Influence of salinity on root hydraulic properties of three olive varieties

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Influence of salinity on root hydraulic properties of three olive varietiesB. Rewalda; C. Leuschnera; Z. Wiesmanb; J. E. Ephrathc

a Department of Plant Ecology, Georg-August University of Göttingen, Untere Karspüle 2, Göttingen,Germany b Department of Biotechnology Engineering, Ben-Gurion University of the Negev, Be'erSheva, Israel c Department of Dryland Agriculture, Ben-Gurion University of the Negev, Campus SedeBoqer, Israel

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To cite this Article Rewald, B. , Leuschner, C. , Wiesman, Z. and Ephrath, J. E.(2011) 'Influence of salinity on roothydraulic properties of three olive varieties', Plant Biosystems - An International Journal Dealing with all Aspects ofPlant Biology, 145: 1, 12 — 22, First published on: 06 January 2011 (iFirst)To link to this Article: DOI: 10.1080/11263504.2010.514130URL: http://dx.doi.org/10.1080/11263504.2010.514130

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Influence of salinity on root hydraulic properties of three olive varieties

B. REWALD1, C. LEUSCHNER1, Z. WIESMAN2, & J. E. EPHRATH3

1Department of Plant Ecology, Georg-August University of Gottingen, Untere Karspule 2, 37073 Gottingen, Germany,2Department of Biotechnology Engineering, Ben-Gurion University of the Negev, Be’er Sheva 84105, Israel, and 3Department

of Dryland Agriculture, Ben-Gurion University of the Negev, Campus Sede Boqer, 84990, Israel

AbstractThree varieties of olive, Barnea, Arbequina and Proline, varying in salt tolerance, were examined to check the sensitivity oftheir root system hydraulic properties to salinity. Up to three levels of saline water (EC¼ 1.2, 4.2 and 7.5 dS m71) were usedfor long-term irrigation of mature trees. Specific conductivities and embolism rates of roots and branches were estimated bylow-pressure conductivity measurement; variability and plasticity of root and branch axial conductivities were calculated.Cross-sections of roots were analysed with respect to xylem anatomy. Barnea, and to a minor degree Arbequina, were foundto be more salt-resistant than Proline. Axial root hydraulics under salt stress reacted in a more plastic fashion than branchconductivities. Increased specific conductivities of roots, different plasticities of root hydraulics and modifications in meanconduit diameters can be dismissed as foremost reasons of the observed differences in salt resistance. Instead, a high within-population variability in root conductivity, as found in the salt-tolerant Barnea and Arbequina varieties, coming to full effectin high conductivity roots of Barnea trees, and an increased bimodal distribution of conduit sizes may represent favourabletraits to enhance water uptake in soils with heterogeneous salinity.

Keywords: Axial conductivity, fine and coarse roots, hydraulic variability, Olea europaea, photosynthetic rate, salt stress

Introduction

Salinisation of agricultural soils is a worldwide

problem of increasing severity, often caused by

irrigation (Kozlowski 1997). Additionally, the use

of saline water for irrigation is intensifying salinisa-

tion in many arid and semi-arid regions (Beltran

1999). Therefore, salinisation has significant eco-

nomic, social and environmental impacts worldwide

(Pannell 2001).

Olive (Olea europaea L.) trees typically tolerate soil

water salinities as high as 3–6 dS m71 (FAO 1985).

However, large variation in salt sensitivity exists

among genotypes (Gucci et al. 1997). Despite a

detailed understanding of salt tolerance and avoid-

ance mechanisms on molecular and physiological

levels (Flowers & Flowers 2005; Verslues et al.

2006), our understanding of salt tolerance mechan-

isms of mature trees is still very limited (Tabatabaei

2006). Photosynthesis and growth of plants are

largely determined by their hydraulic conductivity

(Tyree 2003; Nardini et al. 2006) as well as by the

vulnerability of the xylem to cavitation (Salleo et al.

2000); therefore it is essential to understand the

resistances that control water movement through the

soil-plant system. In different olive varieties, above-

ground growth and yield are intrinsically tied to soil

water availability (Tognetti et al. 2008; d’Andria

et al. 2009). Variability and plasticity of the hydraulic

system under salt stress (Joly 1989; Azaizeh &

Steudle 1991) are far less understood than altered

growth pattern, salt exclusion or osmoregulation

mechanisms (e.g. Tattini & Traversi 2009). Further-

more, although the root system is the first plant

organ to be affected by salt stress, and root traits are

thought to be among the most useful tools in

evaluating and screening of salt tolerance (e.g. for

olive see Bracci et al. 2008), most studies have

focussed on above-ground organs (e.g. Demiral

2005; Junghans et al. 2006).

