Non-structural carbohydrate concentrations of Fagus sylvatica and Pinus sylvestris fine roots are linked to ectomycorrhizal enzymatic activity during spring reactivation

. 2020 May ; 30 (2-3) : 197-210. [epub] 20200220

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32078049

Grantová podpora
GPF333996 H2020 Marie Skłodowska-Curie Actions
LO1415 Bundesministerium für Verkehr, Innovation und Technologie

Odkazy

PubMed 32078049
PubMed Central PMC7228962
DOI 10.1007/s00572-020-00939-x
PII: 10.1007/s00572-020-00939-x
Knihovny.cz E-zdroje

We evaluated whether changes in fine root non-structural carbohydrate reserves of Fagus sylvatica and Pinus sylvestris trees influence potential enzymatic activities of their ectomycorrhizal symbionts from winter towards spring reactivation, and whether these changes influence potential soil enzymatic activities. We analyzed sugar and starch concentrations in the fine roots of Fagus sylvatica and Pinus sylvestris and potential activities of ß-glucosidase, ß-xylosidase, and cellobiohydrolase (as proxies for carbon-degrading enzymes) as well as leucine aminopeptidase and chitinase (as proxies for nitrogen-degrading enzymes) of their dominant ectomycorrhizal symbionts as well as in the soil. Sugar concentrations in the fine roots were significantly positively correlated with enzymatic activities of the ectomycorrhizal symbionts. In Pinus sylvestris, both carbon- and nitrogen-degrading enzyme activities showed significant positive correlations with fine root sugar concentrations. In Fagus sylvatica, fine root sugar concentrations were explicitly positively correlated with the activity of nitrogen-degrading enzymes. The chitinase activity in the soil was found to be strongly positively correlated with the enzymatic activity of the ectomycorrhizal symbionts as well as with fine root sugar concentrations. Fine root carbohydrate concentrations of Fagus sylvatica and Pinus sylvestris trees and enzymatic activities of their associated ectomycorrhizal fungi are connected. The specific nutrient demand of the tree species during spring reactivation may affect ectomycorrhizal enzymatic activity via carbon mobilization in the fine roots of Fagus sylvatica and Pinus sylvestris. Moreover, our results suggest that trees indirectly contribute to the degradation of fungal necromass by stimulating ectomycorrhizal chitinase activity in the soil.

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Agerer R. Colour atlas of ectomycorrhizae. Schwäbisch Gmünd: Einhorn-Verlag; 1987.

Averill C, Hawkes CV. Ectomycorrhizal fungi slow soil carbon cycling. Ecol Lett. 2016;19:937–947. PubMed

Baber K, Otto P, Kahl T, Gossner MM, Wirth C, Gminder A, Bässler C. Disentangling the effects of forest-stand type and dead-wood origin of the early successional stage on the diversity of wood-inhabiting fungi. For Ecol Manag. 2016;377:161–169.

Barbaroux C, Bréda N. Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiol. 2002;22:1201–1210. PubMed

Barbaroux C, Bréda N, Dufrêne E. Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica) New Phytol. 2003;157:605–615. PubMed

Bazot S, Barthes L, Blanot D, Fresneau C. Distribution of non-structural nitrogen and carbohydrate compounds in mature oak trees in a temperate forest at four key phenological stages. Trees. 2013;27:1023–1034.

Bödeker I, Clemmensen KE, Boer W, Martin F, Olson Å, Lindahl BD. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol. 2014;203:245–256. PubMed

Brunner I, Bakker MR, Björk RG, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset TD, Helmisaari H-S, Jourdan C. Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil. 2013;362:357–372.

Buée M, Vairelles D, Garbaye J. Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza. 2005;15:235–245. PubMed

Chapin FS, Johnson DA, McKendrick JD (1980) Seasonal movement of nutrients in plants of differing growth form in an Alaskan tundra ecosystem: implications for herbivory. J Ecol:189–209

Chapin FS, Kedrowski RA. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology. 1983;64:376–391.

