Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms
Abstract
In this study, there is little quantitative information about the relationship between root traits and the extent of arbuscular mycorrhizal fungi (AMF) colonization. We expected that ancestral species with thick roots will maximize AMF habitat by maintaining similar root traits across root orders (i.e., high root trait integration), whereas more derived species are expected to display a sharp transition from acquisition to structural roots. Moreover, we hypothesized that interspecific morphological differences rather than soil conditions will be the main driver of AMF colonization We analyzed 14 root morphological and chemical traits and AMF colonization rates for the first three root orders of 34 temperate tree species grown in two common gardens. We also collected associated soil to measure the effect of soil conditions on AMF colonization Results Thick-root magnoliids showed less variation in root traits along root orders than more-derived angiosperm groups. Variation in stele:root diameter ratio was the best indicator of AMF colonization within and across root orders. Root functional traits rather than soil conditions largely explained the variation in AMF colonization among species. In conclusion, not only the traits of first order but the entire structuring of the root system varied among plant lineages, suggesting alternative evolutionary strategiesmore »
- Authors:
-
- Kent State Univ., Kent, OH (United States)
- Kent State Univ., Kent, OH (United States); The Holden Arboretum, Kirtland, OH (United States)
- Publication Date:
- Research Org.:
- Kent State Univ., Kent, OH (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1247638
- Grant/Contract Number:
- SC0004335
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant and Soil
- Additional Journal Information:
- Journal Name: Plant and Soil; Journal ID: ISSN 0032-079X
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; root functional traits; angiosperm evolution; arbuscular mycorrhizal fungi; root order integration; cortex area; nutrient uptake strategies
Citation Formats
Valverde-Barrantes, Oscar J., Horning, Amber L., Smemo, Kurt A., and Blackwood, Christopher B. Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. United States: N. p., 2016.
Web. doi:10.1007/s11104-016-2820-6.
Valverde-Barrantes, Oscar J., Horning, Amber L., Smemo, Kurt A., & Blackwood, Christopher B. Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. United States. https://doi.org/10.1007/s11104-016-2820-6
Valverde-Barrantes, Oscar J., Horning, Amber L., Smemo, Kurt A., and Blackwood, Christopher B. Wed .
"Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms". United States. https://doi.org/10.1007/s11104-016-2820-6. https://www.osti.gov/servlets/purl/1247638.
@article{osti_1247638,
title = {Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms},
author = {Valverde-Barrantes, Oscar J. and Horning, Amber L. and Smemo, Kurt A. and Blackwood, Christopher B.},
abstractNote = {In this study, there is little quantitative information about the relationship between root traits and the extent of arbuscular mycorrhizal fungi (AMF) colonization. We expected that ancestral species with thick roots will maximize AMF habitat by maintaining similar root traits across root orders (i.e., high root trait integration), whereas more derived species are expected to display a sharp transition from acquisition to structural roots. Moreover, we hypothesized that interspecific morphological differences rather than soil conditions will be the main driver of AMF colonization We analyzed 14 root morphological and chemical traits and AMF colonization rates for the first three root orders of 34 temperate tree species grown in two common gardens. We also collected associated soil to measure the effect of soil conditions on AMF colonization Results Thick-root magnoliids showed less variation in root traits along root orders than more-derived angiosperm groups. Variation in stele:root diameter ratio was the best indicator of AMF colonization within and across root orders. Root functional traits rather than soil conditions largely explained the variation in AMF colonization among species. In conclusion, not only the traits of first order but the entire structuring of the root system varied among plant lineages, suggesting alternative evolutionary strategies of resource acquisition. Understanding evolutionary pathways in below ground organs could open new avenues to understand tree species influence on soil carbon and nutrient cycling.},
doi = {10.1007/s11104-016-2820-6},
journal = {Plant and Soil},
number = ,
volume = ,
place = {United States},
year = {Wed Feb 10 00:00:00 EST 2016},
month = {Wed Feb 10 00:00:00 EST 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 58 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Variation of first-order root traits across climatic gradients and evolutionary trends in geological time: Root trait variation and evolution
journal, February 2013
- Chen, Weile; Zeng, Hui; Eissenstat, David M.
