Diversity of the endophytic filamentous fungal leaf community at different development stages of eucalyptus
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摘要
Fungal endophytic species inhabiting the leaves of eucalypts are capable of utilising leaf sugars and can influence both plant growth and health. Endophytic fungal symbionts can use simple soluble sugars in leaves as their main carbon source. This study set out to determine the diversity and distribution of the endophytic filamentous fungal leaf community in the hybrid Eucalyptus urograndis due to its economic importance. The fungal leaf community was characterised using denaturing gradient electrophoresis(DGGE) and correlated with levels of leaf nutrients and sugars throughout plant development.Sequencing of DGGE bands revealed the presence of Basidiomycota and Ascomycota phyla. Fourteen species and three genera of filamentous fungi were identified, and the population structure was affected by the plant developmental stage. Levels of K, Cu, N and Mn influenced communities from the clonal garden, whereas leaves in the field had higher glucose, fructose and sucrose. Many fungi were found to be specific to a certain development stages:Diplomitoporus crustulinus, Podosphaera tridactyla and Aspergillus restrictus to the clonal garden stage; Chaetomella acutiseta and Ascotricha chartarum to the shading stage; Erratomyces patelii and Saxomyces sp. to the shading output stage; Lepidostroma sp. and Saxomyces sp. to the dispatch stage; and Mycosphaerella populicola to the field stage. Teratosphaeria toledana and Teratosphaeria acidotherma were found at more than one developmental stage. Cladosporium sp. and Rhodosporidium fluviale colonized and persisted in plants at the dispatch and field stages. This is the first report of P. tridactyla, A. restrictus,E. patelii, Saxomyces and Lepidostroma sp. as endophytes in eucalipt.
Fungal endophytic species inhabiting the leaves of eucalypts are capable of utilising leaf sugars and can influence both plant growth and health. Endophytic fungal symbionts can use simple soluble sugars in leaves as their main carbon source. This study set out to determine the diversity and distribution of the endophytic filamentous fungal leaf community in the hybrid Eucalyptus urograndis due to its economic importance. The fungal leaf community was characterised using denaturing gradient electrophoresis(DGGE) and correlated with levels of leaf nutrients and sugars throughout plant development.Sequencing of DGGE bands revealed the presence of Basidiomycota and Ascomycota phyla. Fourteen species and three genera of filamentous fungi were identified, and the population structure was affected by the plant developmental stage. Levels of K, Cu, N and Mn influenced communities from the clonal garden, whereas leaves in the field had higher glucose, fructose and sucrose. Many fungi were found to be specific to a certain development stages:Diplomitoporus crustulinus, Podosphaera tridactyla and Aspergillus restrictus to the clonal garden stage; Chaetomella acutiseta and Ascotricha chartarum to the shading stage; Erratomyces patelii and Saxomyces sp. to the shading output stage; Lepidostroma sp. and Saxomyces sp. to the dispatch stage; and Mycosphaerella populicola to the field stage. Teratosphaeria toledana and Teratosphaeria acidotherma were found at more than one developmental stage. Cladosporium sp. and Rhodosporidium fluviale colonized and persisted in plants at the dispatch and field stages. This is the first report of P. tridactyla, A. restrictus,E. patelii, Saxomyces and Lepidostroma sp. as endophytes in eucalipt.
Fungal endophytic species inhabiting the leaves of eucalypts are capable of utilising leaf sugars and can influence both plant growth and health. Endophytic fungal symbionts can use simple soluble sugars in leaves as their main carbon source. This study set out to determine the diversity and distribution of the endophytic filamentous fungal leaf community in the hybrid Eucalyptus urograndis due to its economic importance. The fungal leaf community was characterised using denaturing gradient electrophoresis(DGGE) and correlated with levels of leaf nutrients and sugars throughout plant development.Sequencing of DGGE bands revealed the presence of Basidiomycota and Ascomycota phyla. Fourteen species and three genera of filamentous fungi were identified, and the population structure was affected by the plant developmental stage. Levels of K, Cu, N and Mn influenced communities from the clonal garden, whereas leaves in the field had higher glucose, fructose and sucrose. Many fungi were found to be specific to a certain development stages:Diplomitoporus crustulinus, Podosphaera tridactyla and Aspergillus restrictus to the clonal garden stage; Chaetomella acutiseta and Ascotricha chartarum to the shading stage; Erratomyces patelii and Saxomyces sp. to the shading output stage; Lepidostroma sp. and Saxomyces sp. to the dispatch stage; and Mycosphaerella populicola to the field stage. Teratosphaeria toledana and Teratosphaeria acidotherma were found at more than one developmental stage. Cladosporium sp. and Rhodosporidium fluviale colonized and persisted in plants at the dispatch and field stages. This is the first report of P. tridactyla, A. restrictus,E. patelii, Saxomyces and Lepidostroma sp. as endophytes in eucalipt.
