Initial Hydraulic Failure Followed by Late-stage Carbon Starvation Leads to Drought-induced Death in the Tree

Overview

Journal Commun Biol

Specialty Biology

Date 2019 Jan 10

PMID 30623104

Citations 13

Authors

Yuri Kono

Atsushi Ishida

Shin-Taro Saiki

Kenichi Yoshimura

Masako Dannoura

Kenichi Yazaki

Fuku Kimura

Jin Yoshimura

Shin-Ichi Aikawa

Affiliations

Soon will be listed here.

Abstract

Drought-induced tree death has become a serious problem in global forest ecosystems. Two nonexclusive hypotheses, hydraulic failure and carbon starvation, have been proposed to explain tree die-offs. To clarify the mechanisms, we investigated the physiological processes of drought-induced tree death in saplings with contrasting Huber values (sapwood area/total leaf area). First, hydraulic failure and reduced respiration were found in the initial process of tree decline, and in the last stage carbon starvation led to tree death. The carbohydrate reserves at the stem bases, low in healthy trees, accumulated at the beginning of the declining process due to phloem transport failure, and then decreased just before dying. The concentrations of non-structural carbohydrates at the stem bases are a good indicator of tree damage. The physiological processes and carbon sink-source dynamics that occur during lethal drought provide important insights into the adaptive measures underlying forest die-offs under global warming conditions.

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References

Sevanto S, Mcdowell N, Dickman L, Pangle R, Pockman W . How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 2013; 37(1):153-61. PMC: 4280888. DOI: 10.1111/pce.12141. View

Yazaki K, Kuroda K, Nakano T, Kitao M, Tobita H, Ogasa M . Recovery of Physiological Traits in Saplings of Invasive Bischofia Tree Compared with Three Species Native to the Bonin Islands under Successive Drought and Irrigation Cycles. PLoS One. 2015; 10(8):e0135117. PMC: 4546390. DOI: 10.1371/journal.pone.0135117. View

Secchi F, Zwieniecki M . Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ. 2010; 34(3):514-24. DOI: 10.1111/j.1365-3040.2010.02259.x. View

Ishida A, Nakano T, Yazaki K, Matsuki S, Koike N, Lauenstein D . Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms. Oecologia. 2008; 156(1):193-202. DOI: 10.1007/s00442-008-0965-6. View

Scoffoni C, Sack L, Ort D . The causes and consequences of leaf hydraulic decline with dehydration. J Exp Bot. 2017; 68(16):4479-4496. DOI: 10.1093/jxb/erx252. View

Sala A, Piper F, Hoch G . Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 2010; 186(2):274-81. DOI: 10.1111/j.1469-8137.2009.03167.x. View

McDowell N, Pockman W, Allen C, Breshears D, Cobb N, Kolb T . Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?. New Phytol. 2008; 178(4):719-739. DOI: 10.1111/j.1469-8137.2008.02436.x. View

Dubois M, GILLES K, Hamilton J, Rebers P, Smith F . A colorimetric method for the determination of sugars. Nature. 1951; 168(4265):167. DOI: 10.1038/168167a0. View

Hartmann H, Moura C, Anderegg W, Ruehr N, Salmon Y, Allen C . Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol. 2018; 218(1):15-28. DOI: 10.1111/nph.15048. View

10.

McDowell N . Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 2011; 155(3):1051-9. PMC: 3046567. DOI: 10.1104/pp.110.170704. View

11.

Zwieniecki M, Holbrook N . Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends Plant Sci. 2009; 14(10):530-4. DOI: 10.1016/j.tplants.2009.07.002. View

12.

Arndt S, Livesley S, Merchant A, Bleby T, Grierson P . Quercitol and osmotic adaptation of field-grown Eucalyptus under seasonal drought stress. Plant Cell Environ. 2008; 31(7):915-24. DOI: 10.1111/j.1365-3040.2008.01803.x. View

13.

Rowland L, da Costa A, Galbraith D, Oliveira R, Binks O, Oliveira A . Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature. 2015; 528(7580):119-22. DOI: 10.1038/nature15539. View

14.

Adams H, Zeppel M, Anderegg W, Hartmann H, Landhausser S, Tissue D . A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol. 2017; 1(9):1285-1291. DOI: 10.1038/s41559-017-0248-x. View

15.

Donovan L, Linton M, Richards J . Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia. 2017; 129(3):328-335. DOI: 10.1007/s004420100738. View

16.

Kamaluddin M, Zwiazek J . Naphthenic acids inhibit root water transport, gas exchange and leaf growth in aspen (Populus tremuloides) seedlings. Tree Physiol. 2002; 22(17):1265-70. DOI: 10.1093/treephys/22.17.1265. View

17.

Xu C, Mcdowell N, Sevanto S, Fisher R . Our limited ability to predict vegetation dynamics under water stress. New Phytol. 2013; 200(2):298-300. DOI: 10.1111/nph.12450. View

18.

Saiki S, Ishida A, Yoshimura K, Yazaki K . Physiological mechanisms of drought-induced tree die-off in relation to carbon, hydraulic and respiratory stress in a drought-tolerant woody plant. Sci Rep. 2017; 7(1):2995. PMC: 5462810. DOI: 10.1038/s41598-017-03162-5. View

19.

Kono Y, Ishida A, Saiki S, Yoshimura K, Dannoura M, Yazaki K . Initial hydraulic failure followed by late-stage carbon starvation leads to drought-induced death in the tree . Commun Biol. 2019; 2:8. PMC: 6323055. DOI: 10.1038/s42003-018-0256-7. View

20.

Sperry J, Ikeda T . Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiol. 1997; 17(4):275-80. DOI: 10.1093/treephys/17.4.275. View