- Global Ecology and Biogeography, Vol. 22, Issue 7
Forward Selection of Explanatory Variables
journal, September 2008
- Blanchet, F. Guillaume; Legendre, Pierre; Borcard, Daniel
- Ecology, Vol. 89, Issue 9
Ephemeral root modules in Fraxinus mandshurica
journal, September 2010
- Xia, Mengxue; Guo, Dali; Pregitzer, Kurt S.
- New Phytologist, Vol. 188, Issue 4
Fine-root mass, growth and nitrogen content for six tropical tree species
journal, December 2006
- Valverde-Barrantes, Oscar J.; Raich, James W.; Russell, Ann E.
- Plant and Soil, Vol. 290, Issue 1-2
Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure
journal, February 2011
- Goebel, Marc; Hobbie, Sarah E.; Bulaj, Bartosz
- Ecological Monographs, Vol. 81, Issue 1
Resource limitation is a driver of local adaptation in mycorrhizal symbioses
journal, January 2010
- Johnson, N. C.; Wilson, G. W. T.; Bowker, M. A.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 5
Variation Partitioning of Species data Matrices: Estimation and Comparison of Fractions
journal, October 2006
- Peres-Neto, Pedro R.; Legendre, Pierre; Dray, Stéphane
- Ecology, Vol. 87, Issue 10
Multi-functionality and biodiversity in arbuscular mycorrhizas
journal, October 1995
- Newsham, K. K.; Fitter, A. H.; Watkinson, A. R.
- Trends in Ecology & Evolution, Vol. 10, Issue 10
Anatomical aspects of angiosperm root evolution
journal, January 2013
- Seago, James L.; Fernando, Danilo D.
- Annals of Botany, Vol. 112, Issue 2
A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies
journal, July 2004
- Treseder, Kathleen K.
- New Phytologist, Vol. 164, Issue 2
Evolutionary Patterns and Biogeochemical Significance of Angiosperm Root Traits
journal, July 2012
- Comas, L. H.; Mueller, K. E.; Taylor, L. L.
- International Journal of Plant Sciences, Vol. 173, Issue 6
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011
- Revell, Liam J.
- Methods in Ecology and Evolution, Vol. 3, Issue 2
Fine roots of trees - a new perspective
journal, May 2002
- Pregitzer, Kurt S.
- New Phytologist, Vol. 154, Issue 2
adephylo: new tools for investigating the phylogenetic signal in biological traits
journal, June 2010
- Jombart, Thibaut; Balloux, François; Dray, Stéphane
- Bioinformatics, Vol. 26, Issue 15
Evo-devo and constraints on selection
journal, July 2006
- Brakefield, Paul M.
- Trends in Ecology & Evolution, Vol. 21, Issue 7
Fine root decay rates vary widely among lowland tropical tree species
journal, May 2009
- Raich, James W.; Russell, Ann E.; Valverde-Barrantes, Oscar
- Oecologia, Vol. 161, Issue 2
Root traits and taxonomic affiliation of nine herbaceous species grown in glasshouse conditions
journal, July 2008
- Roumet, Catherine; Lafont, Françoise; Sari, Muhaymina
- Plant and Soil, Vol. 312, Issue 1-2
Darkness visible: reflections on underground ecology
journal, April 2005
- Fitter, A. H.
- Journal of Ecology, Vol. 93, Issue 2
Specific root length as an indicator of environmental change
journal, November 2007
- Ostonen, I.; Püttsepp, Ü.; Biel, C.
- Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, Vol. 141, Issue 3
Are trade-offs in allocation pattern and root morphology related to species abundance? A congeneric comparison between rare and common species in the south-western Australian flora
journal, February 2003
- Poot, Pieter; Lambers, Hans
- Journal of Ecology, Vol. 91, Issue 1
Phylogenetic distribution and evolution of mycorrhizas in land plants
journal, May 2006
- Wang, B.; Qiu, Y. -L.