Responses of the hydraulic system to saline

water sources, along with an increased spatial

Correspondence: Boris Rewald, Department of Plant Ecology, Georg-August University of Gottingen, Untere Karspule 2, 37073 Gottingen, Germany.

Tel: þ49 551 2006943/þ972 54 2879279. Fax: þ49 551 3922029. Email: [email protected]

Plant Biosystems, Vol. 145, No. 1, March 2011, pp. 12–22

ISSN 1126-3504 print/ISSN 1724-5575 online ª 2011 Societa Botanica Italiana

DOI: 10.1080/11263504.2010.514130

Downloaded By: [Rewald, Boris] At: 15:04 3 March 2011

heterogeneity and a decrease in soil water potentials

(Oron et al. 1999), may emerge as changes in

biomass allocation or conductivities (Garcia-Sanchez

& Syvertsen 2006; Lovelock et al. 2006). Because it

has been shown that root biomass is a rather

inadequate parameter to reflect the ability of root

systems to absorb and conduct water (Krasowski &

Caputa 2005), we define plasticity of the hydraulic

system as environment-induced variation of anato-

mical and morphological root traits. Plasticity is thus

distinguished from the phenotypic variation that

characterises the amplitude within a population and

a given environment, and is rather induced by

environmental heterogeneity and genotype (Scheiner

1993). Although total root conductivity (Lpr) is

thought to be mainly controlled by radial resistance

(Frensch & Steudle 1989), we have focused on axial

resistance because it is a significant, often neglected,

component of Lpr during water scarcity (via embo-

lism; Hacke et al. 2000), particularly in mature

woody plants with greater path length (Vanninen

et al. 1996; Addington et al. 2006).

In this article, we present the results of a study on

three varieties of mature olive trees under long-term

salt stress. Study aims were (i) to compare the salt

sensitivities of the common olive varieties Barnea and

Arbequina with the less-known Proline variety, (ii) to

test whether salinity has a major influence on root

and shoot axial conductivity, degree of embolism,

and root xylem anatomy and (iii) to analyse whether

salt-resistant olive varieties possess a higher varia-

bility and/or plasticity of axial root and shoot

hydraulics than less salt-resistant varieties.

Materials and methods

Study site

The study was conducted during December 2006 in

the Ramat Negev Experimental Station located in

the Israeli Negev Desert (3180500000N, 3484100300E,

altitude 305 m a.s.l.). The soil type is Typic

Torrifluvent derived from loess, with a clay content

of 6–8% (pHKCl: 7.9–8.2). Maximal and minimal

daily temperatures are about 358C (July/August) and

5.58C (January), respectively. The annual precipita-

tion in this area is approx. 90 mm (November–

April). Rooted cuttings of three olive (Olea europaea

L.) varieties, Barnea, Arbequina and Proline, were

planted in 1997 in plots irrigated either by freshwater

or saline water. Barnea is an olive variety originating

from native olive trees grown in the western Negev

Desert, Israel (Wiesman 2009). Barnea trees are

large and high yielding; the average oil content of the

olives is 18% with strong and bitter taste quality.

Barnea trees are suggested to be relatively highly

tolerant to salinity (Wiesman et al. 2004). Arbequina

variety originates from, and is widely cultivated in,

Catalonia, Spain. The tree is relatively small-sized,

but high yielding. The olives are small with an

average oil content, but can be used for both produc-

tion of high quality oil, and as table olives. Arbequina

trees are accepted as moderately tolerant to saline

irrigation water (Aragues et al. 2005; Weisbein et al.

2008). Proline is part of the Israeli olive germplasm

collection, and is of unknown origin (Wiesman

2009). The trees are average in size and produce

olives with average oil content, but a delicate

aromatic flavour. A preliminary survey showed that

Proline trees are sensitive to salt stress (Wiesman,

personal communication).

The experimental site was divided into two plots.

The first plot contains the three olive varieties,

arranged in rows in random order. The distance

between individuals in a row was 4 m, with a

distance of 6 m between rows. Rows were either

irrigated with freshwater (control; electrical conduc-

tivity, EC¼ 1.2 dS m71), or moderately saline water

(EC 4.2 dS m71, moderate salinity). In addition, a

second plot (approx. 150 m away) of Barnea trees

was irrigated with water of a higher level of NaCl (EC

7.5 dS m71, high salinity). Both plots have the same

soil characteristics and the trees were planted in the

same grid structure (4 m6 6 m).

