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Breaking new ground at the interface of dendroecology and mycology Ulf Bu¨ntgen1,2,3 and Simon Egli1 1
Swiss Federal Research Institute WSL, Birmensdorf, Switzerland Oeschger Centre for Climate Change Research, Bern, Switzerland 3 Global Change Research Centre AS CR, Brno, Czech Republic 2
New insight on the mycorrhizal fungus–host association, expected to emerge from combining dendrochronology, wood anatomy and mycology, may help to understanding better and disentangle biotic, abiotic, and combined edaphic factors of the mutualistic relation between ectomycorrhizal fungi and their perennial partners. Terrestrial ecosystems, in which the vast majority of higher plants are reciprocally associated with mycorrhizal fungal root symbionts [1], cover most of the landmass of the Earth [2]. Complex mycorrhizal fungus–host interactions thus can have substantial effects on the global carbon cycle [3]. Disentangling biotic (host plants, fungal partners, and rhizospheric bacteria), abiotic (climate, pollution, and land cover), and combined edaphic (soil and microbes) factors of the mutualistic relation between 20 000 ectomycorrhizal fungi and 6000 perennial host species from all biogeographic zones [4], however, describes a considerably challenging task. Many interactions related to the intimate fungus–host dialog therefore remain poorly understood among a wide range of spatial and temporal scales. One little explored way to look at such compound associations emerges at the interface of mycology and dendrochronology, including wood anatomy. Although some first attempts in relating tree growth and plant phenology to mushroom fruiting appear promising [5–8], systematic crossdisciplinary efforts are scarce and the list of pending issues is long. Modern dendroecological studies integrate aspects of historical climatology, ecosystem productivity, plant physiology, and wood anatomy. Mounting evidence, for instance, compels local- to large-scale approaches, biometric and eddy-covariance calculations, high-resolution dendrometer measurements, as well as quantitative wood anatomical parameters, with the latter providing detailed insight on the intra-annual course of cell formation. Meanwhile, advancements in mycological research that focus on longterm monitoring settings and data mining initiatives, enable – at least to a certain degree – changes in fungal phenology and productivity to be linked with local- to synoptic-scale temperature and/or hydroclimatic variability [5– 11]. Meteorological influences, however, may only explain Corresponding author: Bu¨ntgen, U. ([email protected]). Keywords: dendroecology; dendrometer; carbon allocation; ectomycorrhizal fungi; forest ecosystems; fungus–host symbiosis; mushroom growth; mycelial networks; mycology; perennial partners; phenology; tree rings; wood anatomy. 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/ j.tplants.2014.07.001
some of the observed variation in fungal phenology and productivity, implying other factors to be considered. Host plants are crucial for carbon partitioning mechanisms, because large fractions of the photosynthetically fixed carbon are directed below ground to the associated mycorrhizal fungi [12]. Tree growth is thus key in governing mycorrhizal mushrooms. In this regard, new genome analyses and transcriptomics appear promising to provide further insight on a wide range of functional aspects related to the fungus–host symbiosis [13]. Moreover, next-generation sequencing techniques illuminate the below-ground structure and richness of fungal communities [14], and emphasize the ecological importance of common mycelial networks, as well as the relative role mycorrhizal fungi and their perennial partners play in carbon metabolizing [15,16]. Although the yet-separated disciplines of dendroecology, wood anatomy, and mycology generally operate on different timescales, recent endeavors in all of these fields suggest unexpected synergies to arise when combining them. Latest advancement in the precision and interpretation of tree-ring chronologies, together with the performance of quantitative wood anatomy that has been consequently supplemented by intra-annual dendrometer measurements, as well as the new awareness from long-term observational networks of mushroom and mycelial formation, are all indicative of a wide range of methodological and scientific overlap. Here, we prioritize eight inter-related research avenues, ordered from higher to lower resolution. (i) Combine continuous high-resolution dendrometer measurements of cell formation and sap flow with mushroom fruiting body observations and mycelial growth patterns to quantify linkages between the phenology and net primary productivity of mycorrhizal fungi webs and their host plants. (ii) Apply isotopic labeling to trace symbiotic carbon, nutrient and water (host–fungus/fungus–host) pathways and fluxes for different species, environments, and climates, to understand better the continuum between plant growth and ectomycorrhizal fungus energy capture and partition. (iii) Perform field and greenhouse experiments with model host–fungus pairings to quantify the weight abiotic factors may have in the reciprocal transfer of nutrients, phosphorus, water, and carbon in order to predict environmental effects on symbiosis functioning. (iv) Utilize the advent of bioinformatic sensor technologies, such as metagenomic and/or metatranscriptomic analyses or biochemical assays to gauge below-ground functional hyphal activity and compare these data with intra-annual tree-ring patterns. (v) Develop chronologies of different tree-ring and wood Trends in Plant Science xx (2014) 1–2
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advancement of this alliance is further envisioned to understanding better and predict forest feedbacks to the terrestrial carbon cycle and global climate system. Acknowledgments C. Colinas, C. Fischer, H. Kauserud, C. Murat, and F. Schweingruber provided useful comments on earlier manuscript versions. Stimulated by the Micosylva+ meeting in Catalonia, 25–29 January 2014 (SOE3/P2/ E533), and supported by the WSL-internal DITREC project, the ClimFun project of the Norwegian Research Council (No. 225043), the Ernst Go¨hner Foundation, as well as the Operational Programme of Education for Competitiveness of Ministry of Education, Youth, and Sports of the Czech Republic (No. CZ.1.07/2.3.00/20.0248).
