Abstract
Endophytic fungi are extremely diverse in natural biomes, which display a unique plant-microbe association inside different living host tissues. Among the plants that shelter endophytes, the endophytic fungal assemblages of Cactaceae remain poorly understood. Our study characterized the taxonomy, diversity, and ecology of endophytic fungal assemblages living in different tissues of the cactus Melocactus ernestii present in the Brazilian Caatinga biome. A total of 222 endophytic fungi were obtained from roots, stems, and spines, which were identified in 99 operational taxonomic units (OTUs) of Ascomycota and Basidiomycota phyla. Most of the fungal taxa were recovered from root tissues, followed by stems and spines. The most abundant orders from Ascomycota were Xylariales, Dothideomycetes, and Eurotiomycetes. Basidiomycota is represented by Cantharellales, Agaricales, and Geastrales. Only Nigrospora sp. and Preussia sp. 1 were common among the three plant tissues, and 78.41% of the species were not shared among the populations and tissues. We detected similar richness patterns among the same tissue types using sample-based rarefaction and extrapolation curves. The multiple site dissimilarity across the plants and tissues showed greater disparities in species richness among M. ernestii fungal assemblages. These results highlight the compartmentalization of endophytic fungal species in the root tissue, and the endophytes sharing observed exclusively between spines and stems may reflect interactions of endophytic fungal assemblages with possible dependency on shared resources in cacti. Overall, our findings will an approach to understand changes in the diversity and the key roles of turnover of endophytic fungal assemblages in semi-arid environments.
Similar content being viewed by others
References
Ali AH, Radwan U, El-Zayat S, El-Sayed MA (2018) Desert plant-fungal endophytic association: the beneficial aspects to their hosts. BFIJ 10:138–145
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389
Andrade CTS, Marques JGW, Zappi DC (2006) Utilização medicinal de cactáceas por sertanejos baianos. Rev Bras Pl Med 8:36–42
Andrioli WJ, Conti R, Araújo MJ, Zanasi R, Cavalcanti BC, Manfrim V, Toledo JS, Tedesco D, Moraes MO, Pessoa C, Cruz AK, Bertucci C, Sabino J, Nanayakkara DNP, Pupo MT, Bastos JK (2014) Mycoleptones A−C and polyketides from the endophyte Mycoleptodiscus indicus. J Nat Prod 77:70–78. https://doi.org/10.1021/np4006822
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical trees biodiversity hot spots? Ecology 88:541–549. https://doi.org/10.1890/05-1459
Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247. https://doi.org/10.1007/s00572-003-0222-0
Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J Arid Environ 51:449–459. https://doi.org/10.1006/jare.2001.0925
Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM (2008) Do symbiotic microbes have a role in regulating plant performance and response to stress? Commun Integr Biol 1:69–73. https://doi.org/10.4161/cib.1.1.6238
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Baselga A (2013) Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol Evol 4:552–557. https://doi.org/10.1111/2041-210X.12029
Baselga A (2017) Partitioning abundance-based multiple-site dissimilarity into components: balanced variation in abundance and abundance gradients. Methods Ecol Evol 8:799–808. https://doi.org/10.1111/2041-210X.12693
Berdugo M, Delgado-Baquerizo M, Soliveres S, Hernández-Clemente R, Zhao Y, Gaitán JJ, Gross N, Saiz H, Maire V, Lehman A, Rillig MC, Solé RV, Maestre FT (2020) Global ecosystem thresholds driven by aridity. Science 367:787–790. https://doi.org/10.1126/science.aay5958