引文
Altschul SF,Gish W,Miller W,Myers EW,Lipman DJ(1990)Basic local alignment search tool.J Mol Biol 215:403-410
Andjic V,Whyte G,Hardy G,Burgess T(2010)New Teratosphaeria species occurring on eucalypts in Australia.Fungal Diver43:27-38
Andrews JH,Harris RF,Spear RN,Lau GW,Nordheim EV(1994)Morphogenesis and adhesion of Aureobasidium pullulans.Can JMicrobiol 40:6-17
Arnold AE(2005)Diversity and ecology of fungal endophytes in tropical forests.In:Deshmukh S(ed)Current trends in mycological research.Oxford&IBH Publishing Co.Pvt.Ltd.,New Delhi,pp 49-68
Arnold AE,Herre EA(2003)Canopy cover and leaf age affect colonization by tropical fungal endophytes:ecological pattern and process in Theobroma cacao(Malvaceae).Mycol95:388-398
Arnold AE,Lutzoni F(2007)Diversity and host range of foliar fungal endophytes:are tropical leaves biodiversity hotspots?Ecology88:541-549
Arnold AE,Maynard Z,Gilbert GS,Coley PD,Kursar TA(2000)Are tropical fungal endophytes hyperdiverse?Ecol Lett 3:267-274
Bago B,Pfeffer PE,Shachar-Hill Y(2000)Carbon metabolism and transport in arbuscular mycorrhizas.Plant Physiol 124:949-958
Bremner JM,Mulvaney CS(1982)Total nitrogen.In:Page AL(ed)Methods of soil analysis.American Society of Agronomy,Madison,pp 595-624
Bresolin JD,Bustamante MMC,Krüger RH,Silva MRSS,Perez KS(2010)Structure and composition of bacterial and fungal community in soil under soybean monoculture in the Brazilian cerrado.Braz J Microbiol 41:391-403
Brooker MIH(2000)A new classification of the genus Eucalyptus L’Her(Myrtaceae).Aust Syst Bot 13:79-148
Brundrett MC(2006)Understanding the roles of multifunctional mycorrhizal and endophytic fungi.In:Schulz BJE,Boyle CJC,Sieber TN(eds)Microbial root endophytes.Springer,Berlin,pp 281-293
Cannon PF,Simmons CM(2002)Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve,Guyana.Mycol 94:210-220
Chambergo FS,Bonaccorsi ED,Ferreira AJ,Ramos AS,Ferreira JR,Abrahao-Neto J,Farah JP,El-Dorry H(2002)Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag(EST)analysis and cDNAmicroarrays.J Biol Chem 277:13983-13988
Cheewangkoon R,Groenewald JZ,Summerell BA,Hyde KD,ToAnun C,Crous PW(2009)Myrtaceae,a cache of fungal biodiversity.Persoonia 23:55-85
Doidy J,Grace E,Kühn C,Simon-Pas F,Casieri L,Wipf D(2012)Sugar transporters in plants and in their interactions with fungi.Trends Plant Sci 17:413-422
Duong LM,Jeewon R,Lumyong S,Hyde KD(2006)DGGEcoupledwith ribosomal DNA gene phylogenies reveal uncharacterizedfungal phylotypes.Fungal Divers 23:121-138
Evans TN,Watson G,Rees GN,Seviour RJ(2014)Comparing activated sludge fungal community population diversity using denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism.Antonie Van Leeuwenhoek105:559-569
FAO(2016)State of the world’s forests 2016.Forests and agriculture:land-use challenges and opportunities.Food and Agriculture Organization of the United Nations,Rome
Fromin N,Hamelin J,Tarnaw Ski S,Roesti D,Jourdain-Miserez K,Forestier N,Teyssier-Cuvelle S,Gillet F,Aragno M,Rossi P(2002)Statistical analysis of denaturing gel electrophoresis(DGE)fingerprinting patterns.Environ Microbiol 11:634-643
Gazis R,Chaverri P(2010)Diversity of fungal endophytes in leaves and stems of wild rubber trees(Hevea brasiliensis)in Peru.Fungal Ecol 3:240-254
Guerrini IA,Trigueiro RM(2004)Atributos físicos e químicos de substratos compostos por biossólidos e casca de arroz carbonizada.Rev Bras Cienc Solo 28:1069-1076
Hammer?,Harper DAT,Ryan PD(2001)PAST:paleontological statistics software package for education and data analysis.Palaeontol Electron 4:9