The saline water came from local wells, and was

adjusted by mixing with freshwater or NaCl. The

olive trees were drip-irrigated; 656 mm were

supplied per year. During the first 3 years after

planting, additional irrigation water was supplied

after each rainfall event to avoid salinisation of the

rhizosphere. Volumetric soil moistures at the time

and place of root harvest were 25.2+ 1.6 vol.%

(mean+SE) in the control, 24.7+ 1.4 vol.% in the

moderate salinity treatment and 28.9+ 3.8 vol.%

under high salinity. Thus, soil moisture levels under

all three irrigation treatments were close to field

capacity (Oron et al. 1999). Usually twice a year, in

March and November, supplements of 100 mm

water were added in order to leach excess salt from

the rhizosphere (Wiesman et al. 2004). During the

experiment in December 2006, neither soil leaching

nor precipitation events occurred at the experi-

mental site. NPKB-fertilisation was based on results

of annual leaf nutrient analyses (Wiesman et al.

2004).

Stem growth and photosynthesis measurements

The stem circumference of 3–5 trees per variety and

salinity treatment was measured (30 cm above the

ground) between October 2002 and October 2005.

The former year (2002) was the second after final

salinity treatments, i.e. without additional irrigation

after each rainfall. Stem growth was expressed as

Olive root hydraulics under salt stress 13


diameter increment per year, and related to the

growth of freshwater-irrigated trees.

The net CO2 assimilation rate (Anet; mmol CO2

m72 s71) was measured with an infrared gas analyser

(LI-6400; Licor, Lincoln, USA). Measurements on

well-lit, randomly chosen leaves (n¼ 6) were per-

formed around midday. Carbon dioxide concentra-

tion was 400 mmol mol71, photosynthetic photon

flux density was set at 1800 mmol m72 s71 and leaf

temperature at 268C. Anet of the different treatments

were related to those of freshwater-irrigated trees.

Root and branch sampling

Three randomly selected trees per variety and salinity

treatment were sampled in December 2006 for roots

and branches. Fine roots (diameter (d)¼ 0.9–2 mm)

and coarse roots (d¼ 2–10 mm) were excavated at a

distance of 0.1–0.2 m to the bole, and 0.1–0.3 m to

the next irrigation-dripper. All root segments

�10 cm in length were collected within the excava-

tion pit (approx. 25 cm wide and 15 cm deep).

Thus, 8–33 fine or coarse root segments per variety

and salinity treatment were gathered in total. Eleven

branches (d¼ 4–6 mm, 30–40 cm in length) per

variety and treatment were collected from the same

three tree individuals.

The sampling took place on three occasions at

weekly intervals during mid-morning (9–11 am

EET). The segments were placed in ice water-filled

polyethylene bags, transported immediately to the

laboratory and stored for up to 6 days at 48C until

measurements were carried out.

Measurement of hydraulic conductivity

Axial hydraulic conductivity in fine roots, coarse

roots and branches was measured according to the

protocol of Sperry et al. (1988). In brief, a gravity-

induced flow with pressure differences of 7–8 kPa

was applied to the root and branch segments.

Filtered tap water (0.25 mm) with a sodium-silver

chloride complex (16 mg l71 Ag, 8 mg l71 NaCl;

Micropur MC 1T; Katadyn, Switzerland) was used

as perfusing solution to prevent decline in conduc-

tivity by bacterial growth. Before entering the root

and branch segments, the solution was forced

through a 0.2-mm membrane filter (Maxi Capsule;

Pall, Port Washington, USA). All samples were razor

blade-trimmed to 5 cm long segments and mounted

on adapters under water. Segment length was chosen

according to data of mean vessel length (275 mm) in

Mediterranean tree and shrub species (Fahn et al.

1986) and by root morphology, i.e. the occurrence of

root sections without ramifications.

Two types of conductivity measurements were

carried out. First, a 5-min flow measurement was

conducted on the segments in order to determine

‘‘native hydraulic conductivity’’ under field condi-

tions. The traversed solution was collected in a pre-

weighed vial filled with cellulose. Second, the

segment was flushed for 5 min at a pressure gradient

of 0.12 MPa in order to remove air bubbles from the

vessels. Maximum conductivity was determined by

repeating the measurement and flushing procedure

at least twice. Subsequently, length and diameter of

the segment were determined and the sample was

stored (in 70% ethanol). The data were expressed as

hydraulic conductivity (kh, m4 s71 MPa71), i.e.

solution mass flow rate (kg s71) through the segment

per pressure gradient (MPa m71). Specific conduc-

tivity (ks, m2 s71 MPa71) was calculated by dividing

kh by the cross-sectional area of the segment. Some

roots had exceptionally high conductivities, which

met the criteria of ‘‘far outliers’’ according to

statistical analysis (see below); these roots were

termed ‘‘high conductivity roots’’. The difference

between native and maximum conductivity, ex-

pressed as a percentage of maximum conductivity,

was used as a measure of the degree of embolism

(Sperry et al. 1988).

