Co-ordination of growth, gas exchange and hydraulics define the carbon safety margin in tree species with contrasting drought strategies

Tree Physiology

Volumn 34, Issue 5, 2014, Pages 443-458

  Mitchell, P J ^a   O'Grady, A P ^a   Tissue, D T ^b   Worledge, D ^a   Pinkard, E A ^a  

^a CSIRO   (Australia)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

drought mortality; growth; non structural carbohydrates; plant strategy; stomatal regulation; water deficit

Indexed keywords

CARBON; DROUGHT; GAS EXCHANGE; GROWTH RATE; METABOLISM; MORTALITY; PHOTOSYNTHESIS; PLANT; SURVIVAL; TRANSPIRATION; TREE; WATER;

GAS; WATER;

CARBOHYDRATE METABOLISM; DROUGHT; EUCALYPTUS; EVAPOTRANSPIRATION; GAS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PINE; PLANT LEAF; PLANT STEM; TREE;

CARBOHYDRATE METABOLISM; DROUGHTS; EUCALYPTUS; GASES; PINUS; PLANT LEAVES; PLANT STEMS; PLANT TRANSPIRATION; TREES; WATER;

EID: 84902290936     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpu014     Document Type: Article

References (64)

1. Allen CD, Macalady AK, Chenchouni H 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.
2. Amthor JS, McCree KJ (1990) Carbon balance of stressed plants: a conceptual model for integrating research results. Wiley-Liss, New York.
3. Anderegg WRL, Berry JA, Field CB (2012a) Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends Plant Sci 17: 693-700.
4. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012b) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109: 233-237.
5. Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytol 190: 1003-1018.
6. Bartlett MK (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecology 15: 393-405.
7. Blackman CJ, Brodribb TJ, Jordan GJ (2009) Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant Cell Environ 32: 1584-1595.
8. Bogeat-Triboulot M-B, Brosché M, Renaut J et al. (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a Poplar growing in arid regions. Plant Physiol 143: 876-892.
9. Boyer JS (1970) Leaf enlargement and metabolic rates in corn, soybean, and sunflower at various leaf water potentials. Plant Physiol 46: 233-235.
10. Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132: 2166-2173.
11. Brodribb TJ, McAdam SAM (2013) ABA mediates a divergence in the drought response of two conifers. Plant Physiol 162: 1370-1377.
12. Chapin FS, Schulze E-d, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21: 423-447.
13. Choat B, Jansen S, Brodribb TJ et al. (2012) Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
14. Claeys H, Inzé D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol 162: 1768-1779.
15. Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla M, Jones HG (1998) The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance Ziziphus mauritiana (Lamk). J Exp Bot 49: 967-977.
16. De Diego N, Rodríguez JL, Dodd IC, Pérez-Alfocea F, Moncaleán P, Lacuesta M (2013) Immunolocalization of IAA and ABA in roots and needles of radiata pine (Pinus radiata) during drought and rewatering. Tree Physiol 33: 537-549.
17. Dewar RC, Ludlow AR, Dougherty PM (1994) Environmental influences on carbon allocation in Pines. Ecol Bull 43: 92-101.
18. Edwards WRN, Warwick NWN (1984) Transpiration from a kiwifruit vine as estimated by the heat pulse technique and the Penman-Monteith equation. N Z J Agric Res 27: 537-543.
19. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot (Lond) 89: 183-189.
20. Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 year after a drought episode. New Phytol 190: 750-759.
21. Galvez DA, Landhäusser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31: 250-257.
22. Genet H, Bréda N, Dufrêne E (2010) Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) using a chronosequence approach. Tree Physiol 30: 177-192.
23. Guehl JM, Clement A, Kaushal P, Aussenac G (1993) Planting stress, water status and non-structural carbohydrate concentrations in Corsican pine seedlings. Tree Physiol 12: 173-183.
24. Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4: 97-115.
25. Hartmann H, Ziegler W, Kolle O, Trumbore S (2013a) Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200: 340-349.
26. Hartmann H, Ziegler W, Trumbore S (2013b) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27: 413-427.
27. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26: 1067-1081.
28. Hsiao TC, Xu LK (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. J Exp Bot 51: 1595-1616.
29. Hsiao TC, Acevedo E, Fereres E, Henderson DW (1976) Water stress, growth, and osmotic adjustment. Philos Trans R Soc Lond B Biol Sci 273: 479-500.
30. Koppenaal RS, Tschaplinski TJ, Colombo SJ (1991) Carbohydrate accumulation and turgor maintenance in seedling shoots and roots of two boreal conifers subjected to water stress. Can J Bot 69: 2522-2528.