Chapin FS, Schulze E, Mooney HA. The ecology and economics of storage in plants. Annu Rev Ecol Syst. 1990;21:423–447.

Cheeke TE, Phillips RP, Brzostek ER, Rosling A, Bever JD, Fransson P. Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol. 2017;214:432–442. PubMed

Chow PS, Landhäusser SM. A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol. 2004;24:1129–1136. PubMed

Courty P-E, Bréda N, Garbaye J. Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol Biochem. 2007;39:1655–1663.

Courty P-E, Franc A, Garbaye J. Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem. 2010;42:2022–2025.

Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol. 2005;167:309–319. PubMed

Cullings K, Courty P-E. Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia. 2009;161:661–664. PubMed

Cullings K, Ishkhanova G, Henson J. Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park. Oecologia. 2008;158:77. PubMed

Dahiya N, Tewari R, Hoondal GS. Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol. 2006;71:773–782. PubMed

Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R. Nonstructural carbon in woody plants. Annu Rev Plant Biol. 2014;65:667–687. PubMed

Drigo B, Anderson IC, Kannangara G, Cairney JW, Johnson D. Rapid incorporation of carbon from ectomycorrhizal mycelial necromass into soil fungal communities. Soil Biol Biochem. 2012;49:4–10.

Ekblad A, Wallander H, Godbold D, Cruz C, Johnson D, Baldrian P, Björk R, Epron D, Kieliszewska-Rokicka B, Kjøller R. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil. 2013;366:1–27.

Finér L, Helmisaari H-S, Lõhmus K, Majdi H, Brunner I, Børja I, Eldhuset T, Godbold D, Grebenc T, Konôpka B. Variation in fine root biomass of three European tree species: beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.), and scots pine (Pinus sylvestris L.) Plant Biosyst. 2007;141:394–405.

Fischer C, Höll W. Food reserves of Scots pine (Pinus sylvestris L.) Trees. 1991;5:187–195.

Furze ME, Huggett BA, Aubrecht DM, Stolz CD, Carbone MS, Richardson AD. Whole-tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species. New Phytol. 2018;221:1466–1477. PubMed PMC

German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem. 2011;43:1387–1397.

Hartmann H, Trumbore S. Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytol. 2016;211:386–403. PubMed

Hobbie EA, Ouimette AP, Schuur EA, Kierstead D, Trappe JM, Bendiksen K, Ohenoja E. Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi. Biogeochemistry. 2013;114:381–389.

Hoch G, Richter A, Körner C. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 2003;26:1067–1081.

Hodge A, Alexander IJ, Gooday GW. Chitinolytic enzymes of pathogenic and ectomycorrhizal fungi. Mycol Res. 1995;99:935–941.

Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs–a hypothesis based on field observations in boreal forest. New Phytol. 2003;160:225–238. PubMed

Högberg MN, Briones MJ, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T. Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol. 2010;187:485–493. PubMed

Hupperts SF, Karst J, Pritsch K, Landhäusser SM. Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest. Funct Ecol. 2017;31:116–126.

IUSS Working Group W (2006) World reference base for soil resources. World Soil Resour Rep 103

Jany J-L, Martin F, Garbaye J. Respiration activity of ectomycorrhizas from Cenococcum geophilum and Lactarius sp. in relation to soil water potential in five beech forests. Plant Soil. 2003;255:487–494.

Jany JL, Garbaye J, Martin F. Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytol. 2002;154:651–659. PubMed

Johnson NC, Angelard C, Sanders IR, Kiers ET. Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol Lett. 2013;16:140–153. PubMed

Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol. 2010;187:843–858. PubMed PMC

Klein T, Vitasse Y, Hoch G. Coordination between growth, phenology and carbon storage in three coexisting deciduous tree species in a temperate forest. Tree Physiol. 2016;36:847–855. PubMed

Körner C. Carbon limitation in trees. J Ecol. 2003;91:4–17.

Kramer P, Kozlowski T. Physiology of woody plants. New York: Academic Press; 1979.