References
TRENDS in Plant Science
Figure 1. Truffle peridium. Microscopic magnification of the surface (peridium) of a belowground Burgundy truffle (Tuber aestivum Vittad.) reveals surprisingly distinct horizontal black/gray layers (i.e., growth rings). These structures are most likely synchronized across the individual verruca and possibly also among individual fruit bodies, therefore, they may reflect daily changes in their environment [18]. However, the origin of these increments remains enigmatic, and thus calls for the installation of high-resolution measurements of microclimatic variability and host vitality by using in situ soil/air sensors and dendrometer bands are required.
anatomical parameters to reconstruct impacts of forest management on fungal phenology and productivity, including the assessment of truffle orchards in drought-prone Mediterranean habitats. (vi) Test if increased photosynthesis (in tandem with increased vegetation growth) fosters carbon sequestration in ectomycorrhizal ecosystems, such as the boreal zone, or whether better carbohydrates access to ectomycorrhizal fungi improves their competitive ability above saprotrophic species, which will tentatively lead to higher carbon accumulation rates. (vii) Relate longterm mushroom monitoring inventories to tree-ring chronologies and meteorological records to analyze direct and indirect climatic drivers of the productivity and phenology of fruit body production, even involving ascomycetes (Figure 1). (viii) Extend crossdisciplinary approaches to the vast number of perennial tree and shrub species symbiotic with ectomycorrhizal fungi, and utilize this new perspective to help parameterize and validate the next generation of general ecosystem models [17]. In summary, we propose merging the yet-separated disciplines of mycology and dendroecology, including wood anatomy, to generate scientific synergy for detecting and disentangling biotic, abiotic, and combined edaphic factors of the mutualistic relation between thousands of ectomycorrhizal fungi and their perennial partners. Conceptual
2
1 Brundrett, M.C. (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 2 Friedl, M.A. (2010) MODIS Collection 5 global land cover: algorithm refinements and characterization of new datasets. Remote Sens. Environ. 114, 168–182 3 Averill, C. et al. (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 4 Tedersoo, L. et al. (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 5 Bu¨ntgen, U. et al. (2012) Linking mushroom productivity and phenology to climate variability. Front. Ecol. Environ. 10, 14–19 6 Bu¨ntgen, U. et al. (2012) Drought-induced decline in Mediterranean truffle harvest. Nat. Clim. Change 2, 827–829 7 Bu¨ntgen, U. et al. (2013) Unraveling environmental drivers of a recent increase in Swiss fungi fruiting. Glob. Change Biol. 19, 2785–2794 8 Egli, S. et al. (2010) Is forest mushroom productivity driven by tree growth? Results from a thinning experiment. Ann. For. Sci. 67, 509 9 Kauserud, H. et al. (2012) Warming-induced shift in European mushroom fruiting phenology. Proc. Natl. Acad. Sci. U.S.A. 109, 14488–14493 10 Diez, J. et al. (2013) Predicting species-specific responses of fungi to climatic variation using historical records. Glob. Change Biol. 19, 3145–3154 11 Boddy, L. et al. (2014) Climate variation effects on fungal fruiting. Fungal Ecol. 10, 20–33 12 Ho¨gberg, P. et al. (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792 13 Martin, F. et al. (2010) Pe´rigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033–1038 14 Lindahl, B.D. et al. (2013) Fungal community analysis by highthroughput sequencing of amplified markers – a user’s guide. New Phytol. 199, 288–299 15 Song, Y.Y. et al. (2014) Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Nat. Sci. Rep. 4, 3915 16 Clemmensen, K.E. et al. (2013) Roots and associated fungi drive longterm carbon sequestration in boreal forest. Science 339, 1615–1618 17 Pruves, D. et al. (2013) Time to model all life on Earth. Nature 493, 295–297 18 Bu¨ntgen, U. et al. (2011) Truffles and climate change. Front. Ecol. Environ. 9, 150–151
Forum
Breaking new ground at the interface of dendroecology and mycology Ulf Bu¨ntgen1,2,3 and Simon Egli1 1
Swiss Federal Research Institute WSL, Birmensdorf, Switzerland Oeschger Centre for Climate Change Research, Bern, Switzerland 3 Global Change Research Centre AS CR, Brno, Czech Republic 2
New insight on the mycorrhizal fungus–host association, expected to emerge from combining dendrochronology, wood anatomy and mycology, may help to understanding better and disentangle biotic, abiotic, and combined edaphic factors of the mutualistic relation between ectomycorrhizal fungi and their perennial partners. Terrestrial ecosystems, in which the vast majority of higher plants are reciprocally associated with mycorrhizal fungal root symbionts [1], cover most of the landmass of the Earth [2]. Complex mycorrhizal fungus–host interactions thus can have substantial effects on the global carbon cycle [3]. Disentangling biotic (host plants, fungal partners, and rhizospheric bacteria), abiotic (climate, pollution, and land cover), and combined edaphic (soil and microbes) factors of the mutualistic relation between 20 000 ectomycorrhizal fungi and 6000 perennial