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Title: Drought impacts on tree phloem: from cell-level responses to ecological significance

Abstract

Abstract On-going climate change is increasing the risk of drought stress across large areas worldwide. Such drought events decrease ecosystem productivity and have been increasingly linked to tree mortality. Understanding how trees respond to water shortage is key to predicting the future of ecosystem functions. Phloem is at the core of the tree functions, moving resources such as non-structural carbohydrates, nutrients, and defence and information molecules across the whole plant. Phloem function and ability to transport resources is tightly controlled by the balance of carbon and water fluxes within the tree. As such, drought is expected to impact phloem function by decreasing the amount of available water and new photoassimilates. Yet, the effect of drought on the phloem has received surprisingly little attention in the last decades. Here we review existing knowledge on drought impacts on phloem transport from loading and unloading processes at cellular level to possible effects on long-distance transport and consequences to ecosystems via ecophysiological feedbacks. We also point to new research frontiers that need to be explored to improve our understanding of phloem function under drought. In particular, we show how phloem transport is affected differently by increasing drought intensity, from no response to a slowdown,more » and explore how severe drought might actually disrupt the phloem transport enough to threaten tree survival. Because transport of resources affects other organisms interacting with the tree, we also review the ecological consequences of phloem response to drought and especially predatory, mutualistic and competitive relations. Finally, as phloem is the main path for carbon from sources to sink, we show how drought can affect biogeochemical cycles through changes in phloem transport. Overall, existing knowledge is consistent with the hypotheses that phloem response to drought matters for understanding tree and ecosystem function. However, future research on a large range of species and ecosystems is urgently needed to gain a comprehensive understanding of the question.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [5]; ORCiD logo [6];
  1. Institute for Atmospheric and Earth System Research/Physics, Faculty of Science, Gustaf Hällströmin katu 2b, University of Helsinki, Helsinki, Finland, Institute for Atmospheric and Earth System Research/Forest Sciences, Faculty of Agriculture and Forestry, Latokartanonkaari 7, University of Helsinki, Helsinki, Finland
  2. Department of Environmental Sciences, University of Basel, Schönbeinstrasse 6, Basel, Switzerland
  3. Earth and Environmental Sciences Division, Los Alamos National Laboratory, PO Box 1663 MA 495, Los Alamos, NM, USA
  4. Institute for Atmospheric and Earth System Research/Forest Sciences, Faculty of Agriculture and Forestry, Latokartanonkaari 7, University of Helsinki, Helsinki, Finland
  5. Kyoto University, Laboratory of Ecosystem Production and Dynamics, Graduate School of Global Environmental Studies, Kyoto, Japan, Kyoto University, Laboratory of Forest Utilization, Graduate School of Agriculture, Kyoto, Japan
  6. Université de Lorraine, AgroParisTech, INRA, UMR Silva, Faculté des Sciences et Technologies, Nancy, France
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1493637
Alternate Identifier(s):
OSTI ID: 1495172
Report Number(s):
LA-UR-19-20138
Journal ID: ISSN 1758-4469
Grant/Contract Number:  
#20160373ER; 89233218CNA000001
Resource Type:
Published Article
Journal Name:
Tree Physiology (Online)
Additional Journal Information:
Journal Name: Tree Physiology (Online) Journal Volume: 39 Journal Issue: 2; Journal ID: ISSN 1758-4469
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Biological Science; Earth Sciences

Citation Formats

Salmon, Yann, Dietrich, Lars, Sevanto, Sanna, Hölttä, Teemu, Dannoura, Masako, Epron, Daniel, and Ryan, ed., Michael. Drought impacts on tree phloem: from cell-level responses to ecological significance. United Kingdom: N. p., 2019. Web. doi:10.1093/treephys/tpy153.
Salmon, Yann, Dietrich, Lars, Sevanto, Sanna, Hölttä, Teemu, Dannoura, Masako, Epron, Daniel, & Ryan, ed., Michael. Drought impacts on tree phloem: from cell-level responses to ecological significance. United Kingdom. https://doi.org/10.1093/treephys/tpy153
Salmon, Yann, Dietrich, Lars, Sevanto, Sanna, Hölttä, Teemu, Dannoura, Masako, Epron, Daniel, and Ryan, ed., Michael. Wed . "Drought impacts on tree phloem: from cell-level responses to ecological significance". United Kingdom. https://doi.org/10.1093/treephys/tpy153.
@article{osti_1493637,
title = {Drought impacts on tree phloem: from cell-level responses to ecological significance},
author = {Salmon, Yann and Dietrich, Lars and Sevanto, Sanna and Hölttä, Teemu and Dannoura, Masako and Epron, Daniel and Ryan, ed., Michael},
abstractNote = {Abstract On-going climate change is increasing the risk of drought stress across large areas worldwide. Such drought events decrease ecosystem productivity and have been increasingly linked to tree mortality. Understanding how trees respond to water shortage is key to predicting the future of ecosystem functions. Phloem is at the core of the tree functions, moving resources such as non-structural carbohydrates, nutrients, and defence and information molecules across the whole plant. Phloem function and ability to transport resources is tightly controlled by the balance of carbon and water fluxes within the tree. As such, drought is expected to impact phloem function by decreasing the amount of available water and new photoassimilates. Yet, the effect of drought on the phloem has received surprisingly little attention in the last decades. Here we review existing knowledge on drought impacts on phloem transport from loading and unloading processes at cellular level to possible effects on long-distance transport and consequences to ecosystems via ecophysiological feedbacks. We also point to new research frontiers that need to be explored to improve our understanding of phloem function under drought. In particular, we show how phloem transport is affected differently by increasing drought intensity, from no response to a slowdown, and explore how severe drought might actually disrupt the phloem transport enough to threaten tree survival. Because transport of resources affects other organisms interacting with the tree, we also review the ecological consequences of phloem response to drought and especially predatory, mutualistic and competitive relations. Finally, as phloem is the main path for carbon from sources to sink, we show how drought can affect biogeochemical cycles through changes in phloem transport. Overall, existing knowledge is consistent with the hypotheses that phloem response to drought matters for understanding tree and ecosystem function. However, future research on a large range of species and ecosystems is urgently needed to gain a comprehensive understanding of the question.},
doi = {10.1093/treephys/tpy153},
journal = {Tree Physiology (Online)},
number = 2,
volume = 39,
place = {United Kingdom},
year = {Wed Feb 06 00:00:00 EST 2019},
month = {Wed Feb 06 00:00:00 EST 2019}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1093/treephys/tpy153