Anatomical analysis

Eight fine root and eight coarse root samples per

variety and salt treatment (Barnea 7.5 dS m71: 10

fine roots) were dehydrated with an ethanol-poly-

ethylene glycol (PEG 2000; Roth, Karlsruhe, Ger-

many) series consisting of PEG concentrations of

25% (temperature: 558C, exposure period: 1 h),

50% (588C, 1 h), 75% (608C, 1 h) and 100% PEG

2000 (608C, 26 1 h). Finally, the samples were

embedded in 100% PEG 2000. Seven to 10 mm thick

cross-sections were cut with a rotating microtome

(2040; Reichert-Jung, Heidelberg, Germany). The

cross-sections were mounted on slides and photo-

graphed at a magnification of 806 using a light

microscope (Photomikroskop III; Zeiss, Jena, Ger-

many), a digital camera (PowerShot A620; Canon,

Tokyo, Japan), and a scale reference (micrometer,

scale resolution: 10 mm). Due to irregular vessel

distribution, 480% of the stele areas were analysed

with ImageJ (v1.38h; NIH, USA; http://rsb.info.

nih.gov/ij) via the ‘‘particle analysis’’-function. All

conduits with lumen areas (A) smaller than 20 mm2

and non-vessel cells (particularly from medullary

rays) with A� 20 mm2 were excluded. Conduits

(A� 20 mm2), which includes vessels and tracheids,

were analysed with respect to number and lumen

area (Core et al. 1979). Idealised radii (r) were cal-

culated out of lumen areas (A¼ r2p) and hydrauli-

cally weighted conduit diameters (HWCD, i.e.

(Sr5 (Sr4)71) were calculated after Lewis and Boose

(1995). The theoretical hydraulic conductivity

14 B. Rewald et al.


(khtheo, m4 s71 MPa71) was calculated with the

Hagen–Poiseuille equation (Huber 1956), and re-

lated to three different conduit diameter classes

(d¼ 5–15 mm, 15–25 mm and 425 mm). For these

calculations, the viscosity coefficient ZH2O/208C was

set to 1.002 1073 Pa s (Zwieniecki et al. 2001).

Index calculation and statistical analyses

To quantify the plasticity of ks to salt stress, we

calculated the Relative Distances Plasticity Index

(RDPI; Valladares et al. 2006). RDPI values range

from 0 to 1; the higher the value, the more plastic is

the response of a variety to salinity. Phenotypic

distances were estimated by calculating the differ-

ences between pairwise combinations of ks values of

different treatments. To estimate the phenotypic

variability of ks of a population within a given

treatment, we calculated the Relative Distances

Variability Index (RDVI). It was obtained from

phenotypic distances estimated for pairwise combi-

nations among ks values from a given olive variety in

a certain treatment. Self–self combinations were

excluded for both calculations.

All data sets were tested for Gaussian distribution

with a Shapiro–Wilk test. We used a parametric

Scheffe multiple comparison procedure to test for

significant differences in Anet, RDPI, RDVI, hydrau-

lically weighted and maximum conduit diameters.

The Tukey–Kramer test was used to test for

differences of stem diameter and stem diameter

increase. Comparisons of normally distributed para-

meters were made with three-way general linear

models (GLM), testing for salinity, olive variety and

organ (fine roots, coarse roots and branches) effects.

A non-parametric Mann–Whitney U test was used to

determine if varieties, treatments and/or organs

differed with respect to measured specific conduc-

tivity, degree of embolism and proportion of conduit

diameter classes on khtheo. Because of the large

variability in specific root conductivity and the

limited number of cross-sections, the proportion of

conduit diameter classes on khtheo was tested on

marginal significance (P5 0.1). Calculations were

conducted with SAS version 9.1 (SAS Institute,

Cary, USA). Outliers in box plots were identified

according to Velleman and Hoaglin (1981; outliers:

ks value¼ 1.5–36 interquartile range, far outliers: ks

value 4 36 interquartile range).