Lindahl BD, Tunlid A. Ectomycorrhizal fungi–potential organic matter decomposers, yet not saprotrophs. New Phytol. 2015;205:1443–1447. PubMed

LoBuglio KF, Rogers SO, Wang C. Variation in ribosomal DNA among isolates of the mycorrhizal fungus Cenococcum geophilum. Can J Bot. 1991;69:2331–2343.

Loewe A, Einig W, Shi L, Dizengremel P, Hampp R. Mycorrhiza formation and elevated CO 2 both increase the capacity for sucrose synthesis in source leaves of spruce and aspen. New Phytol. 2000;145:565–574. PubMed

Marschner H (2011) Marschner's mineral nutrition of higher plants. Academic press

Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol. 2016;14:760. PubMed

Marx M-C, Wood M, Jarvis S. A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem. 2001;33:1633–1640.

Mei L, Xiong Y, Gu J, Wang Z, Guo D. Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees. Oecologia. 2015;177:333–344. PubMed

Miller M, Palojärvi A, Rangger A, Reeslev M, Kjøller A. The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol. 1998;64:613–617. PubMed PMC

Nehls U. Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot. 2008;59:1097–1108. PubMed

Nehls U, Göhringer F, Wittulsky S, Dietz S. Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol. 2010;12:292–301. PubMed

Nehls U, Mikolajewski S, Magel E, Hampp R. Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol. 2001;150:533–541.

Ögren E. Maintenance respiration correlates with sugar but not nitrogen concentration in dormant plants. Physiol Plant. 2000;108:295–299.

Phillips LA, Ward V, Jones MD. Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME J. 2014;8:699–713. PubMed PMC

Piispanen R, Saranpää P. Variation of non-structural carbohydrates in silver birch (Betula pendula Roth) wood. Trees. 2001;15:444–451.

Pretzsch H, Del Río M, Ammer C, Avdagic A, Barbeito I, Bielak K, Brazaitis G, Coll L, Dirnberger G, Drössler L. Growth and yield of mixed versus pure stands of scots pine (Pinus sylvestris L.) and European beech (Fagus sylvatica L.) analysed along a productivity gradient through Europe. Eur J For Res. 2015;134:927–947.

Pringle EG. Integrating plant carbon dynamics with mutualism ecology. New Phytol. 2016;210:71–75. PubMed

Pritsch K, Courty PE, Churin J-L, Cloutier-Hurteau B, Ali MA, Damon C, Duchemin M, Egli S, Ernst J, Fraissinet-Tachet L. Optimized assay and storage conditions for enzyme activity profiling of ectomycorrhizae. Mycorrhiza. 2011;21:589–600. PubMed

Pritsch K, Garbaye J. Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter. Ann For Sci. 2011;68:25–32.

Pritsch K, Raidl S, Marksteiner E, Blaschke H, Agerer R, Schloter M, Hartmann A. A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system. J Microbiol Methods. 2004;58:233–241. PubMed

Rastin N, Rosenplänter K, Hüttermann A. Seasonal variation of enzyme activity and their dependence on certain soil factors in a beech forest soil. Soil Biol Biochem. 1988;20:637–642.

Rastin N, Schlechte G, Hüttermann A, Rosenplänter K. Seasonal fluctuation of some biological and biochemical soil factors and their dependence on certain soil factors on the upper and lower slope of a spruce forest. Soil Biol Biochem. 1990;22:1049–1061.

Read D, Perez-Moreno J. Mycorrhizas and nutrient cycling in ecosystems–a journey towards relevance? New Phytol. 2003;157:475–492. PubMed

Ribbons RR, Levy-Booth DJ, Masse J, Grayston SJ, McDonald MA, Vesterdal L, Prescott CE. Linking microbial communities, functional genes and nitrogen-cycling processes in forest floors under four tree species. Soil Biol Biochem. 2016;103:181–191.

