Embolism Resistance in Petioles and Leaflets of Palms

Embolism resistance in petioles and leaflets of palms Thaise Emilio, Laurent Lamarque, Jose Torres Ruiz, Andrew King, Guillaume Charrier, Régis Burlett, Maria Conejero, Paula J Rudall, William J Baker, Sylvain Delzon

To cite this version:

Thaise Emilio, Laurent Lamarque, Jose Torres Ruiz, Andrew King, Guillaume Charrier, et al.. Em- bolism resistance in petioles and leaflets of palms. Annals of Botany, Oxford University Press (OUP), 2019, 124 (7), pp.1173-1183. 10.1093/aob/mcz104. hal-02306103

HAL Id: hal-02306103 https://hal.archives-ouvertes.fr/hal-02306103 Submitted on 4 Oct 2019

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., Company. All rights reserved. permissions, For please e The© Author(s) 2019. PublishedOxford by University Press behalf on of the Annals of Botany University ofCampinas Clermont 1 de Pós Guillaume Charrier Royal Gardens, Botanic Richmond, Kew, TW9 Surrey, 3AB,UK

Bordeaux, 33615 Pessac, FranceBordeaux, 33615Pessac, Thaise EmilioThaise -

Accepted Manuscript(PNPD),Doutorado - Ferrand, France palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 Embolism resistance inpetioles and leaflets ofpalms *For [email protected] Email 1 ,2 , * , Laurent J.Lamarque Comment citer cedocument: 4 – , Burlett Régis UNICAMP.

, ofBiology, Programa de em PósGraduação Ecologia, Institute –

Synchrotron SOLEIL,L’Orme 91190Saint de Merisiers, BP48, Gif Baker

4 P.O. - Université 1 3 sur , & Sylvain Delzon Maria Conejero

- Box: 6109, Brazil Box: Yvette Cedex,Yvette 3 , José M. Torres

Clermont - mail: [email protected]. France 1 3 - ,

Auvergne, INRA, PIAF,Auvergne, 63000, INRA, Paula J.Rudall ,

3 BIOGECO, INRA, -

Ruiz ,

2 Programa Nacionalde 4 , Andrew King , Andrew

1 ,

William J. Université -

Aubin 5 ,

Accepted Manuscript palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 replaceability. may segregation hydraulic happens, in petioles and leaflets between segmentation as three almost an showed long in provid adaptations and hydraulic understanding biomes across palms in embolism Conclusions (r =with conduitsize 0.37,p= 0.11). petioles. than embolism to vulnerable species. within blades No SE). from Key centrifuge techniques: habit in differing species palm 50% Methods resistance todrought remain drought and temperature dicotyl and and Background

large as that reported in reported that as large results of embolism or embolism of - 2.2±0.4 MPa in MPa 2.2±0.4

difference

We quantified embolism resistance via via resistance embolism quantified We and edonous angiosperms edonous

Comment citer cedocument: Our results show that show results Our

n vivo in hs td rpeet te is etmt o drought of estimate first the represents study This the

optical vulnerabilityoptical method. a ims -

r ek ifrne wr fud ewe ptoe ad leaf and petioles between found were differences weak or induced embolism embolism induced loss of hydraulic conductivity) in petioles or leaflets of leaflets or petioles in conductivity) hydraulic of loss X Dypsis baronii Dypsis -

Surprisingly, fold range of embolism resista embolism of range fold ray Hydraulic studies are currently biased towards conifers conifers towards biased currently are studies Hydraulic all - ae micro based angi ;

poorly responses of of responses t n pyoeei rltdes using relatedness phylogenetic and at os P Embolism resistance in palms is not correlated not is palms in resistance Embolism 50 perms hr dfeecs occurred, differences where

lack

to of petiole of in palms known - 5.8±0.3 MPa in MPa 5.8±0.3

- . a clear relationship with organ cost or or cost organ with relationship clear a optd tomography, computed W e found found e arborescent monocots arborescent

. This study aims to assess xylem assess to aims study This . s - liv .

palms varies d roecn monocots arborescent ed P es the first step towards towards step first the es 50 little evidence for hydraulic forevidence little

, palm between nce

greatly suggesting that when it it when that suggesting Rhapis excelsa Rhapis ylem pressure inducing inducing pressure ylem

in the palm family palm the in leaflets - nue xylem induced in situ situ in to increasing increasing to

were (Mean ± (Mean species, three three

flow . less

six It 2

Accepted Manuscript method, P Key

words: words: palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 50 , synchrotron, xylem resistance. embolism Arecaceae, Comment citer cedocument: palms,

drought resistance, resistance, drought micro

- CT x CT - ray, optical vulnerability optical ray, 3

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h pl fml (Are family palm The Accepted Manuscriptimportant economically including species, angiosperm of 25% for account Monocots decline palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 , 2016). Dramatic changes in dry and wet periods are predicted for even the most most the even for predicted are periods wet and dry in changes Dramatic 2016). , recent differ strongly, both strongly, differ g abrset am can palms arborescent rge

in tropical forests tropical in relatively poorly relatively

under climate change have been neglected due to a relative lack of of lack relative a to due neglected been have change climate under

decades et al. et Comment citer cedocument: , , 2015). Therefore, it is critical to reliably predict the likelihood of likelihood the predict reliably to critical is Therefore, it 2015). , the caceae) includes more than 2,600 species and 181 genera genera 181 and species 2,600 than more includes caceae) available information is strongly biased towards conifers and conifers towards stronglybiased is information available

studied (though see Renninger see (though studied . Yet the role of palms as ecosystem engineers and their their and engineers ecosystem as palms of role the Yet .

et al. et morphologic et al. et , 2016). , , 2012). In contrast, hydraulics contrast, In 2012). , also

et al. et ally and functionally and ally cu i eteey rd lmts uh as such climates arid extremely in occur Although data Although , 2015) and water cycling (Ren cycling water and 2015) , on and - and induced mo induced xylem

Dransfield, 2016). Over 2016). Dransfield,

Phillips, 2011). Palms 2011). Phillips, from t al. et and of of vulnerability monocots remain remain monocots

, 2011), though though 2011), , other species in species other Janssen, 2009). 2009). Janssen, rtality are best best are rtality and in the the in ninger ninger

Fu, 2014; Fu, 2014;

palm palm ha and ve 4

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., 61 to up grow leaf(Petit to root from flow water to resistance hydrodynamic overcome to plant the of apex the to base the from vessels their vasc any of length the exceed that stems climbing develop and trees eudicot as tall as heights achieve can species growth secondary 'true' lack they though tropica other all of that to equivalent have range broad to a appear displaying by palms limitation However, this overcome 2012). (Carlquist, transpiration and flow water size, parts aerial makes efficient thesp inavoiding monocots more in vessels of lack relative The 2012). (Carlquist, leaf and stem the in system vessel a combine monocots achi when transport water secure for efficiency reduced in result dominance inmonocots ofherbaceous life Alves (e.g. differences constraints These as water. expressed soil deep to access restricts root) tap branching that root primary Third, lifespan. individual an throughout functional remain to need cells phloem and xylem both and cambium vascular a lack monocots) all (like palms Second, conditions. environmental unfavourable seasonally avoid long to mechanisms perennial dormancy lacking are palms First, features. key three to linked potentially are distinct hydraulically palms make that factors the of Most 2006). (Tomlinson, environments and worldwide forests dominate that the including ecosystems, respective their

