Functionnal and ecological significance of cavitation in trees UMR PIAF INRA-Université Blaise Pascal Clermont-Ferrand Louuvain, Hervé Cochard A L I M E N T A T I O N A G R I C U L T U R E E N V I R O N N E M E N T Salt & Water Stress in Plants Newry August 2014

Cohesion-Tension Theory (Dixon 1896) 0 P xylem, MPa Daily time course of xylem pressure Ash trees CAVITATION

Cavitation: a common phenomenon Cavitation in trees? Positive? Negative? What is its biological significance?

% CAVITATION Sap pressure, MPa P50 Xylem vulnerability curves to cavitation P50 = Sap pressure provoking 50% cavitation

Methods to measure cavitation Acoustic Emissions Tyree et al 1985 Hydraulic conductance loss Sperry et al 1988 Air injection Cochard et al r Centrifuge technique Alder et al 1997, Cochard 2002 Dehydration How vulnerable are tree species to cavitation?

% cavitation Stomatal Conductance Martin St Paul et al (in press) Highly cavitation-resistant species Sap pressure, MPa Quercus ilex P x-min Sigmoidal curve

Jacobsen & Pratt 2012 Vitis Zufferey, et al 2011 % cavitation Sap pressure, MPa Low cavitation-resistance species Stomatal Conductance % cavitation P x-min Exponential curve Sap pressure, MPa

Two ‘strategies’ for tree hydraulics Stomatal conductance % cavitation Sap pressure, MPa Low cavitation-resistance: -Cavitation forms as soon as P x <0 -Cavitation and repair are routine on a daily basis -Water release by cavitation sustain stomatal opening & carbon gain High cavitation-resistance: -Cavitation forms when P x <P cav -Stomatal control of cavitation -Cavitation occurs only under intense drought conditions -Refilling is seasonal The same species have been found to display both strategies !!! 50/50 Cochard & Delzon 2013 What is the biological significance of cavitation ? P x-min

Pitfalls in hydraulic methods ?

Air dehydration Air injection Centrifugation ConiferousDiffuse-porousRing-porous Sigmoidal Exponential SigmoidalSigmoidal Sigmoidal Sigmoidal Exponential Exponential Exponential Sigmoidal Literature survey > 1000 curves > 500 species Cochard et al 2013 Open vessel artifact? Cochard et al 2010 Refilling artifact Jacobsen et al 2012 Open vessel artifact? Ennajeh et al 2011 Indirect and invasive methods

Need for a Reference technique : X-ray Tomography (HRCT) Direct observation, non-invasive, non-destructive High resolution (<1µm), measures density variations Affordable laboratory systems now available (more invasive)

Experiments using synchrotron light and living trees S Jansen B Choat S Delzon E Badel H Cochard R Burlett T Brodribb

Oak HR-CT Dehydration unpublished -2.9 MPa -5.1 MPa -3.5 MPa Centrifugation % cavitation P x-min

Air injection % cavitation Olive Sap pressure, -MPa Torres et al (in press) HR-CT P x-min

HR-CT Laurel (Laurus nobilis) Sap pressure, MPa % cavitation Cochard et al (in press) P x-min ?

Tension sample Relaxed sample Tension sample Relaxed sample But see Trifilo et al (in press)! % cavitation

MPa Intact Cut under tension Intact Cut under tension unpublished -3.6MPa Eucalyptus potted plants Cutting artifact Wheeler et al Refilling artifact Trifilo et al % cavitation

Sap pressure, MPa P x-min High cavitation-resistance strategy has been validated (Oak, Eucalypt, Laurel, Olive, Poplar, Acer, Pinus, Abies,Vitis, Pteris) Low cavitation-resistance strategy still needs to be confirmed What is the biological significance of cavitation in trees ? ?

Oak Xylem Pressure, MPa Stomatal conductance Stomatal / Hydraulic Coordination Cochard et al 1996 Maize Wheat Cochard 2002 Neghliz, Cochard & Martre unpublished % Cavitation “Stomatal control of cavitation”

Xylem pressure, MPa % Cavitation Stomatal conductace Xerophilous species Hygrophilous species Mesophilous species Stomatal conductace % Cavitation Xylem pressure, MPa Stomatal / Hydraulic coordination across species unpublished Xylem pressure at 10% Cavitation, MPa Xylem pressure at 90% stomatal closure, MPa

Populus x cv ‘peace’   Cochard, Ridolfi, Dreyer 1996 % Cavitation Distance to apex, cm % Cavitation Stomatal conductance Xylem Pressure, MPa Why trees do their best to avoid cavitation at the cost of less carbon uptake ? Water-stress

Hydraulic failure kills trees under extreme drought conditions Barigah et al 2013 % cavitation Dry till death experiment

% Cavitation % Mortality Critical cavitation level for mortality after extreme drought event: 50% cavitation Gymnosperms (Brodribb & Cochard 2010; Brodribb et al 2011) 90% cavitation Angiosperms (Ulri et al 2013, Barigah et al 2013) Gymnosperms Angiosperms Cavitation can delay mortality Hydraulic failure-induced mortality Vulnerability to cavitation, P50 MPa

0 % Cavitation Drought stress intensity DecennialSeasonalNo droughtCentennial P cav P 50 P 90 <<0 Delzon & Cochard 2014 Sap pressure, MPa Gymnosperms Angiosperms Pmin : Minimum field xylem pressure under drought conditions Tree safety margin for hydraulic failure-induced mortality Gymnosperms: Pmin-P50 Angiosperms: Pmin-P90

Safety margins are >0 but constant across forest biomes Modified from Choat et al. Nature 2012 Global convergence in the vulnerability of forests to drought

Xerophilous Mesophilous Hygrophilous Crops Cochard, Picon-Cochard, unpublished Cavitation resistance in Poaceae (grasses) Vulnerability to cavitation, P50 MPa

Tixier et al 2013 % cavitation S Herbette

Melzer et al 2008 Lens et al 2013 “Woody” Arabidopsis (soc1-6 ful7 mutants) % cavitation

Xylem Pressure (P min, MPa) 0 % Function intensity Cavitation Transpiration Photosynthesis Mortality Drought stress intensity DecennialSeasonalNo droughtCentennial P cav P 50 P 90 <<0 P midday Take-home-doggy-bag message 1.Cavitation and repair and not routine in trees (plants?) 2.Coordination between stomatal and hydraulic functions 3.Cavitation forms under intense drought conditions 4.Hydraulic failure can induce tree mortality under extreme drought conditions 5.There is a future for Arabidopsis (in plant hydraulics)

A L I M E N T A T I O N A G R I C U L T U R E E N V I R O N N E M E N T Photo Sylvain Delzon