- Mycorrhiza, Vol. 16, Issue 5
The distribution of below-ground traits is explained by intrinsic species differences and intraspecific plasticity in response to root neighbours
journal, June 2013
- Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Feinstein, Larry M.
- Journal of Ecology, Vol. 101, Issue 4
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
journal, July 1990
- McGONIGLE, T. P.; Miller, M. H.; Evans, D. G.
- New Phytologist, Vol. 115, Issue 3
Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions
journal, April 2007
- Hishi, Takuo
- Journal of Forest Research, Vol. 12, Issue 2
Coevolution of roots and mycorrhizas of land plants
journal, May 2002
- Brundrett, Mark C.
- New Phytologist, Vol. 154, Issue 2
Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies
journal, July 2014
- Comas, Louise H.; Callahan, Hilary S.; Midford, Peter E.
- Ecology and Evolution, Vol. 4, Issue 15
Predicting fine root lifespan from plant functional traits in temperate trees
journal, June 2012
- Luke McCormack, M.; Adams, Thomas S.; Smithwick, Erica A. H.
- New Phytologist, Vol. 195, Issue 4
Inferring the historical patterns of biological evolution
journal, October 1999
- Pagel, Mark
- Nature, Vol. 401, Issue 6756
Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology
journal, June 2013
- Hempel, Stefan; Götzenberger, Lars; Kühn, Ingolf
- Ecology, Vol. 94, Issue 6
Within-Species Variation and Measurement Error in Phylogenetic Comparative Methods
journal, April 2007
- Ives, Anthony R.; Midford, Peter E.; Garland, Theodore
- Systematic Biology, Vol. 56, Issue 2
Carbon allocation in forest ecosystems
journal, October 2007
- Litton, Creighton M.; Raich, James W.; Ryan, Michael G.
- Global Change Biology, Vol. 13, Issue 10
Matching roots to their environment
journal, July 2013
- White, Philip J.; George, Timothy S.; Gregory, Peter J.
- Annals of Botany, Vol. 112, Issue 2
Comparisons of Structure and life span in Roots and Leaves Among Temperate Trees
journal, August 2006
- Withington, Jennifer M.; Reich, Peter B.; Oleksyn, Jacek
- Ecological Monographs, Vol. 76, Issue 3
Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test
journal, September 2002
- Treseder, Kathleen K.; Allen, Michael F.
- New Phytologist, Vol. 155, Issue 3
Factors causing variation in fine root biomass in forest ecosystems
journal, January 2011
- Finér, Leena; Ohashi, Mizue; Noguchi, Kyotaro
- Forest Ecology and Management, Vol. 261, Issue 2
Quantifying Phylogenetically Structured Environmental Variation
journal, November 2003
- Desdevises, Yves; Legendre, Pierre; Azouzi, Lamia
- Evolution, Vol. 57, Issue 11
Avoiding inaccuracies in tree calibration and phylogenetic community analysis using Phylocom 4.2
journal, May 2013
- Gastauer, Markus; Meira-Neto, João Augusto Alves
- Ecological Informatics, Vol. 15
The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon
journal, November 2001
- Gaudinski, J.; Trumbore, S.; Davidson, E.
- Oecologia, Vol. 129, Issue 3
Angiosperm Gymnostoma trees produce root nodules colonized by arbuscular mycorrhizal fungi related to Glomus
journal, January 2001
- Duhoux, E.; Rinaudo, G.; Diem, H. G.
- New Phytologist, Vol. 149, Issue 1
Root anatomy of Pinus taeda L.: seasonal and environmental effects on development in seedlings
journal, September 2007
- Kumar, Prem; Hallgren, Stephen W.; Enstone, Daryl E.
