Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T01:03:44.874Z Has data issue: false hasContentIssue false
  • English
  • Français

Radiocarbon Suggests the Hemiparasitic Annual Melampyrum Lineare Desr. May Acquire Carbon from Stressed Hosts

Published online by Cambridge University Press:  25 October 2017

Lucas E Nave ,
Katherine A Heckman ,
Alexandra B Muñoz  and
Christopher W Swanston
Lucas E Nave*
Affiliation:
University of Michigan, Biological Station, Pellston, MI 49769USA University of Michigan, Dept. of Ecology and Evolutionary Biology, Ann Arbor, MI 48109USA
Katherine A Heckman
Affiliation:
USDA Forest Service, Northern Research Station, Houghton, MI 49931USA
Alexandra B Muñoz
Affiliation:
University of Michigan, Biological Station, Pellston, MI 49769USA University of Copenhagen, Copenhagen, Denmark
Christopher W Swanston
Affiliation:
USDA Forest Service, Northern Research Station, Houghton, MI 49931USA
*
*Corresponding author. Email: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Hemiparasitic plants obtain water and solutes from their hosts, but much remains to be learned about these transfers. We used a forest girdling experiment to investigate how leaf gas exchange, carbon and nitrogen cycling in the root hemiparasite Melampyrum lineare Desr. responded to disturbance and changes in physiology of potential host trees. By preventing belowground C allocation by 35% of the canopy, girdling decreased the starch and soluble sugar contents of bulk forest floor fine roots. Photosynthetic rates of M. lineare were statistically significantly lower in the girdled plot, but their hypothesized drivers (foliar N, stomatal conductance and transpiration) had no statistically significant differences between girdled and non-girdled plots. However, M. lineare in the girdled plot had higher foliar C concentrations and Δ14C than in the control plot, suggesting possible photosynthetic down-regulation in the girdled plot due to influx of older (e.g., host-derived) C into the leaves of M. lineare. Within the girdled plot (but not the control plot), M. lineare foliar C concentrations were positively correlated with foliar Δ14C and δ15N, suggesting that M. lineare may respond to changes in both C and N biogeochemistry during the decline of dominant canopy species.

