林木共生菌系统及其作用机制——以杨树为例
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  • 英文篇名:Tree-associated symbiotic microbes and underlying mechanisms of ecological interactions: a case study of poplar
  • 作者:袁志林 ; 潘雪玉 ; 靳微
  • 英文作者:YUAN Zhilin;PAN Xueyu;JIN Wei;Institute of Subtropical Forestry,Chinese Academy of Forestry;
  • 关键词:菌根真菌 ; 内生真菌 ; 内生细菌 ; 根际微生物组
  • 英文关键词:mycorrhizal fungi;;endophytic fungi;;endophytic bacteria;;rhizosphere microbiome
  • 中文刊名:STXB
  • 英文刊名:Acta Ecologica Sinica
  • 机构:中国林业科学研究院亚热带林业研究所;
  • 出版日期:2019-01-08
  • 出版单位:生态学报
  • 年:2019
  • 期:v.39
  • 基金:国家自然科学基金项目(31370704,31722014)
  • 语种:中文;
  • 页:STXB201901038
  • 页数:17
  • CN:01
  • ISSN:11-2031/Q
  • 分类号:385-401
摘要
杨树(Populus)是重要造林树种,也是研究林木基础生物学性状的模式材料。不仅如此,杨树可与多种细菌(内生细菌、内生固氮菌和根际促生菌)和真菌(外生菌根真菌、丛枝菌根真菌和内生真菌)类群建立共生关系,为揭示树木和微生物之间的互惠共生机制提供了理想模型。这些共生菌能积极调控林木生长发育、营养吸收和生理生态过程。目前在杨树-双色蜡蘑(Laccaria bicolor)形成的外生菌根发育、提高杨树耐盐、耐重金属的生理与分子机制、叶片内生真菌群落结构与病害发生、菌根辅助细菌和菌丝内共生细菌-真菌-杨树形成的三重跨界共生等方面取得多项突破。近年来,一批模式草本植物微生物组(microbiome)计划相继实施,对共生菌群落结构和功能的认识有了革命性的进步。以美洲黑杨、毛果杨和胶杨为代表的林木微生物组研究也已启动,表明宿主基因型和环境因子可显著影响共生菌群落结构与物种组成;在根际(rhizosphere)和内生(endosphere)环境存在结构和功能迥异的菌群。另一方面,以根系为诱饵,通过宿主表型来推测菌群功能的反向"钓鱼"策略将推动林木根际微生物工程研究,为揭示杨树-微生物群落的相互关系、菌群进化搭建了研究模型。总之,深入认识多元微生物对林木表型和生理代谢的表观遗传学调控机制将为今后创制新型菌剂并用于高效育苗和抗性育种提供新的思路,具有重要的科学意义和应用价值。
        Populus has been increasingly recognized as an important model tree genus,not only due to its wide distribution around the world and an associated great economic and ecological significance,but also the availability of several poplar genomes. Apart from these advantages,Populus is also an ideal organism for investigating physiological and molecular mechanisms underlying tree-microbe interactions,as poplar trees are able to establish multiple symbiotic relationships with a variety of microorganisms thriving in both above-and belowground tissues. Representative poplar-associated beneficial microbes include ectomycorrhizal fungi,arbuscular mycorrhizal fungi,fungal endophytes,nitrogen-fixing bacteria,and plant-growth-promoting rhizobacteria( PGPR),which generally improve poplar growth,nutrition acquisition,and different types of stress tolerance. Rapid progress has been made in understanding the molecular interactions in the development of ectomycorrhizae in the Laccaria bicolor-poplar system and the mechanisms underlying the ectomycorrhizal fungi-mediated poplar abiotic tolerance. Intriguingly,the ecological significance of mycorrhizal helper bacteria and endohyphal bacterial hasbeen recently appreciated. More importantly,a plant microbiome research project was initiated recently; it extensively revolutionizes our understanding of the structure and functions of plant-associated microbiota. The rhizosphere,endosphere,and phyllosphere microbiomes of several poplar species have been uncovered,indicating that both host genotypes and environmental factors influence the microbial community composition. It has been widely accepted that the rhizosphere and endosphere often harbor distinctive microbiota. Promisingly,the strategy of rhizosphere microbiome engineering will shed light on the contributions that soil microbial communities make in improving tree fitness under stress conditions. Looking forward,it will provide a basis for generating robust microbial inoculants that can be utilized in planting seedlings.
引文
[1] Wani N R,Malik T H. Role of poplars in agroforestry systems in India. New York Science Journal,2014,7(2):50-56.
    [2] Kecˇa L,Kecˇa N,Pantic'D. Net present value and internal rate of return as indicators for assessment of cost-efficiency of poplar plantations:a serbian case study. International Forestry Review,2012,14(2):145-156.
    [3]方升佐.中国杨树人工林培育技术研究进展.应用生态学报,2008,19(10):2308-2316.
    [4] Kecˇa N,Milenkovic'I,Kecˇa L. Mycological complex of poplars in Serbia. Journal of Forensic Sciences,2015,61(4):169-174.