host species from all biogeographic zones [4], however, describes a considerably challenging task. Many interactions related to the intimate fungus–host dialog therefore remain poorly understood among a wide range of spatial and temporal scales. One little explored way to look at such compound associations emerges at the interface of mycology and dendrochronology, including wood anatomy. Although some first attempts in relating tree growth and plant phenology to mushroom fruiting appear promising [5–8], systematic crossdisciplinary efforts are scarce and the list of pending issues is long. Modern dendroecological studies integrate aspects of historical climatology, ecosystem productivity, plant physiology, and wood anatomy. Mounting evidence, for instance, compels local- to large-scale approaches, biometric and eddy-covariance calculations, high-resolution dendrometer measurements, as well as quantitative wood anatomical parameters, with the latter providing detailed insight on the intra-annual course of cell formation. Meanwhile, advancements in mycological research that focus on longterm monitoring settings and data mining initiatives, enable – at least to a certain degree – changes in fungal phenology and productivity to be linked with local- to synoptic-scale temperature and/or hydroclimatic variability [5– 11]. Meteorological influences, however, may only explain Corresponding author: Bu¨ntgen, U. ([email protected]). Keywords: dendroecology; dendrometer; carbon allocation; ectomycorrhizal fungi; forest ecosystems; fungus–host symbiosis; mushroom growth; mycelial networks; mycology; perennial partners; phenology; tree rings; wood anatomy. 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/ j.tplants.2014.07.001
some of the observed variation in fungal phenology and productivity, implying other factors to be considered. Host plants are crucial for carbon partitioning mechanisms, because large fractions of the photosynthetically fixed carbon are directed below ground to the associated mycorrhizal fungi [12]. Tree growth is thus key in governing mycorrhizal mushrooms. In this regard, new genome analyses and transcriptomics appear promising to provide further insight on a wide range of functional aspects related to the fungus–host symbiosis [13]. Moreover, next-generation sequencing techniques illuminate the below-ground structure and richness of fungal communities [14], and emphasize the ecological importance of common mycelial networks, as well as the relative role mycorrhizal fungi and their perennial partners play in carbon metabolizing [15,16]. Although the yet-separated disciplines of dendroecology, wood anatomy, and mycology generally operate on different timescales, recent endeavors in all of these fields suggest unexpected synergies to arise when combining them. Latest advancement in the precision and interpretation of tree-ring chronologies, together with the performance of quantitative wood anatomy that has been consequently supplemented by intra-annual dendrometer measurements, as well as the new awareness from long-term observational networks of mushroom and mycelial formation, are all indicative of a wide range of methodological and scientific overlap. Here, we prioritize eight inter-related research avenues, ordered from higher to lower resolution. (i) Combine continuous high-resolution dendrometer measurements of cell formation and sap flow with mushroom fruiting body observations and mycelial growth patterns to quantify linkages between the phenology and net primary productivity of mycorrhizal fungi webs and their host plants. (ii) Apply isotopic labeling to trace symbiotic carbon, nutrient and water (host–fungus/fungus–host) pathways and fluxes for different species, environments, and climates, to understand better the continuum between plant growth and ectomycorrhizal fungus energy capture and partition. (iii) Perform field and greenhouse experiments with model host–fungus pairings to quantify the weight abiotic factors may have in the reciprocal transfer of nutrients, phosphorus, water, and carbon in order to predict environmental effects on symbiosis functioning. (iv) Utilize the advent of bioinformatic sensor technologies, such as metagenomic and/or metatranscriptomic analyses or biochemical assays to gauge below-ground functional hyphal activity and compare these data with intra-annual tree-ring patterns. (v) Develop chronologies of different tree-ring and wood Trends in Plant Science xx (2014) 1–2
1
TRPLSC-1203; No. of Pages 2
Forum
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
advancement of this alliance is further envisioned to understanding better and predict forest feedbacks to the terrestrial carbon cycle and global climate system. Acknowledgments C. Colinas, C. Fischer, H. Kauserud, C. Murat, and F. Schweingruber provided useful comments on earlier manuscript versions. Stimulated by the Micosylva+ meeting in Catalonia, 25–29 January 2014 (SOE3/P2/ E533), and supported by the WSL-internal DITREC project, the ClimFun project of the Norwegian Research Council (No. 225043), the Ernst Go¨hner Foundation, as well as the Operational Programme of Education for Competitiveness of Ministry of Education, Youth, and Sports of the Czech Republic (No. CZ.1.07/2.3.00/20.0248).
