Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species

Ecology and Evolution

Volumn 5, Issue 23, 2015, Pages 5711-5721

  Maguire, Andrea J ^a   Kobe, Richard K ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Carbon reserves; Carbon starvation; Nonstructural carbohydrates; Soluble sugars; Starch; Stress

Indexed keywords

EID: 84953637163     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1819     Document Type: Article

References (51)

1. Adams, H. D., M. Guardiola-Claramonte, G. A. Barron-Gafford, J. C. Villegas, D. D. Breshears, C. B. Zou, et al. 2009. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc. Natl Acad. Sci. USA 106:7063-7066.
2. Adams, H. D., M. J. Germino, D. D. Breshears, G. A. Barron-Gafford, M. Guardiola-Claramonte, C. B. Zou, et al. 2013. Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol. 197:1142-1151.
3. Allen, C. D., A. K. Macalady, H. Chenchouni, D. Bachelet, N. G. McDowell, M. Vennetier, et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manage. 259:660-684.
4. Anderegg, W. R. L., J. A. Berry, D. D. Smith, J. S. Sperry, L. D. L. Anderegg, and C. B. Field . 2012. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc. Natl Acad. Sci. USA 109:233-237.
5. Bolker, B. 2012. bbmle R package. R Development Core Team. Version 1.0.5.2. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.r-project.org/.
6. Bréda, N., R. Huc, A. Granier, and E. Dreyer . 2006. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 63:625-644.
7. Breshears, D. D., O. B. Myers, C. W. Meyer, F. J. Barnes, C. B. Zou, C. D. Allen, et al. 2009. Tree die-off in response to global change-type drought, mortality insights from a decade of plant water potential measurements. Front. Ecol. Environ. 7:185-189.
8. Burnham, K. P., and D. R. Anderson . 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer, New York.
9. Burns, R. M., and Honkala B. H. 1990. Silvics of North America: Volume 2. Hardwoods. Agriculture Handbook 654. U.S. Department of Agriculture, Forest Service, Washington, DC.
10. Canham, C. D., R. K. Kobe, E. F. Latty, and R. L. Chazdon . 1999. Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:1-11.
11. Carnicer, J., M. Coll, M. Ninyerola, X. Pons, G. Sánchez, and J. Peñuelas . 2011. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc. Natl Acad. Sci. USA 108:1474-1478.
12. Chapin, F. S., E.-D. Schulze, and H. A. Mooney . 1990. The ecology and economics of storage in plants. Annu. Rev. Ecol. Syst. 21:423-447.
13. Chapin, F. S., K. Autumn, and F. Pugnaire . 1993. Evolution of suites of traits in response to environmental stress. Am. Nat. 142:S78-S92.
14. Choat, B., S. Jansen, T. J. Brodribb, H. Cochard, S. Delzon, R. Bhaskar, et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491:752-756.
15. Dietze, M. C., A. Sala, M. S. Carbone, C. I. Czimczik, J. A. Mantooth, A. D. Richardson, et al. 2014. Nonstructural carbon in woody plants. Annu. Rev. Plant Biol. 65:667-687.
16. DuBois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. E. Smith . 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356.
17. Eyles, A., E. A. Pinkard, and C. Mohammed . 2009. Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol. 29:753-764.
18. Fisher, R., N. G. McDowell, D. Purves, P. Moorcroft, S. Sitch, P. Cox, et al. 2010. Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytol. 187:666-681.
19. Galiano, L., J. Martínez-Vilalta, and F. Lloret . 2011. Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol. 190:750-759.
20. Galvez, D. A., S. M. Landhäusser, and M. T. Tyree . 2011. Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol. 31:250-257.
21. Gibon, Y., E. T. Pyl, R. Sulpice, J. E. Lunn, M. Höhne, M. Günther, et al. 2009. Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ. 32:859-874.
22. Gruber, A., D. Pirkebner, C. Florian, and W. Oberhuber . 2011. No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress. Plant Biol. 14:142-148.