Accepted Manuscript may and growth thickening restricts monocots in cambium vascular a of lack The palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 metres characterizes ular plant (Tomlinson, 2006). Like dicot trees, arborescent palms taper palms arborescent trees, dicot Like 2006). (Tomlinson, plant ular in height (Bernal height in Comment citer cedocument: - based root xylem system with an entirely tracheid entirely an with system xylem root based all monocots (which in dicotyledonous trees develops into a a into develops trees dicotyledonous in (which monocots all et al. et

l plant groups combined (Couvreur combined groups plant l t al. et , 2014). The tallest palm ( palm tallest The 2014). , the the et al. et

- large woody trees (dicotyledonous and coniferous and (dicotyledonous trees woody large forms y en o a aclr cambium vascular a of means by 20; olno, 2006) Tomlinson, 2004; , small herbaceous grasses that dominate open open dominate that grasses herbaceous small , 2018) and there is no evidence for hydraulic hydraulic for evidence no is there and 2018) , other read of air embolism, but also restricts plant butalsorestrictsread embolism, air plant of than trees. of ie n got frs almost forms, growth and size Ceroxylon quindiuense Ceroxylon eving greater stature. Many Many stature. greater eving

the early loss of the the of loss early the –

et al. et r linked are , different palm palm different , , 2015). Even Even 2015). , - – - based xylem xylem based l

vd plants ived sometimes sometimes to ) can the 5

)

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., the same bundle (Tomlinson Calamus, genus the of palms rattan climbing in observed is xylem stem and leaf between segmentation (Tyree vessels between spread parenchymat of share not may palms in vessels sy xylem axial the and likely, more is embolism where leaves, transpiring between distance long a securing 1990), (Tomlinson, cylinder stem central the within deep occurs connection mainly are tracheids palms in which 1990), (Tomlinson, elements protoxylem via entirely occurs (Tyree vessels leaf and stem for hydraulic safety(Gleason limit upper an imposes still diameter conduit thought, previously than weaker is safety and trade the Although 2012). (Carlquist, embolism to vulnerable vesse strategy this but transport, water in efficient palms make vessels Broader 2012). (Carlquist, organs vegetative oth with contrast In 2014). (Olson dicots than vessels broader have general, in monocots as palms, because is This (Renninger trees temperate and tropical all of conductivity hydraulic theoretical (Renninger limitation stem, where where stem, l diameter (Hacke diameter l

Accepted ManuscriptStructurall vascular the of efficiency hydraulic The

rather than vessels (Tomlinson (Tomlinson vessels than rather in which there is no connection between connection no is there which in palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 in and egt o lre aoy am lvn udr non under living palms canopy large for height embolism

Phillips, 2011). Phillips, ous can have have can y, xylem safeguarding in palms in safeguarding xylem y,

cells Comment citer cedocument: et al. et

, must be avoided at all costs. all at avoided be must

its drawbacks. Embolism resistance Embolism drawbacks. its er monocots, many palms have broad vessels distributed along all along distributed vessels broad have palms many monocots, er potentially et al. and et al. , 2006), which suggests that palm xylem palm that suggests which 2006), ,

inter

, 2001). Zimmermann, 2002). Leaf 2002). Zimmermann, , 2016). and

cell

represent Zimmerman ular

t al. et path ing ways but ways 21) Te rtxlm n metaxylem and protoxylem The 2011). , can be achieve be can

, an adaptation for preventing embolism embolism preventing for adaptation an

protoxylem and metaxylem even within within even metaxylem and protoxylem

rhtcue f am srass the surpasses palms of architecture 2002). Even within the same vascular bundle, bundle, vascular same the within Even can -

trace linkage to the stem xylem stem the to linkage trace xrm eape o xylem of examples Extreme - be separated by several layers several by separated be off between xylem efficiency xylem between off can d - iiig ae conditions water limiting

decrease with increase in in increase with decrease by discontinuity between between discontinuity would

potentially be be potentially et al. et , 2013). 2013). , et al. et 6

am rl o early on rely Palms Accepted Manuscript plants in dehydration of threshold lethal the describes resistance Embolism hypothesi early was It

embolism embolism

et al. et resistant to embolism onset (Sperry, 1985; Renninger 1985; (Sperry, onset embolism to resistant palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 i n hs ae, we paper, this In n some resistance, but the but resistance, , 2015, Renninger Renninger 2015, ,

and compare them compare and it is unlikely that palm species rely exclusively on hydraulic segmentation segmentation hydraulic on exclusively rely species palm that unlikely is it - et al. et

generat to s dicot

to recover to - vessel connections and higher proportions of parenchymatous tissue tissue parenchymatous of proportions higher and connections vessel Comment citer cedocument: , yledonous 2016), ing - formed xylem vessels for their entire life, which can in some some in can which life, entire their for vessels xylem formed

z determine ed that palms restrict embolism to their expendable leaves expendable their to embolism restrict palms that ed reesbe aae o hi long their to damage irreversible

Zimmermann, 1982; 1982; Zimmermann, are (Urli

but extent to which they render palms more or less vulnerable less or more palms render they which to extent et al. et insufficient to identify the range of variation in variation of range the identify to insufficient

50% of the cross the of 50% with with trees coniferous and it can it et al. et , 2009, Renninger and Phillips, 2010b). Phillips, and Renninger 2009, , the the broad range of embolism resistance previously resistance embolism of range broad the , t al. et be significant be

2013). Thus, embolism resistance sets the upper upper the sets resistance embolism Thus, 2013). moim resistance embolism , 2012). Palms have wider vessels, smaller smaller vessels, wider have Palms 2012). Zimmermann and Sperry, 1983; Sperry, 1983; Sperry, and Zimmermann - sectional area (Renninger and Phillips, and (Renninger area sectional

in plants in eaiey ml aons of amounts small relatively - and ie ses and stems lived of such as such

Phillips, 2011), but the but 2011), Phillips, six

palm

(B palms r

od This effect is effect This species of water in in water of ribb ,

embolism to in which in , beyond

assure

2 som from 00 9 to to 7

e )

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A first set of twelve plants was shipped to the SOLEIL synchrotron (Paris, France) in in France) (Paris, synchrotron SOLEIL the to shipped was plants twelve of set first A Accepted Manuscript ef eils rm dl pat of plants adult from petioles leaf Chamaedorea radicalis Chamaedorea palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

Chabaud, Chabaud, and compare leafandand petiole compare P50 twelve

palm species for the experiments ( experiments the for species palm

Rhapis subtilis Rhapis Comment citer cedocument: Trachycarpus tions (Richmond, Unitedtions Kingdom). Burret, - T iulzto o ebls frain w dy bfr t before days two formation embolism of visualization CT ts MATERIAL AND METHODS yss baronii Dypsis was Dypsis lutescens Dypsis

Mart.,

used for experiments at the UMR the at experiments for used

fortunei

Becc., o et h hdalc emnain yohss w hypothesis, segmentation hydraulic the test To Howea forsteriana Howea

- ramosiana Salacca values (Hook.) H.Wendl. were used for direct micro direct for used were H.Wendl. (Hook.)

