, Tamayo‐Navarrete MI, García‐Garrido JM. 2020. Functional analysis of plant genes related to arbuscular mycorrhiza symbiosis using Agrobacterium rhizogenes‐mediated root transformation and hairy root production. In: Srivastava V, Mehrotra S, Mishra S, eds. Hairy root cultures based applications: methods and protocols. Singapore City, Singapore: Springer, 191–215.
Hou S, Thiergart T, Vannier N, Mesny F, Ziegler J, Pickel B, Hacquard S. 2021. A microbiota–root–shoot circuit favours Arabidopsis growth over defence under suboptimal light. Nature Plants 7: 1078–1092.
Huang AC, Jiang T, Liu YX, Bai YC, Reed J, Qu B, Goossens A, Nützmann H, Bai Y, Osbourn A. 2019. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364: eaau6389.
Huang AC, Osbourn A. 2019. Plant terpenes that mediate below‐ground interactions: prospects for bioengineering terpenoids for plant protection. Pest Management Science 75: 2368–2377.
Huang XF, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM. 2014. Rhizosphere interactions: root exudates microbes and microbial communities. Botany 92: 267–275.
Irmisch S, Jiang Y, Chen F, Gershenzon J, Köllner TG. 2014. Terpene synthases and their contribution to herbivore‐induced volatile emission in western balsam poplar Populus trichocarpa. BMC Plant Biology 14: 1–16.
Kazan K, Manners JM. 2013. MYC2: the master in action. Molecular Plant 6: 686–703.
Lackus ND, Lackner S, Gershenzon J, Unsicker SB, Köllner TG. 2018. The occurrence and formation of monoterpenes in herbivore‐damaged poplar roots. Scientific Reports 8: 17936.
Lackus ND, Morawetz J, Xu H, Gershenzon J, Dickschat JS, Köllner TG. 2021. The sesquiterpene synthase PtTPS5 produces 1 S 5 S 7 R 10 R‐Guaia‐4 15‐en‐11‐ol and 1 S 7 R 10 R‐Guaia‐4‐en‐11‐ol in oomycete‐infected poplar roots. Molecules 26: 555.
Langmead B, Salzberg SL. 2012. Fast gapped‐read alignment with Bowtie 2. Nature Methods 9: 357–359.
Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, Morgan T, Carey VJ. 2013. Software for computing and annotating genomic ranges. PLoS Computational Biology 9: e1003118.
Lee HJ, Park OK. 2019. Lipases associated with plant defense against pathogens. Plant Science 279: 51–58.
Li R, Weldegergis BT, Li J, Jung C, Qu J, Sun Y, Qian H, Tee C, van Loon JJA, Dicke M et al. 2014. Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26: 4991–5008.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biology 15: 1–21.
Marqués‐Gálvez JE, Veneault‐Fourrey C, Kohler A. 2022. Ectomycorrhizal symbiosis: from genomics to trans‐kingdom molecular communication and signaling. In: Horwitz BA, Mukherjee PK, eds. Microbial cross‐talk in the rhizosphere. Singapore City, Singapore: Springer, 273–296.
Martin F, Kohler A, Murat C, Veneault‐Fourrey C, Hibbett DS. 2016. Unearthing the roots of ectomycorrhizal symbioses. Nature Reviews. Microbiology 14: 760–773.
Melotto M, Mecey C, Niu Y, Chung H, S Katsir L, Yao J, Zeng W, Thines B, Staswick P, Brwose J et al. 2008. A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine‐and jasmonoyl isoleucine‐dependent interactions with the COI1 F‐box protein. The Plant Journal 55: 979–988.
Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez‐Pérez R, Møller BL, Bak S. 2008. β‐glucosidases as detonators of plant chemical defense. Phytochemistry 69: 1795–1813.
Neb D, Das A, Hintelmann A, Nehls U. 2017. Composite poplars: a novel tool for ectomycorrhizal research. Plant Cell Reports 36: 1959–1970.
Nguyen TH, Thiers L, Van Moerkercke A, Bai Y, Fernández‐Calvo P, Minne M, Depuydt T, Colinas M, Verstaen K, Van Isterdael G et al. 2023. A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis. Nature Plants 9: 926–937.
Niu Y, Figueroa P, Browse J. 2011. Characterization of JAZ‐interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. Journal of Experimental Botany 62: 2143–2154.
Panda S, Jozwiak A, Sonawane PD, Szymanski J, Kazachkova Y, Vainer A, Kilambi HV, Almekias‐Siegl E, Dikaya V, Bocobza S et al. 2022. Steroidal alkaloids defence metabolism and plant growth are modulated by the joint action of gibberellin and jasmonate signalling. New Phytologist 233: 1220–1237.
