Spring to autumn changes in the arbuscular mycorrhizal fungal community composition in the different propagule types associated to a Mediterranean shrubland

Springer Science and Business Media LLC - Tập 408 - Trang 107-120 - 2016
Sara Varela-Cervero1, Álvaro López-García1, José M. Barea1, Concepción Azcón-Aguilar1
1Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín (CSIC), Granada, Spain

Tóm tắt

Arbuscular mycorrhizal fungi (AMF) appear differentially represented among propagule forms [intraradical mycelium (IRM) in colonized roots, spores and extraradical mycelium (ERM)]. However, spring to autumn changes in the AMF communities harboured in the different propagule forms has not been studied, being this the aim of the present study. A terminal restriction fragment length polymorphism approach was used to monitor, in spring and autumn, the AMF community composition present in the three propagule types associated to five shrub species in a semi-arid Mediterranean environment. The AMF community composition in roots was significantly different between spring and autumn; however, no significant differences were detected in soil propagules (spores and ERM). Different trends were identified according to the preferential biomass allocation patterns of AMF phylotypes, suggesting different life strategies: those allocating mainly into IRM (belonging to the Glomeraceae), ERM (Diversisporaceae and Gigasporaceae) or spores (Pacisporaceae and Paraglomeraceae). Differences of AMF taxa in the biomass allocation patterns among propagules are maintained throughout the year. Progress in the knowledge of functional features of AMF communities and their responses to seasonal variations are important for the AMF application in Mediterranean ecosystems.