CT) aau longipinna Calamus (Becc.) Beentje & J.Dransf., J.Dransf., & Beentje (Becc.)

subfamilies Arecoideae and Coryphoideae. and Arecoideae subfamilies

(H.Wendl.) Beentje & J.Dransf., J.Dransf., & Beentje (H.Wendl.) .

Supplementary data Supplementary

(F.Muell.) Becc, (F.Muell.)

Supplementary data data Supplementary with

Mogea, were sourced from from sourced were Mogea,

.cu. Lauterb., & K.Schum. - different amounts of of amounts different BIOGECO laboratory laboratory BIOGECO Table S1), most S1), Table yss decaryi Dypsis Rhapis excelsa Rhapis - BIOGECO, BIOGECO, Fig. - Phoenix Phoenix watered

S2). he he ly ly 8

e -

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., an Subsequently, 100%. near was percentage embolism plant the when ended experiment did we and plant per taken apa hours 6 spaced were scans The scan. next the until dry to allowed then was plant The scan. Scholander and r method Paganin the using to up and on scanned was petiole Each slices. image TIFF 2048 ofyielded stacka and sample eachfor s 120 was time scanThe scintillator. LuAG Naka K.K., Photonics (Hamamatsu camera sCMOS 50 a with collected were X process. the accelerate to fan a to them exposing and irrigation stopping three the in induced progressively was Dehydration near selected also were sections cross imaging stage, rotation the of aperture central free and capacity load high the to Thanks mode. rotation continuous a using mm photons 2016) their petioles weretherisk tominimize fixed ofmo the of duration the for bench the and stage rotating the in placed was plant intact the scan, each on For days). 6 to (3 experiments dry to allowed were plants Uprooted roots. the soil the and pots the from removed were plants scan, first the After to potted still were they while plants esulted in2 .

The petioles of three 1.5 three of petioles The

h wtr oeta o te ln ws esrd rm dtce la wt a with leaf detached a from measured was plant the of potential water The Accepted ManuscriptO bservations rt, depending on the species and dehydration stage. dehydration and species the on depending rt, 1 palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 - 1 type pressure chamber (DG Meca, Gradignan, France) immediately after each each after immediately France) Gradignan, Meca, (DG chamber pressure type

petioles were scanned per species. Tomographic reconstructions were conducted conducted were reconstructions Tomographic species. per scanned were petioles − 2 ) , -

bit volumic images volumic bit a with 3.02 25

keV monochromatic X monochromatic keV were Comment citer cedocument: - ms exposure time during rot during time exposure ms

conducted at the at conducted

(Paganin n o t observe - m tall intact palms intact tall m

et al. et quantify

any evidence of damage during the experiments. the during damage of evidence any ,

ce throughout ce 2002) SOLEIL microCT PSICHÉ beamline microCT SOLEIL - ray beam, while being rotated from 0 from rotated being while beam, ray the presence of any native embolism events. embolism native any of presence the μm voxel resolution. voxel μm

in PyHST2 software PyHST2 in vements during tomography. the - ku, Japan) equipped with a 250 a with equipped Japan) ku, w ation and recorded with an Orca an with recorded and ation ere bare

the scanned using a high a using scanned A maximum of maximum A - dehydration of dehydration rooted the middle of the petiole. petiole. the of middle the

carefully removed from from removed carefully lns e seis by species per plants (Mirone (Mirone - four each ray projections projections ray flux et al. et (King

scans were were scans individual individual

- ° to 180° to ° μm thick thick μm

(3.1011 ,

2014) - et al. et flash flash The – 24 24 9

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., Brodribb technique, OV method vulnerability optical the (hereafter using species per individuals six to five on monitored inEmbolism visualization detached theoretical conductivity. K where theoretical conductivity: e in observed vessels functional the of the conductivity from calculated then was scan each for (PLC) conductance xylem of loss percentage s MPa (1.002 water of viscosity the is η and diameter vessel the is D where according tothe Hagen potential water each at conductivity theoretical the calculate to used experiment dry bench the during taken scans the from and conductivity theoretical maximum the calculate to used diameter conduit of sum The vessel. the of area the is A where as calculated was vessel following: each for (D) diameter Conduit (NIH). software J Image using reference area vessels. toestimate scan themaximum ofembolized ( area a dditional scan was performed after removing the segment immediately above the scanned scanned the above immediately segment the removing after performed was scan dditional ca

h ost n acmlto o ebls drn pl la dscain were desiccation leaf palm during embolism of accumulation and onset The Accepted Manuscript The

psi 1 mm) to embolize all the vessels artifactually. This final cut scan was then used as used then was scan cut final This artifactually. vessels the all embolize to mm) 1

palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 is the theoretical conductivity of the functional vessels and K and vessels functional the of conductivity theoretical the is areas of embolized and functional vessels were determined in each scan image image scan each in determined were vessels functional and embolized of areas – Comment citer cedocument:

Poiseuille equation:Poiseuille PLC(1 = 100× K

leaves (OVleaves technique) D = 2×√(A/ th

= ΣπD

t al. et 4 – /128 η(Eq.2)

K π psi ) (Eq.1) /K 21; ul eal aalbe a available details full 2016; , ach scan as a function of the maximum maximum the of function a as scan ach max ) (Eq. 3)

from the reference scans was was scans reference the from

max

is the maximum maximum the is - 1

at 20 at °C ). The The ). 10

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., (Cavitron) ofembolismHydraulic resistance measurements percent potential water corresponding cumulative and 2016 ( dehydration throughout occurred that events using On France). pressure Gradignan, Meca, (DG Scholander chamber a using leaflets neighbouring on potentials water xylem measuring leaflets. scanned the below NSW, Armidale, International, (AutoIt cells mesophyll until turned brown 3) scan automatically Each was leaflet veins. cross and main both in embolisms of visualization optimize to set were area leaf as well as contrast and brightness magnification, Scan dehydration. during movement tran a with fixed and Japan) Suwa, EPSON, hours afterexcision plant targeted the psychrometer, and scanner the of installation complete non and set experimental the During measurements. http://www.opensourceov.org

at least 30 cm from the scan location scan the from cm 30 least at ImageJ (National Institute of Health, New York, NY, USA) to highlight embolism embolism highlight to USA) NY, York, New Health, of Institute (National ImageJ age

