How do trees die? A test of the hydraulic failure and carbon starvation hypotheses

Plant, Cell and Environment

Volumn 37, Issue 1, 2014, Pages 153-161

  Sevanto, Sanna ^a   Mcdowell, Nate G ^a   Dickman, L Turin ^a   Pangle, Robert ^b   Pockman, William T ^b  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Cavitation; Forest mortality; Hydraulic conductance; Non structural carbohydrates; Phloem; Xylem

Indexed keywords

CARBOHYDRATE; CARBON; CONIFEROUS TREE; DROUGHT STRESS; HYDRAULIC CONDUCTIVITY; MORTALITY; OSMOSIS; PHLOEM; PHYSIOLOGY; XYLEM;

PINUS EDULIS;

CARBOHYDRATE; CARBON; WATER;

ARTICLE; CAVITATION; CELL RESPIRATION; DROUGHT; EVAPOTRANSPIRATION; FOREST MORTALITY; HYDRAULIC CONDUCTIVITY; NON-STRUCTURAL CARBOHYDRATES; OSMOSIS; PHLOEM; PHOTOSYNTHESIS; PHYSIOLOGY; PINE; TIME; TREE; XYLEM;

CAVITATION; FOREST MORTALITY; HYDRAULIC CONDUCTANCE; NON-STRUCTURAL CARBOHYDRATES; PHLOEM; XYLEM;

CARBOHYDRATES; CARBON; CELL RESPIRATION; DROUGHTS; OSMOSIS; PHLOEM; PHOTOSYNTHESIS; PINUS; PLANT TRANSPIRATION; TIME FACTORS; TREES; WATER; XYLEM;

EID: 84897039950     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12141     Document Type: Article

References (41)

1. Adams H.D., Guardiola M., Barron-Gafford G.A., Villegas J.C., Breshears D.D., Zou C.B., Torch P.A. & Huxman T.E. (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America 106, 7063-7066.
2. Allen C.D., Macalady A., Chenchouni H., etal. (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.
3. Anderegg W.R., Berry J.A. & Field C.B. (2012) Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends in Plant Science 17, 693-700.
4. Anderegg W.R.L., Berry J.A., Smith D.D., Sperry J.S., Anderegg L.D.L. & Field C.B. (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proceedings of the National Academy of Sciences of the United States of America 109, 233-237.
5. Atkin O.K. & Macherel D. (2009) The critical role of plant mitochondria in orchestrating drought tolerance. Annals of Botany 103, 581-597.
6. Boyer J.S. (1968) Relationship of water potential to growth of leaves. Plant Physiology 43, 1056-1062.
7. Breshears D.D., Myers O.B., Meyer C.W., Barnes F.J., Zou C.B., Allen C.D., McDowell N.G. & Pockman W.T. (2009) Tree die-off in response to global-change-type drought: mortality insights from a decade of plant water potential measurements. Frontiers in Ecology and the Environment 7, 185-189.
8. Burgess S.S.O., Adams M.A., Turner N.C., Beverly C.R., Ong C.K., Khan A.A.H. & Bleby T.M. (2001) An improved heat pulse method to measure low and reverse rates of sap flow in woody plants. Tree Physiology 21, 589-598.
9. Carnicer J., Coll M., Ninverola M., Pons X., Sánchez 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 of the United States of America 10, 1474-1478.
10. Choat B., Jensen S., Brodribb T.J., etal. (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752-756.
11. Fisher R., McDowell N., Purves D., Moorcroft P., Sitch S., Cox P., Huntinford C., Meir P. & Woodward F.I. (2010) Assessing uncertainties in a second-generation dynamic vegetation model due to ecological scale limitations. New Phytologist 187, 666-681.
12. Freeland R.O. (1952) Effect of age of leaves upon the rate of photosynthesis in some conifers. Plant Physiology 27, 685-690.
13. Friedlingstein P., Cox P., Betts R., etal. (2006) Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison. Journal of Climate 19, 3337-3353.
14. 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.
15. Holbrook N.M. & Zwieniecki M.A. (1999) Embolism repair and xylem tension; do we need a miracle? Plant Physiology 120, 7-10.
16. Hölttä 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.
17. Kaufmann M.R. & Thor G.L. (1982) Measurement of water stress in subalpine trees: effects of temporary tissue storage methods and needle age. Canadian Journal of Forest Research 12, 969-972.
18. +, osmoregulation and drought tolerance - An overview. Proceedings of Indian National Science Academy B61, 51-56.
19. McDowell N.G. (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155, 1051-1059.
20. McDowell N.G. & Sevanto S. (2010) The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytologist 186, 264-266.
21. McDowell N., Pockman W.T., Allen C.D., etal. (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719-739.
22. van Mantgem P.J., Stephenson N.L., Byrne J.C., etal. (2009) Widespread increase of tree mortality rates in the Western United States. Science 323, 521-524.
23. Martinez-Vilalta J., Sala A. & Piñol J. (2004) The hydraulic architecture of Pinaceae - a review. Plant Ecology 171, 3-13.
24. Mencuccini M., Hölttä T., Sevanto S. & Nikinmaa E. (2013) Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal. New Phytologist 198, 1143-1154.
25. Mitchell P.J., O'Gardy A.P., Tissue D.T., White D.A., Ottenschlaeger M.L. & Pinkard E.A. (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytologist 197, 862-872.
26. 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 & Environment 36, 655-669.
27. Peng C., Ma Z., Lei X., etal. (2011) A drought-induced pervasive increase in tree mortality across Canada's boreal forests. Nature Climate Change 1, 467-471.
28. Peterson C.A. (1979) Selective vital staining of companion cells of potato tuber and parsnip root with neutral red. Stain Technology 54, 135-139.
29. Phillips O.L., Aragão L.E.O., Lewis S.L., etal. (2009) Drought sensitivity of the Amazon rainforest. Science 323, 1344-1347.
30. Plaut J.A., Yepez E.A., Hill J., Pangle R., Sperry J.S., Pockman W.T. & McDowell N.G. (2012) Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought. Plant, Cell & Environment 35, 1601-1617.
31. Sala A., Piper F. & Hoch G. (2010) Physiological mechanisms of drought induced tree mortality are far from being resolved. New Phytologist 186, 274-281.
32. Secchi F. & Zwieniecki M.A. (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant, Cell & Environment 34, 514-524.
33. Sevanto S., Hölttä T. & Holbrook N.M. (2011) Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. Plant, Cell & Environment 34, 690-703.
34. Sitch S., Huntingford C., Gedney N., etal. (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs). Global Change Biology 14, 2015-2039.
35. Sovonick-Dunford S., Lee D.R. & Zimmermann M.H. (1981) Direct and indirect measurements of phloem turgor pressure in White Ash. Plant Physiology 68, 121-126.
36. Sperry J.S., Donnelly J.R. & Tyree M.T. (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35-40.
37. Sperry J.S., Adler F.R., Campbell G.S. & Comstock J.C. (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell & Environment 21, 347-359.
38. Stitt M. & Zeeman S.C. (2012) Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282-292.
39. Talbott L.D. & Zeiger E. (1996) Central roles for potassium and sucrose in guard-cell osmoregulation. Plant Physiology 111, 1051-1057.
40. Tardieu F. & Simonneau T. (1998) Variability of species among stomatal control under fluctuating soil water status and evaporative demand: modeling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419-432.
41. Turgeon R. & Wolf S. (2009) Phloem transport: cellular pathways and molecular trafficking. Annual Review of Plant Biology 60, 207-221.