Keywords

nonstructural carbohydratesphysiological stressphotosynthesisplant mixotrophytranspiration
Type
Research Article
Information
Radiocarbon , Volume 60 , Issue 1 , February 2018 , pp. 269 - 281
Copyright
© 2017 by the Arizona Board of Regents on behalf of the University of Arizona 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barbehenn, RV, Chen, Z, Karowe, D, Spickard, A. 2004. C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2 . Global Change Biology 10:1565–1575.Google Scholar
Bell, T, Adams, M. 2011. Attack on all fronts: functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiology 31:3–15.CrossRefGoogle ScholarPubMed
Bennet, JR, Matthews, S. 2006. Phylogeny of the parasitic plant family Orobanchaceae inferred from Phytochrome A. American Journal of Botany 93:1039–1051.Google Scholar
Calvin, M. 1948. Investigation of reaction mechanisms and photosynthesis with radiocarbon. Nucleonics 2:40–51.Google Scholar
Cantlon, JE, Curtis, EJC, Malcolm, WM. 1963. Studies of Melampyrum lineare . Ecology 44:466–474.CrossRefGoogle Scholar
Craine, JM, Brookshire, ENJ, Cramer, MD, Hasselquist, NJ, Koba, K, Marin-Spiotta, E, Wang, L. 2015a. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant and Soil 396:1–26.Google Scholar
Craine, JM, Elmore, AJ, Wang, L, Augusto, L, Baisden, WT, Brookshire, ENJ, Cramer, MD, Hasselquist, NJ, Hobbie, EA, Kahmen, A, Koba, K, Kranabetter, JM, Mack, MC, Marin-Spiotta, E, Mayor, JR, McLauchlan, KK, Michelsen, A, Nardoto, GB, Oliveira, RS, Perakis, SS, Peri, PL, Quesada, CA, Richter, A, Schipper, L, Stevenson, BA, Turner, BL, Viani, RAG, Wanek, W, Zeller, B. 2015b. Convergence of soil nitrogen isotopes across global climate gradients. Scientific Reports 5:8280.Google Scholar
Curtis, PS, Vogel, CS, Wang, X, Pregitzer, KS, Zak, DR, Lussenhop, J, Kubiske, M, Teeri, JA. 2000. Gas exchange, leaf nitrogen, and growth efficiency of Populus tremuloides in a CO2 enriched atmosphere. Ecological Applications 10:3–17.Google Scholar
Davis, JC, Proctor, ID, Southon, JR, Caffee, MW, Heikkinen, DW, Roberts, ML, Moore, TL, Turteltaub, KW, Nelson, DE, Loyd, DH, Vogel, JS. 1990. LLNL/US AMS facility and research program. Nuclear Instruments and Methods in Physics B 52:269–272.Google Scholar
Fer, A, Simier, P, Arnaud, MC, Rey, L, Renaudin, S. 1993. Carbon acquisition and metabolism in a root hemiparasitic angiosperm, Thesium humile (Santalaceae) growing on wheat (Triticum vulgare). Australian Journal of Plant Physiology 20:15–24.Google Scholar
Fisher, DS, Mayland, HF, Burns, JC. 1999. Variation in ruminants’ preference for tall fescue hays cut either at sundown or sunup. Journal of Animal Science 77:762–768.CrossRefGoogle ScholarPubMed
Gauslaa, Y. 1990. Water relations and mineral nutrients in Melampyrum pratense (Scrophulariaceae) in oligotrophic and mesotrophic boreal forests. Acta Oecologica-International Journal of Ecology 11:525–537.Google Scholar
Gibson, W. 1993. Selective advantages to hemiparasitic annuals, genus Melampyrum, of a seed-dispersal mutualism involving ants. 1. Favorable nest sites. Oikos 67:334–344.Google Scholar
Goldschmidt, EE, Huber, SC. 1992. Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiology 99:1443–1448.CrossRefGoogle ScholarPubMed
Gordon, JC, Larson, PR. 1966. Seasonal course of photosynthesis, respiration, and distribution of 14C in young Pinus resinosa trees as related to wood formation. Plant Physiology 43:1617–1624.Google Scholar
Gough, CM, Vogel, CS, Harrold, KH, George, K, Curtis, PS. 2007. The legacy of harvest and fire on ecosystem carbon storage in a north temperate forest. Global Change Biology 13:1935–1949.CrossRefGoogle Scholar
Gough, CM, Flower, CE, Vogel, CS, Dragoni, D, Curtis, PS. 2009. Whole-ecosystem labile carbon production in a north temperate deciduous forest. Agricultural and Forest Meteorology 149:1531–1540.CrossRefGoogle Scholar