Accepted (ICT psychrometer stem a using min 30 every recorded were potentials ManuscriptWater Photo, V800 (Perfection scanner a on placed were leaflets two individual, each For - scanned leaves were kept bagged to avoid water loss by transpiration. Only after after Only transpiration. by loss water avoid to bagged kept were leaves scanned

the website the palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 embolism function of water function embolism potential. percent , age

confirming wasembolism caused thatnodetectableleaf excision. by https://github.com/OpenSourceOV/image Comment citer cedocument:

emboli A ). Briefly, all individuals were kept well hydrated prior to to prior hydrated well kept were individuals all Briefly, ). ned every five minutes using a computer automation software automation computer a using minutes five every ned crc o te edns a double was readings the of ccuracy

Australia) that was was that Australia) zed sequences

area . The first The aae obtained dataset - sparent glass and adhesive tape to tape adhesive and glass sparent V . up ,

ce completed, stacks of images were were images of stacks completed, ce for the detailed procedure, detailed the for indicating cell death.indicating ,

where palms had to be up be to had palms where

ulnerability curves were constructed as as constructed were curves ulnerability

attached to the petiole a few centimetres few a petiole the to attached embolism event was observed at least 12 least at observed wasevent embolism

was - processing

leaf leaf - hn coupled then checked by periodically periodically by checked was was see Brodribb see - rooted, both roots roots both rooted, instructions excized excized minimize with analyzed analyzed from the from ). The The ). et al. et

leaf the 11

Embolism Embolism Accepted Manuscriptopen No As drought to Resistance . palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 ehius ht ul vleaiiy uvs rm ln sections plant from curves vulnerability build that techniques e ehiu (airn Cochard (Cavitron, technique ge tance of the petioles was calculated at different xylem pressures from from pressures xylem different at calculated was petioles the of tance E measurement of measurement - ecp for except , ight 2 vessel artefact was detected for four palm species: palm four for detected was artefact vessel MPa 2 for resistance in plants is commonly expressed by the xylem pressure induc pressure xylem the by commonlyexpressed is plants in resistance

in deionized ultrapure water. Centrifugal force was used to generate generate to used was force Centrifugal water. ultrapure deionized in

. For those species, petioles were recut under water with a razor blade to blade razor a with water under recut were petioles species, those For . open species species - 1 Comment citer cedocument: s - any 1 ) was calculated under low xylem pressures. The percentage loss of loss percentage The pressures. xylem low under calculated was ) - vessel artefact (Torres artefact vessel

- of the species for which we which for species the of . fortunei T. - induced embolism embolism induced ald h open the failed validation among all techniques.validation among all

- xylem conductance under negative pressure using the custom the using pressure negative under conductance xylem or its equivalent in embolized area (P area embolized in equivalent its or Ruiz infiltrated with a reference ionic solution of 1 of solution ionic reference a with infiltrated

2017, Cochard 2017, ,

where only a negligible loss of conductance was was conductance of loss negligible a only where

embolism our analysis. our - vessel artefact test, produced unsatisfactory unsatisfactory produced test, artefact vessel t al. et in the petioles petioles the in - Ruiz Ruiz .

et al. et 2005) ,

et al. et with a rotor of 0.27 m diameter. This This diameter. m 0.27 of rotor a with

collected data using microCT and microCT using data collected , Unfortunately, we were unable to unable were we Unfortunately, 2013) ,

2017) by injecting air at 2 bars bars 2 at air injecting by 2017) t h GNBI hydraulic GENOBOIS the at

was determined was , three samples per species species per samples three , D. baronii D. 50 :

Choat can , D. decaryi D. 0 mm 25 KCl KCl 25 mm 0 et al. et

using using suffer from from suffer - 0.8 to 0.8 , 2012) , in - , situ ing D. D. 12 - 9

- dimensional graph relating percentage of xylem conductance loss and xylem pressure pressure xylem and loss conductance xylem of percentage relating graph dimensional late the value of embolism resistance per species, the values of P of values the species, per resistance embolism of value the late - T O ad C and OV CT, AcceptedTo cavitron. and OV from sample per obtained were curves vulnerability Individual Manuscript 50

et al. et (MPa) isthexylem 50%ofconductivity loss a and (% S pressureMPa inducing palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 , 2013). Vulnerability curves were obtained with the three differen three the with obtained were curves Vulnerability 2013). ,

Comment citer cedocument: PLC (S/25*(P =exp 100/(1+ vto) Fr ah ape te eainhp ewe pe between relationship the sample, each For avitron). /percentage of embolized pixels embolized of /percentage

- sample t sample

- test, since only a single vulnerability curve curve vulnerability single a only since test, and i

– Vander Willigen, 1998):

and xylem water pressure was fitted was pressure water xylem and P from 50 bls rssac i ptoe by petioles in resistance mbolism ))) (Eq. 4)

ye vleaiiy uvs a curves, vulnerability xylem

50 50

of of all the samples samples the all of

the single curve single the - CT method. In method. CT

t techniques techniques t cnae of rcentage - wise wise - 1) 13

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., 011, in = p 0.37, = r correlation data Supplementary (Pearson’ species across size conduit with correlated or 0.909) 0.013) = ( species threestudied No naturally across angiosperms for observed that to equivalent range show petioles palm Moreover, 1). (Table species other all from in MPa 0.3 from ranging 1), Table p<0.01, 71.3, = (F species method. vulnerability optical techniques: ( relatedness phylogenetic and habitat E Embolism resistance Development 2018)unless Team, otherwise stated. All 2012). (Limaye, tool rem presentation and exploration volume Drishti with generated Three USA). NC, Cary, bls resistance mbolism C. radicalis radicalis C. difference aining data manipulation, analysis and plots were performed in R v.3.5.1 (R Core Core (R v.3.5.1 R in performed were plots and analysis manipulation, data aining

Accepted Manuscript Vul ,

(

show Fig. . forsteriana H. palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 nerability curve fitting with the NLIN procedure in SAS 9.4 (SAS Institute Inc., Institute (SAS 9.4 SAS in procedure NLIN the with fitting curve nerability R. excelsa R. in vivo in 1 or weak differences in P in differences weak or and ing ).

H. forsteriana lea X

Fig. in palm leavesin palm andpetioles - was flets Fig.

ray based micro based ray (Mean ± SE). Embolism resistance in resistance Embolism SE). ± (Mean Comment citer cedocument:

- S

dimensional reconstructions visualizations of plant petioles were were petioles plant of visualizations reconstructions dimensional 2

t = (t 3 characterized more resistant than petioles, but not but petioles, than resistant more ). Th ). ). Larger vessels embolized first in first embolized vessels Larger ).

- e on a ag ad infcn vrain in variation significant and large a found We e .5, = .6) Ebls rssac i ptoe i not is petioles in resistance Embolism 0.068). = p 2.456,

( difference was significant significant was difference Fig.

- 3 50 computed tomography, tomography, computed upeetr data Supplementary ,

Supplementary dataSupplementary were observed between petiole and leaflet across the across leaflet and petiole between wereobserved n h petiole the in RESULTS

2.24 ± 0.4 MPa in MPa 0.4 ± 2.24 s

of all six onlyin the biomes the al S1) Table Table S R. excelsa R.

in situ situ in palm species species palm R. excelsa R. in

ed R. excelsa R.