Hardoim PR,Overbeek LSV,Elsas KDV(2008)Properties of bacterial endophytes and their proposed role in plant growth.Trends Microbiol 16:463-471
Hoekstra FA,Buitink J(2001)Mechanisms of plant desiccation tolerance.Trends Plant Sci 8:431-438
Hubbard M,Germida JJ,Vujanovic V(2014)Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability.J Appl Microbiol116:109-122
Jia M,Chen L,Xin HL,Zheng CJ,Rahman K,Han T,Qin LP(2016)A friendly relationship between endophytic fungi and medicinal plants:a systematic review.Front Microbiol 7:1-14
Kemler M,Garnas J,Wingfield MJ,Gryzenhout M,Pillay KA,Slippers B(2013)Ion torrent PGM as tool for fungal community analysis:a case study of endophytes in Eucalyptus grandis reveals high taxonomic diversity.PLoS ONE 8:e81718
Kharwar RN,Gond SK,Kimar A,Misha A(2010)A comparative study of endophytic and epiphytic fungal association with leaf of Eucalyptus citriodora Hook,and their antimicrobial activity.World J Microb Biot 26:1941-1948
Kittelmann S,Naylor GE,Koolaard JP,Janssen PH(2012)Aproposed taxonomy of anaerobic fungi(Class Neocallimastigomycetes)suitable for large-scale sequence-based community structure analysis.PLoS ONE 7:1-13
Laplante K,Derome N(2011)Parallel changes in the taxonomical structure of bacterial communities exposed to a similar environmental disturbance.Ecol Evol 4:489-501
Lisec J,Schaeur N,Kopka J,Willmitzer L,Fernie AR(2006)Gas chromatography mass spectrometry-based metabolite profiling in plants.Nat Protoc 1:387-396
Lumyong S,Lumyong P,Mckenzie EH,Hyde KD(2002)Enzymatic activity of endophytic fungi of six native seedling species from oi Suthep-Pui National Park,Thailand.Can J Microbiol48:1109-1112
Lupo S,Tiscornia S,Bettucci L(2001)Endophytic fungi from flowers,capsules and seeds of Eucalyptus globulus.Rev Iberoam Micol 18:38-41
Marschener H(1998)Role of root growth,arbuscular mycorrhiza,and root exudates for the efficiency in nutrient acquisition.Field Crops Res 56:203-207
Maxwell A,Hardy GESTJ,Wingfield MJ,Dell B(2000)First record of Mycosphaerella lateralis on Eucalyptus in Australia.Australas Plant Pathol 29:279
Maxwell A,Jackson SL,Dell B,Hardy GESJ(2005)PCR-identification of Mycosphaerella species associated with leaf diseases of Eucalyptus.Mycol Res 109:992-1004
May LA,Smiley B,Schmidt MG(2001)Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage.Can J Microbiol47:829-841
Miguel PSB,de Oliveira MNV,Delvaux JC,de Jesus GL,Chaer AC,Tótola MR,Neves JCL,Costa MD(2016)Diversity and distribution of the endophytic bacterial community at different stages of Eucalyptus growth.Antonie Van Leeuwenhoek109(6):755-771
Miguel PSB,Delvaux JC,Oliveira MNV,Moreira BC,Freitas FS,Costa MD,Tótola MR,Neves JCL,Costa MD(2017)Diversity and distribution of the endophytic fungal community in eucalyptus leaves.Afr J Microbiol 11:92-105
Minitab I(2006)MINITAB statistical software.Version:Release.15
Oliveira MNV,Santos TMA,Vale HMM,Delvaux JC,Cordero AP,Ferreira AB,Miguel PSB,Tótola MR,Costa MD,Moraes CA,Borges AC(2013)Endophytic microbial diversity in coffee cherries of Coffea arabica from southeastern Brazil.Can JMicrobiol 59:221-230
Omacini M,Chaneton EJ,Ghersa CM,Muller CB(2001)Symbiotic fungal endophytes control insect host-parasite interaction webs.Nature 409:78-81
Oros-Sichler M,Gomes NCM,Neuber G,Smalla K(2006)A new semi-nested PCR protocol to amplify large 18S rRNA gene fragments for PCR-DGGE analysis of soil fungal communities.J Microbiol Meth 65:63-75