Richardson AD, Carbone MS, Huggett BA, Furze ME, Czimczik CI, Walker JC, Xu X, Schaberg PG, Murakami P. Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytol. 2015;206:590–597. PubMed PMC

Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami P, Schaberg PG, Xu X. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol. 2013;197:850–861. PubMed

Rineau F, Courty P-E. Secreted enzymatic activities of ectomycorrhizal fungi as a case study of functional diversity and functional redundancy. Ann For Sci. 2011;68:69–80.

Saiya-Cork K, Sinsabaugh R, Zak D. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem. 2002;34:1309–1315.

Scartazza A, Moscatello S, Matteucci G, Battistelli A, Brugnoli E. Seasonal and inter-annual dynamics of growth, non-structural carbohydrates and C stable isotopes in a Mediterranean beech forest. Tree Physiol. 2013;33:730–742. PubMed

Schädel C, Blöchl A, Richter A, Hoch G. Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol. 2009;29:901–911. PubMed

Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau F, Canbäck B, Floudas D, Carleer R, Lackner G. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 2016;209:1705–1719. PubMed PMC

Simard SW, Jones MD, Durall DM (2003) Carbon and nutrient fluxes within and between mycorrhizal plants. Mycorrhizal ecology. Springer

Sinsabaugh RL, Carreiro MM, Alvarez S. Enzyme and microbial dynamics of litter decomposition. New York: Enzymes in the Environment, Activity, Ecology, and Applications Marcel Dekker; 2002. pp. 249–265.

Sinsabaugh RL, Follstad Shah JJ. Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst. 2012;43:313–343.

Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME. Stoichiometry of soil enzyme activity at global scale. Ecol Lett. 2008;11:1252–1264. PubMed

Smith MG, Miller RE, Arndt SK, Kasel S, Bennett LT. Whole-tree distribution and temporal variation of non-structural carbohydrates in broadleaf evergreen trees. Tree Physiol. 2017;38:570–581. PubMed

Smith S, Read D. Mycorrhizal symbiosis. 3. San Diego: Academic Press; 2008.

Swaty RL, Gehring CA, Van Ert M, Theimer TC, Keim P, Whitham TG. Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites. New Phytol. 1998;139:733–739.

Talbot J, Allison S, Treseder K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol. 2008;22:955–963.

Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol Biochem. 2013;57:282–291.

Trap J, Akpa-Vinceslas M, Margerie P, Boudsocq S, Richard F, Decaëns T, Aubert M. Slow decomposition of leaf litter from mature Fagus sylvatica trees promotes offspring nitrogen acquisition by interacting with ectomycorrhizal fungi. J Ecol. 2017;105:528–539.

Trumbore S, Czimczik CI, Sierra CA, Muhr J, Xu X. Non-structural carbon dynamics and allocation relate to growth rate and leaf habit in California oaks. Tree Physiol. 2015;35:1206–1222. PubMed

van der Heijden MG, Bardgett RD, van Straalen NM. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett. 2008;11:296–310. PubMed

Wallander H, Massicotte H, Nylund J. Seasonal variation in ergosterol, chitin and protein in ectomycorrhizal roots collected in a Swedish pine forest. Soil Biol Biochem. 1997;29:45–53.

Wallander H, Nilsson LO, Hagerberg D, Bååth E. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol. 2001;151:753–760. PubMed

Winston JE (1999) Describing species: practical taxonomic procedure for biologists. Columbia University Press

Wong B, Baggett K, Rye A. Cold-season patterns of reserve and soluble carbohydrates in sugar maple and ice-damaged trees of two age classes following drought. Botany. 2009;87:293–305.

Zanella A, Jabiol B, Ponge J-F, Sartori G, De Waal R, Van Delft B, Graefe U, Cools N, Katzensteiner K, Hager H. A European morpho-functional classification of humus forms. Geoderma. 2011;164:138–145.

Zhang H, Ziegler W, Han X, Trumbore S, Hartmann H. Plant carbon limitation does not reduce nitrogen transfer from arbuscular mycorrhizal fungi to Plantago lanceolata. Plant Soil. 2015;396:369–380.

Žifčáková L, Větrovský T, Howe A, Baldrian P. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol. 2016;18:288–301. PubMed

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