Bezerra JL, Ram AA (1986) Crosta negra da baunilha (Vanilla fragans) causada por Mycoleptodiscus indicus (Moniliales, Hiphomycetes). Fitopatol Bras 11(717):724
Bezerra JD, Santos MG, Svedese VM, Lima DM, Fernandes MJ, Paiva LM, Souza-Motta CM (2012) Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28:1989–1995. https://doi.org/10.1007/s11274-011-1001-2
Bezerra JDP, Santos MGS, Barbosa RN, Svedese VM, Lima DMM, Fernandes MJS, Gomes BS, Paiva LM, Almeida-Cortez JS, Souza-Motta CM (2013) Fungal endophytes from cactus Cereus jamacaru in Brazilian tropical dry forest: a first study. Symbiosis 60:53–63. https://doi.org/10.1007/s13199-013-0243-1
Bezerra JDP, Oliveira RJV, Paiva LM, Silva GA, Groenewald JZ, Crous PW, Souza-Motta CM (2017) Bezerromycetales and Wiesneriomycetales ord. nov. (class Dothideomycetes), with two novel genera to accommodate endophytic fungi from Brazilian cactus. Mycol Prog 16:297–309. https://doi.org/10.1007/s11557-016-1254-0
Bonfim A, Albuquerque GMR, Bezerra JDP, Silva DCV, Svedese VM, Paiva LM, Souza-Motta CM (2013) Fungos fitopatogênicos de Opuntia ficus-indica (L.) Mill. cultivada em área de floresta tropical seca no Brasil. Bol Soc Latin Carib Cact Suc 10:27–33
Budka A, Łacka A, Szoszkiewicz K (2019) The use of rarefaction and extrapolation as methods of estimating the effects of river eutrophication on macrophyte diversity. Biodivers Conserv 28:385–400. https://doi.org/10.1007/s10531-018-1662-3
Camarena-Pozos DA, Flores-Núñez VM, Lopez MG, Partida-Martínez LP (2021) Fungal volatiles emitted by members of the microbiome of desert plants are diverse and capable of promoting plant growth. Environ Microbiol 23:2215–2229. https://doi.org/10.1111/1462-2920.15395
Card S, Johnson L, Teasdale S, Caradus J (2016) Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiol Ecol 92(8). https://doi.org/10.1093/femsec/fiw114
Carvalho CR, Wedge DE, Cantrell CL, Silva-Hughes AF, Pan Z, Moraes RM, Madoxx VL, Rosa LH (2016) Molecular phylogeny, diversity, and bioprospecting of endophytic fungi associated with wild ethnomedicinal north American plant Echinacea purpurea (Asteraceae). Chem Biodivers 13:918–930. https://doi.org/10.1002/cbdv.201500299
Castellani A (1967) A maintenance and cultivation of the common pathogenic fungi of man in sterile distilled water: further researches. J trop Med Hyg 70:181–184
Castoria R, de Curtis F, Lima G, Caputo L, Pacifico S, de Cicco V (2001) Aureobasidium pullulans (LS-30) an antagonist of postharvest pathogens of fruits: study on its modes of action. Postharvest Biol Technol 22:7–17. https://doi.org/10.1016/S0925-5214(00)00186-1
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21. https://doi.org/10.1093/jpe/rtr044
Decruse SW, Neethu RS, Pradeep NS (2018) Seed germination and seedling growth promoted by a Ceratobasidiaceae clone in Vanda thwaitesii Hook. f., an endangered orchid species endemic to South Western Ghats, India and Sri Lanka. S Afr J Bot 116:222–229. https://doi.org/10.1016/j.sajb.2018.04.002
Delgado-Baquerizo M, Maestre F, Gallardo A et al (2013) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–676. https://doi.org/10.1038/nature12670
Dewar CL, Sigler L (2010) Fungal arthritis of the knee caused by Mycoleptodiscus indicus. Clin Rheumatol 29:1061–1065. https://doi.org/10.1007/s10067-010-1448-9
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086
Fisher PJ, Sutton BC, Petrini LE, Petrini O (1994) Fungal endophytes from Opuntia stricta: a first report. Nova Hedwigia 59:195–200
Fonseca-García C, Coleman-Derr D, Garrido E, Visel A, Tringe SG, Partida-Martínez LP (2016) The cacti microbiome: interplay between habitat-filtering and host-specificity. Front Microbiol 12:150. https://doi.org/10.3389/fmicb.2016.00150