    [5] Shakya M,Gottel N,Castro H,Yang Z K,Gunter L,LabbéJ,Muchero W,Bonito G,Vilgalys R,Tuskan G,Podar M,Schadt C W. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One,2013,8(10):e76382.
    [6]尹佟明,朱其慧,黄敏仁,王明庥.多年生植物模式物种基因组研究的历史及进展.植物分类学报,2004,42(5):464-479.
    [7] Ma T,Wang J Y,Zhou G K,Yue Z,Hu Q J,Chen Y,Liu B B,Qiu Q,Wang Z,Zhang J,Wang K,Jiang D C,Gou C Y,Yu L L,Zhan D L,Zhou R,Luo W C,Ma H,Yang Y Z,Pan S K,Fang D M,Luo Y D,Wang X,Wang G N,Wang J,Wang Q,Lu X,Chen Z,Liu J C,Lu Y,Yin Y,Yang H M,Abbott R J,Wu Y X,Wan D S,Li J,Yin T M,Lascoux M,Di Fazio S P,Tuskan G A,Wang J,Liu J Q. Genomic insights into salt adaptation in a desert poplar. Nature Communications,2013,4:2797.
    [8] Tuskan G A,Difazio S,Jansson S,Bohlmann J,Grigoriev I,Hellsten U,Putnam N,Ralph S,Rombauts S,Salamov A,Schein J,Sterck L,Aerts A,Bhalerao R,Bhalerao R P,Blaudez D,Boerjan W,Brun A,Brunner A,Busov V,Campbell M,Carlson J,Chalot M,Chapman J,Chen G L,Cooper D,Coutinho P M,Couturier J,Covert S,Cronk Q,Cunningham R,Davis J,Degroeve S,Déjardin A,de Pamphilis C,Detter J,Dirks B,Dubchak I,Duplessis S,Ehlting J,Ellis B,Gendler K,Goodstein D,Gribskov M,Grimwood J,Groover A,Gunter L,Hamberger B,Heinze B,Helariutta Y,Henrissat B,Holligan D,Holt R,Huang W,Islam-Faridi N,Jones S,Jones-Rhoades M,Jorgensen R,Joshi C,Kangasjrvi J,Karlsson J,Kelleher C,Kirkpatrick R,Kirst M,Kohler A,Kalluri U,Larimer F,Leebens-Mack J,LepléJ C,Locascio P,Lou Y,Lucas S,Martin F,Montanini B,Napoli C,Nelson D R,Nelson C,Nieminen K,Nilsson O,Pereda G,Peter G,Philippe R,Pilate G,Poliakov A,Razumovskaya J,Richardson P,Rinaldi C,Ritland K,RouzéP,Ryaboy D,Schmutz J,Schrader J,Segerman B,Shin H,Siddiqui A,Sterky F,Terry A,Tsai C,Uberbacher E,Unneberg P,Vahala J,Wall K,Wessler S,Yang G,Yin T,Douglas C,Marra M,Sandberg G,Van de Peer Y,Rokhsar D. The genome of black cottonwood,Populus trichocarpa(Torr.&Gray). Science,2006,313(5793):1596-1604.
    [9] Jansson S,Douglas C J. Populus:a model system for plant biology. Annual Review of Plant Biology,2007,58:435-458.
    [10] Bulgarelli D,Schlaeppi K,Spaepen S,van Themaat E V L,Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology,2013,64:807-838.
    [11] Utturkar S M,Cude W N,Robeson M S Jr,Yang Z K,Klingeman D M,Land M L,Allman S L,Lu T Y S,Brown S D,Schadt C W,Podar M,Doktycz M J,Pelletier D A. Enrichment of root endophytic bacteria from Populus deltoides and single-cell-genomics analysis. Applied and Environmental Microbiology,2016,82(18):5698-5708.
    [12] Hacquard S,Schadt C W. Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytologist,2015,205(4):1424-1430.
    [13] Hollis J P. Bacteria in healthy potato tissue. Phytopathology,1951,41:350-366.
    [14] Wilson D. Endophyte:the evolution of a term,and clarification of its use and definition. Oikos,1995,73(2):274-276.
    [15] Kloepper J W,Schroth M N. Plant growth-promoting rhizobacteria on radishes//Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. Tours:Gilbert-Clary,1978:879-882.
    [16] Rosenblueth M,Martínez-Romero E. Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions,2006,19(8):827-837.
    [17] Ulrich K,Ulrich A,Ewald D. Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiology Ecology,2008,63(2):169-180.
    [18] Fang W,Li Y,Xue H,Tian G Z,Wang L F,Guo M W,Piao C G. Corticibacter populi gen. nov.,sp. nov.,a new member of the family Comamonadaceae,from the bark of Populus euramericana. International Journal of Systematic and Evolutionary Microbiology,2015,65(10):3333-3338.
    [19]吾尔麦提汗·麦麦提明,卡依尔·玉素甫,热孜亚·艾肯,布阿依夏姆·阿木提,努丽曼姑·司马义,买孜拉木·肉扎洪,麦合甫再木·阿布都热合曼,马相汝,艾尔肯·热合曼.塔里木胡杨林可培养胡杨内生细菌多样性与群落结构的时空演变格局.生态学报,2014,34(22):6622-6639.