Gough, CM, Vogel, CS, Hardiman, BS, Curtis, PS. 2010. Wood net primary production resilience in an unmanaged forest transitioning from early to middle succession. Forest Ecology and Management 260:36–41.Google Scholar
Gough, CM, Hardiman, BS, Nave, LE, Bohrer, G, Maurer, KD, Vogel, CS, Nadelhoffer, KJ, Curtis, PS. 2013. Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest. Ecological Applications 23:1202–1215.Google Scholar
Hansen, J, Beck, E. 1994. Seasonal changes in the utilization and turnover of assimilation products in 8-year-old Scots pine (Pinus sylvestris L.) trees. Trees- Structure and Function 8:172–182.Google Scholar
Hattenschwiler, S, Korner, C. 1997. Growth of autotrophic and root-hemiparasitic understory plants under elevated CO2 and increased N deposition. Acta Oecologica-International Journal of Ecology 18:327–333.Google Scholar
Hobbie, EA, Hogberg, P. 2012. Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytologist 196:367–382.Google Scholar
Högberg, P. 1990. Forests losing large quantities of nitrogen have elevated N-15:N-14 ratios. Oecologia 84:229–231.Google Scholar
Hua, Q, Barbetti, M. 2004. Review of tropospheric bomb (14C) data for carbon cycle modeling and age calibration purposes. Radiocarbon 46(3):1273–1298.Google Scholar
Hua, Q, Barbetti, M, Rakowski, AZ. 2013. Atmospheric radiocarbon for the period 1950-2010. Radiocarbon 55(4):2059–2072.CrossRefGoogle Scholar
Ländhausser, SM, Lieffers, VJ. 2012. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26:653–661.CrossRefGoogle Scholar
Leavitt, SW, Paul, EA, Kimball, BA, Hendrey, GR, Mauney, JR, Rauschkolb, R, Rogers, H, Lewin, KF, Nagy, J, Pinter, PJ, Johnson, NB. 1994. Carbon-isotope dynamics of free-air CO2-enriched cotton and soils. Agricultural and Forest Meteorology 70:87–101.Google Scholar
Lechowski, Z. 1996. Gas exchange in leaves of the root hemiparasite Melampyrum arvense L before and after attachment to the host plant. Biologia Plantarum 38:85–93.Google Scholar
Mumera, LM, Below, FE. 1993. Role of nitrogen in resistance to Striga parasitism of maize. Crop Science 33:758–763.Google Scholar
Nave, LE, Gough, CM, Maurer, KD, Bohrer, G, Hardiman, BS, Le Moine, J, Muñoz, AB, Nadelhoffer, KJ, Sparks, JP, Strahm, BD, Vogel, CS, Curtis, PS. 2011. Disturbance and the resilience of coupled carbon and nitrogen cycling in a northern temperate forest. Journal of Geophysical Research- Biogeosciences 116:G04016.Google Scholar
Nave, LE, Nadelhoffer, KJ, Le Moine, J, van Diepen, LTA, Cooch, JK, van Dyke, NJ. 2013. Nitrogen uptake by trees and mycorrhizal fungi in a successional northern temperate forest: insights from multiple isotopic methods. Ecosystems 16:590–603.CrossRefGoogle Scholar
Nave, LE, Sparks, JP, Le Moine, J, Hardiman, BS, Nadelhoffer, KJ, Tallant, JT, Vogel, CS, Strahm, BD, Curtis, PS. 2014. Changes in soil nitrogen cycling in a northern temperate forest ecosystem during succession. Biogeochemistry 171:471–488.Google Scholar
Paul, MJ, Foyer, CH. 2001. Sink regulation of photosynthesis. Journal of Experimental Botany 52:1383–1400.Google Scholar
Pennings, SC, Callaway, RM. 2002. Parasitic plants: parallels and contrasts with herbivores. Oecologia 131:479–489.Google Scholar
Press, MC, Phoenix, GK. 2005. Impacts of parasitic plants on natural communities. New Phytologist 166:737–751.Google Scholar
Press, MC, Shah, N, Tuohy, JM, Stewart, GR. 1987. Carbon isotope ratios demonstrate carbon flux from C-4 host to C-3 parasite. Plant Physiology 85:1143–1145.Google Scholar
Quested, HM, Cornelissen, JHC, Press, MC, Callaghan, TV, Aerts, R, Trosien, F, Riemann, P, Gwynn-Jones, D, Kondratchuk, A, Jonasson, SE. 2003. Decomposition of sub-arctic plants with differing nitrogen economies: A functional role for hemiparasites. Ecology 84:3209–3221.Google Scholar
Reich, PB, Walters, MB, Ellsworth, DS. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the United States of America 94:13730–13734.CrossRefGoogle ScholarPubMed