C. radicalis C.

4 n moim resistance embolism an flow centrifuge flow ).

D. baronii D.

using three different different three using in which in differ , whereas not whereas ,

(t = (t that ed

(t = (t P significantly palms palms - 50

differ 0.121, p = = p 0.121, to

- between

3.463, p 3.463, and and - 5.82 ± 5.82 ed grow at all at the

14 in

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., ( hours 12 within embolism first the observed embolism of Optical visualization spread le inpalm space the within proportion. tissue than rather shrinkage of trends with coincides species of in 14% of area remarkable ( displaysspecies between differences shrinkage Petiole shrink. petioles and contracts tissue parenchyma in in (85% parenchyma of consists tissue petiole hydrated of proportion high radicalis amount high observed We spaces. intercellular and novulnerabilitycurve wasfor obtained this for observed embolized were vessels the excelsa R. obser were events vessels of most towards experiments. dry bench the of start the after ( plants intact of petioles Micro H. forsteriana H. embolism - CT observation of embolism formation in palm petioles observation inpalm ofembolism formation CT

Embolism spread in the leaflet was visualized visualized was leaflet the in spread Embolism Accepted Manuscript well In High

and palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 and -

eouin micro resolution when most of most when T. fortunei T. H. forsteriana H. - - C hydrated plants, water is stored not only in parenchyma cells but also in in also but cells parenchyma in only not stored is water plants, hydrated 5.8 MPa in MPa 5.8 C. radicalis C. , 74% in in 74% , . radicalis . ved below below ved Comment citer cedocument:

with micro with Fig. R. excelsa R. following , 40% in 40% , the in T. fortunei T.

, and smaller amount smaller and , - petiole reducedshrinkagearea for species. this

2 MPa in MPa 2 cf. 4 - all species species all T mgs loe vsaiain f esl moim in embolism vessel of visualization allowed images CT vessels were embolized. embolized. were vessels days 3 to 1 within events embolism first the observed We ).

Fig.

H CT was CT

small changes in water potential. The first embolism embolism first The potential. water in changes small for the samples shown in Fig. in shown samples the for 4 . forsteriana . . Within six to 24 hours after the first events, most of most events, first the after hours 24 to six Within . ). C

. radicalis . We observed a reduction in petiole cross petiole in reduction a observed We except After After ca - 4.0 Mpa in Mpa 4.0

highly resistant 4% at 4% T. fortunei T. s s

onset of onset aflets and 60% in 60% and , in f ae i itrellr pcs in spaces intercellular in water of - 2.2 MPa in MPa 2.2 R. excelsa R. - using the OV technique ( technique OV the using 8 MPa ( MPa 8 Xylem embolism resistance between between resistance embolism Xylem

R. excelsa R. . The largest amount of emb of amount largest The . embolism, the e the embolism,

R. excelsa R. species. species. Supplementary data data Supplementary

H. forsteriana H. and 4 ) to 30 days ( days 30 to ) ). When leaves dry out, out, dry leaves When ). T. fortunei T.

at advanced stages stages advanced at

C. r C. Expansion of air air of Expansion

mbolism spread mbolism adicalis ,

Fig. 5.3 MPa in MPa 5.3 ( - Fig. 3.41 MPa MPa 3.41 - sectional sectional Fig.

, 75% , ). We We ). olism 5

). A ). S 15 C. C. 5

s )

Accepted Manuscript bench the during shrinkage leaflet observed We 10

occurred palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 it in , ). was possible to observe embolism spread (as change in reflectance inside the inside reflectance in change (as spread embolism observe to possible was , –

) after the start of the experiments. Within 1 ( 1 Within experiments. the of start the after ) yss baronii Dypsis 8% to almost 40% ( 40% almost to 8% pre (base) right to (tip) left the from front dehydration the of advance the tracking This a range of range a viously viously and after embolism onsetembolism after C. radicalis C.

shrinkage C

R. excelsa R. . radicalis . Comment citer cedocument: hlis 21) Ser (95 fud that found (1985) Sperry 2011). Phillips, ot f h srnae n am leaflets palm in shrinkage the of Most been investigated in only four palm species (Sperry, 1985; Cobb, Cobb, 1985; (Sperry, species palm four only in investigated been different biomes. Our results add novel information to previous to information novel add results Our biomes. different

- was most ev most was ) after the first events, all vessels were embolized. The time to time The were embolized. vessels all events, firstafter the ) od n am ( palms in fold o high to .

took from twenty to forty days to dehydrate, compared with compared dehydrate, to daysforty twentyto from took Large p Large Supplementary data data Supplementary

the DISCUSSION

major veins. major in in arallel veins were the first to be embolized (Fig 4a, 4a, (Fig embolized be to first the were veins arallel

all three palm species ident i ident hps excelsa Rhapis

- upeetr data Supplementary induced xylem embolism resistance in palms resistancein xylemembolism induced n C

Within . radicalis . minor minor Table S Table - . dry experiments using the OV OV the using experiments dry - pa To our knowledge, embolism embolism knowledge, our To 10.11 MPa in MPa 10.11 species, longitudinal shrinkage shrinkage longitudinal species, rallel andcross rallel 7

). Interestingly ). ( ( Supplementary data Supplementary Supplementary dataSupplementary occurs in of Fig. . excelsa R. embolism resistance embolism

ogtdnly as longitudinally

6 lf) In left). S6, R. excelsa R. - veins. ,

most most

embolism embolism

) to 18 18 to ) Movie Movie Movie Movie leaflet leaflet

our our 16 a

occur

were more resistant to embolism than embolism to resistant more were 2017)

Pit membrane thickness, an important predictor of embolism resistance in woody woody in resistance embolism of predictor important an thickness, membrane Pit Accepted Manuscript such achieve palms which by mechanisms The found – (Dominguez

s other angiospermspecies without a clear relationship a organwithout orreplaceability clear with cost . radicalis C. clear palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

( tog i woy angiosper woody in though , Tyree & Zimmerman 2002 & Tyree t al., et no embolism at r at embolism no These observations are observations These

and

petioles in palms. in petioles 2013 - f

Rodriguez . This result offers novel evidence showing that hydraulic segregation segregation hydraulic that showing evidence novel offers result This . merit when xylem when

Comment citer cedocument: -

where ;

Li ute inves further t al., et elatively

e bevd infcn dfeecs ewe poia and proximal between differences significant observed we t al et pressure

, including both both , including Iriartea deltoidea Iriartea

03, is 2013), Th . in agreement with the results of previous studies that studies previous of results the with agreement in ).

high high 2018, Klepsch Klepsch 2018, is nce between organs of an herbaceous plant herbaceous an of organs between nce However tigation. s yrui sgetto ses o e species be to seems segmentation hydraulic ms only result falls below falls I. deltoidea I. water potentials water n Phillips and also n t fw eaye vessel metaxylem few to one relatively is consistent with the with consistent is , w

h h The herbs and trees. niey o ly mjr role major a play to unlikely e found little evidence little for e found

(P a ca ,

50 t al., et demonstrating wide range of embolism resistance embolism of range wide

ydraulic - ih in high = 3 (2011) found low resistance to to resistance low found (2011) - MPa.