Freire KTLS, Araújo GR, Bezerra JDP et al (2015) Fungos endofíticos de Opuntia ficus-indica (L.) Mill. (Cactaceae) sadia e infestada por Dactylopius opuntiae (Cockerell, 1896) (Hemiptera: Dactylopiidae). Revista Gaia Scientia 9:104–110
Ganter PF, Morais PB, Rosa CA (2017) Yeasts in cacti and tropical fruit. In: Buzzini P, Lachance MA, Yurkov A (eds) Yeasts in natural ecosystems: diversity. Springer, Cham. https://doi.org/10.1007/978-3-319-62683-3_8
Gargouri M, Karray F, Chebaane A, Mhiri N, Partida-Martínez LP, Sayadi S, Mliki A (2021) Increasing aridity shapes beta diversity and the network dynamics of the belowground fungal microbiome associated with Opuntia ficus-indica. Sci Total Environ 773:145008. https://doi.org/10.1016/j.scitotenv.2021.145008
Geisen S, Kostenko O, Cnossen MC, Ten Hooven FC, Vreš B, van der Putten WH (2017) Seed and root endophytic fungi in a range expanding and a related plant species. Front Microbiol 8:1645. https://doi.org/10.3389/fmicb.2017.01645
Goettsch B, Hilton-Taylor C, Cruz-Piñón G, Duffy JP, Frances A, Hernández HM, Inger R, Pollock C, Schipper J, Superina M, Taylor NP, Tognelli M, Abba AM, Arias S, Arreola-Nava HJ, Baker MA, Bárcenas RT, Barrios D, Braun P, Butterworth CA, Búrquez A, Caceres F, Chazaro-Basañez M, Corral-Díaz R, del Valle Perea M, Demaio PH, Duarte de Barros WA, Durán R, Yancas LF, Felger RS, Fitz-Maurice B, Fitz-Maurice WA, Gann G, Gómez-Hinostrosa C, Gonzales-Torres LR, Patrick Griffith M, Guerrero PC, Hammel B, Heil KD, Hernández-Oria JG, Hoffmann M, Ishihara MI, Kiesling R, Larocca J, León-de la Luz JL, Loaiza S. CR, Lowry M, Machado MC, Majure LC, Ávalos JGM, Martorell C, Maschinski J, Méndez E, Mittermeier RA, Nassar JM, Negrón-Ortiz V, Oakley LJ, Ortega-Baes P, Ferreira ABP, Pinkava DJ, Porter JM, Puente-Martinez R, Gamarra JR, Pérez PS, Martínez ES, Smith M, Manuel Sotomayor M. del C. J, Stuart SN, Muñoz JLT, Terrazas T, Terry M, Trevisson M, Valverde T, van Devender TR, Véliz-Pérez ME, Walter HE, Wyatt SA, Zappi D, Alejandro Zavala-Hurtado J, Gaston KJ (2015) High proportion of cactus species threatened with extinction. Nat Plants 5:15142. https://doi.org/10.1038/nplants.2015.142
González V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42. https://doi.org/10.1007/s13225-010-0073-x
Gonzalez-Menendez V, Martin J, Siles JA, Gonzalez-Tejero MR, Reyes F, Platas G, Tormo JR, Genilloud O (2017) Biodiversity and chemotaxonomy of Preussia isolates from the Iberian Peninsula. Mycol Prog 16(7):713–728. https://doi.org/10.1007/s11557-017-1305-1
González-Menéndez V, Crespo G, DE Pedro N et al (2018) Fungal endophytes from arid areas of Andalusia: high potential sources for antifungal and antitumoral agents. Sci Rep 8:9729. https://doi.org/10.1038/s41598-018-28192-5
Grandi RAP, Silva TV (2006) Fungos Anamorfos decompositores do folhedo de Caesalpinia echinata Lam. Rev Bras Bot 29:275–287. https://doi.org/10.1590/S0100-84042006000200009
Herrera J, Khidir HH, Eudy DM, Porras-Alfaro A, Natvig DO, Sinsabaugh RL (2010) Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 102(5):1012–1026. https://doi.org/10.3852/09-264
Hill M (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
Hsieh TC, Ma KH, Chao A (2019) ‘iNEXT’: iNterpolation and EXTrapolation for species diversity. R package version 2.0.20. https://CRAN.R-project.org/package=iNEXT. Accessed 10 Dec 2020 https://doi.org/10.1890/13-0133.1
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 Microbiol 116:109–122. https://doi.org/10.1111/jam.12311
