Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales
Wu,Gang; Miyauchi,Shingo; Morin,Emmanuelle; Kuo,Alan; Drula,Elodie; Varga,Torda; Kohler,Annegret; Feng,Bang; Cao,Yang; Lipzen,Anna; Daum,Christopher; Hundley,Hope; Pangilinan,Jasmyn; Johnson,Jenifer; Barry,Kerrie; LaButti,Kurt; Ng,Vivian; Ahrendt,Steven; Min,Byoungnam; Choi,In-Geol; Park,Hongjae; Plett,Jonathan M.; Magnuson,Jon; Spatafora,Joseph W.; Nagy,Laszlo G.; Henrissat,Bernard; Grigoriev,Igor V.; Yang,Zhu-Liang; Xu,Jianping; Martin,Francis M.
Source PublicationNEW PHYTOLOGIST
AbstractWe aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives. Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae. Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay. This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes.
KeywordBoletales brown-rot fungi CAZymes comparative genomics ectomycorrhizal fungi trait evolution R/BIOCONDUCTOR PACKAGE PHYLOGENETIC ANALYSIS HOST-SPECIFICITY FUNGI GENUS DIVERSITY
WOS IDWOS:000728229300001
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Affiliation1.Chinese Acad Sci, Kunming Inst Bot, CAS Key Lab Plant Div & Biogeog East Asia, Kunming 650201, Yunnan, Peoples R China
2.Wu, Gang; Miyauchi, Shingo; Morin, Emmanuelle; Kohler, Annegret; Martin, Francis M.] Univ Lorraine, Ctr INRAE Grand Est Nancy, INRAE, UMR Interact Arbres Microorganismes, F-54280 Champenoux, France
3.Yunnan Key Lab Fungal Divers & Green Dev, Kunming 650201, Yunnan, Peoples R China
4.Kuo, Alan; Lipzen, Anna; Daum, Christopher; Hundley, Hope; Pangilinan, Jasmyn; Johnson, Jenifer; Barry, Kerrie; LaButti, Kurt; Ng, Vivian; Ahrendt, Steven; Min, Byoungnam; Grigoriev, Igor V.] Lawrence Berkeley Natl Lab, US Dept Energy DOE, Joint Genome Inst JGI, Berkeley, CA 94720 USA
5.INRAE, Architecture & Fonct Macromol Biol USC1408, F-13009 Marseille, France
6.Biol Res Ctr, Synthet & Syst Biol Unit, H-6726 Szeged, Hungary
7.Yunnan Inst Trop Crops, Jinghong 666100, Yunnan, Peoples R China
8.Korea Univ, Dept Biotechnol, Coll Life Sci & Biotechnol, Seoul 02841, South Korea
9.Czech Acad Sci, Inst Hydrobiol, Dept Aquat Microbial Ecol, Ctr Biol, Ceske Budejovice 37005, Czech Republic
10.Plett, Jonathan M.] Western Sydney Univ, Hawkesbury Inst Environm, Richmond, NSW 2753, Australia
11.Pacific Northwest Natl Lab, Chem & Biol Proc Dev Grp, Richland, WA 99354 USA
12.Spatafora, Joseph W.] Oregon State Univ, Dept Bot & Plant Pathol, Corvallis, OR 97331 USA
13.Nagy, Laszlo G.] Eotvos Lorand Univ, Inst Biol, Dept Plant Anat, H-1117 Budapest, Hungary
14.Aix Marseille Univ, CNRS, Architecture & Fonct Macromol Biol, F-13009 Marseille, France
15.King Abdulaziz Univ, Dept Biol Sci, Jeddah 21589, Saudi Arabia
16.Grigoriev, Igor V.] Univ Calif Berkeley, Dept Plant & Microbial Biol, Berkeley, CA 94720 USA
17.McMaster Univ, Dept Biol, Hamilton, ON L8S 4K1, Canada
18.Martin, Francis M.] Beijing Forestry Univ, Beijing Adv Innovat Ctr Tree Breeding Mol Design, Beijing 100083, Peoples R China
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Wu,Gang,Miyauchi,Shingo,Morin,Emmanuelle,et al. Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales[J]. NEW PHYTOLOGIST,2022,233(3):1383-1400.
APA Wu,Gang.,Miyauchi,Shingo.,Morin,Emmanuelle.,Kuo,Alan.,Drula,Elodie.,...&Martin,Francis M..(2022).Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales.NEW PHYTOLOGIST,233(3),1383-1400.
MLA Wu,Gang,et al."Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales".NEW PHYTOLOGIST 233.3(2022):1383-1400.
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