1.4 MPa). 1.4 in both leaves and petioles and leaves both in

08 Losso 2018, - ln prs ht are that parts plant Similarly, emnain hypothesis segmentation

fact

that that A ll the palms the ll

that palms do not do palms that palms can be can palms our study our s t al., et

segmentation segmentation per vascular vascular per in the in (Skelton in

2018)

in our in

mor palm of sole . At . 17 R. R. as e

- .

Significative amounts of petiole shrinka petiole of amounts Significative

Accepteddehydration of threshold lethal the describes resistance Embolism ManuscriptThe h dy season dry the and may contribute to embolism resistance. Our microCT observations on the most most the on observations microCT Our resistance. embolism to contribute may and an , s

these

, palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

o recover to , be connected connected be relatively unusual unusual relatively

cies, cies, s e d we as

1990). Those transversal commissures a commissures transversal Those 1990). taeyt oewt drough with cope to strategy a observation previously previously , T. fortunei T.

Borya

and tissue capacitance) will dictate how fast a plant approaches this this approaches plant a fast how dictate will capacitance) tissue and , ad hrfr, moim ped ocr i tasesl commissures transversal via occur spread) embolism therefore, (and s

i 2017). 2017). d lethal embolism. embolism. lethal

(Urli (Urli Comment citer cedocument:

Crqit 2012) (Carlquist, , i , not observe functional functional observe not through - walled tracheids maintain the water column under higher tension tension higher under column water the maintain tracheids walled n s sn te ae method same the using , support this hypothesis. For this species, we observed that two that observed we species, this For hypothesis. this support ,

t al., et which indicate palm palm For the first time in intact palms, we imaged leaf petiole petiole leaf imaged we palms, intact in time first the For co -

one of these commissures without spread of embolism from embolism spreadof without commissures these of one occurrence of tracheid of occurrence

petiole

vessel elements can offer a rapid supply of water in the in water of supply rapid a offer can elements vessel 03. ay te hdalc ris eg rooting (e.g. traits hydraulic other Many 2013).

that water storage in palm petioles ( petioles palm in storage water that Supplementary data The proportion of parenchyma that we observed in in observed we that parenchyma of proportion The . s are no are s

oee, o However, t , as found in found as , ge occur even before the plant reaches plant the before even occur ge the t ice tracheids s (e.g. Cochard Cochard (e.g. s leafwaterpotential a re bly higher than th than higher bly ur data do not offer support to this this to support offer not do data ur

s smaller in diameter than metaxylem metaxylem than diameter in smaller

and vessels in palms in vessels and Fig.

another monocot, another in the presence of embolized embolized of presence the in

S11). S11). t al., et

decreases (cf. ose as well as well as

beyond which the which beyond 05 Nolf 2015;

observed in observed the Australian Australian the has also been been also has et al. et s

in stems) in between , 2016). , a Fig. depth, depth, t al., et

water water other other

1). 18

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., from result to likely most is shape this that shown been recently has it as caution, with interpreted exponentia in changes measure hydraulically to air an vessels where anatomy monocot air caryotoides difficult challenging. was where potential water the achieving even that embolism Challenges andperspectives embolism resistance inestimating inpalms changing resistance.embolism climates as water until transpiration seasonality when especiallyimportant may be mortality andtolerance (Meinzer xylem the to parenchyma capacitance high with species predicted features structural xylem by solely rate. maintaining while embolism preventing in role important an play could - seeding pressure and wide variation that this technique is unsatisfactory is technique this that variation wide and pressure seeding

an - pressure method ( method pressure

Accepted study, this in species palm the of One Manuscript of threshold the extends palms in capacitance Petiole Cb (06 maue ebls rssac fr h cibn palm climbing the for resistance embolism measured (2006) Cobb . open based on based sae f their of shape l palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

rather than rather using the single the using - vessel

Even in less extreme cases, estimating estimating cases, extreme less in Even their largevessels. their artefact

Comment citer cedocument: merely Washingtonia robusta Washingtonia again - (Torres vessel air vessel unrblt cre for curves vulnerability decreasing rainfall decreasing ht can that occur become ,

rendering palm xylem more resistant more xylem palm rendering - Ruiz Ruiz This mechanism was already described for tropical treetropicalalreadyfor was described mechanism This t al. et -

seeding technique seeding in isolation. Renninger isolation. in the

s et al. vi ebls b r by embolism avoid

available , 2008). 2008). , ye conductivity xylem ) and a bench a and ) ,

2014) T .

fortunei . T he ability to store water that that water store to ability he The role of water storage storage water of role The . ol ultimately could

, ahntna robusta Washingtonia

the the but concluded from the low mean low the from concluded but moim eitne n palm in resistance embolism apae t b s rssat to resistant so be to appeared , - dry method ( method dry drought result drought plant and ruh tolerance drought eleasing stored water from from water stored eleasing

of palms. However, the the However, palms. of Phillips (2011) used both used (2011) Phillips has

lost 50% of function of 50% lost e s motn in important as be than was previously was than a Iriartea deltoidea Iriartea high transpiration transpiration high s from s for species with species for

can i

should n drought drought n increasing conferred Calamus Calamus

sustain

s is is s be 19

)

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., micro per mean vessel estimated and Observed conduits. embolized of area mean the and pressure xylem between Relationship water of gradients the along optimum occurrence followin available are data Supplementary and drought their susceptibility to that underpin ou resistance improve palm across lineagesshould long in sustained be can resistance embolism high how showing by palms in adaptations hydraulic embolism by embolism from vessels xylem mobil large their protect they that likely is not it are clear, vessels entirely wide their in resistance embolism achieve palms which by mechanisms est first the provides study This systems. agricultural and natural both in drought to respond plants represent palms as important economically drought of Knowledge particularly phenotyping for drought promising palm leaflets. study - lived arborescent monocots. Further investigations of mechanisms of embolism embolism of mechanisms of investigations Further monocots. arborescent lived zn wtr rm aecya ise t te vessels the to tissues parenchyma from water izing indicate

Accepted Manuscript The weak difference mt o drought of imate g. In this sense, the novel non novel the sense, this In - ind palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 Table S1 Table ucing tensions ucing that that : s : in pecies studied, their distribution and habitat. and distribution their studied, pecies Comment citer cedocument: am species palm eitne taeis n pat ru ta i a is that group plant a in strategies resistance - induced xylem embolism in palms across biomes. Although the the Although biomes. across palms in embolism xylem induced s . This investigation provides provides investigation This .

in embolism resistanceembolism found in between leaflets andpetiole SUPPLEMENTARY DATA online at https://academic.oup.com/aob and consist of the of consist and https://academic.oup.com/aob at online

- ,

invasive optical method (Brodribb method optical invasive CONCLUSIONS P 50

can s

a significant step towards understanding how how understanding towards step significant a be s -

