Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality

Plant Physiology

Volumn 155, Issue 3, 2011, Pages 1051-1059

  McDowell, Nathan G ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79952306080     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.170704     Document Type: Article

References (94)

1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91-94
2. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20: 2117-2129
3. Adams HD, Guardiola-Claramonte M, Barron-Gafford G, Camilo Villegasa J, Breshears D, Zou C, Troch P, Huxman T (2009a) Reply to Sala: Temperature sensitivity in drought-induced tree mortality hastens the need to further resolve a physiological model of death. Proc Natl Acad Sci USA 106: E69
4. Adams HD, Guardiola-Claramonte M, Barron-Gafford G, Camilo Villegasa J, Breshears D, Zou C, Troch P, Huxman T (2009b) Reply to Leuzinger et al.: Drought-induced tree mortality temperature sensitivity requires pressing forward with best available science. Proc Natl Acad Sci USA 106: E107
5. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009c) 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
6. Ainsworth EA, Bush DR (2010) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155: 64-69
7. Allen CD, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Gonzales P, Hogg T, Rigling A, Breshears D, et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259: 660-684
8. Amthor JS (1994) Plant respiratory responses to the environment and their effects on the carbon balance. In RE Wilkinson, ed, Plant-Environment Interactions. Marcel Dekker, New York, pp 501-554
9. Amthor JS, McCree KJ (1990) Carbon balance of stressed plants: a conceptual model for integrating research results. In RG Alscher, JR Cumming, eds, Stress Responses in Plants: Adaptation and Acclimation Mechanisms. Wiley-Liss, New York, pp 1-15
10. Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot (Lond) 103: 581-597
11. Atkin OK, Scheurwater I, Pons TL (2007) Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures. New Phytol 174: 367-380
12. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8: 343-351
13. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24: 23-58
14. Bieleski RL, Ripperda J, Newman JP, Reid MS (1992) Carbohydrate changes and leaf blackening in cut flower stems of Protea eximia. J Am Soc Hortic Sci 117: 124-127
15. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33: 1597-1613
16. Boyle MG, Boyer JS, Morgan PW (1991) Stem infusion of liquid culture medium prevents reproductive failure of maize at low water potential. Crop Sci 31: 1246-1252
17. Bre ́da N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann Sci 63: 625-644
18. Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT (2009) Tree die-off in response to globalchange- type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ 7: 185-189
19. Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149: 575-584
20. Brodribb TJ, Holbrook NM (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant Cell Environ 29: 2205-2215
21. Brouquisse R, Gaudille ́re JP, Raymond P (1998) Induction of a carbonstarvation- related proteolysis in whole maize plants submitted to light/ dark cycles and to extended darkness. Plant Physiol 117: 1281-1291
22. Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg L, Da SL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26: 1633-1645
23. Cernusak LA, Arthur DJ, Pate JS, Farquhar GD (2003)Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiol 131: 1544-1554
24. Chapin FS III, Schulze ED,Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21: 423-447
25. Coulson RN (1979) Population dynamics of bark beetles. Annu Rev Entomol 24: 417-447
26. Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142: 1574-1588
27. De ́jardin A, Sokolov LN, Kleczkowski LA (1999) Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem J 344: 503-509
28. Eilmann B, Zweifel R, Buchmann N, Fonti P, Rigling A (2009) Droughtinduced adaptation of the xylem in Scots pine and pubescent oak. Tree Physiol 29: 1011-1020
29. Estiarte M, Peñuelas J (1999) Excess carbon: the relationship with phenotypical plasticity in storage and defense functions of plants. Orsis 14: 159-203
30. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Sust Agric 29: 185-212
31. Flexas J, Galmes J, Ribas-Carbo M, Medrano H (2005) The effects of water stress on plant respiration. In H Lambers, M Ribas-Carbo, eds, Plant Respiration. Springer, Dordrecht, The Netherlands, pp 85-94
32. Fukuda K, Utsuzawa S, Sakaue D (2007) Correlation between acoustic emission, water status and xylem embolism in pine wilt disease. Tree Physiol 27: 969-976
33. Gaff DF (1971) Desiccation-tolerant flowering plants in southern Africa. Science 174: 1033-1034
34. Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M(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
35. Guérard N, Maillard P, Brechet C, Lieutier F, Dreyer E (2007) Do trees use reserve or newly assimilated carbon for their defense reactions? A 13C labeling approach with young Scots pines inoculated with a bark-beetleassociated fungus (Ophiostoma brunneo ciliatum). Ann Sci 64: 601-608
36. Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue: embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125: 779-786
37. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin- GID1-DELLA growth regulatory mechanism: how an "inhibitor of an inhibitor" enables flexible response to fluctuating environments. Plant Cell 21: 1328-1339
38. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67: 282-335
39. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26: 1067-1081
40. Hölttä T, Cochard H, Nikinmaa E, Mencuccini M (2009a) Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant Cell Environ 32: 10-21
41. Hölttä T, Mencuccini M, Nikinmaa E (2009b) Linking phloem function to structure: analysis with a coupled xylem-phloem transport model. J Theor Biol 259: 325-337
42. Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on the mineral nutrition of plants. J Plant Nutr Soil Sci 168: 541-549
43. Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteillé M, Stitt M, et al (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154: 357-372
44. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45: 771-787
45. Kobe K (1997) Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80: 226-233
46. Körner C (2003) Carbon limitation in trees. J Ecol 91: 4-17
47. Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68: 270-334
48. Langenheim JH (2003) Plant Resins: Chemistry, Evolution, Ecology and Ethnobotany. Timber Press, Portland, OR
49. Leuzinger S, Bigler C, Wolf A, Körner C (2009) Poor methodology for predicting large-scale tree die-off. Proc Natl Acad Sci USA 106: E106; author reply E107
50. Lewinsohn E, Gijzen M, Croteau R (1991) Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiol 96: 44-49
51. Limousin JM, Rambal S, Ourcival JM, Rocheteau A, Joffre R, Rodriguez- Cortinta R (2009) Long-term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest. Glob Change Biol 15: 2163-2175
52. Luxmoore RJ, Oren R, Sheriff DW, Thomas RB (1995) Source-sink-storage relationships of conifers. In WK Smith, TM Hinckley, eds, Resource Physiology of Conifers: Acquisition, Allocation and Utilization. Academic Press, San Diego, pp 179-216
53. Marshall JD, Waring RH (1985) Predicting fine root production and turnover by monitoring root starch and soil temperature. Can J Res 15: 791-800
54. McDowell NG, Allen CG, Marshall L (2010) Growth, carbon isotope discrimination, and mortality across a ponderosa pine elevation transect. Glob Change Biol 16: 399-415
55. McDowell NG, 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 Phytol 178: 719-739
56. McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol 186: 264-266
57. McLaughlin JE, Boyer JS (2004) Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems. Ann Bot (Lond) 94: 75-86
58. Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23: 922-930
59. Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM (2010) The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164: 287-296
60. Millard P, Sommerkorn M, Grelet GA (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175: 11-28
61. Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd NP, Jones JD (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18: 650-655
62. Oxford English Dictionary (2009) Oxford University Press, Oxford
63. Paine TD, Raffa KF, Harrington TC (1997) Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42: 179-206
64. Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62: 869-882
65. Piper FI, Reyes-Diáz EM, Corcuera LJ, Lusk CH (2009) Carbohydrate storage, survival, and growth of two evergreen Nothofagus species in two contrasting light environments. Ecol Res 24: 1233-1241
66. Poorter H, Villar R (1997) The fate of acquired carbon in plants: chemical composition and construction costs. In FA Bazzaz, B Jones, eds, Plant Resource Allocation. Academic Press, New York, pp 39-72
67. Pratt RB, Jacobsen AL, North GB, Sack L, Schenk HJ (2008) Plant hydraulics: new discoveries in the pipeline. New Phytol 179: 590-593
68. Rice KJ, Matzner SL, Byer W, Brown JR (2004) Patterns of tree dieback in Queensland, Australia: the importance of drought stress and the role of resistance to cavitation. Oecologia 139: 190-198
69. Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F (2006) Starvationinduced expression of autophagy-related genes in Arabidopsis. Biol Cell 98: 53-67
70. Rufty TW, Huber SC, Volk RJ (1988) Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol 88: 725-730
71. Sala A (2009) Lack of direct evidence for the carbon-starvation hypothesis to explain drought-induced mortality in trees. Proc Natl Acad Sci USA 106: E68; author reply E69
72. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186: 274-281
73. Salleo S, Trifilo P, Esposito S, Nardini A, LoGullo M (2009) Starch-tosugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36: 815-825
74. Sardans J, Peñ uelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol Biochem 37: 455-461
75. Schoenweiss DF (1981) Water stress as a predisposing factor in plant disease. In TT Kozlowski, ed, Water Deficits and Plant Growth. Academic Press, New York, pp 61-99
76. Smith AM, Stitt M(2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149
77. Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ 31: 632-645
78. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78: 23-55
79. Steele CL, Lewinsohn E, Croteau R (1995) Induced oleoresin biosynthesis in grand fir as a defense against bark beetles. Proc Natl Acad Sci USA 92: 4164-4168
80. Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilization of carbon in a fluctuating environment. Funct Plant Biol 34: 526-549
81. Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism: more than the icing on the cake. Plant J 61: 1067-1091
82. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC, Von, et al (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106: 10348-10353
83. Tschaplinski TJ, Hanson PJ (2003) Dormant season nonstructural carbohydrate storage. In PJ Hanson, SD Wullschleger, eds, North American Temperate Deciduous Forest Responses to Changing Precipitation Regimes. Springer, New York, pp 67-84
84. Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T (1993) Droughtinduced leaf shedding in walnut: evidence for vulnerability segmentation. Plant Cell Environ 16: 879-882
85. Vilagrosa A, Bellot J, Vallejo VR, Gil-Pelegrin E (2003) Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. J Exp Bot 54: 2015-2024
86. Vilagrosa A, Morales F, Abadĺa A, Bellot J, Cochard H, Gil-Pelegrin E (2010) Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species. Environ Exp Bot 69: 233-242
87. Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68: 223-251
88. Wang ZP, Deloire A, Carbonneau A, Federspiel B, Lopez F (2003) An in vivo experimental system to study sugar phloem unloading in ripening grape berries during water deficiency stress. Ann Bot (Lond) 92: 523-528
89. Willson CJ, Manos PS, Jackson RB (2008) Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). Am J Bot 95: 299-314
90. Wullschleger SD, McLaughlin SB, Ayres MP (2004) High-resolution analysis of stem increment and sap flow for loblolly pine trees attacked by southern pine beetle. Can J Res 34: 2387-2393
91. Würth MKR, Peláez-Riedl S, Wright SJ, Körner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143: 11-24
92. Xingsheng L, Cope MB, Johnson MS, Smith DL Jr, Nagy TR (2010) Mild calorie restriction induces fat accumulation in female C57BL/6J mice. Obesity (Silver Spring) 18: 456-562
93. Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Glob Change Biol 12: 27-41
94. Zwieniecki MA, Holbrook NM (2009) Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends Plant Sci 14: 530-534