外生菌根共生:共生真菌多样性及菌根形成的分子机制
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摘要
大约2%的维管植物能够与17～18个目约280个属的真菌形成外生菌根关系.外生菌根关系的形成、宿主植物的专一化和宿主转移等事件可能是共生真菌物种分化的重要驱动力.比较基因组学研究发现,外生菌根真菌丢失了大量与植物细胞壁物质降解相关的基因.在外生菌根形成过程中,真菌与宿主植物之间借助多样化的信号分子完成相互识别,并且外生菌根真菌能够借助分泌效应蛋白抑制宿主植物的防御反应,促进菌根形成.本文对外生菌根真菌的多样性和分布规律,以及外生菌根形成的分子机制等方面进行了综述,并据此对后续研究提出展望.
Approximately 2% of vascular plants are involved in ectomycorrhizal symbioses with about 280 genera of higher fungi from 17–18 fungal orders.The development of ectomycorrhizal symbiosis,host specificity,and host-switch events appear to be key drivers for the speciation of ectomycorrhizal fungi.Comparative genomics indicates that ectomycorrhizal fungi have lost a set of genes that control the decay of organic matter contained in plant cell walls.During the formation of ectomycorrhizae,mycobionts and host plants require diversified signaling molecules to induce their bilateral communication;at the same time,mycobionts can release some mycorrhizal-induced small secreted proteins,which can help them escape plant defenses and thereby enable them to colonize plant roots.We present a review on the diversity and geographical distribution pattern of ectomycorrhizal fungi and on molecular mechanisms contributing to the development of ectomycorrhizae.Based on this,we also suggeste several future prospects.
Approximately 2% of vascular plants are involved in ectomycorrhizal symbioses with about 280 genera of higher fungi from 17–18 fungal orders.The development of ectomycorrhizal symbiosis,host specificity,and host-switch events appear to be key drivers for the speciation of ectomycorrhizal fungi.Comparative genomics indicates that ectomycorrhizal fungi have lost a set of genes that control the decay of organic matter contained in plant cell walls.During the formation of ectomycorrhizae,mycobionts and host plants require diversified signaling molecules to induce their bilateral communication;at the same time,mycobionts can release some mycorrhizal-induced small secreted proteins,which can help them escape plant defenses and thereby enable them to colonize plant roots.We present a review on the diversity and geographical distribution pattern of ectomycorrhizal fungi and on molecular mechanisms contributing to the development of ectomycorrhizae.Based on this,we also suggeste several future prospects.
引文
1 Brundrett M C,Tedersoo L.Evolutionary history of mycorrhizal symbioses and global host plant diversity.New Phytol,2018,220:1108-1115
2 Smith M E,Read D.Mycorrhizal Symbiosis.3rd ed.New York:Elsevier,2008
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4 Selosse M A,Le Tacon F.The land flora:A phototroph-fungus partnership?Trends Ecol Evol,1998,13:15-20
5 Brundrett M C.Coevolution of roots and mycorrhizas of land plants.New Phytol,2002,154:275-304
6 Martin F,Kohler A,Murat C,et al.Unearthing the roots of ectomycorrhizal symbioses.Nat Rev Microbiol,2016,14:760-773
7 Tedersoo L,Smith M E.Ectomycorrhizal fungal lineages:Detection of four new groups and notes on consistent recognition of ectomycorrhizal taxa in high-throughput sequencing studies.In:Tedersoo L,ed.Biogeography of Mycorrhizal Symbiosis.Gewerbestrasse:Springer,2017.125-142
8 Tedersoo L,May T W,Smith M E.Ectomycorrhizal lifestyle in fungi:Global diversity,distribution,and evolution of phylogenetic lineages.Mycorrhiza,2010,20:217-263
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11 Choi J J,Kim S H.A genome tree of life for the fungi kingdom.Proc Natl Acad Sci USA,2017,114:9391-9396
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39 Lagrange H,Jay-Allgmand C,Lapeyrie F.Rutin,the phenolglycoside from eucalyptus root exudates,stimulates Pisolithus hyphal growth at picomolar concentrations.New Phytol,2001,149:349-355