CT scan, species and xylem wat xylem and species scan, CT the role intropical of ecosystems. palms

r understanding of both species distribution r understandingofboth characteri - induced embolism resistance. embolism induced - al dph n aridity. and depth table

the thus , z

first step towards understanding understanding towards step first ed from either leaf petioles or or petioles leaf either from ed

preventing preventing

Fig ure et al. et s

S2 ecologically and and ecologically civmn of achievement , 2016) , : Palm specie Palm er Figure

al S Table potential. potential. appears in our

S 20 4: 3

s :

Trachycarpus fortunei Trachycarpus nae ecnae pr sample per percentages inkage ure sampling living collections and Chrissie Prychid for her help in the imaging labs at the the at labs imaging the in help her for Prychid Chrissie and collections living sampling

Accepted Manuscript S 5 Chamaredorea ra Chamaredorea y h Codnço de Coordenação the by . ); : – - palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 ct image analysis at UMR at analysis image ct Finance 001. Code

Two Fig h porm Ivsmns o te uue (rn nme ANR number (grant Future” the for “Investments program the We thank Scott Taylor, David Cook, Silke Roch and Wanyi Zuo for their help their for Zuo Wanyi and Roch Silke Cook, David Taylor, Scott thank We . ure

- dimensional (2D) digital cross digital (2D) dimensional -

doctoral Program (grant number UB1 number (grant Program doctoral S11 OEL sync SOLEIL Comment citer cedocument: t : . ases scin of section ransverse dicalis F ig ure

ACKNOWLEDGEMENTS ,

S6 preçaet d Psol e íe Superior Nível de Pessoal de Aperfeiçoamento Howea, forsteriana Howea,

rto fclt, SCE emie gat number: (grant beamline PSICHE facility, hrotron . : -

Movie BIOGECO Accumulation of embolisms over time for time over embolisms of Accumulation FUNDING s

S - 8 section X section rcyaps fortunei Trachycarpus , Amy Zanne for her help with Synchrot with help her for Zanne Amy , – - Curie grant agreement No 706011 706011 No agreement grant Curie S 10

e :

and 01 CR1024 01 xample - ray microtomography (micro microtomography ray Rhapis excelsa Rhapis

of leaf dehydration and and dehydration leaf of - R s/CR1024 R . oi S12. Movie ). ). Table S Table - 10 - 6M to L. J. L. to 6M - three palm three EQPX 7: l 7: -

Brasil eaflet Time Time - CT) CT) - ron 16, 16, 21

analysis hydraulic reveals cross that explain traits Acta Brasilica Botanica Accepted– Manuscript 11. palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

113 . Botanical Journal of the Linnean Society ofthe Linnean Botanical Journal 2012 Plant Science Plant . 2017 : 4865

78 . MonocotInformation, XylemNew Revisited: New Paradigms. . Progressingfrom ‘functional’tomechanistic traits. : 87 Xylem hydraulic thefunctionalof physiology: terrestrial backboneplant – Proceedings of the National AcademyProceedings ofthe National theUnited States ofSciences of 4869. Comment citer cedocument: – . 153. . 2016

2009 177

18 : Academy National Proceedings ofthe Sciences . Beyond Palmarum: Genera progress palm andprospects in . Monocots. In:. Monocots. Hedges S, SB, Kumar 245 : 369 . LITERATURE CITED

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– 233.

Palms

eds. Timetreeeds. oflife. New Phytologist

62 : 5 Euterpe edulis

– 113 16. The - induced induced : 5024 .

2016

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Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., Feldpausch Lopez TR, Fauset MO, M Gloor A,BrienenMonteagudo RJW, M, S,Johnson Baker TR, the United drought inthe wetAmazon. periods and PB, P,Duffy Brando CB GP,Field Asner his Global diversification agrowth tropical of Environmental plant correlates form: and JC,RoweCouvreur WD,CondamineKissling FL,Svenning NP, TLP, Baker WJ Biology tropical rain CouvreurForest TLP,F, Baker WJ Plantarum new for centrifugegeneration rapidof xylem technique vulnerability curves. Cochard H,Damour I, C, Bodet G, Tharwat 64 measuring plant vulnerability Acritical to cavitation: review. HerbetteCochard E, H,Badel S Delzon ChoatB,Jansen S, S, Envi technologyfor high 2015. Cochard E. Badel H,Delzon S, AR Cobb drought. Gleason SM, HackeUG, : 4779 torical climbing contingencies palms. in Accepted Manuscriptronment

9 – Nature : 44. . 4791. palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 States of America States of 2006 124

forests: Inferences forests: genuscompletefrom a

: 410

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Plant, Cell & Cell Plant, . Evaluation ofa Physiologia BMC rests to . 2015 23 .

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Lens F,Lens Picon palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

- 2012. Drishti: aDrishti: and volume exploration presentation2012. tool. W, Choat B, Delzon S, W, ChoatB,Delzon S, Nature Cli Nature

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2016. International and Optics Societyfor – . Is. xylemangiosperm of leaveslessresistant . - 171. induced thanangiosperm embolism trees. 2006 . Accelerated under expansion dryland Linking xylem storage with water

26 Tree physiology . Scalingangiosperm of xylem

87 : 689 : 093704. et al. rbieux C,Buttler A,Cochard –

6 701. : 6857.

2016

. Herbaceous New Phytologist New

36 In Developments X in :

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Accepted Manuscript 6 . Intervessel. membrane pit asa resistance thickness embolism key determinant of in . 2017 New Phytologist

- palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 49 vega R Oecologia

: 891 16 . Hydraulics link leaf. Hydraulics link shapeand environmentalniche interrestrial bromeliads. : 287 . – IAWA JournalIAWA 2008 902. –

292. 156 Comment citer cedocument:

. Coordinationof leaf stem and water propert transport

: 31 221 Nuclear Instruments Research Methods and inPhysics Section – : Sperry Jansen JS, Herbette S, S 41. 1831

: 152 - 1842. - C, Goldstein G,Goldstein Campanello PI,GattiC, MG, – 171.

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et al. et 324 ights fromvivomicroights in New Phytologist :

41 2016 – 48. . . A global analysis ofparenchyma. Aglobal analysis 2014

. The hybrid PyHST2 . 2013

209 Current Opinion in Opinionin Current : 1553 . Embolism . Embolism ‐ CT analysis:CT - – Cabrera HI, Cabrera HI, 1 ies intropical 565.

Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 by INRA (Institut National de la Recherche Agronomique) user on 25 June 2019 June 25 on user Agronomique) Recherche la de National (Institut INRA by https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz104/5521952 from Downloaded Version preprint Rudall, P. J.,Baker,W. J.,Delzon,S. (2019).Embolism resistance inpetiolesand leafletsof Emilio, T., Lamarque,L., TorresRuiz, J.,King,A.,Charrier, G.,Burlett, R.,Conejero, M., Renninger HJ,Phillips N developmentgrowing and environment. palmtwo Amazonian species ( Renninger HJ,Phillips N Rain Forest Palm AcceptedRenninger HJ,Phillips N of a palm species( Renninger KA,N Phillips HJ,McCulloh Computing. R Core DevelopmentTeam arborescent monocots. ManuscriptPetitG, FAJ, DeClerckT, Carrer N Phillips M, Anfodillo curves vulnerability illustration ofxylem tocavitation. Pammenter NW,Vander C Willigen Microscopy and amplitude extraction fromobject. asingledefocused ofa image homogeneous Paganin D Ecology Letters Vessel stem diameterlength with and angiosperm scales across climates. habits lineages, Alvarado ME, AnfodilloOlson T, Rosell Ja.,Petit measurements. of by xylemVisualization embolism X - Cárdenas Castorena LO, M palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 , Mayo SC, Gureyev TE, Miller PR, Wilkins , Mayo GureyevPR, SC, MillerSW Wilkins TE,

206 New Phytologist

: 33 17 Iriartea deltoidea Iriartea Iriartea deltoidea Iriartea : 988 – 40. Tree Phys Comment citer cedocument: –

997. . . . 2010a 2011 2010b .

2018 Iriartea deltoidea

214: . Hydraulic of offrom properties fronds palms iology . Wet . Intrinsic hydraulic. and extrinsic in factors . R: A Language A Statistical . R: and Environment for .

) withtypes. other wood Biotropica 890 . ‐

- raya microtomography: directtest against hydraulic 34 1998 .

American JournalAmerican ofBotany - vs .Dry 2014 89 : 137

. G, León S, CrivellaroA,Isnard 8. 2013 . Amathematical andstatistical analysis ofthe

. Universal hydraulics of the flowering. Universal hydraulics plants: ofthe –

145. and and - . Acomparison the of efficiency hydraulic Season TranspirationinanAmazonian : 470

Mauritia flexuosaMauritia Tree Physiology – 478. . Tree Physiology Tree

2014 . 2002 . Axial vessel. Axial widening in . Simultaneous phase

97 ) differing in

: 1926 18 : 589 -

Gómez C, varying of sizes 33 – 1936. – varying : 152 593. Journal of

– 160.

Accepted Manuscript 14. 88 : 797 . palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 ‐ 1985 Dominguez C,Brodribb CM, Lucani 2018. TJ. MR, Carins Murphy Washingtonia robusta . . , HornJW,Fisher – 2006 1990 809. . Xylem inthe palm embolism Oecologia . 2014 rowth. rowth.

. . The uniqueness of palms. uniqueness. The ofpalms. . 2015 The structural biology ofpalms The structural

218 Comment citer cedocument: . A Drier Future? . ADrierFuture? :1025 . Palm stemanatomy:. Palm phylogenetic signal? orclimatic Trees

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35. : 911 ) of varying for implications heights: hydraulic limitation . – . 2017 . –

2011 Calamoideae 2009 – 935. 488. – 921. . Casting onxylem vulnerability light inan Science .

. Comparativeanatomic hydraulicandproperties The anatomy ofpalms : ArecaceaeThe

Rhapis excelsa Botanical Jour

New Phytologist 343 – . . NewUniversity York: Oxford Press.

Calaminae). Calaminae). 20 : 737 2001 Journal ofex 15 . Direct vivoevidence in of – . Stem Vascular Architecture. Stem in 739. . nal of theLinneannal of Society IAWA Bulletin IAWA

American Journal of American 214

66 : 561 : 333 – 569.

– 6 338. : 283 -

Palmae Botanical

– 292.

Accepted Manuscript- - Ruiz JM, Cochard H, Choat B, Jansen B,Jansen L,Tomáskova H,Choat Rosana I,PadillaS, Cochard Ruiz JM, H,Mayr Beikircher Cochard S, Diaz Ruiz JM, B,

current palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 - - year furtheran shoots: evidence open of rlett King A, R, injection techniques. . 1982 Berlin Heidelberg.Berlin Comment citer cedocument:

. Functional anatomy xylem ofangiosperm Arnold ArboretumofHarvard University . . 1983 2002 et al.

. Anatomy of the palm. Anatomy of . Xylem Structure andtheSap Ascent of Physiologia Plantarum Physiologia

2017 . 2014 . Xylem resistance to embolism: presenting resistancea. Xylem toembolism: . Vulnerability in tocavitation New Phytologist - vessel artifact with vessel associated - Rhapis excelsa Espejo A, Rodriguez A,Espejo –

70. 152 Tree Physiology Tree

. : 465 215 2013

trees. In:trees. Baas ed. P, : 489

64 – . Xylem embolism 474. : 599 : , IX., Xylem – 499. . Berlin,

– Olea

609. 33

- : 672

- Díaz – 28

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3 4 . .

Accepted ManuscriptDrought Freq Embolism resistance in palms species occurring in different biomes in comparison comparison in biomes different in occurring species palms in resistance Embolism Two , Howea, forsteriana palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 et al. et - uency distribution vessel area and stage. embolism species uency distribution per

- micro iesoa (D dgtl cross digital (2D) dimensional t al. et -

induced xyleminduced resistance ( embolism species for threepalm (2011). The asteristic (*) denotes that we could not obtain P obtain not could we that denotes (*) asteristic The (2011). - 50 (D CT, dashed ofdetachedlines) andCT, vulnerability leaves (optical leaflets ,

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6 5 . .

aredorea radicalis Two Accepted Manuscript spreadin leavesEmbolism lighttransmission imaged ascanner.Species using palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104 , - Rhapis excelsa andTrachycarpus fo ) in columns. Embolism events) incolumns. Embolism are colouredinrelation thetime ofoc to dimensional (2D)sections digital X longitudinal

Comment citer cedocument: , Howea forsteriana

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arethe xylem potential associatedwith 12%, 50% and loss88% of hydraulic conductance, respectively.Values are meanand -

sections, pleasecheck Comparison vulnerability of leaf between curves parameters speciesand section.

palms. Annals ofBotany, 11 p.,DOI :10.1093/aob/mcz104

section Petiole Petiole Blade Leaf Leaf Comment citer cedocument: Fig.

50 vulnerability

representsignificative differences betweenspecies followingresultsthe ofstatisca MicroCT Cavitron - Method Optical Optical wiseconfidencelevel,

TABLES ------2.23±0.29 - 3.75±0.29 3.12±0.15 - 1.58±0.21 1.51±0.23 1.17±0.27 5.56±0.18 5.3±0.18 2.9±0.18

P12

Supplementary data

B b

ab A A c a a a

- - - 4.08±0.38 - 5.85±0.13 3.3±0.16 - 5.82±0.2 - - 2.59±0.09 ab 2.59±0.09 - - 2.79±0.12 b 2.79±0.12 2.24±0.16 a 2.24±0.16 3.14±0.04b 2.63±0.1ab P50 TableNoteS4). that comparisons weredrawn

c A B

------4.41±0.49 3.47±0.18 4.06±0.09 - 3.6±0.09 3.31±0.12 6.09±0.33 3.38±0.12 6.4±0.25 3.03±0.1

Forresults comparisons on P88

ab a B

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