    [20]胥丽娜,徐亮,李磊,邹玉峰,赵春青,张卫光,刘振宇.枯草芽孢杆菌对杨树水泡溃疡病菌菌丝生长的抑制作用.菌物研究,2007,5(3):165-168.
    [21]陈越渠,李立梅,毛赫,张立民,王牧原,李殿锋,张晓军.杨树烂皮病内生拮抗菌的筛选及鉴定.植物保护,2015,41(6):126-131.
    [22] Moore F P,Barac T,Borremans B,Oeyen L,Vangronsveld J,Van Der Lelie D,Campbell C D,Moorea E R B. Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site:the characterisation of isolates with potential to enhance phytoremediation. Systematic and Applied Microbiology,2006,29(7):539-556.
    [23] Van Der Lelie D,Taghavi S,Monchy S,Schwender J,Miller L,Ferrieri R,Rogers A,Wu X,Zhu W,Weyens N,Vangronsveld J,Newman L.Poplar and its bacterial endophytes:coexistence and harmony. Critical Reviews in Plant Sciences,2009,28(5):346-358.
    [24] Kang J W,Khan Z,Doty S L. Biodegradation of trichloroethylene by an endophyte of hybrid poplar. Applied and Environmental Microbiology,2012,78(9):3504-3507.
    [25] Ryan R P,Germaine K,Franks A,Ryan D J,Dowling D N. Bacterial endophytes:recent developments and applications. FEMS Microbiology Letters,2008,278(1):1-9.
    [26] Zhu D L,Ouyang L M,Xu Z H,Zhang L L. Rhizobacteria of Populus euphratica promoting plant growth against heavy metals. International Journal of Phytoremediation,2015,17(10):973-980.
    [27]李冠喜,吴小芹,叶建仁.多噬伯克霍尔德氏菌WS-J9对杨树光合作用和生物量的影响.浙江农林大学学报,2014,31(4):570-576.
    [28] Timm C M,Campbell A G,Utturkar S M,Jun S R,Parales R E,Tan W A,Robeson M S,Lu T Y S,Jawdy S,Brown S D,Ussery D W,Schadt C W,Tuskan G A,Doktycz M J,Weston D J,Pelletier D A. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. Frontiers in Microbiology,2015,6(27):1118.
    [29] Henning J A,Weston D J,Pelletier D A,Timm C M,Jawdy S S,Classen A T. Root bacterial endophytes alter plant phenotype,but not physiology. PeerJ,2016,4(8):e2606.
    [30] Taghavi S,Garafola C,Monchy S,Newman L,Hoffman A,Weyens N,Barac T,Vangronsveld J,Van Der Lelie D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Applied and Environmental Microbiology,2009,75(3):748-757.
    [31] Timm C M,Pelletier D A,Jawdy S S,Gunter L E,Henning J A,Engle N,Aufrecht J,Gee E,Nookaew I,Yang Z M,Lu T Y,Tschaplinski T J,Doktycz M J,Tuskan G A,Weston D J. Two poplar-associated bacterial isolates induce additive favorable responses in a constructed plantmicrobiome system. Frontiers in Plant Science,2016,7:497.
    [32] Doty S L,Dosher M R,Singleton G L,Moore A L,Van Aken B,Stettler R F,Strand S E,Gordon M P. Identification of an endophytic Rhizobium in stems of Populus. Symbiosis,2005,39(1):27-35.
    [33] Doty S L,Oakley B,Xin G,Kang J W,Singleton G,Khan Z,Vajzovic A,Staley J T. Diazotrophic endophytes of native black cottonwood and willow. Symbiosis,2009,47(1):23-33.
    [34] Kandel S L,Herschberger N,Kim S H,Doty S L. Diazotrophic endophytes of poplar and willow for growth promotion of rice plants in nitrogenlimited conditions. Crop Science,2015,55(4):1765-1772.
    [35] Khan Z,Rho H,Firrincieli A,Hung S H,Luna V,Masciarelli O,Kim S H,Doty S L. Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Current Plant Biology,2016,6:38-47.
    [36] Knoth J L,Kim S H,Ettl G J,Doty S L. Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytologist,2014,201(2):599-609.
    [37] Khan Z,Guelich G,Phan H,Redman R,Doty S. Bacterial and yeast endophytes from poplar and willow promote growth in crop plants and grasses.ISRN Agronomy,2012,2012:890280.
    [38] Doty S L,Sher A W,Fleck N D,Khorasani M,Bumgarner R E,Khan Z,Ko A W K,Kim S H,De Luca T H. Variable nitrogen fixation in wild Populus. PLoS One,2016,11(5):e0155979.
    [39]赵秀云,韩素芬.杨树根际固氮菌的分离、筛选和鉴定.南京林业大学学报,2000,24(3):17-20.
    [40] Xin G,Zhang G Y,Kang J W,Staley J T,Doty S L. A diazotrophic,indole-3-acetic acid-producing endophyte from wild cottonwood. Biology and Fertility of Soils,2009,45(6):669-674.