Porras-Alfaro A,Bayman P(2011)Hidden fungi,emergent properties:endophytes and microbiomes.Phytopathol 49:291
Rayner ADM,Boddy L(1986)Population structure and the infection biology of wood-decay fungi in living trees.Adv Plant Pathol5:119-160
Rho H,Kim SH(2017)Endophyte effects on photosynthesis and water use of plant hosts:a meta-analysis.In:Doty S(ed)Functional importance of the plant microbiome.Springer,Cham
Robl D,Da Delabona P,Mergel CM,Rojas JD,Dos Costa P,Pimentel IC,Padilha G(2013)The capability of endophytic fungi for production of hemicellulases and related enzymes.BMC Biotechnol 13:1-12
Saikkonen K,Wali P,Helander M,Taeth SH(2004)Evolution of endophyte-plant symbioses.Trends Plant Sci 9:275-280
Saitou N,Nei M(1987)The neighbor-joining method:a new method for reconstructing phylogenetic trees.Mol Biol Evol 4:406-425
Sánchez Márquez S,Bills GF,Zabalgogeazcoa I(2011)Fungal species diversity in juvenile and adult leaves of Eucalyptus globulus from plantations affected by Mycosphaerella leaf disease.Ann Appl Biol 158:177-187
Schneider H(2007)Métodos de análise filogenética:um guia prático[Methods for phylogenetic analysis:a practical guide].Holos Editora e Sociedade Brasileira de Genética,Ribeira?o Preto
Soto-Barajas MC,I?igo Z,Gómez-Fuertes J,González-Blanco V,Vázquez de Aldana BR(2016)Epichloe¨endophytes affect the nutrient and fiber content of Lolium perenne regardless of plant genotype.Plant Soil 405:265-277
Systat Software,Inc(2008)Sigma plot for windows,version 11.0
Vainio EJ,Hantula J(2000)Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA.Mycol Res 104:927-936
You YH,Kang SM,Choo YS,Lee JM(2012)Fungal diversity and plant growth promotion of endophytic fungi from six halophytes in Suncheon Bay.J Microbiol Biotechnol 22:1549-1556
Andjic V,Whyte G,Hardy G,Burgess T(2010)New Teratosphaeria species occurring on eucalypts in Australia.Fungal Diver43:27-38
Andrews JH,Harris RF,Spear RN,Lau GW,Nordheim EV(1994)Morphogenesis and adhesion of Aureobasidium pullulans.Can JMicrobiol 40:6-17
Arnold AE(2005)Diversity and ecology of fungal endophytes in tropical forests.In:Deshmukh S(ed)Current trends in mycological research.Oxford&IBH Publishing Co.Pvt.Ltd.,New Delhi,pp 49-68
Arnold AE,Herre EA(2003)Canopy cover and leaf age affect colonization by tropical fungal endophytes:ecological pattern and process in Theobroma cacao(Malvaceae).Mycol95:388-398
Arnold AE,Lutzoni F(2007)Diversity and host range of foliar fungal endophytes:are tropical leaves biodiversity hotspots?Ecology88:541-549
Arnold AE,Maynard Z,Gilbert GS,Coley PD,Kursar TA(2000)Are tropical fungal endophytes hyperdiverse?Ecol Lett 3:267-274
Bago B,Pfeffer PE,Shachar-Hill Y(2000)Carbon metabolism and transport in arbuscular mycorrhizas.Plant Physiol 124:949-958
Bremner JM,Mulvaney CS(1982)Total nitrogen.In:Page AL(ed)Methods of soil analysis.American Society of Agronomy,Madison,pp 595-624
Bresolin JD,Bustamante MMC,Krüger RH,Silva MRSS,Perez KS(2010)Structure and composition of bacterial and fungal community in soil under soybean monoculture in the Brazilian cerrado.Braz J Microbiol 41:391-403
Brooker MIH(2000)A new classification of the genus Eucalyptus L’Her(Myrtaceae).Aust Syst Bot 13:79-148
Brundrett MC(2006)Understanding the roles of multifunctional mycorrhizal and endophytic fungi.In:Schulz BJE,Boyle CJC,Sieber TN(eds)Microbial root endophytes.Springer,Berlin,pp 281-293
Cannon PF,Simmons CM(2002)Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve,Guyana.Mycol 94:210-220