Hughes FM, Jacobi CM, Borba EL (2016) Fate of cohorts in Melocactus (Cactaceae) species is affected by rainfall uncertainty and microrelief structures. Braz J Bot 39:197–205. https://doi.org/10.1007/s40415-014-0116-8
Hughes FM, Figueira JEC, Jacobi CM, Borba EL (2018) Demographic processes and anthropogenic threats of lithophytic cacti in eastern Brazil. Braz J Bot 41:631–640. https://doi.org/10.1007/s40415-018-0483-7
Ippolito A, EL Ghaouth A, Wilson CL, Wisniewski M (2000) Control of postharvest decay of apple fruit by Aureobasidium pullulans and induction of defense responses. Postharvest Biol Technol 19:265–272. https://doi.org/10.1016/S0925-5214(00)00104-6
Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Do N, Sinsabaugh RL (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J Arid Environ 74:35–42. https://doi.org/10.1016/j.jaridenv.2009.07.014
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi. CAB International, Wallingford
Kurtzman C, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier
Lachance MA, Bowles JM, Starmer T, Barker JS (1999) Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 45:172–177. https://doi.org/10.1139/w98-225
Lana TG, Azevedo JL, Pomella AW, Monteiro RT, Silva CB, Araújo WL (2011) Endophytic and pathogenic isolates of the cacao fungal pathogen Moniliophthora perniciosa (Tricholomataceae) are indistinguishable based on genetic and physiological analysis. Genet Mol Res 10:326–334. https://doi.org/10.4238/vol10-1gmr895
Leal IR, Silva JMC, Tabarelli M, Lacher TE Jr (2005) Changing the course of biodiversity conservation in the caatinga of northeastern Brazil. Conserv Biol 19:701–706. https://doi.org/10.1111/j.1523-1739.2005.00703.x
Leslie J, Summerell BA (2006) The Fusarium laboratory manual. Blackwell, Iowa
Liu QY, Liu MH, Li T, Chen JH, Zhang FG, Hu J (2017) First report of summer patch of Kentucky bluegrass caused by Magnaporthe poae in China. Plant Dis 101(1):250–250
Lüttge U (2004) Ecophysiology of Crassulacean acid metabolism (CAM). Ann Bot 93:629–652. https://doi.org/10.1093/aob/mch087
Luz JS, de Oliveira Silva RL, da Silveira EB, Cavalcante UMT (2006) Atividade enzimática de fungos endofíticos e efeito na promoção do crescimento de mudas de maracujazeiro-amarelo. Rev Caatinga 19:128–134
Maboni G, Krimer P, Baptista R, Lorton A, Anderson C, Sanchez S (2019) Laboratory diagnostics, phylogenetic analysis and clinical outcome of a subcutaneous Mycoleptodiscus indicus infection in an immunocompetent cat. BMC Vet Res 15:354. https://doi.org/10.1186/s12917-019-2132-1
Mandyam K, Junpponem A (2005) Seeking the elusive function of the root-colonising dark sepatele endophyte. Stud Micol 53:173–189. https://doi.org/10.3114/sim.53.1.173
Martorell C, Montañana DM, Ureta C, Mandujano MC (2015) Assessing the importance of multiple threats to an endangered globose cactus in Mexico: cattle grazing, looting and climate change. Biol Conserv 181:73–81. https://doi.org/10.1016/j.biocon.2014.10.035
Massimo NC, Devan MN, Arendt KR, Wilch MH, Riddle JM, Furr SH, Steen C, U'Ren JM, Sandberg DC, Arnold AE (2015) Fungal endophytes in aboveground tissues of desert plants: infrequent in culture, but highly diverse and distinctive symbionts. Microb Ecol 70(1):61–76. https://doi.org/10.1007/s00248-014-0563-6
Mauseth JD (2004) The structure of photosynthetic succulent stems in plants other than cacti. Int J Plant Sci 165:1–9. https://doi.org/10.1086/380978
Mauseth JD (2006) Structure–function relationships in highly modified shoots of Cactaceae. Ann Bot 98:901–926. https://doi.org/10.1093/aob/mcl133
Moraes WS, Zambolim L, Lima JD (2006) Incidence of mushroons in post harvest of banana (Musa spp.) Prata Anã (AAB). Summa Phytopathol 32:67–70