    [41] Xin G,Glawe D,Doty S L. Characterization of three endophytic,indole-3-acetic acid-producing yeasts occurring in Populus trees. Mycological Research,2009,113(9):973-980.
    [42] Knoth J L,Kim S H,Ettl G J,Doty S L. Effects of cross host species inoculation of nitrogen-fixing endophytes on growth and leaf physiology of maize. GCB Bioenergy,2013,5(4):408-418.
    [43] Szuba A. Ectomycorrhiza of Populus. Forest Ecology and Management,2015,347:156-169.
    [44]赵之伟.菌根真菌在陆地生态系统中的作用.生物多样性,1999,7(3):240-244.
    [45]梁宇,郭良栋,马克平.菌根真菌在生态系统中的作用.植物生态学报,2002,26(6):739-745.
    [46]于富强,刘培贵.外生菌根研究及应用的回顾与展望.生态学报,2002,22(12):2217-2226.
    [47]花晓梅.林木菌根生物工程.世界林业研究,2001,14(1):22-29.
    [48] Taylor A F S,Alexander I. The ectomycorrhizal symbiosis:life in the real world. Mycologist,2005,19(3):102-112.
    [49] Miller R M,Jastrow J D. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biology and Biochemistry,1990,22(5):579-584.
    [50]朱教君,徐慧,许美玲,康宏樟.外生菌根菌与森林树木的相互关系.生态学杂志,2003,22(6):70-76.
    [51] Cripps C,Miller O K Jr. Ectomycorrhizal fungi associated with aspen on three sites in the north-central Rocky Mountains. Canadian Journal of Botany,1993,71(11):1414-1420.
    [52] Jakucs E,Kovács G M,Agerer R,Romsics C,Er9s-Honti Z. Morphological-anatomical characterization and molecular identification of Tomentella stuposa ectomycorrhizae and related anatomotypes. Mycorrhiza,2005,15(4):247-258.
    [53] Kovács G M,Jakucs E. Morphological and molecular comparison of white truffle ectomycorrhizae. Mycorrhiza,2006,16(8):567-574.
    [54] Katanic'M,Grebenc T,Orlovi c'S,Matavuly M,Kova cˇevi c'B,Bajc M,Kraigher H. Ectomycorrhizal fungal community associated with autochthonous white poplar from Serbia. i Forest-Biogeosciences and Forestry,2015,9:330-336.
    [55] Gryta H,Carriconde F,Charcosset J Y,Jargeat P,Gardes M. Population dynamics of the ectomycorrhizal fungal species Tricholoma populinum and Tricholoma scalpturatum associated with black poplar under differing environmental conditions. Environmental Microbiology,2006,8(5):773-786.
    [56] Cripps C L. Native mycorrhizal fungi with aspen on smelter-impacted sites in the Northern Rocky Mountains:occurrence and potential use in reclamation//National Meeting of the American Society of Mining and Reclamation and the 9th Billings Land Reclamation Symposium. Lexington,KY,USA:ASMR,2003:193-208.
    [57] Cripps C L. Ectomycorrhizal fungi above and below ground in a small,isolated aspen stand:a simple system reveals fungal fruiting strategies and an edge effect//Cripps C L,ed. Fungi in Forest Ecosystems:Systematics,Diversity,and Ecology. New York:The New York Botanical Garden,2004:249-265.
    [58] De Bellis T,Kernaghan G,Bradley R,Widden P. Relationships between stand composition and ectomycorrhizal community structure in boreal mixed-wood forests. Microbial Ecology,2006,52(1):114-126.
    [59] Long D F,Liu J J,Han Q S,Wang X B,Huang J. Ectomycorrhizal fungal communities associated with Populus simonii and Pinus tabuliformis in the hilly-gully region of the Loess Plateau,China. Scientific Reports,2016,6:24336.
    [60] Stefani F O P,Moncalvo J M,Séguin A,BérubéJ A,Hamelin R C. Impact of an 8-year-old transgenic poplar plantation on the ectomycorrhizal fungal community. Applied and Environmental Microbiology,2009,75(23):7527-7536.
    [61] Danielsen L,Lohaus G,Sirrenberg A,Karlovsky P,Bastien C,Pilate G,Polle A. Ectomycorrhizal colonization and diversity in relation to tree biomass and nutrition in a plantation of transgenic poplars with modified lignin biosynthesis. PLoS One,2013,8(3):e59207.
    [62] Danielsen L,Thürmer A,Meinicke P,Buée M,Morin E,Martin F,Pilate G,Daniel R,Polle A,Reich M. Fungal soil communities in a young transgenic poplar plantation form a rich reservoir for fungal root communities. Ecology and Evolution,2012,2(8):1935-1948.
    [63] Kaldorf M,Renker C,Fladung M,Buscot F. Characterization and spatial distribution of ectomycorrhizas colonizing aspen clones released in an experimental field. Mycorrhiza,2004,14(5):295-306.