Chambergo FS,Bonaccorsi ED,Ferreira AJ,Ramos AS,Ferreira JR,Abrahao-Neto J,Farah JP,El-Dorry H(2002)Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag(EST)analysis and cDNAmicroarrays.J Biol Chem 277:13983-13988
Cheewangkoon R,Groenewald JZ,Summerell BA,Hyde KD,ToAnun C,Crous PW(2009)Myrtaceae,a cache of fungal biodiversity.Persoonia 23:55-85
Doidy J,Grace E,Kühn C,Simon-Pas F,Casieri L,Wipf D(2012)Sugar transporters in plants and in their interactions with fungi.Trends Plant Sci 17:413-422
Duong LM,Jeewon R,Lumyong S,Hyde KD(2006)DGGEcoupledwith ribosomal DNA gene phylogenies reveal uncharacterizedfungal phylotypes.Fungal Divers 23:121-138
Evans TN,Watson G,Rees GN,Seviour RJ(2014)Comparing activated sludge fungal community population diversity using denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism.Antonie Van Leeuwenhoek105:559-569
FAO(2016)State of the world’s forests 2016.Forests and agriculture:land-use challenges and opportunities.Food and Agriculture Organization of the United Nations,Rome
Fromin N,Hamelin J,Tarnaw Ski S,Roesti D,Jourdain-Miserez K,Forestier N,Teyssier-Cuvelle S,Gillet F,Aragno M,Rossi P(2002)Statistical analysis of denaturing gel electrophoresis(DGE)fingerprinting patterns.Environ Microbiol 11:634-643
Gazis R,Chaverri P(2010)Diversity of fungal endophytes in leaves and stems of wild rubber trees(Hevea brasiliensis)in Peru.Fungal Ecol 3:240-254
Guerrini IA,Trigueiro RM(2004)Atributos físicos e químicos de substratos compostos por biossólidos e casca de arroz carbonizada.Rev Bras Cienc Solo 28:1069-1076
Hammer?,Harper DAT,Ryan PD(2001)PAST:paleontological statistics software package for education and data analysis.Palaeontol Electron 4:9
Hardoim PR,Overbeek LSV,Elsas KDV(2008)Properties of bacterial endophytes and their proposed role in plant growth.Trends Microbiol 16:463-471
Hoekstra FA,Buitink J(2001)Mechanisms of plant desiccation tolerance.Trends Plant Sci 8:431-438
Hubbard M,Germida JJ,Vujanovic V(2014)Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability.J Appl Microbiol116:109-122
Jia M,Chen L,Xin HL,Zheng CJ,Rahman K,Han T,Qin LP(2016)A friendly relationship between endophytic fungi and medicinal plants:a systematic review.Front Microbiol 7:1-14
Kemler M,Garnas J,Wingfield MJ,Gryzenhout M,Pillay KA,Slippers B(2013)Ion torrent PGM as tool for fungal community analysis:a case study of endophytes in Eucalyptus grandis reveals high taxonomic diversity.PLoS ONE 8:e81718
Kharwar RN,Gond SK,Kimar A,Misha A(2010)A comparative study of endophytic and epiphytic fungal association with leaf of Eucalyptus citriodora Hook,and their antimicrobial activity.World J Microb Biot 26:1941-1948
Kittelmann S,Naylor GE,Koolaard JP,Janssen PH(2012)Aproposed taxonomy of anaerobic fungi(Class Neocallimastigomycetes)suitable for large-scale sequence-based community structure analysis.PLoS ONE 7:1-13
Laplante K,Derome N(2011)Parallel changes in the taxonomical structure of bacterial communities exposed to a similar environmental disturbance.Ecol Evol 4:489-501
Lisec J,Schaeur N,Kopka J,Willmitzer L,Fernie AR(2006)Gas chromatography mass spectrometry-based metabolite profiling in plants.Nat Protoc 1:387-396
Lumyong S,Lumyong P,Mckenzie EH,Hyde KD(2002)Enzymatic activity of endophytic fungi of six native seedling species from oi Suthep-Pui National Park,Thailand.Can J Microbiol48:1109-1112
Lupo S,Tiscornia S,Bettucci L(2001)Endophytic fungi from flowers,capsules and seeds of Eucalyptus globulus.Rev Iberoam Micol 18:38-41
