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Genetic variation in plant below-ground response to elevated CO2 and two herbivore species

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Abstract

Aims

It is unclear how changing atmospheric conditions, including rising carbon dioxide concentration, influence interactions between above and below-ground systems and if intraspecific variation exists in this response.

Methods

We assessed interactive effects of atmospheric CO2 concentration, above-ground herbivory, and plant genotype on root traits and mycorrhizal associations. Plants from five families of Asclepias syriaca, a perennial forb, were grown under ambient and elevated atmospheric CO2 concentrations. Foliar herbivory by either lepidopteran caterpillars or phloem-feeding aphids was imposed. Mycorrhizal colonization, below-ground biomass, root biomass, and secondary defensive chemistry in roots were quantified.

Results

We observed substantial genetic variation among A. syriaca families in their mycorrhizal colonization levels in response to elevated CO2 and herbivory treatments. Elevated CO2 treatment increased root biomass in all genetic families, whereas foliar herbivory tended to decrease root biomass. Root cardenolide concentration and composition varied greatly among plant families, and elevated CO2 treatment increased root cardenolides in two of the five plant families. Moreover, herbivores differentially affected the composition of cardenolides expressed below ground.

Conclusions

Increased atmospheric CO2 has the potential to influence interactions among plants, herbivores and mycorrhizal fungi and intraspecific variation suggests that such interactions can evolve.

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References

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500

    Article  Google Scholar 

  • Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111

    Article  PubMed Central  Google Scholar 

  • Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868

    Article  PubMed  CAS  Google Scholar 

  • Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268

    Article  Google Scholar 

  • Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford

    Google Scholar 

  • Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

  • Bryant JP, Chapin FS, Klein DR (1983) Carbon nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087

    Article  PubMed  CAS  Google Scholar 

  • Chung HG, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol 13:980–989

    Article  Google Scholar 

  • R Core Development Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing. 2.15.2 edn, Vienna, Austria

  • Crous KY, Reich PB, Hunter MD, Ellsworth DS (2010) Maintenance of leaf N controls the photosynthetic CO2 response of grassland species exposed to 9 years of free-air CO2 enrichment. Glob Chang Biol 16:2076–2088

    Article  Google Scholar 

  • Currie AF, Murray PJ, Gange AC (2006) Root herbivory by Tipula paludosa larvae increases colonization of Agrostis capillaris by arbuscular mycorrhizal fungi. Soil Biol Biochem 38:1994–1997

    Article  CAS  Google Scholar 

  • Dang Q-L, Maepea JM, Parker WH (2008) Genetic variation of ecophysiological responses to CO2 in Picea glauca seedlings. The Open Forest Sci J 1:68–79

    Article  CAS  Google Scholar 

  • de Román M, Fernández I, Wyatt T, Sahrawy M, Heil M, Pozo MJ (2011) Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J Ecol 99:36–45

    Article  Google Scholar 

  • Erwin AC, Züst T, Ali JG, Agrawal AA (2014) Above-ground herbivory by red milkweed beetles facilitates above- and below-ground conspecific insects and reduces fruit production in common milkweed. Journal of Ecology

  • Gamper H, Hartwig UA, Leuchtmann A (2005) Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure. New Phytol 167:531–542

    Article  PubMed  CAS  Google Scholar 

  • Gange AC (2007) Insect-mycorrhizal interactions: patterns, processes, and consequences. In: Ohgushi T, Craig T, Price P (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge

    Google Scholar 

  • Gange AC, Bower E, Brown VK (2002) Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia 131:103–112

    Article  Google Scholar 

  • Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255

    Article  PubMed  CAS  Google Scholar 

  • Gill RA, Jackson RB (2008) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31

    Article  Google Scholar 

  • Gold JJ, Shore JS (1995) Multiple paternity in Asclepias syriaca using a paired-fruit analysis. Can J Bot-Rev Can Bot 73:1212–1216