References
TRENDS in Plant Science
Figure 1. Truffle peridium. Microscopic magnification of the surface (peridium) of a belowground Burgundy truffle (Tuber aestivum Vittad.) reveals surprisingly distinct horizontal black/gray layers (i.e., growth rings). These structures are most likely synchronized across the individual verruca and possibly also among individual fruit bodies, therefore, they may reflect daily changes in their environment [18]. However, the origin of these increments remains enigmatic, and thus calls for the installation of high-resolution measurements of microclimatic variability and host vitality by using in situ soil/air sensors and dendrometer bands are required.
anatomical parameters to reconstruct impacts of forest management on fungal phenology and productivity, including the assessment of truffle orchards in drought-prone Mediterranean habitats. (vi) Test if increased photosynthesis (in tandem with increased vegetation growth) fosters carbon sequestration in ectomycorrhizal ecosystems, such as the boreal zone, or whether better carbohydrates access to ectomycorrhizal fungi improves their competitive ability above saprotrophic species, which will tentatively lead to higher carbon accumulation rates. (vii) Relate longterm mushroom monitoring inventories to tree-ring chronologies and meteorological records to analyze direct and indirect climatic drivers of the productivity and phenology of fruit body production, even involving ascomycetes (Figure 1). (viii) Extend crossdisciplinary approaches to the vast number of perennial tree and shrub species symbiotic with ectomycorrhizal fungi, and utilize this new perspective to help parameterize and validate the next generation of general ecosystem models [17]. In summary, we propose merging the yet-separated disciplines of mycology and dendroecology, including wood anatomy, to generate scientific synergy for detecting and disentangling biotic, abiotic, and combined edaphic factors of the mutualistic relation between thousands of ectomycorrhizal fungi and their perennial partners. Conceptual
2
1 Brundrett, M.C. (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 2 Friedl, M.A. (2010) MODIS Collection 5 global land cover: algorithm refinements and characterization of new datasets. Remote Sens. Environ. 114, 168–182 3 Averill, C. et al. (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 4 Tedersoo, L. et al. (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 5 Bu¨ntgen, U. et al. (2012) Linking mushroom productivity and phenology to climate variability. Front. Ecol. Environ. 10, 14–19 6 Bu¨ntgen, U. et al. (2012) Drought-induced decline in Mediterranean truffle harvest. Nat. Clim. Change 2, 827–829 7 Bu¨ntgen, U. et al. (2013) Unraveling environmental drivers of a recent increase in Swiss fungi fruiting. Glob. Change Biol. 19, 2785–2794 8 Egli, S. et al. (2010) Is forest mushroom productivity driven by tree growth? Results from a thinning experiment. Ann. For. Sci. 67, 509 9 Kauserud, H. et al. (2012) Warming-induced shift in European mushroom fruiting phenology. Proc. Natl. Acad. Sci. U.S.A. 109, 14488–14493 10 Diez, J. et al. (2013) Predicting species-specific responses of fungi to climatic variation using historical records. Glob. Change Biol. 19, 3145–3154 11 Boddy, L. et al. (2014) Climate variation effects on fungal fruiting. Fungal Ecol. 10, 20–33 12 Ho¨gberg, P. et al. (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792 13 Martin, F. et al. (2010) Pe´rigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033–1038 14 Lindahl, B.D. et al. (2013) Fungal community analysis by highthroughput sequencing of amplified markers – a user’s guide. New Phytol. 199, 288–299 15 Song, Y.Y. et al. (2014) Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Nat. Sci. Rep. 4, 3915 16 Clemmensen, K.E. et al. (2013) Roots and associated fungi drive longterm carbon sequestration in boreal forest. Science 339, 1615–1618 17 Pruves, D. et al. (2013) Time to model all life on Earth. Nature 493, 295–297 18 Bu¨ntgen, U. et al. (2011) Truffles and climate change. Front. Ecol. Environ. 9, 150–151