Tài liệu tham khảo

Allen H (2009) Vegetation and ecosystem dynamics. In: Woodward JC (ed) The physical geography of the Mediterranean. Oxford University Press, Oxford, pp 203–227 Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511 Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301 Bates ST, Clemente JC, Flores GE, Walters WA, Parfrey LW, Knight R, Fierer N (2012) Global biogeography of highly diverse protistan communities in soil. ISME J 7:652–659 Bennett AE, Daniell TJ, Öpik M, Davison J, Moora M, Zobel M, Selosse MA, Evans D (2013) Arbuscular mycorrhizal fungal networks vary throughout the growing season and between successional stages. PLoS ONE 8, e83241 Bever JD, Richardson SC, Brandy ML, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21 Brito I, De Carvalho M, Goss MJ (2011) Summer survival of arbuscular mycorrhiza extraradical mycelium and the potential for its management through tillage options in Mediterranean cropping systems. Soil Use Manag 27:350–356 Brundrett M, Melville L, Peterson L (1994) Practical methods in Mycorrhiza research. Mycologue Publications, University of Guelph, Guelph Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491 Chytrý M, Tichý L, Holt J, Botta-Dukát Z (2002) Determination of diagnostic species with statistical fidelity measures. J Veg Sci 13:79–90 Collins RE, Rocap G (2007) REPK: an analytical web server to select restriction endonucleases for terminal restriction fragment length polymorphism analysis. Nucleic Acids Res 35:W58–W62 Cornejo P, Azcón-Aguilar C, Barea JM, Ferrol N (2004) Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol Lett 241:265–270 Cotton TEA, Dumbrell AJ, Helgason T (2014) What goes in must come out: testing for biases in molecular analysis of arbuscular mycorrhizal fungal communities. PLoS ONE. doi:10.1371/journal.pone.0109234 Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS ONE 7, e41938 De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574 De Souza FA, Declerck S (2003) Mycelium development and architecture, and spore production of Scutellospora reticulata in monoxenic culture with Ri T-DNA transformed carrot roots. Mycologia 95:1004–1012 Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:775–785 Diaz G, Honrubia M (1994) A mycorrhizal survey of plants growing on mine wastes in Southeast Spain. Arid Land Res Manag 8:59–68 Doncaster CC (1962) Nematode feeding mechanisms. 1. Observations on Rhabditis and Pelodera. Nematologica 8:313–320 Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804 Fitzjohn RG, Dickie IA (2007) TRAMPR: AN R package for analysis and matching of terminal restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7:583–587 Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from the soil by wet sieving and decanting. T Br Mycol Soc 46:235–244 Grabherr G, Nagy L, Thompson O (2003) An outline of Europe’s alpine areas. In: Nagy L, Grabherr G, Korner Ch, Thompson OBA (eds) Alpine biodiversity in Europe. Ecological Series Berlin, Heidelberg Springer 167:3–12 Gryndler M, Hršelová H, Cajthaml T, Havránková M, Řezáčová V, Gryndlerová H, Larsen J (2009) Influence of soil organic matter decomposition on arbuscular mycorrhizal fungi in terms of asymbiotic hyphal growth and root colonization. Mycorrhiza 19:255–266 Hart MM, Reader JR (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344 Hart MM, Reader JR, Klironomos JN (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93:1186–1194 Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384 Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938 Hetrick BAD, Bloom J (1986) The influence of host plant on production and colonization ability of vesicular-arbuscular mycorrhizal spores. Mycologia 78:32–36 Holland SM (2008) Analytic Rarefaction 1.3. Available at http://strata.uga.edu/software/anRareReadme.html Joner EJ, Jakobsen I (1995) Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. Soil Biol Biochem 27:1153–1159 Jung SC, Martínez-Medina A, López-Ráez JA, Pozo MJ (2012) Mycorrhiza induced resistance and priming of plant defenses. J Chem Ecol 38:651–664 Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M et al (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551 Kjøller R, Rosendahl S (2000) Detection of arbuscular mycorrhizal fungi (Glomales) in roots by nested PCR and SSCP (Single Strand Conformation Polymorphism). Plant Soil 226:189–196 Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184 Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163 Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349 Leifheit EF, Veresoglou SD, Lehmann A et al (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374:523–537 Li LF, Li T, Zhang Y, Zhao ZW (2010) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71:418–427 Liu Y, He L, An LZ, Helgason T, Feng HY (2009) Arbuscular mycorrhizal dynamics in a chronosequence of Caragana korshinskii plantations. FEMS Microbiol Ecol 67:81–92 López-García A, Azcón-Aguilar C, Barea JM (2014a) The interactions between plant life form and fungal traits of arbuscular mycorrhizal fungi determine the symbiotic community. Oecologia 176:1075–1086 López-García A, Palenzuela J, Barea JM, Azcón-Aguilar C (2014b) Life-history strategies of arbuscular mycorrhizal fungi determine succession into roots of Rosmarinus officinalis L., a characteristic woody perennial plant species from Mediterranean ecosystems. Plant Soil 379:247–270 López-Sánchez ME, Honrubia M (1992) Seasonal variation of vesicular-arbuscular mycorrhizae in eroded soils from southern Spain. Mycorrhiza 2:33–39 Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179 Mandyam K, Jumpponen A (2008) Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tall grass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza 18:145–155 Martínez-García LB, Armas C, Miranda JD, Padilla FM, Pugnaire FI (2011) Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environment. Soil Biol Biochem 43:682–689 Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576 Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112 Mayr R, Godoy R (1989) Seasonal patterns in vesicular–arbuscular mycorrhiza in Melic-Beech Forest. Agric Ecosyst Environ 29:281–288 Mcardle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297 Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501 Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364 Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268 Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2015) Vegan: community ecology package. R package version 2.3-1. Available at http://CRAN.R-project.org/package=vegan Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790 Öpik M, Moora M, Zobel M, Saks Ü, Wheatley R, Wright F, Daniell TJ (2008) High diversity of arbuscular mycorrhizal fungi in a boreal, herb rich, coniferous forest. New Phytol 179:867–876 Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437 Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241 Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Br Mycol Soc 55:158–161 Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. P Roy Soc B-Biol Sci 276:4237–4245 Pozo MJ, Lopez-Raez JA, Azcon-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436 Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893 Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53 Rodríguez-Echeverría S, Gera Hol WH, Freitas H, Eason, Cook R (2008) Arbuscular mycorrhizal fungi of Ammophila arenaria (L.) Link: spore abundance and root colonisation in six locations of the European coast. Eur J Soil Biol 44:30–36 Royston P, Remark AS (1995) R94: a remark on Algorithm AS 181: the W test for normality. Appl Stat 44:547–551 Russo SE, Legge R, Weber KA, Brodie EL, Goldfarb KC, Benson AK, Tan S (2012) Bacterial community structure of contrasting soils underlying Bornean rain forests: inferences from microarray and next-generation sequencing methods. Soil Biol Biochem 55:48–59 Sánchez-Castro I, Ferrol N, Cornejo P, Barea JM (2012) Temporal dynamics of arbuscular mycorrhizal fungi colonizing roots of representative shrub species in a semi-arid Mediterranean ecosystem. Mycorrhiza 22:449–460 Santos-Gonzalez JC, Finlay RD, Tehler A (2007) Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Appl Environ Microbiol 73:5613–5623 Sikes BA, Maherali H, Klironomos JN (2014) Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession. Mycorrhiza 24:219–226 Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular–arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295 Sivakumar N (2013) Effect of edaphic factors and seasonal variation on spore density and root colonization of arbuscular mycorrhizal fungi in sugarcane fields. An Microbiol 63:151–160 Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic, Amsterdam Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20 Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 Tichy L, Chytry M (2006) Statistical determination of diagnostic species for site groups of unequal size. J Veg Sci 17:809–818 van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091 van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72 van der Heijden MGA, Scheublin TR, Brader A (2004) Taxonomic and functional diversity in arbuscular mycorrhizal fungi–is there any relationship? New Phytol 164:201–204 van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310 van der Heijden MGA, Martin FM, Selosse MA, Sanders I (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423 Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095 Varela-Cervero S, Vasar M, Davison J, Barea JM, Öpik M, Azcón-Aguilar C (2015) The composition of arbuscular mycorrhizal fungal communities differs among the roots, spores and extraradical mycelia associated with five Mediterranean plant species. Environ Microbiol 17:2882–2895 Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562 Yang H, Zang Y, Yuan Y, Tang J, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:50–62 Zangaro W, Rostirola L, Souza P, Almeida AR, Lescano L, Rondina A, Nogueira M, Carrenho R (2013) Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221–233