    Article  Google Scholar 

  • Hunter MD (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agric For Entomol 3:3–9

    Article  Google Scholar 

  • Jarvis S, Woodward S, Alexander IJ, Taylor AFS (2013) Regional scale gradients of climate and nitrogen deposition drive variation in ectomycorrhizal fungal communities associated with native Scots pine. Glob Chang Biol 19:1688–1696

    Article  PubMed  CAS  Google Scholar 

  • Johnson NC, Wolf J, Koch GW (2003) Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition. Ecol Lett 6:532–540

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kabat SM, Dick CW, Hunter MD (2010) Isolation and characterization of microsatellite loci in the common milkweed, Asclepias syriaca (Apocynaceae). Am J Bot 97:E37–E38

    Article  PubMed  CAS  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    Article  PubMed  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Karowe DN, Grubb C (2011) Elevated CO2 increases constitutive phenolics and trichomes, but decreases inducibility of phenolics in Brassica rapa (Brassicaceae). J Chem Ecol 37:1332–1340

    Article  PubMed  CAS  Google Scholar 

  • King JS, Pregitzer KS, Zak DR, Holmes WE, Schmidt K (2005) Fine root chemistry and decomposition in model communities of north-temperate tree species show little response to elevated atmospheric CO2 and varying soil resource availability. Oecologia 146:318–328

    Article  PubMed  CAS  Google Scholar 

  • Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466:96–99

    Article  PubMed  CAS  Google Scholar 

  • Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proceedings of the National Academy of Sciences

  • Lau JA, Shaw RG, Reich PB, Tiffin P (2014) Indirect effects drive evolutionary responses to global change. New Phytol 201:335–343

    Article  PubMed  CAS  Google Scholar 

  • Leakey ADB, Lau JA (2012) Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO2]. Philos Trans of the Royal Soc B: Biol Sci 367:613–629

    Article  CAS  Google Scholar 

  • Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21

    Article  PubMed  CAS  Google Scholar 

  • Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomologia Exp Et Appl 80:193–196

    Article  CAS  Google Scholar 

  • Markkola A, Kuikka K, Rautio P, Harma E, Roitto M, Tuomi J (2004) Defoliation increases carbon limitations in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140:234–240

    Article  PubMed  Google Scholar 

  • Matros A, Amme S, Kettig B, Buck-Sorlin GH, Sonnewald UWE, Mock H-P (2006) Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y. Plant Cell Environ 29:126–137

    Article  PubMed  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives and objective-measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci U S A 101:9689–9693

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Orians CM, Thorn A, Gomez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9

    Article  PubMed  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Article  PubMed  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2012) nlme: Linear and Nonlinaer Mixed Effects Models

  • Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, Vogel CS (1995) Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytol 129:579–585

    Article  Google Scholar 

  • Pregitzer KS, Zak DR, Maziasz J, DeForest J, Curtis PS, Lussenhop J (2000) Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecol Appl 10:18–33

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2010) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol: no-no

  • Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99:16–25

    Article  CAS  Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman & Hall, New York

    Book  Google Scholar 

  • Schröter D, Brussaard L, De Deyn G, Poveda K, Brown VK, Berg MP, Wardle DA, Moore J, Wall DH (2004) Trophic interactions in a changing world: modelling aboveground ‚Äìbelowground interactions. Basic and Appl Ecology 5:515–528

    Article  Google Scholar 

  • Smith SE, Read DR (2008) Mycorrhizal symbiosis. Academic, Amsterdam; New York; Boston

    Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    Article  PubMed  CAS  Google Scholar 

  • Stevens M, Gusse A, Lindroth R (2014) Root chemistry in Populus tremuloides: effects of soil nutrients, defoliation, and genotype. J Chem Ecol 40:31–38

    Article  PubMed  CAS  Google Scholar 

  • Stout MJ, Workman J, Duffey SS (1994) Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20:2575–2594