Morgan DP, Michailides TJ (2004) First report of melting decay of “red globe” grapes in California. Plant Dis 88:1047
Moro MF, Nic Lughadha E, de Araújo FS, Martins FR (2016) A phytogeographical metaanalysis of the semiarid caatinga domain in Brazil. Bot Rev 82:91–148. https://doi.org/10.1007/s12229-016-9164-z
Morsy MR, Oswald J, He J, Tang Y, Roossinck MJ (2010) Teasing apart a three-way symbiosis: transcriptome analyses of Curvularia protuberata in response to viral infection and heat stress. Biochem Biophys Res Commun 401:225–230. https://doi.org/10.1016/j.bbrc.2010.09.034
Pennington RT, Lavin M, Oliveira-Filho A (2009) Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annu Rev Ecol Evol Syst 40:37–57. https://doi.org/10.1146/annurev.ecolsys.110308.120327
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/
Redman RS, Sheehan KB, Stout TG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298(5598):1581. https://doi.org/10.1126/science.1072191
Ritz CM, Martins L, Mecklenburg R, Goremykin V, Hellwig FH (2007) The molecular phylogeny of Rebutia (Cactaceae) and its allies demonstrates the influence of paleogeography on the evolution of south American mountain cacti. Am J Bot 94:1321–1332. https://doi.org/10.3732/ajb.94.8.1321
Rocha EA, Agra MF (2002) Flora do Pico do Jabre, Paraíba, Brasil: Cactaceae Juss. Acta Bot Bras 16:15–21. https://doi.org/10.1590/S0102-33062002000100004
Rosa LH, Gonçalves VN, Caligiorne RB, Almeida Alves TM, Rabelo ALT, Sales PA, Romanha AJ, Sobral MEG, Rosa CA, Zani CL (2010) Leishmanicidal, trypanocidal, and cytotóxic activities of endophytic fungi associated with bioactive plants in Brazil. Braz J Microbiol 41:1–11. https://doi.org/10.1590/S1517-83822010000200024
Rosa LH, Tabanca N, Techen N, Wedge DE, Pan Z, Bernier UR, Becnel JJ, Agramonte NM, Walker LA, Moraes RM (2012) Diversity and biological activities of endophytic fungi associated with micropropagated medicinal plant Echinacea purpurea (L.) Moench. Am. J. Plant Sci 3:1105–1114. https://doi.org/10.4236/ajps.2012.38133
Schill R, Barthlott W (1973) Kakteendornen als wasserabsorbierende organe. Die Naturwissenschaften 60:202–203. https://doi.org/10.1007/BF00599438
Schulz BJE, Boyle CJC (2006) What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer-Verlag, Berlin, pp 1–13
Shade A, Jacques MA, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22. https://doi.org/10.1016/j.mib.2017.03.010
Shymanovich T, Faeth SH (2019) Environmental factors affect the distribution of two Epichloë fungal endophyte species inhabiting a common host grove bluegrass (Poa alsodes). Ecol Evol 9(11):6624–6642. https://doi.org/10.1002/ece3.5241
Silva RLDO, Luz JS, Silveira EBD, Cavalcante UMT (2006) Fungos endofíticos em Annona spp.: isolamento, caracterização enzimática e promoção do crescimento em mudas de pinha (Annona squamosa L.). Acta Bot Bras 20:649–655. https://doi.org/10.1590/S0102-33062006000300015
Silva-Hughes AF, Wedge DE, Cantrell CL, Carvalho CR, Pan Z, Moraes RM, Madoxx ML, Rosa LH (2015) Diversity and antifungal activity of the endophytic fungi associated with the native medicinal cactus Opuntia humifusa (Cactaceae) from the United States. Microbiol Res 175:67–77. https://doi.org/10.1016/j.micres.2015.03.007
Souza AEF, Nascimento LC, Araújo E, Lopes EB, Souto FM (2010) Occurrence and identification of the etiologic agents of plant diseases in cactus (Opuntia ficus-indica Mill.) in the semi-arid region of Paraiba. Biotemas 23:11–20. https://doi.org/10.5007/2175-7925.2010v23n3p11
Sterflinger K, Tesei D, Zakharova K (2012) Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecol 5:453–462. https://doi.org/10.1016/j.funeco.2011.12.007