    [64] Lacercat-Didier L,Berthelot C,Foulon J,Errard A,Martino E,Chalot M,Blaudez D. New mutualistic fungal endophytes isolated from poplar roots display high metal tolerance. Mycorrhiza,2016,26(7):657-671.
    [65] Bois G,PichéY,Fung M Y P,Khasa D P. Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza,2005,15(3):149-158.
    [66] Martin F,Aerts A,Ahrén D,Brun A,Danchin E G J,Duchaussoy F,Gibon J,Kohler A,Lindquist E,Pereda V,Salamov A,Shapiro H J,Wuyts J,Blaudez D,Buée1 M,Brokstein P,Canbck B,Cohen D,Courty P E,Coutinho P M,Delaruelle C,Detter J C,Deveau A,Di Fazio S,Duplessis S,Fraissinet-Tachet L,Lucic E,Frey-Klett P,Fourrey C,Feussner I,Gay G,Grimwood J,Hoegger P J,Jain P,Kilaru S,LabbéJ,Lin YC,LeguéV,Le Tacon F,Marmeisse R,Melayah D,Montanini B,Muratet M,Nehls U,Niculita-Hirzel H,Oudot-Le Secq M P,Peter M,Quesneville H,Rajashekar B,Reich M,Rouhier N,Schmutz J,Yin T,Chalot M,Henrissat B,Kües U,Lucas S,Van De Peer Y,Podila G K,Polle A,Pukkila P J,Richardson P M,RouzéP,Sanders I R,Stajich J E,Tunlid A,Tuskan G,Grigoriev I V. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature,2008,452(7183):88-92.
    [67] Ditengou F A,Müller A,Rosenkranz M,Felten J,Lasok H,Van Doorn M M,LeguéV,Palme K,Schnitzle J P,Polle A. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nature Communications,2015,6:6279.
    [68] Plett J M,Yin H F,Mewalal R,Hu R B,Li T,Ranjan P,Jawdy S,De Paoli H C,Butler G,Burch-Smith T M,Guo H B,Chen C J,Kohler A,Anderson I C,LabbéJ L,Martin F,Tuskan G A,Yang X H. Populus trichocarpa encodes small,effector-like secreted proteins that are highly induced during mutualistic symbiosis. Scientific Reports,2017,7(1):382.
    [69] Plett J M,Kemppainen M,Kale S D,Kohler A,LeguéV,Brun A,Tyler B M,Pardo A G,Marti F. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology,2011,21(14):1197-1203.
    [70] Plett J M,Daguerre Y,Wittulsky S,Vayssières A,Deveau A,Melton S J,Kohler A,Morrell-Falvey J L,Brun A,Veneault-Fourrey C,Martin F.Effector Mi SSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid(JA)responsive genes.Proceedings of the National Academy of Sciences of the United States of America,2014,111(22):8299-8304.
    [71] Martin F,Kohler A,Murat C,Veneault-Fourrey C,Hibbett D S. Unearthing the roots of ectomycorrhizal symbioses. Nature Reviews Microbiology,2016,14(12):760-773.
    [72] Zhang H,Li J,Chen S L,Lu C F,Wang R G,Dai S X,Zhu H J,Zhang Y X,Shi Y,Wang M J,Lu Y J,Li L S,Langenfeld-Heyser R,Eberhard F,Polle A. Effect of Na Cl on growth and ion relations in two salt-tolerant strains of Paxillus involutus. Forestry Studies in China,2008,10(2):95-100.
    [73] Gafur A,Schützendübel A,Langenfeld-Heyser R,Fritz E,Polle A. Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar(Populus×canescens)differ in H2O2production. Plant Biology,2004,6(1):91-99.
    [74] Langenfeld-Heyser R,Gao J,Ducic T,Tachd P,Lu C F,Fritz E,Gafur A,Polle A. Paxillus involutus mycorrhiza attenuate Na Cl-stress responses in the salt-sensitive hybrid poplar Populus×canescens. Mycorrhiza,2007,17(2):121-131.
    [75] Luo Z B,Li K,Gai Y,G9beld C,Wildhagen H N,Jiang X N,Feunerd I,Rennenberg H,Polle A. The ectomycorrhizal fungus(Paxillus involutus)modulates leaf physiology of poplar towards improved salt tolerance. Environmental and Experimental Botany,2011,72(2):304-311.
    [76] Li J,Bao S Q,Zhang Y H,Ma X J,Mishra-Knyrim M,Sun J,Sa G,Shen X,Polle A,Chen S L. Paxillus involutus strains MAJ and NAU mediate K+/Na+homeostasis in ectomycorrhizal Populus×canescens under sodium chloridestress. Plant Physiology,2012,159(4):1771-1786.
    [77] Ma X J,Sun M,Sa G,Zhang Y H,Li J,Sun J,Shen X,Polle A,Chen S L. Ion fluxes in Paxillus involutus-inoculated roots of Populus×canescens under saline stress. Environmental and Experimental Botany,2014,108:99-108.