    Article  PubMed  CAS  Google Scholar 

  • Tang JJ, Chen J, Chen X (2006) Response of 12 weedy species to elevated CO2 in low-phosphorus-availability soil. Ecol Res 21:664–670

    Article  CAS  Google Scholar 

  • Tao L, Hunter MD (2013) Allocation of resources away from sites of herbivory under simultaneous attack by aboveground and belowground herbivores in the common milkweed, Asclepias syriaca. Arthropod Plant Interact 7:217–224

    Article  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • van Dam NM, Harvey JA, Wackers FL, Bezemer TM, van der Putten WH, Vet LEM (2003) Interactions between aboveground and belowground induced responses against phytophages. Basic and Appl Ecol 4:63–77

    Article  Google Scholar 

  • van der Putten WH (2003) Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280

    Article  Google Scholar 

  • van der Putten WH, Vet LEM, Harvey JA, Wackers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Article  Google Scholar 

  • van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schadler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Vannette RL, Hunter MD (2011a) Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2. Glob Chang Biol 17:1277–1288

    Article  Google Scholar 

  • Vannette RL, Hunter MD (2011b) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76

    Article  Google Scholar 

  • Vannette RL, Hunter MD (2013) Mycorrhizal abundance affects the expression of plant resistance traits and herbivore performance. J Ecol 101:1019–1029

    Article  CAS  Google Scholar 

  • Vannette RL, Rasmann S (2012) Arbuscular mycorrhizal fungi mediate belowground plant-herbivore interactions: a phylogenetic study. Functional Ecology

  • Vannette RL, Hunter MD, Rasmann S (2013) Arbuscular mycorrhizal fungi alter above-and below-ground chemical defense expression differentially among Asclepias species. Front in Plant Sci 4:361

    Article  Google Scholar 

  • Wason EL, Hunter MD (2014) Genetic variation in plant volatile emission does not result in differential attraction of natural enemies in the field. Oecologia 174:479–491

    Article  PubMed  Google Scholar 

  • Wearn JA, Gange AC (2007) Above-ground herbivory causes rapid and sustained changes in mycorrhizal colonization of grasses. Oecologia 153:959–971

    Article  PubMed  Google Scholar 

  • Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461

    Article  PubMed  Google Scholar 

  • Zak D, Pregitzer K, Curtis P, Teeri J, Fogel R, Randlett D (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151:105–117

    Article  CAS  Google Scholar 

  • Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222

    Article  CAS  Google Scholar 

  • Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053

    Article  PubMed  CAS  Google Scholar 

  • Zuur AF (2009) Mixed effects models and extensions in ecology with R. Springer.

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Acknowledgments

The authors thank S. Kabat and M. Tyner for help with the experiment, D. Karowe for use of the CO2 chamber array, the University of Michigan Biological Station staff and facilities for support. We are also grateful to the Hunter lab and multiple reviewers for their helpful comments on previous versions of this manuscript. This work was supported by the National Science Foundation (NSF) DEB 0814340 to MDH and RLV, an NSF-IGERT (BART) Fellowship to RLV and an NSF DDIG to RLV.

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Authors and Affiliations

  1. Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

    Rachel L. Vannette & Mark D. Hunter

  2. Department of Biology, Stanford University, 488 Herrin Labs, 371 Serra Mall, Stanford, CA, 94305, USA

    Rachel L. Vannette

  3. Department of Ecology and Evolutionary Biology, 2053 Kraus Natural Science Building, 830 North University, Ann Arbor, MI, 48109-1048, USA

    Mark D. Hunter

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  1. Rachel L. Vannette
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Correspondence to Rachel L. Vannette.

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Responsible Editor: Thom W. Kuyper.

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Vannette, R.L., Hunter, M.D. Genetic variation in plant below-ground response to elevated CO2 and two herbivore species. Plant Soil 384, 303–314 (2014). https://doi.org/10.1007/s11104-014-2203-9

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