Marschener H(1998)Role of root growth,arbuscular mycorrhiza,and root exudates for the efficiency in nutrient acquisition.Field Crops Res 56:203-207
Maxwell A,Hardy GESTJ,Wingfield MJ,Dell B(2000)First record of Mycosphaerella lateralis on Eucalyptus in Australia.Australas Plant Pathol 29:279
Maxwell A,Jackson SL,Dell B,Hardy GESJ(2005)PCR-identification of Mycosphaerella species associated with leaf diseases of Eucalyptus.Mycol Res 109:992-1004
May LA,Smiley B,Schmidt MG(2001)Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage.Can J Microbiol47:829-841
Miguel PSB,de Oliveira MNV,Delvaux JC,de Jesus GL,Chaer AC,Tótola MR,Neves JCL,Costa MD(2016)Diversity and distribution of the endophytic bacterial community at different stages of Eucalyptus growth.Antonie Van Leeuwenhoek109(6):755-771
Miguel PSB,Delvaux JC,Oliveira MNV,Moreira BC,Freitas FS,Costa MD,Tótola MR,Neves JCL,Costa MD(2017)Diversity and distribution of the endophytic fungal community in eucalyptus leaves.Afr J Microbiol 11:92-105
Minitab I(2006)MINITAB statistical software.Version:Release.15
Oliveira MNV,Santos TMA,Vale HMM,Delvaux JC,Cordero AP,Ferreira AB,Miguel PSB,Tótola MR,Costa MD,Moraes CA,Borges AC(2013)Endophytic microbial diversity in coffee cherries of Coffea arabica from southeastern Brazil.Can JMicrobiol 59:221-230
Omacini M,Chaneton EJ,Ghersa CM,Muller CB(2001)Symbiotic fungal endophytes control insect host-parasite interaction webs.Nature 409:78-81
Oros-Sichler M,Gomes NCM,Neuber G,Smalla K(2006)A new semi-nested PCR protocol to amplify large 18S rRNA gene fragments for PCR-DGGE analysis of soil fungal communities.J Microbiol Meth 65:63-75
Porras-Alfaro A,Bayman P(2011)Hidden fungi,emergent properties:endophytes and microbiomes.Phytopathol 49:291
Rayner ADM,Boddy L(1986)Population structure and the infection biology of wood-decay fungi in living trees.Adv Plant Pathol5:119-160
Rho H,Kim SH(2017)Endophyte effects on photosynthesis and water use of plant hosts:a meta-analysis.In:Doty S(ed)Functional importance of the plant microbiome.Springer,Cham
Robl D,Da Delabona P,Mergel CM,Rojas JD,Dos Costa P,Pimentel IC,Padilha G(2013)The capability of endophytic fungi for production of hemicellulases and related enzymes.BMC Biotechnol 13:1-12
Saikkonen K,Wali P,Helander M,Taeth SH(2004)Evolution of endophyte-plant symbioses.Trends Plant Sci 9:275-280
Saitou N,Nei M(1987)The neighbor-joining method:a new method for reconstructing phylogenetic trees.Mol Biol Evol 4:406-425
Sánchez Márquez S,Bills GF,Zabalgogeazcoa I(2011)Fungal species diversity in juvenile and adult leaves of Eucalyptus globulus from plantations affected by Mycosphaerella leaf disease.Ann Appl Biol 158:177-187
Schneider H(2007)Métodos de análise filogenética:um guia prático[Methods for phylogenetic analysis:a practical guide].Holos Editora e Sociedade Brasileira de Genética,Ribeira?o Preto
Soto-Barajas MC,I?igo Z,Gómez-Fuertes J,González-Blanco V,Vázquez de Aldana BR(2016)Epichloe¨endophytes affect the nutrient and fiber content of Lolium perenne regardless of plant genotype.Plant Soil 405:265-277
Systat Software,Inc(2008)Sigma plot for windows,version 11.0
Vainio EJ,Hantula J(2000)Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA.Mycol Res 104:927-936
You YH,Kang SM,Choo YS,Lee JM(2012)Fungal diversity and plant growth promotion of endophytic fungi from six halophytes in Suncheon Bay.J Microbiol Biotechnol 22:1549-1556