Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism

New Phytologist

Volumn 197, Issue 4, 2013, Pages 1142-1151

  Adams, Henry D ^a,b,c   Germino, Matthew J ^d,e   Breshears, David D ^a,b   Barron Gafford, Greg A ^b   Guardiola Claramonte, Maite ^b   Zou, Chris B ^f   Huxman, Travis E ^a,b,g  

^a The University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d FOREST AND RANGELAND ECOSYSTEM SCIENCE CENTER   (United States)

^e Nucl Eng Idaho State University   (United States)

^f OKLAHOMA STATE UNIVERSITY   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biosphere atmosphere feedbacks; Carbon starvation; Drought impacts; Global change; Hydraulic failure; Mortality mechanism; Nonstructural carbohydrates (NSCs); Tree mortality

Indexed keywords

CARBON; WATER;

CARBOHYDRATE; CARBON FLUX; CLIMATE CHANGE; CONCENTRATION (COMPOSITION); DROUGHT; LEAF; METABOLISM; MORTALITY; PHYSIOLOGY; STARCH; SUGAR;

ARTICLE; CARBOHYDRATE METABOLISM; CLIMATE CHANGE; DROUGHT; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PINE; PLANT LEAF; TEMPERATURE; XYLEM;

CARBOHYDRATE METABOLISM; CARBON; CLIMATE CHANGE; DROUGHTS; PINUS; PLANT LEAVES; STRESS, PHYSIOLOGICAL; TEMPERATURE; WATER; XYLEM;

PINUS EDULIS;

EID: 84873266731     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12102     Document Type: Article

References (88)