Pieterse CMJ, León‐Reyes A, Van Der Ent S, Van Wees SCM. 2009. Networking by small‐molecule hormones in plant immunity. Nature Chemical Biology 5: 308–316.
Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, Melton SJ, Kohler A, Morrell‐Falvey JL, Brun A, Veneault‐Fourrey C et al. 2014. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid JA responsive genes. Proceedings of the National Academy of Sicences, USA 111: 8299–8304.
Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler BM, Pargo AG, Martin F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21: 1197–1203.
Pozo MJ, Van Der Ent S, Van Loon LC, Pieterse CMJ. 2008. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria‐induced systemic resistance in Arabidopsis thaliana. New Phytologist 180: 511–523.
Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V. 2013. Jasmonate signaling in plant development and defense response to multiple abiotic stresses. Plant Cell Reports 32: 1085–1098.
Sasaki‐Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K. 2013. Basic helix–loop–helix transcription factors JASMONATE‐ASSOCIATED MYC2‐LIKE1 JAM1 JAM2 and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiology 163: 291–304.
Schindelin J, Arganda‐Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. 2012. Fiji: an open‐source platform for biological‐image analysis. Nature Methods 9: 676–682.
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
Schweizer F, Fernández‐Calvo P, Zander M, Diez‐Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P. 2013. Arabidopsis basic helix–loop–helix transcription factors MYC2 MYC3 and MYC4 regulate glucosinolate biosynthesis insect performance and feeding behavior. Plant Cell 25: 3117–3132.
Sheard LB, Tan X, Mao H, Withers J, Ben‐Nissan G, Hinds TR, Kobayashi Y, Hsu F, Sharon M, Browse J et al. 2010. Jasmonate perception by inositol‐phosphate‐potentiated COI1–JAZ co‐receptor. Nature 468: 400–405.
Song JT, Lu H, McDowell JM, Greenberg JT. 2004. A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. The Plant Journal 40: 200–212.
Song S, Huang H, Wang J, Liu B, Qi T, Xie D. 2017. MYC5 is involved in jasmonate‐regulated plant growth leaf senescence and defense responses. Plant Cell Physiology 58: 1752–1763.
Song S, Qi T, Wasternack C, Xie D. 2014. Jasmonate signaling and crosstalk with gibberellin and ethylene. Current Opinion in Plant Biology 21: 112–119.
Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Villareal‐Ruiz L, Vasco‐Palacios AM, Thu PQ, Suija A et al. 2014. Global diversity and geography of soil fungi. Science 346: 1256688.
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661–665.
Tholl D, Hossain O, Weinhold A, Röse US, Wei Q. 2021. Trends and applications in plant volatile sampling and analysis. The Plant Journal 106: 314–325.
Toffolatti SL, Maddalena G, Passera A, Casati P, Bianco PA, Quaglino F. 2021. Role of terpenes in plant defense to biotic stress. In: Jogaiah S, ed. Biocontrol agents and secondary metabolites. Sawston, UK: Elsevier, 401–417.
Wang J, Wu D, Wang Y, Xie D. 2019. Jasmonate action in plant defense against insects. Journal of Experimental Botany 70: 3391–3400.
Wang X, Du Y, Yu D. 2019. Trehalose phosphate synthase 5‐dependent trehalose metabolism modulates basal defense responses in Arabidopsis thaliana. Journal of Integrative Plant Biology 61: 509–527.
Wasternack C, Hause B. 2013. Jasmonates: biosynthesis perception signal transduction and action in plant stress response growth and development an update to the 2007 review in Annals of Botany. Annals of Botany 111: 1021–1058.
Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F et al. 2009. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21: 2220–2236.
Yang J, Duan G, Li C, Liu L, Han G, Zhang Y, Wang C. 2019. The crosstalks between jasmonic acid and other plant hormone signaling highlight the involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Frontiers in Plant Science 10: 1349.
Yang Z, Li Y, Gao F, Jin W, Li S, Kimani S, Yang S, Bao T, Gao X, Wang L. 2020. MYB21 interacts with MYC2 to control the expression of terpene synthase genes in flowers of Freesia hybrida and Arabidopsis thaliana. Journal of Experimental Botany 71: 4140–4158.
Yu G, Wang LG, He QY. 2015. ChIPseeker: an R/Bioconductor package for ChIP peak annotation comparison and visualization. Bioinformatics 31: 2382–2383.
Zander M, Lewsey MG, Clark NM, Yin L, Bartlett A, Saldierna Guzmán JP, Hann E, Langford AE, Jow B, Wise A et al. 2020. Integrated multi‐omics framework of the plant response to jasmonic acid. Nature Plants 6: 290–302.
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W et al. 2008. Model‐based analysis of ChIP‐Seq MACS. Genome Biology 9: 1–9.