- Trees, Vol. 21, Issue 6
Is there an association between root architecture and mycorrhizal growth response?
journal, July 2014
- Maherali, Hafiz
- New Phytologist, Vol. 204, Issue 1
Roots: evolutionary origins and biogeochemical significance
journal, March 2001
- Raven, J. A.; Edwards, D.
- Journal of Experimental Botany, Vol. 52, Issue suppl 1
Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest
journal, June 2004
- Guo, Dali L.; Mitchell, Robert J.; Hendricks, Joseph J.
- Oecologia, Vol. 140, Issue 3
Phylomatic: tree assembly for applied phylogenetics
journal, March 2005
- Webb, Campbell O.; Donoghue, Michael J.
- Molecular Ecology Notes, Vol. 5, Issue 1
Carbon Metabolism and Transport in Arbuscular Mycorrhizas
journal, November 2000
- Bago, Berta; Pfeffer, Philip E.; Shachar-Hill, Yair
- Plant Physiology, Vol. 124, Issue 3
Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species
journal, April 2014
- Gu, J.; Xu, Y.; Dong, X.
- Tree Physiology, Vol. 34, Issue 4
Leading dimensions in absorptive root trait variation across 96 subtropical forest species
journal, May 2014
- Kong, Deliang; Ma, Chengen; Zhang, Qian
- New Phytologist, Vol. 203, Issue 3
Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species
journal, July 1995
- Vogt, Kristiina A.; Vogt, Daniel J.; Palmiotto, Peter A.
- Plant and Soil, Vol. 187, Issue 2
Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas
journal, January 2007
- Janos, David P.
- Mycorrhiza, Vol. 17, Issue 2
The Plant-Fungal Marketplace
journal, August 2011
- Selosse, M. -A.; Rousset, F.
- Science, Vol. 333, Issue 6044
Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees
journal, December 2014
- Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Blackwood, Christopher B.
- Functional Ecology, Vol. 29, Issue 6
Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales: Tansley review
journal, December 2009
- Johnson, Nancy Collins
- New Phytologist, Vol. 185, Issue 3
Natural Selection and Developmental Constraints in the Evolution of Allometries
journal, February 2005
- Frankino, W. A.
- Science, Vol. 307, Issue 5710
A global budget for fine root biomass, surface area, and nutrient contents
journal, July 1997
- Jackson, R. B.; Mooney, H. A.; Schulze, E. - D.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 14
Costs and benefits of constructing roots of small diameter
journal, June 1992
- Eissenstat, David M.
- Journal of Plant Nutrition, Vol. 15, Issue 6-7
Global patterns in root decomposition: comparisons of climate and litter quality effects
journal, November 2001
- Silver, Whendee L.; Miya, Ryan K.
- Oecologia, Vol. 129, Issue 3
Patterns in root trait variation among 25 co-existing North American forest species
journal, March 2009
- Comas, L. H.; Eissenstat, D. M.
- New Phytologist, Vol. 182, Issue 4
Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport
journal, January 1990
- Smith, S. E.; Smith, F. A.
- New Phytologist, Vol. 114, Issue 1
Fine root decomposition of evergreen broadleaved and coniferous tree species in mid-subtropical China: dynamics of dry mass, nutrient and organic fractions
journal, September 2010
- Lin, Chengfang; Yang, Yusheng; Guo, Jianfen
- Plant and Soil, Vol. 338, Issue 1-2
Mycorrhizal Community Dynamics Following Nitrogen Fertilization: a Cross-Site test in five Grasslands
journal, November 2007
- Egerton-Warburton, Louise M.; Johnson, Nancy Collins; Allen, Edith B.
- Ecological Monographs, Vol. 77, Issue 4
Fine root Architecture of nine North American Trees
journal, May 2002
- Pregitzer, Kurt S.; DeForest, Jared L.; Burton, Andrew J.