    [78] Luo Z B,Li K,Jiang X N,Polle A. Ectomycorrhizal fungus(Paxillus involutus)and hydrogels affect performance of Populus euphratica exposed to drought stress. Annals of Forest Science,2009,66(1):106-106.
    [79] Szuba A,Karliński L,Krzesowska M,Hazubska-PrzybyT. Inoculation with a Pb-tolerant strain of Paxillus involutus improves growth and Pb tolerance of Populus×canescens under in vitro conditions. Plant and Soil,2017,412(1/2):253-266.
    [80] Ma Y L,He J L,Ma C F,Luo J,Li H,Liu T X,Polle A,Peng C H,Luo Z B. Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus×canescens. Plant,Cell and Environment,2014,37(3):627-642.
    [81] Zhang Y H,Sa G,Zhang Y N,Zhu Z M,Deng S R,Sun J,Li N F,Li J,Yao J,Zhao N,Zhao R,Ma X J,Polle A,Chen S L. Paxillus involutus-facilitated Cd2+influx through plasma membrane Ca2+-permeable channels is stimulated by H2O2and H+-ATPase in ectomycorrhizal Populus×canescens under cadmium stress. Frontiers in Plant Science,2017,7:1975.
    [82] Jiang Y N,Wang W X,Xie Q J,Liu N,Liu L X,Wang D P,Zhang X W,Yang C,Chen X Y,Tang D Z,Wang E T. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science,2017,356(6343):1172-1175.
    [83] Liu T,Wang C Y,Chen H,Fang F R,Zhu X Q,Tang M. Effects of arbuscular mycorrhizal colonization on the biomass and bioenergy production of Populus×canadensis‘Neva’in sterilized and unsterilized soil. Acta Physiologiae Plantarum,2014,36(4):871-880.
    [84] Rooney D C,Prosser J I,Bending G D,Baggs E M,Killham K,Hodge A. Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy. Biomass and Bioenergy,2011,35(11):4605-4612.
    [85] Liu T,Li Z,Hui C,Tang M,Zhang H Q. Effect of Rhizophagus irregularis on osmotic adjustment,antioxidation and aquaporin PIP genes expression of Populus×canadensis‘Neva’under drought stress. Acta Physiologiae Plantarum,2016,38(8):191.
    [86] Wu N,Li Z,Wu F,Tang M. Comparative photochemistry activity and antioxidant responses in male and female Populus cathayana cuttings inoculated with arbuscular mycorrhizal fungi under salt. Scientific Reports,2016,6:37663.
    [87] Li Z,Wu N,Liu T,Chen H,Tang M. Sex-related responses of Populus cathayana shoots and roots to AM fungi and drought stress. PLoS One,2015,10(6):e0128841.
    [88] Chen L H,Zhang D J,Yang W Q,Liu Y,Zhang L,Gao S. Sex-specific responses of Populus deltoides to Glomus intraradices colonization and Cd pollution. Chemosphere,2016,155:196-206.
    [89]陈娟,李春阳.漫谈雌雄异株植物.生命世界,2015,(11):40-45.
    [90] Calabrese S,Kohler A,Niehl A,Veneault-Fourrey C,Boller T,Courty P E. Transcriptome analysis of the Populus trichocarpa-Rhizophagus irregularis mycorrhizal symbiosis:regulation of plant and fungal transportomes under nitrogen starvation. Plant and Cell Physiology,2017,58(6):1003-1017.
    [91] Neville J,Tessier J L,Morrison I,Scarratt J,Canning B,Klironomos J N. Soil depth distribution of ecto-and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Applied Soil Ecology,2002,19(3):209-216.
    [92] Gehring C A,Mueller R C,Whitham T G. Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia,2006,149(1):158-164.
    [93] Comas L H,Callahan H S,Midford P E. Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas:implications for the evolution of belowground strategies. Ecology and Evolution,2014,4(15):2979-2990.
    [94] Chen Y L,Brundrett M C,Dell B. Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas,alone or in competition,on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytologist,2000,146(3):545-555.
    [95] Lodge D J. Ecto-or arbuscular mycorrhizas-which are best? New Phytologist,2000,146(3):353-354.
    [96]赵桂华,石立岩,杨怀光,孟庆兰,闵祥宏.杨树内生真菌的分离和鉴定.南京林业大学学报:自然科学版,2008,32(2):76-78.
    [97]袁秀英,白红霞,白玉明,呼达古拉,刘俊霞.杨树内生真菌的分离和拮抗生防菌的筛选.林业科学研究,2006,19(6):713-717.
    [98]白红霞,袁秀英.内蒙古地区杨树内生真菌多样性调查.浙江林学院学报,2006,23(6):629-635.
    [99]李永,朴春根,贺伟,常聚普,王海明,郭立民,谢守江,郭民伟. 2个欧美杨品种树皮内生真菌多样性及优势种群动态变化.林业科学,2013,49(6):90-96.
    [100] Yan D H,Gao Q,Sun X M,Song X Y,Li H C. ITS2 sequence-structure phylogeny reveals diverse endophytic Pseudocercospora fungi on poplars.Genetica,2018,146(2):187-198.