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2 Smith M E,Read D.Mycorrhizal Symbiosis.3rd ed.New York:Elsevier,2008
3 Strullu-Derrien C,Selosse M A,Kenrick P,et al.The origin and evolution of mycorrhizal symbioses:From palaeomycology to phylogenomics.New Phytol,2018,220:1012-1030
4 Selosse M A,Le Tacon F.The land flora:A phototroph-fungus partnership?Trends Ecol Evol,1998,13:15-20
5 Brundrett M C.Coevolution of roots and mycorrhizas of land plants.New Phytol,2002,154:275-304
6 Martin F,Kohler A,Murat C,et al.Unearthing the roots of ectomycorrhizal symbioses.Nat Rev Microbiol,2016,14:760-773
7 Tedersoo L,Smith M E.Ectomycorrhizal fungal lineages:Detection of four new groups and notes on consistent recognition of ectomycorrhizal taxa in high-throughput sequencing studies.In:Tedersoo L,ed.Biogeography of Mycorrhizal Symbiosis.Gewerbestrasse:Springer,2017.125-142
8 Tedersoo L,May T W,Smith M E.Ectomycorrhizal lifestyle in fungi:Global diversity,distribution,and evolution of phylogenetic lineages.Mycorrhiza,2010,20:217-263
9 Tedersoo L,Smith M E.Lineages of ectomycorrhizal fungi revisited:Foraging strategies and novel lineages revealed by sequences from belowground.Fungal Biol Rev,2013,27:83-99
10 Tedersoo L,Brundrett M C.Evolution of ectomycorrhizal symbiosis in plants.In:Tedersoo L,ed.Biogeography of Mycorrhizal Symbiosis.Gewerbestrasse:Springer,2017.407-467
11 Choi J J,Kim S H.A genome tree of life for the fungi kingdom.Proc Natl Acad Sci USA,2017,114:9391-9396
12 Hibbett D S,Bauer R,Binder M,et al.Agaricomycetes.In:Mc Laughlin D J,Spatafora J W,eds.The Mycota:A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research.Heidelberg:Springer,2014.373-429
13 Hibbett D S,Binder M,Bischoff J F,et al.A higher-level phylogenetic classification of the fungi.Mycol Res,2007,111:509-547
14 Byng J W,Chase M W,Christenhusz M J M,et al.Angiosperm Phylogeny G.An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG IV.Botan J Linnean Soc,2016,181:1-20
15 Ran J H,Shen T T,Wang M M,et al.Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms.Proc R Soc B,2018,285:20181012
16 Dearnaley J D W,Martos F,et al.Orchid mycorrhizas:Molecular ecology,physiology,evolution and conservation aspects.In:Hock B,ed.Fungal Associations.2nd ed.Gewerbestrasse:Springer,2012.207-230
17 Midgley D J,Rosewarne C P,Greenfield P,et al.Genomic insights into the carbohydrate catabolism of Cairneyella variabilis gen.nov.sp.nov.,the first reports from a genome of an ericoid mycorrhizal fungus from the southern hemisphere.Mycorrhiza,2016,26:345-352
18 Tedersoo L,Bahram M,Jairus T,et al.Spatial structure and the effects of host and soil environments on communities of ectomycorrhizal fungi in wooded savannas and rain forests of Continental Africa and Madagascar.Mol Ecol,2011,20:3071-3080
19 Wang B,Qiu Y L.Phylogenetic distribution and evolution of mycorrhizas in land plants.Mycorrhiza,2006,16:299-363
20 Hibbett D S,Matheny P B.The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses.BMC Biol,2009,7:13
21 Tedersoo L,Bahram M,P?lme S,et al.Global diversity and geography of soil fungi.Science,2014,346:1256688
22 Wilson A W,Hosaka K,Mueller G M.Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria.New Phytol,2017,213:1862-1873
23 Wu G,Feng B,Xu J,et al.Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic clades in the fungal family Boletaceae.Fungal Divers,2014,69:93-115
24 Cui Y Y,Cai Q,Tang L P,et al.The family Amanitaceae:Molecular phylogeny,higher-rank taxonomy and the species in China.Fungal Divers,2018,91:5-230