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Drought-Induced Reduction in Global Terrestrial Net Primary Production from 2000 Through 2009
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Variation of soil and biomass carbon pools in beech forests across a precipitation gradient
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Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects
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Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis
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Paradigm shift in plant growth control
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Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux
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Vitamin C and the Abscisic Acid-Insensitive 4 Transcription Factor Are Important Determinants of Aphid Resistance in Arabidopsis
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Phloem loading and its development related to plant evolution from trees to herbs
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Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know
journal, March 2016

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Drought impact on forest carbon dynamics and fluxes in Amazonia
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Regulation of Sucrose Transporters and Phloem Loading in Response to Environmental Cues
journal, November 2017

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The crucial role of plant mitochondria in orchestrating drought tolerance
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How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die?
journal, June 2013

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The Physiology of the Sieve Tube: PRELIMINARY EXPERIMENTS USING APHID MOUTH PARTS
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Anthropogenic effects on interaction outcomes: examples from insect-microbial symbioses in forest and savanna ecosystems
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Do water-limiting conditions predispose Norway spruce to bark beetle attack?
journal, November 2014

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Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi
journal, April 2011


MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco
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Dynamics of Cold Induced Inhibition of Phloem Transport
journal, January 1983

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Plant Responses to Water Stress
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Phloem Transport: Cellular Pathways and Molecular Trafficking
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Drought impacts on phloem transport
journal, June 2018


Water Deficit-Induced Changes in Concentrations in Proline and Some Other Amino Acids in the Phloem Sap of Alfalfa
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Seasonal variations drive short-term dynamics and partitioning of recently assimilated carbon in the foliage of adult beech and pine
journal, August 2016

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Phloem loading, plant growth form, and climate
journal, December 2010


Maintenance of carbohydrate transport in tall trees
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Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review
journal, January 2011


Environment and ontogeny modify loblolly pine response to induced acute water deficits and bark beetle attack
journal, May 1995

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Water Stress, Growth, and Osmotic Adjustment
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Are phloem sieve tubes leaky conduits supported by numerous aquaporins?
journal, May 2017

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What actually is the Münch hypothesis? A short history of assimilate transport by mass flow: A history of the Münch hypothesis
journal, May 2017

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Comparison of phloem and xylem hydraulic architecture in Picea abies stems
journal, August 2014

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An analysis of irreversible plant cell elongation
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Impact of interspecific competition and drought on the allocation of new assimilates in trees
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A Simpler Iterative Steady State Solution of Münch Pressure-Flow Systems Applied to Long and Short Translocation Paths
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Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1.
journal, October 2010

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Mechanisms Linking Drought, Hydraulics, Carbon Metabolism, and Vegetation Mortality
journal, January 2011


Assimilate transport in phloem sets conditions for leaf gas exchange: Transport stoma
journal, October 2012

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Transport of hormones in the phloem of higher plants
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Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation: Xylem-phloem hydraulic coupling and phloem diameter variation
journal, February 2011


Phloem transport and drought
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Death from drought in tropical forests is triggered by hydraulics not carbon starvation
journal, November 2015

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Regional vegetation die-off in response to global-change-type drought
journal, October 2005

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Sucrose transporters and plasmodesmal regulation in passive phloem loading: Mechanism and regulation of passive phloem loading
journal, May 2017

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Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon?
journal, October 2009

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Seasonal variations of belowground carbon transfer assessed by in situ 13 CO 2 pulse labelling of trees
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Influence of Host Tree Condition on the Performance of Tetropium fuscum (Coleoptera: Cerambycidae)
journal, October 2011

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Real-time imaging of phloem unloading in the root tip of Arabidopsis
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Buffering growth variations against water deficits through timely carbon usage
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Ectomycorrhizas and water relations of trees: a review
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Ecophysiology of phloem loading in source leaves
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Are outbreaks of cambium-feeding beetles generated by nutritionally enhanced phloem of drought-stressed trees?
journal, December 2014

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Tree physiology and bark beetles
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Evidence for solution flow in the phloem of willow
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Consequences of phloem pathway unloading/reloading on equilibrium flows between source and sink: a modelling approach
journal, January 2017

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Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control: Tansley review
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In vivo Observation of Tree Drought Response with Low-Field NMR and Neutron Imaging
journal, May 2016

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The role of nutrients in drought-induced tree mortality and recovery
journal, November 2016

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Phenological variation in xylem and phloem formation in Fagus sylvatica from two contrasting sites
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Estimation of the Volumetric Elastic Modulus and Membrane Hydraulic Conductivity of Willow Sieve Tubes
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Climate Change and Bark Beetles of the Western United States and Canada: Direct and Indirect Effects
journal, September 2010

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