31. Körner C (2003) Carbon limitation in trees. J Ecol 91: 4-17.
32. Lambers H, Chapin FS, Pons TL (1998) Growth and allocation plant physiological ecology. Springer, New York, 321 p.
33. Martin-StPaul NK, Limousin J-M, Vogt-Schilb H, Rodríguez- Calcerrada J, Rambal S, Longepierre D, Misson L (2013) The temporal response to drought in a Mediterranean evergreen tree: comparing a regional precipitation gradient and a throughfall exclusion experiment. Glob Change Biol 19: 2413-2426.
34. McDowell NG, Beerling DJ, Breshears DD, Fisher Ra, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26: 523-532.
35. Mencuccini M, Hölttä T (2010) The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytol 185: 189-203.
36. Mitchell PJ, O'Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol 197: 862-872.
37. Mitchell PJ, O'Grady AP, Hayes KR, Pinkard EA (2014) Exposure of trees to drought-induced die-off is defined by a common climatic threshold across different vegetation types. Ecol Evol doi:10.1002/ece3.1008.
38. Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (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.
39. Myers BJ, Theiveyanathan S, O'Brien ND, Bond WJ (1996) Growth and water use of Eucalyptus grandis and Pinus radiata plantations irrigated with effluent. Tree Physiol 16: 211-219.
40. Nardini A, Battistuzzo M, Savi T (2013) Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytol 200: 322-329.
41. Newell E, Mulkey S, Wright J (2002) Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia 131: 333-342.
42. Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36: 655-669.
43. Palacio S, Hoch G, Sala A, Körner C, Millard P (2013) Does carbon storage limit tree growth? New Phytol 201: 1096-1100.
44. Pereira JS, Chaves MM, Fonseca F, Araújo MC, Torres F (1992) Photosynthetic capacity of leaves of Eucalyptus globulus (Labill.) growing in the field with different nutrient and water supplies. Tree Physiol 11: 381-389.
45. Pinkard EA, Eyles A, O'Grady AP (2011) Are gas exchange responses to resource limitation and defoliation linked to source:sink relationships? Plant Cell Environ 34: 1652-1665.
46. Piper F (2011) Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Ann For Sci 68: 415-424.
47. Poyatos R, Aguadé D, Galiano L, Mencuccini M, Martínez- Vilalta J (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol 200: 388-401.
48. Quick WP, Chaves MM, Wendler R et al. (1992) The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions. Plant Cell Environ 15: 25-35.
49. Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32: 764-775.
50. Sands R, Kriedemann PE, Cotterill PP (1984) Water relations and photosynthesis in three families of radiata pine seedlings known to differ in their response to weed control. For Ecol Manag 9: 173-184.
51. Schulte PJ, Hinckley AR (1985) A comparison of pressure-volume curve data analysis techniques. J Exp Bot 36: 1590-1602.
52. Silpi U, Lacointe A, Kasempsap P et al. (2007) Carbohydrate reserves as a competing sink: evidence from tapping rubber trees. Tree Physiol 27: 881-889.
53. Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agric For Meteorol 104: 13-23.
54. Swanson RH, Whitfield DWA (1981) A numerical analysis of heat pulse velocity theory and practice. J Exp Bot 32: 221-239.
55. Tang A-C, Boyer JS (2002) Growth-induced water potentials and the growth of maize leaves. J Exp Bot 53: 489-503.
56. Tardieu F, Granier C, Muller B (2011) Water deficit and growth. Co-ordinating processes without an orchestrator? Curr Opin Plant Biol 14: 283-289.
57. Tissue DT, Nobel PS (1990) Carbon relations of flowering in a semelparous clonal desert perennial. Ecology 71: 273-281.
58. Tissue DT, Wright SJ (1995) Effect of seasonal water availability on phenology and the annual shoot carbohydrate cycle of tropical forest shrubs. Funct Ecol 9: 518-527.
59. Turner NC (1988) Measurement of plant water status by the pressure chamber technique. Irrigat Sci 9: 289-308.
60. Warton DI, Wright IJ, Falster DS (2006) Bivariate line-fitting methods for allometry. Biol Rev 81: 259-291.
61. White DA, Beadle CL, Worledge D (1996) Leaf water relations of Eucalyptus globulus ssp. globulus and E. nitens: seasonal, drought and species effects. Tree Physiol 16: 469-476.
62. White DA, Beadle CL, Sands PJ, Worledge D, Honeysett JL (1999) Quantifying the effect of cumulative water stress on stomatal conductance of Eucalyptus globulus and Eucalyptus nitens: a phenomenological approach. Funct Plant Biol 26: 17-27.
63. Whitehead D, Jarvis P (1981) Coniferous forests and plantations. In: Kozlowski T (ed) Plant growth and water deficit. Academic Press, London, pp 49-152.
64. Woodruff DR, Meinzer FC (2011) Water stress, shoot growth and storage of non-structural carbohydrates along a tree height gradient in a tall conifer. Plant Cell Environ 34: 1920-1930.