1. Adams HD, Allen CD, Breshears DD, Hale VC, Huxman TE, Luce CH, Smith AMS, Weiler M. 2012. Ecohydrological consequences of drought- and infestation-triggered tree die-off. Ecohydrology 5: 145-159.
2. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE. 2009a. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proceedings of the National Academy of Sciences, USA 106: 7063-7066.
3. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE. 2009b. Reply to Sala: temperature sensitivity in drought-induced tree mortality hastens the need to further resolve a physiological model of death. Proceedings of the National Academy of Sciences, USA 106: E69.
4. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE. 2009c. Reply to Leuzinger et al.: drought-induced tree mortality temperature sensitivity requires pressing forward with best available science. Proceedings of the National Academy of Sciences, USA 106: E107.
5. Allen CD, Breshears DD. 1998. Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proceedings of the National Academy of Sciences, USA 95: 14839-14842.
6. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259: 660-684.
7. Anderegg WRL. 2012. Complex aspen forest carbon and root dynamics during drought. Climatic Change 111: 983-991.
8. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB. 2012b. The roles of hydraulic failure and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences, USA 109: 233-237.
9. Anderegg WRL, Callaway ES. 2012. Infestation and hydraulic consequences of induced carbon starvation. Plant Physiology 159: 1866-1874.
10. Anderegg WRL, Kane JM, Anderegg LDL. 2012a. Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Climate Change. doi:10.1038/nclimate1635.
11. Bansal S, Germino MJ. 2008. Carbon balance of conifer seedlings at timberline: relative changes in uptake, storage, and utilization. Oecologia 158: 217-227.
12. Bansal S, Germino MJ. 2009. Temporal variation of nonstructural carbohydrates in montane conifers: similarities and differences among developmental stages, species and environmental conditions. Tree Physiology 29: 559-568.
13. Bansal S, Germino MJ. 2010a. Variation in ecophysiological properties among conifers at an ecotonal boundary: comparison of establishing seedlings and established adults at timberline. Journal of Vegetation Science 21: 133-142.
14. Bansal S, Germino MJ. 2010b. Unique responses of respiration, growth, and non-structural carbohydrate storage in sink tissue of conifer seedlings to an elevation gradient at timberline. Environmental and Experimental Botany 69: 313-319.
15. Bansal S, Reinhardt K, Germino MJ. 2011. Linking carbon balance to establishment patterns: comparison of whitebark pine and Engelmann spruce seedlings along an herb cover exposure gradient at treeline. Plant Ecology 212: 219-228.
16. Bonan GB. 2008. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320: 1444-1449.
17. Breshears DD, Allen CD. 2002. The importance of rapid, disturbance-induced losses in carbon management and sequestration. Global Ecology and Biogeography 11: 1-5.
18. Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, Floyd ML, Belnap J et al. 2005. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences, USA 102: 15144-15148.
19. Breshears DD, Lopez-Hoffman L, Graumlich LJ. 2011. When ecosystem services crash: preparing for big, fast, patchy climate change. Ambio 40: 256-263.
20. Breshears DD, Myers OB, Barnes FJ. 2009. Horizontal heterogeneity in the frequency of plant-available water with woodland intercanopy-canopy vegetation patch type rivals that occurring vertically by soil depth. Ecohydrology 2: 503-519.
21. Carnicer J, Coll M, Ninyerola M, Pons X, Sanchez G, Peñuelas J. 2011. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences, USA 108: 1474-1478.
22. Chapin FS, Randerson JT, McGuire AD, Foley JA, Field CB. 2008. Changing feedbacks in the climate-biosphere system. Frontiers in Ecology and the Environment 6: 313-320.
23. Chiou TJ, Bush DR. 1998. Sucrose is a signal molecule in assimilate partitioning. Proceedings of the National Academy of Sciences, USA 95: 4784-4788.
24. da Costa ACL, Galbraith D, Almeida S, Portela BTT, da Costa M, Silva JD, Braga AP, de Goncalves PHL, de Oliveira AAR, Fisher R et al. 2010. Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. New Phytologist 187: 579-591.
25. Field CB, Lobell DB, Peters HA, Chiariello NR. 2007. Feedbacks of terrestrial ecosystems to climate change. Annual Review of Environment and Resources 32: 1-29.
26. Fisher R, McDowell N, Purves D, Moorcroft P, Sitch S, Cox P, Huntingford C, Meir P, Woodward FI. 2010. Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytologist 187: 666-681.
27. Foxx TS, Tierney GD. 1987. Rooting patterns in the pinyon-juniper woodland. 69-79. In: Proceedings-Pinyon-Juniper Conference. Richard L. Everett, comp. USDA Forest Service, General Technical Report INT-215. Ogden, UT, USA: Intermountain Forest and Range Experiment Station, 581.