Regier, N, Streb, S, Zeeman, SC, Frey, B. 2010. Seasonal changes in starch and sugar content of poplar (Populus deltoids x nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiology 30:979–987.Google Scholar
Richardson, AD, Carbone, MS, Keenan, TF, Czimczik, CI, Hollinger, DY, Murakami, P, Schaberg, PG, Xu, X. 2013. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytologist 197:850–861.CrossRefGoogle ScholarPubMed
Rothstein, DE, Zak, DR, Pregitzer, KS, Curtis, PS. 2000. Kinetics of nitrogen uptake by Populus tremuloides in relation to atmospheric CO2 and soil nitrogen availability. Tree Physiology 20:265–270.Google Scholar
Salonen, V, Setala, H, Puustinen, S. 2000. The interplay between Pinus sylvestris, its root hemiparasite Melampyrum pretense, and ectomycorrhizal fungi: influences on plant growth and reproduction. Ecoscience 7:195–200.Google Scholar
Seel, WE, Press, MC. 1993. Influence of the host on 3 subarctic annual facultative root hemiparasites. 1. Growth, mineral accumulation and aboveground dry matter partitioning. New Phytologist 125:131–138.Google Scholar
Seel, WE, Press, MC. 1994. Influence of the host on 3 subarctic annual facultative root hemiparasites. 2. Gas exchange characteristics and resource use efficiency. New Phytologist 127:37–44.Google Scholar
Seel, WE, Cooper, RE, Press, MC. 1993. Growth, gas exchange and water use efficiency of the facultative hemiparasite Rhinanthus minor associated with hosts differing in foliar nitrogen concentration. Physiologia Plantarum 89:64–70.Google Scholar
Selosse, M-A, Charpin, M, Not, F. 2017. Mixotrophy everywhere on land and in water: the grand écart hypothesis. Ecology Letters 20:246–263.CrossRefGoogle ScholarPubMed
Selosse, MA, Roy, M. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Science 14:64–70.Google Scholar
Sparks, JP, Ehleringer, JR. 1997. Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects. Oecologia 109:362–367.Google Scholar
Stewart, GR, Press, MC. 1990. The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 41:127–151.Google Scholar
Stuiver, M, Polach, HA. 1977. Discussion: reporting of 14C data. Radiocarbon 19(3):355–363.Google Scholar
Swanston, CW, Torn, MS, Hanson, PJ, Southon, JR, Garten, CT, Hanlon, EM, Ganio, L. 2003. Initial characterization of processes of soil carbon stabilization using forest stand-level radiocarbon enrichment. Geoderma 128:52–62.Google Scholar
Těšitel, J, Placvová, L, Cameron, D. 2010. Interactions between hemiparasitic plants and their hosts. Plant Signaling and Behavior 5:1072–1076.CrossRefGoogle ScholarPubMed
Těšitel, J, Tesitelova, T, Fisher, JP, Leps, J, Cameron, DD. 2015. Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytologist 205:350–360.CrossRefGoogle ScholarPubMed
Treseder, KK, Torn, MS, Masiello, CA. 2006. An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biology and Biochemistry 38:1077–1082.Google Scholar
Vogel, JS, Southon, JR, Nelson, DE. 1987. Catalyst and binder effects in the use of filamentous graphite for AMS. Nuclear Instruments and Methods in Physics Research B 29:50–56.Google Scholar
Westwood, JH, Yoder, JI, Timko, MP, dePamphilis, CW. 2010. The evolution of parasitism in plants. Trends in Plant Science 15:227–235.Google Scholar
Wickett, NJ, Honaas, LA, Wafula, EK, Das, M, Huang, K, Wu, BA, Landherr, L, Timko, MP, Yoder, J, Westwood, JH, dePamphilis, CW. 2011. Transcriptomes of the parasitic plant family Orobanchaceae reveal surprising conservation of chlorophyll synthesis. Current Biology 21:2098–2104.Google Scholar
Wyka, T. 1999. Carbohydrate storage and use in an alpine population of the perennial herb. Oxytropis sericea. Oecologia 120:198–208.Google Scholar
Supplementary material: File

Nave et al supplementary material

Nave et al supplementary material 1

Download Nave et al supplementary material(File)
File 20.9 KB