25 Sato H,Tanabe A S,Toju H.Host shifts enhance diversification of ectomycorrhizal fungi:Diversification rate analysis of the ectomycorrhizal fungal genera Strobilomyces and Afroboletus with an 80-gene phylogeny.New Phytol,2017,214:443-454
26 Han L H,Feng B,Wu G,et al.African origin and global distribution patterns:Evidence inferred from phylogenetic and biogeographical analyses of ectomycorrhizal fungal genus Strobilomyces.J Biogeogr,2018,45:201-212
27 Looney B P,Ryberg M,Hampe F,et al.Into and out of the tropics:Global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi.Mol Ecol,2016,25:630-647
28 Li Y C,Yang Z L,Tolgor B.Phylogenetic and biogeographic relationships of Chroogomphus species as inferred from molecular and morphological data.Fungal Divers,2009,38:85-104
29 Qin J,Horak E,Popa F,et al.Species diversity,distribution patterns,and substrate specificity of Strobilurus.Mycologia,2018,110:584-604
30 Kohler A,Kuo A,Nagy L G,et al.Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists.Nat Genet,2015,47:410-415
31 Floudas D,Binder M,Riley R,et al.The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes.Science,2012,336:1715-1719
32 Nagy L G,Riley R,Tritt A,et al.Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities.Mol Biol Evol,2016,33:959-970
33 Martinez D,Challacombe J,Morgenstern I,et al.Genome,transcriptome,and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion.Proc Natl Acad Sci USA,2009,106:1954-1959
34 Hori C,Gaskell J,Igarashi K,et al.Genomewide analysis of polysaccharides degrading enzymes in 11 white-and brown-rot Polyporales provides insight into mechanisms of wood decay.Mycologia,2013,105:1412-1427
35 Tisserant E,Malbreil M,Kuo A,et al.Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis.Proc Natl Acad Sci USA,2013,110:20117-20122
36 Peter M,Kohler A,Ohm R A,et al.Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum.Nat Commun,2016,7:12622
37 Martin F,Kohler A,Murat C,et al.Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis.Nature,2010,464:1033-1038
38 Martin F,Aerts A,Ahrén D,et al.The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis.Nature,2008,452:88-92
39 Lagrange H,Jay-Allgmand C,Lapeyrie F.Rutin,the phenolglycoside from eucalyptus root exudates,stimulates Pisolithus hyphal growth at picomolar concentrations.New Phytol,2001,149:349-355
40 Daguerre Y,Plett J M,Veneault-Fourrey C.Signaling pathways driving the development of ectomycorrhizal symbiosis.In:Martin F,ed.Molecular Mycorrhizal Symbiosis.New Jersey:Wiley Blackwell,2017.141-157
41 Vayssières A,Pěn?ík A,Felten J,et al.Development of the poplar-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism,signaling,and response.Plant Physiol,2015,169:890-902
42 Krause K,Henke C,Asiimwe T,et al.Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinumspruce ectomycorrhiza.Appl Environ Microbiol,2015,81:7003-7011
43 Felten J,Kohler A,Morin E,et al.The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling.Plant Physiol,2009,151:1991-2005
44 Ditengou F A,Müller A,Rosenkranz M,et al.Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture.Nat Commun,2015,6:6279
45 Plett K L.Fresh knowledge for an old relationship:New discoveries in molecular mycorrhizal research.New Phytol,2018,217:26-28
46 Maillet F,Poinsot V,AndréO,et al.Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Nature,2011,469:58-63
47 Gough C,Bécard G.Strigolactones and lipochitooligosaccharides as molecular communication signals in the arbuscular mycorrhizal symbiosis.In:Martin F,ed.Molecular Mycorrhizal Symbiosis.New Jersey:Wiley Blackwell,2017.107-123
48 Martin F M,Uroz S,Barker D G.Ancestral alliances:Plant mutualistic symbioses with fungi and bacteria.Science,2017,356:eaad4501
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