28. Fritsch FN, Carlson RE. 1980. Monotone piecewise cubic interpolation. SIAM Journal on Numerical Analysis 17: 238-246.
29. Galiano L, Martinez-Vilalta J, Lloret F. 2011. Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytologist 190: 750-759.
30. Galvez DA, Landhäusser SM, Tyree MT. 2011. Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiology 31: 250-257.
31. Gitlin AR, Sthultz CM, Bowker MA, Stumpf S, Paxton KL, Kennedy K, Munoz A, Bailey JK, Whitham TG. 2006. Mortality gradients within and among dominant plant populations as barometers of ecosystem change during extreme drought. Conservation Biology 20: 1477-1486.
32. Gruber A, Pirkebner D, Florian C, Oberhuber W. 2012. No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress. Plant Biology 14: 142-148.
33. Guardiola-Clararnonte M, Troch PA, Breshears DD, Huxman TE, Switanek MB, Durcik M, Cobb NS. 2011. Decreased streamflow in semi-arid basins following drought-induced tree die-off: a counter-intuitive and indirect climate impact on hydrology. Journal of Hydrology 406: 225-233.
34. Guardiola-Clararnonte M, Troch PA, Breshears DD, Huxman TE, Switanek MB, Durcik M, Cobb NS. 2012. Corrigendum to "Decreased streamflow in semi-arid basins following drought-induced tree die-off: a counter-intuitive and indirect climate impact on hydrology". Journal of Hydrology 414: 560-560.
35. Hacke UG, Sperry JS. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology Evolution and Systematics 4: 97-115.
36. Hacke UG, Sperry JS, Ewers BE, Ellsworth DS, Schafer KVR, Oren R. 2000. Influence of soil porosity on water use in Pinus taeda. Oecologia 124: 495-505.
37. Hill JP, Germino MJ, Alongi DA. 2011. Carbon-use efficiency in green sinks is increased when a blend of apoplastic fructose and glucose is available for uptake. Journal of Experimental Botany 62: 2013-2022.
38. Hoch G. 2007. Cell wall hemicelluloses as mobile carbon stores in non-reproductive plant tissues. Functional Ecology 21: 823-834.
39. Hoch G, Popp M, Körner C. 2002. Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98: 361-374.
40. Hoffmann WA, Marchin RM, Abit P, Lau OL. 2011. Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought. Global Change Biology 17: 2731-2742.
41. Höltta T, Mencuccini M, Nikinmaa E. 2009. Linking phloem function to structure: analysis with a coupled xylem-phloem transport model. Journal of Theoretical Biology 259: 325-337.
42. Huynh H, Feldt LS. 1976. Estimation of the Box correction for degrees of freedom from sample data in randomized block and split-plot designs. Journal of Educational Statistics 1: 69-82.
43. Kane JM, Kolb TE. 2010. Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164: 601-609.
44. Kane JM, Meinhardt KA, Chang T, Cardall BL, Michalet R, Whitham TG. 2011. Drought-induced mortality of a foundation species (Juniperus monosperma) promotes positive afterlife effects in understory vegetation. Plant Ecology 212: 733-741.
45. Kim YT, Colombo SJ, Hickie DF, Noland TL. 1999. Amino acid, carbohydrate, glutathione, mineral nutrient and water potential changes in non-water-stressed Picea mariana seedlings after transplanting. Scandinavian Journal of Forest Research 14: 416-424.
46. Klenner W, Arsenault A. 2009. Ponderosa pine mortality during a severe bark beetle (Coleoptera: Curculionidae, Scolytinae) outbreak in southern British Columbia and implications for wildlife habitat management. Forest Ecology and Management 258: S5-S14.
47. Knoblauch M, Peters WS. 2010. Münch, morphology, microfluidics - our structural problem with the phloem. Plant, Cell & Environment 33: 1439-1452.
48. Koch KE. 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 509-540.
49. Koepke DF, Kolb TE, Adams HD. 2010. Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163: 1079-1090.
50. Körner C. 2003. Carbon limitation in trees. Journal of Ecology 91: 4-17.
51. Kozlowski TT, Pallardy SG. 1997. Physiology of woody plants. San Diego, CA, USA: Academic Press.
52. Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L. 2008a. Mountain pine beetle and forest carbon feedback to climate change. Nature 452: 987-990.
53. Kurz WA, Stinson G, Rampley GJ, Dymond CC, Neilson ET. 2008b. Risk of natural disturbances makes future contribution of Canada's forests to the global carbon cycle highly uncertain. Proceedings of the National Academy of Sciences, USA 105: 1551-1555.
54. Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM. 1999. The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11: 707-726.
55. Landhäusser SM, Lieffers VJ. 2012. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees-Structure and Function 26: 653-661.
56. Leuzinger S, Bigler C, Wolf A, Körner C. 2009. Poor methodology for predicting large-scale tree die-off. Proceedings of the National Academy of Sciences, USA 106: E106.