Sun PF, Chien IA, Xiao HS, Fang WT, Hsu CH, Chou JY (2019) Intra specific variation in plant growth-promoting traits of Aureobasidium pullulans. Chiang Mai J Sci 46(1):15–31
Suryanarayanan T, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109(5):635–639. https://doi.org/10.1017/s0953756205002753
Taylor NP, Zappi DC (2004) Cacti of eastern Brazil. Royal Botanic Gardens, Kew
Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary succession gradient in northern Finland. Fungal Divers 41(1):125–134. https://doi.org/10.1007/s13225-009-0016-6
Toju H, Yamamoto S, Sato H, Tanabe AS, Gilbert GS, Kadowaki K (2013) Community composition of root-associated fungi in a Quercus-dominated temperate forest: "codominance" of mycorrhizal and root-endophytic fungi. Ecol Evol 3:1281–1293. https://doi.org/10.1002/ece3.546
Toju H, Guimarães P, Olesen J, Thompson J (2014) Assembly of complex plant–fungus networks. Nat Commun 5:5273. https://doi.org/10.1038/ncomms6273
Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18(11):607–621. https://doi.org/10.1038/s41579-020-0412-1
Unterseher M, Siddique AB, Brachmann A, Peršoh D (2016) Diversity and composition of the leaf mycobiome of beech (fagus sylvatica) are affected by local habitat conditions and leaf biochemistry. PloS one 11(4):e0152878. https://doi.org/10.1371/journal.pone.0152878
U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host- and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–9143. https://doi.org/10.3732/ajb.1100459
Veldre V, Abarenkov K, Bahram M, Martos F, Selosse MA, Tamm H, Koljalg U, Tedersoo L (2013) Evolution of nutritional modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) as revealed from publicly available ITS sequences. Fungal Ecol 6(4):256–268. https://doi.org/10.1016/j.funeco.2013.03.004
Vergara C, Araujo KEC, Alves LS, Souza SR, Santos LA, Santa-Catarina C, Silva K, Pereira GMD, Xavier GR, Zilli JE (2018) Contribution of dark septate fungi to the nutrient uptake and growth of rice plants. Braz J Microbiol 49:67–78. https://doi.org/10.1016/j.bjm.2017.04.010
Vieira ML, Hughes AF, Gil VB, Vaz AB, Alves TM, Zani CL, Rosa CA, Rosa LH (2012) Diversity and antimicrobial activities of the fungal endophyte community associated with the traditional Brazilian medicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol 58:54–66. https://doi.org/10.1139/w11-105
Völz R, Park JY, Kim S, Park SY, Harris W, Chung H, Lee YH (2020) The rice/maize pathogen Cochliobolus spp. infect and reproduce on Arabidopsis revealing differences in defensive phytohormone function between monocots and dicots. Plant J 103:412–429. https://doi.org/10.1111/tpj.14743
Wachowska U, Głowacka K (2014) Antagonistic interactions between Aureobasidium pullulans and Fusarium culmorum, a fungal pathogen of winter wheat. BioControl 59:635–645. https://doi.org/10.1007/s10526-014-9596-5
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Zimmermann HG, Granata G (2002) Insect pests and diseases. In: NOBEL PS (ed) Cacti: biology and uses. University of California Press, Berkeley, pp 235–254
Acknowledgements
Alice Ferreira-Silva was financially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (grant:141684/2010-0). Frederic M. Hughes acknowledges CNPq grant 302381/2020-1. The study was supported by FAPEMIG, CAPES and CNPq.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ferreira-Silva, A., Hughes, F.M., Rosa, C.A. et al. Higher turnover of endophytic fungal assemblages in the tissues of globose cactus Melocactus ernestii from Brazilian semi-arid biome. Symbiosis 85, 79–91 (2021). https://doi.org/10.1007/s13199-021-00795-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-021-00795-z