- Ecological Monographs, Vol. 72, Issue 2
Darwin's abominable mystery: Insights from a supertree of the angiosperms
journal, February 2004
- Davies, T. Jonathan; Barraclough, Timothy G.; Chase, Mark W.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 7
Comparative anatomy of roots and mycorrhizae of common Ontario trees
journal, March 1990
- Brundrett, Mark; Murase, Gracia; Kendrick, Bryce
- Canadian Journal of Botany, Vol. 68, Issue 3
Separating root and soil microbial contributions to soil respiration: A review of methods and observations
journal, January 2000
- Hanson, P. J.; Edwards, N. T.; Garten, C. T.
- Biogeochemistry, Vol. 48, Issue 1, p. 115-146
Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest
journal, May 2015
- Eissenstat, David M.; Kucharski, Joshua M.; Zadworny, Marcin
- New Phytologist, Vol. 208, Issue 1
Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species
journal, November 2008
- Guo, Dali; Xia, Mengxue; Wei, Xing
- New Phytologist, Vol. 180, Issue 3
Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation
journal, March 2007
- Swenson, N. G.; Enquist, B. J.
- American Journal of Botany, Vol. 94, Issue 3
Roots: evolutionary origins and biogeochemical significance
journal, March 2001
- Raven, J. A.; Edwards, D.
- Journal of Experimental Botany, Vol. 52, Issue suppl_1
Works referencing / citing this record:
Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation
journal, March 2017
- Kramer-Walter, Kris R.; Laughlin, Daniel C.
- Plant and Soil, Vol. 416, Issue 1-2
Multiple phosphorus acquisition strategies adopted by fine roots in low-fertility soils in Central Amazonia
journal, February 2019
- Lugli, Laynara F.; Andersen, Kelly M.; Aragão, Luiz E. O. C.
- Plant and Soil, Vol. 450, Issue 1-2
Effects of plant species and soil history on root morphology, arbuscular mycorrhizal colonization of roots, and biomass in four tallgrass prairie species
journal, December 2019
- Impastato, Charles J.; Carrington, Mary E.
- Plant Ecology, Vol. 221, Issue 2
Nonlinearity of root trait relationships and the root economics spectrum
journal, May 2019
- Kong, Deliang; Wang, Junjian; Wu, Huifang
- Nature Communications, Vol. 10, Issue 1
Climate, soil and plant functional types as drivers of global fine-root trait variation
journal, April 2017
- Freschet, Grégoire T.; Valverde-Barrantes, Oscar J.; Tucker, Caroline M.
- Journal of Ecology, Vol. 105, Issue 5
Multi-dimensional patterns of variation in root traits among coexisting herbaceous species in temperate steppes
journal, April 2018
- Zhou, Meng; Bai, Wenming; Zhang, Yushi
- Journal of Ecology, Vol. 106, Issue 6
Nitrogen fixation and foliar nitrogen do not predict phosphorus acquisition strategies in tropical trees
journal, August 2018
- Soper, Fiona M.; Nasto, Megan K.; Osborne, Brooke B.
- Journal of Ecology, Vol. 107, Issue 1
Community‐level economics spectrum of fine‐roots driven by nutrient limitations in subalpine forests
journal, November 2018
- Li, Fanglan; Hu, Hui; McCormlack, Michael Luke
- Journal of Ecology, Vol. 107, Issue 3
Towards a multidimensional root trait framework: a tree root review
journal, May 2016
- Weemstra, Monique; Mommer, Liesje; Visser, Eric J. W.
- New Phytologist, Vol. 211, Issue 4
A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants
journal, April 2017
- Valverde-Barrantes, Oscar J.; Freschet, Grégoire T.; Roumet, Catherine
- New Phytologist, Vol. 215, Issue 4
The fungal collaboration gradient dominates the root economics space in plants
journal, July 2020
- Bergmann, Joana; Weigelt, Alexandra; van der Plas, Fons
- Science Advances, Vol. 6, Issue 27
Nonlinearity of root trait relationships and the root economics spectrum
journal, May 2019
- Kong, Deliang; Wang, Junjian; Wu, Huifang
- Nature Communications, Vol. 10, Issue 1