    [101] Unterseher M,Petzold A,Schnittler M. Xerotolerant foliar endophytic fungi of Populus euphratica from the Tarim River basin,Central China are conspecific to endophytic ITS phylotypes of Populus tremula from temperate Europe. Fungal Diversity,2012,54(1):133-142.
    [102] Doty S L. Growth-promoting endophytic fungi of forest trees//PirttilA M,Frank A C,eds. Endophytes of Forest Trees:Biology and Applications.Dordrecht,Netherlands:Springer,2011:151-156.
    [103] Martín-García J,Müller M M,Diez J J. ITS-based comparison of endophytic mycota in twigs of native Populus nigra and cultivated P. x euramericana(cv. I-214)stands in northern Spain. Annals of Forest Science,2012,69(1):49-57.
    [104] Bonito G,Hameed K,Ventura R,Krishnan J,Schadt C W,Vilgalys R. Isolating a functionally relevant guild of fungi from the root microbiome of Populus. Fungal Ecology,2016,22:35-42.
    [105] Bonito G,Hameed K,Toome-Heller M,Healy R,Reid C,Liao H L,Aime M C,Schadt C,Vilgalys R. Atractiella rhizophila,sp. nov.,an endorrhizal fungus isolated from the Populus root microbiome. Mycologia,2017,109(1):18-26.
    [106] Vélez J M,Tschaplinski T J,Vilgalys R,Schadt C W,Bonito G,Hameed K,Engle N,Hamilton C E. Characterization of a novel,ubiquitous fungal endophyte from the rhizosphere and root endosphere of Populus trees. Fungal Ecology,2017,27:78-86.
    [107] Jumpponen A,Trappe J M. Dark septate endophytes:a review of facultative biotrophic root-colonizing fungi. New Phytologist,1998,140(2):295-310.
    [108] Mandyam K,Jumpponen A. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in Mycology,2005,53:173-189.
    [109] Berthelot C,Leyval C,Foulon J,Chalot M,Blaudez D. Plant growth promotion,metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiology Ecology,2016,92(10):fiw144.
    [110] Berthelot C,Blaudez D,Leyval C. Differential growth promotion of poplar and birch inoculated with three dark septate endophytes in two trace element-contaminated soils. International Journal of Phytoremediation,2017,19(12):1118-1125.
    [111] Pan X Y,Qin Y,Yuan Z L. Potential of a halophyte-associated endophytic fungus for sustaining Chinese white poplar growth under salinity.Symbiosis,2018,doi:10.1007/s13199-018-0541-8.
    [112] Arnold A E,Mejía L C,Kyllo D,Rojas E I,Maynard Z,Robbins N,Herre E A. Fungal endophytes limit pathogen damage in a tropical tree.Proceedings of the National Academy of Sciences of the United States of America,2003,100(26):15649-15654.
    [113] Mejia L C,Herre E A,Sparks J P,Winter K,García M N,Van Bael S A,Stitt J,Shi Z,Zhang Y F,Guiltinan M J,Maximova S N. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology,2014,5:479.
    [114] Raghavendra A K H,Newcombe G. The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytologist,2013,197(3):909-918.
    [115] Busby P E,Zimmerman N,Weston D J,Jawdy S S,Houbraken J,Newcombe G. Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen,Drepanopeziza populi. Ecosphere,2013,4(10):1-12.
    [116] Busby P E,Peay K G,Newcombe G. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytologist,2016,209(4):1681-1692.
    [117] Albrectsen B R,Bj9rkén L,Varad A,Hagner,Wedin M,Karlsson J,Jansson S. Endophytic fungi in European aspen(Populus tremula)leaves-diversity,detection,and a suggested correlation with herbivory resistance. Fungal Diversity,2010,41(1):17-28.
    [118] Kaldorf M,Koch B,Rexer K H,Kost G,Varma A. Patterns of interaction between Populus Esch5 and Piriformospora indica:a transition from mutualism to antagonism. Plant Biology,2005,7(2):210-218.
    [119] Qin Y,Pan X Y,Kubicek C,Druzhinina I,Chenthamara K,LabbéJ,Yuan Z L. Diverse plant-associated pleosporalean fungi from saline areas:ecological tolerance and nitrogen-status dependent effects on plant growth. Frontiers in Microbiology,2017,8:158.
    [120] Lundberg D S,Lebeis S L,Paredes S H,Yourstone S,Gehring J,Malfatti S,Tremblay J,Engelbrektson A,Kunin V,Del Rio T G,Edgar R C,Eickhorst T,Ley R E,Hugenholtz P,Tringe S G,Dangl J L. Defining the core Arabidopsis thaliana root microbiome. Nature,2012,488(7409):86-90.
    [121] Bulgarelli D,Rott M,Schlaeppi K,Van Themaat E V L,Ahmadinejad N,Assenza F,Rauf P,Huettel B,Reinhardt R,Schmelzer E,Peplies J,Gloeckner F O,Amann R,Eickhorst T,Schulze-Lefert P. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature,2012,488(7409):91-95.