57. Linton MJ, Sperry JS, Williams DG. 1998. Limits to water transport in Juniperus osteosperma and Pinus edulis: implications for drought tolerance and regulation of transpiration. Functional Ecology 12: 906-911.
58. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719-739.
59. McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155: 1051-1059.
60. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M. 2011. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology and Evolution 26: 523-532.
61. McDowell NG, Sevanto S. 2010. The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytologist 186: 264-266.
62. Metcalfe DB, Meir P, Aragao L, Lobo-do-Vale R, Galbraith D, Fisher RA, Chaves MM, Maroco JP, da Costa ACL, de Almeida SS et al. 2010. Shifts in plant respiration and carbon use efficiency at a large-scale drought experiment in the eastern Amazon. New Phytologist 187: 608-621.
63. Minchin PEH, Lacointe A. 2005. New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytologist 166: 771-779.
64. Münch E. 1930. Die Stoffbewegungen in der Pflanze. Jena, Germany: Gustav Fischer.
65. Murakeozy EP, Smirnoff N, Nagy Z, Tuba Z. 2002. Seasonal accumulation pattern of pinitol and other carbohydrates in Limonium gmelini subsp hungarica. Journal of Plant Physiology 159: 485-490.
66. Myers DA, Thomas RB, DeLucia EH. 1999. Photosynthetic responses of loblolly pine (Pinus taeda) needles to experimental reduction in sink demand. Tree Physiology 19: 235-242.
67. Nelson JM, Bartels PG. 1998. Irrigation effects on pinitol content of jojoba leaf blades and floral buds. Industrial Crops and Products 8: 159-165.
68. Obendorf RL. 1997. Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7: 63-74.
69. Ogren E, Nilsson T, Sundblad LG. 1997. Relationship between respiratory depletion of sugars and loss of cold hardiness in coniferous seedlings over-wintering at raised temperatures: indications of different sensitivities of spruce and pine. Plant, Cell & Environment 20: 247-253.
70. Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BWM, Cushman JC. 2011. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23: 1231-1248.
71. Piper FI. 2011. Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Annals of Forest Science 68: 415-424.
72. Plaut JA, Yepez EA, Hill J, Pangle R, Sperry JS, Pockman WT, McDowell NG. 2012. Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought. Plant, Cell & Environment 35: 1601-1617.
73. Rotenberg E, Yakir D. 2010. Contribution of semi-arid forests to the climate system. Science 327: 451-454.
74. Royer PD, Cobb NS, Clifford MJ, Huang CY, Breshears DD, Adams HD, Villegas JC. 2011. Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. Journal of Ecology 99: 714-723.
75. Ryan MG. 2011. Tree responses to drought. Tree Physiology 31: 237-239.
76. Sala A. 2009. Lack of direct evidence for the carbon-starvation hypothesis to explain drought-induced mortality in trees. Proceedings of the National Academy of Sciences, USA 106: E68.
77. Sala A, Hoch G. 2009. Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant, Cell & Environment 32: 22-30.
78. Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186: 274-281.
79. Sala A, Woodruff DR, Meinzer FC. 2012. Carbon dynamics in trees: feast or famine? Tree Physiology 32: 764-775.
80. Sayer MAS, Haywood JD. 2006. Fine root production and carbohydrate concentrations of mature longleaf pine (Pinus palustris P. Mill.) as affected by season of prescribed fire and drought. Trees-Structure and Function 20: 165-175.
81. Sergeant K, Spiess N, Renaut J, Wilhelm E, Hausman JF. 2011. One dry summer: a leaf proteome study on the response of oak to drought exposure. Journal of Proteomics 74: 1385-1395.
82. Smeekens S. 2000. Sugar-induced signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51: 49-81.
83. Sthultz CM, Gehring CA, Whitham TG. 2009. Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species. Global Change Biology 15: 1949-1961.
84. Strimbeck GR, Kjellsen TD, Schaberg PG, Murakami PF. 2008. Dynamics of low-temperature acclimation in temperate and boreal conifer foliage in a mild winter climate. Tree Physiology 28: 1365-1374.
85. Tierney GD, Foxx TS. 1987. Root lengths of plants on Los Alamos National Laboratory Lands. US Department of Energy, Technical Report LA-10865-MS. Los Alamos, NM, USA: Los Alamos National Laboratory.
86. Wiley E, Helliker B. 2012. A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytologist 195: 285-289.
87. Würth MKR, Pelaez-Riedl S, Wright SJ, Körner C. 2005. Non-structural carbohydrate pools in a tropical forest. Oecologia 143: 11-24.
88. Zeppel MJB, Adams HD, Anderegg WRL. 2011. Mechanistic causes of tree drought mortality: recent results, unresolved questions and future research needs. New Phytologist 192: 800-803.