23. Hartley, I. P., A. F. Armstrong, R. Murthy, G. Barron-Gafford, P. Ineson, and O. K. Atkin . 2006. The dependence of respiration on photosynthetic substrate supply and temperature: integrating leaf, soil and ecosystem measurements. Glob. Change Biol. 12:1954-1968.
24. Hoch, G., A. Richter, and C. Körner . 2003. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 26:1067-1081.
25. Kitajima, K. 1994. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419-428.
26. Kobe, R. K. 1997. Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226-233.
27. Kobe, R. K., M. Iyer, and M. B. Walters . 2010. Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 91:166-179.
28. Kozlowski, T. T. 1992. Carbohydrate sources and sinks in woody plants. Bot. Rev. 58:107-222.
29. Landhäusser, S. M., and V. J. Lieffers . 2011. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26:653-661.
30. Machado, R. A. R., A. P. Ferrieri, C. A. M. Robert, G. Glauser, M. Kallenbach, I. T. Baldwin, et al. 2013. Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol. 200:1-13.
31. McDowell, N. G. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 155:1051-1059.
32. McDowell, N. G., W. T. Pockman, C. D. Allen, D. D. Breshears, N. Cobb, T. Kolb, et al. 2008. Mechanisms of plant survival and mortality during drought, why do some plants survive while others succumb to drought? New Phytol. 178:719-739.
33. Meier, I. C., and C. Leuschner . 2008. Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Glob. Change Biol. 14:2081-2095.
34. Millard, P., M. Sommerkorn, and G. Grelet . 2007. Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol. 175:11-28.
35. Mitchell, P. J., A. P. O'Grady, D. T. Tissue, D. A. White, M. L. Ottenschlaeger, and E. A. Pinkard . 2013. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol. 197:862-872.
36. Muller, B., F. Pantin, M. Génard, O. Turc, S. Freixes, M. Piques, et al. 2011. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J. Exp. Bot. 62:1715-1729.
37. Myers, J. A., and K. Kitajima . 2007. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J. Ecol. 95:383-395.
38. Nardini, A., M. A. Lo Gullo, and S. Salleo . 2011. Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci. 180:604-611.
39. O'Brien, M. J., S. Leuzinger, C. D. Philipson, J. Tay, and A. Hector . 2014. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Chang. 4:1-5.
40. Piper, F. I., M. Reyes-Díaz, L. J. Corcuera, and C. H. Lusk . 2009. Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments. Ecol. Res. 24:1233-1241.
41. Poorter, L., and K. Kitajima . 2007. Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 88:1000-1011.
42. Quentin, A. G., C. L. Beadle, A. P. O'Grady, and E. A. Pinkard . 2011. Effects of partial defoliation on closed canopy Eucalyptus globulus Labilladière: growth, biomass allocation and carbohydrates. For. Ecol. Manage. 261:695-702.
43. R Development Core Team. 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.
44. Sack, L., and P. J. Grubb . 2002. The combined impacts of deep shade and drought on the growth and biomass allocation of shade-tolerant woody seedlings. Oecologia 131:175-185.
45. Sala, A., F. Piper, and G. Hoch . 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 186:274-281.
46. Sala, A., D. R. Woodruff, and F. C. Meinzer . 2012. Carbon dynamics in trees: feast or famine? Tree Physiol. 32:764-775.
47. Secchi, F., and M. A. Zwieniecki . 2011. Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ. 34:514-524.
48. Sevanto, S., N. G. McDowell, L. T. Dickman, R. Pangle, and W. T. Pockman . 2014. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37:153-161.
49. Smith, A. M., and M. Stitt . 2007. Coordination of carbon supply and plant growth. Plant Cell Environ. 30:1126-1149.
50. Van Der Heyden, F., and W. D. Stock . 1996. Regrowth of a semiarid shrub following simulated carbon browsing: the role of reserve carbon. Funct. Ecol. 10:647-653.
51. Williams, A. P., C. D. Allen, C. I. Millar, T. W. Swetnam, J. Michaelsen, C. J. Still, et al. 2010. Forest responses to increasing aridity and warmth in the southwestern United States. Proc. Natl Acad. Sci. USA 107:21289-21294.