    [122] Peiffer J A,Spor A,Koren O,Zhao J,Tringe S G,Dangl J L,Buckler E S,Ley R E. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America,2013,110(16):6548-6553.
    [123] Bai Y,Müller D B,Srinivas G,Garrido-Oter R,Potthoff E,Rott M,Dombrowski N,Münch P C,Spaepen S,Remus-Emsermann M,Hüttel B,Mc Hardy A C,Vorholt J A,Schulze-Lefert P. Functional overlap of the Arabidopsis leaf and root microbiota. Nature,2015,528(7582):364-369.
    [124] Bulgarelli D,Garrido-Oter R,Münch P C,Weiman A,Dr9ge J,Pan Y,Mc Hardy A C,Schulze-Lefert P. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host&Microbe,2015,17(3):392-403.
    [125] Gottel N R,Castro H F,Kerley M,Yang Z M,Pelletier D A,Podar M,Karpinets T,Uberbacher E,Tuskan G A,Vilgalys R,Doktycz M J,Schadt C W. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Applied and Environmental Microbiology,2011,77(17):5934-5944.
    [126] Bálint M,Tiffin P,Hallstr9m B,O'Hara R B,Olson M S,Fankhauser J D,Piepenbring M,Schmitt I. Host genotype shapes the foliar fungal microbiome of balsam poplar(Populus balsamifera). PLoS One,2013,8(1):e53987.
    [127] Bálint M,Bartha L,O'Hara R B,Olson M S,Otte J,Pfenninger M,Robertson A L,Tiffin P,Schmitt I. Relocation,high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Molecular Ecology,2015,24(1):235-248.
    [128] Zhu W X,Chu Y G,Ding C J,Huang Q J,Zhang B Y,Zhang W X,Su X H. Assessing bacterial communities in the rhizosphere of 8-year-old genetically modified poplar(Populus spp.). Journal of Forestry Research,2016,27(4):939-947.
    [129] Hur M,Lim Y W,Yu J J,Cheon S U,Choi Y M,Yoon S H,Park S C,Kim D I,Yi H N. Fungal community associated with genetically modified poplar during metal phytoremediation. Journal of Microbiology,2012,50(6):910-915.
    [130] Beckers B,De Beeck M O,Weyens N,Van Acker R,Van Montagu M,Boerjan W,Vangronsveld J. Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome. Proceedings of the National Academy of Sciences of the United States of America,2016,113(8):2312-2317.
    [131] Morris M H,Pérez-Pérez M A,Smith M E,Bledsoe C S. Multiple species of ectomycorrhizal fungi are frequently detected on individual oak root tips in a tropical cloud forest. Mycorrhiza,2008,18(8):375-383.
    [132] Deveau A,LabbéJ. Mycorrhiza helper bacteria//Martin F,ed. Molecular Mycorrhizal Symbiosis. New York,NJ:Wiley-Blackwell,2016:437-450.
    [133] LabbéJ L,Weston D J,Dunkirk N,Pelletier D A,Tuskan G A. Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus.Frontiers in Plant Science,2014,5:579.
    [134] Frey-Klett P,Garbaye J. Mycorrhiza helper bacteria:a promising model for the genomic analysis of fungal-bacterial interactions. New Phytologist,2005,168(1):4-8.
    [135] Zhao L,Wu XQ,Ye J R,Li H,Li G E. Isolation and characterization of a mycorrhiza helper bacterium from rhizosphere soils of poplar stands.Biology and Fertility of Soils,2014,50(4):593-601.
    [136] Uehling J,Gryganskyi A,Hameed K,Tschaplinski T,Misztal P K,Wu S,DesiròA,Vande Pol N,Du Z,Zienkiewicz A,Zienkiewicz K,Morin E,Tisserant E,Splivallo R,Hainaut M,Henrissat B,Ohm R,Kuo A,Yan J,Lipzen A,Nolan M,La Butti K,Barry K,Goldstein A H,LabbéJ,Schadt C,Tuskan G,Grigoriev I,Martin F,Vilgalys R,Bonito G. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environmental Microbiology,2017,19(8):2964-2983.
    [137] Li Z,Yao Q M,Dearth S P,Entler M R,Gonzalez H F C,Uehling J K,Vilgalys R J,Hurst G B,Campagna S R,LabbéJ L,Pan C L.Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal-endobacterial system. Environmental Microbiology,2017,19(3):1041-1053.
    [138] Partida-Martínez L P. The fungal holobiont:evidence from early diverging fungi. Environmental Microbiology,2017,19(8):2919-2923.
    [139] Niu B,Paulson J N,Zheng X Q,Kolter R. Simplified and representative bacterial community of maize roots. Proceedings of the National Academy of Sciences of the United States of America,2017,114(12):E2450-E2459.
    [140] Panke-Buisse K,Poole A C,Goodrich J K,Ley R E,Kao-Kniffin J. Selection on soil microbiomes reveals reproducible impacts on plant function.The ISME Journal,2015,9(4):980-989.
    [141] Mueller U G,Sachs J L. Engineering microbiomes to improve plant and animal health. Trends in Microbiology,2015,23(10):606-617.

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