Results

Stem increment and photosynthetic assimilation rate

Although the stem diameters of the three olive

varieties were not found to be significantly different

in the second year of differing irrigation, stem

increment within the following 3-year period

(2002–2005) and photosynthetic net assimilation

rate (Anet) were significantly lower in var. Proline

under moderate salinity (Table I). In contrast, both

traits, i.e. annual stem increment and Anet, were

neither restricted in moderately salt-stressed Barnea

and Arbequina trees, nor in var. Barnea under high

salinity.

Specific conductivity and degree of embolism of roots and

branches

The specific conductivities (ks) of coarse roots and

branches were found to be significantly higher than

in fine roots (Figure 1, Table II). Coarse roots ks of

both Proline and Arbequina varieties were signifi-

cantly increased (Table II) under moderate salt

stress. In contrast, specific conductivities of Barnea

coarse roots were constant under different salt

treatments. Large differences in ks fine roots existed

between Barnea and Proline trees under freshwater

and moderate saline irrigation, with the latter

showing about three times higher conductivities

Table I. Stem diameter 5 years after planting (2002), annual diameter increase in the following 3-year period (2002–2005), and net

photosynthetic assimilation rate (Anet) of three Olea europaea varieties under freshwater (control; 1.2 dS m71), moderately saline (4.2 dS m71)

and highly saline (7.5 dS m71) irrigation.

Olive

variety

Salinity

treatment

Stem diameter

2002 (cm)

Annual diameter

increase (cm yr71)

Relative diameter

increase (%)*

Anet (mmol

CO2 m72 s71)

Relative

assimilation rate (%)*

Barnea Control 13.5 a 1.59+0.07 a 100.0 18.5+2.3 a 100.0

Barnea Moderate salinity 12.2 a 2.06+0.15 a 129.3 20.7+0.7 a 112.0

Barnea High salinity 13.3 a 1.71+0.12 a 107.3 20.9+1.3 a 113.4

Arbequina Control 11.2 a 1.66+0.16 a 100.0 24.8+2.0 a 100.0

Arbequina Moderate salinity 10.6 a 1.58+0.12 a 95.5 24.6+0.3 a 99.2

Proline Control 10.5 a 1.99+0.09 a 100.0 25.6+1.5 a 100.0

Proline Moderate salinity 9.7 a 1.49+0.10 b 74.5 20.7+0.4 b 80.7

*Stem diameter increase/Anet within salinity treatment, compared to diameter increase/Anet under freshwater irrigation. Significant

differences between treatments within varieties are indicated by different letters (stem diameter: Tukey–Kramer, P5 0.05, mean (+SE),

n¼3–5; Anet: Scheffe, P5 0.05, mean+SE, n¼6).



(Figure 1a). Under severe salt stress, 20% of var.

Barnea fine roots possessed 4100-fold higher root ks

(‘‘high conductivity roots’’; Figure 2), resulting in a

significant increase in fine root conductivities. No

significant differences were found between ks branches

under freshwater and saline treatments (Figure 1c,

Table II).

The degree of embolism in fine roots, coarse roots

and branches of the three olive varieties was not

significantly higher in salt-stressed treatments than

under freshwater irrigation (Table II). The degree of

embolism in branches of Arbequina and Proline trees

was significantly higher than in branches of var.

Barnea (Table II).

Variability and plasticity of root and branch specific

conductivity

A significantly higher intra-environmental variability

(RDVI) in ks roots than in ks branches was found

(Table III). Varieties Barnea and Arbequina under

moderate salinity possessed a significantly higher

variability (RDVI) in ks coarse roots than var. Proline.

Under freshwater and moderate saline irrigation,

some fine roots, one var. Barnea coarse root, and

four branch segments had up to 106 higher specific

conductivities (see triangles marking ‘‘outliers’’ in

Figure 1a–c) than the mean of the respective

samples. The ‘‘high conductivity roots’’ (see crosses

marking ‘‘far outliers’’ in Figures 1a and b and 2)

resulted in significantly higher within-population

variability (RDVI) of fine and coarse root ks in

Barnea variety under high salinity (Table III).

The hydraulic systems of branches reacted in a

significantly less plastic manner (RDPI values 0.14–

0.26) to saline irrigation than those of roots (0.46–

0.62; Table III). No significant differences in

plasticity appeared between olive varieties ks roots

under moderate salt stress, whereas the ks of Barnea

coarse roots was significantly more plastic under

severe salinity.

Xylem conduit diameter

The hydraulically weighted conduit diameter

(HWCD) and the maximum conduit diameter in

coarse roots of Barnea trees irrigated with fresh-

water and moderately saline water were significantly

higher than in fine roots (Table IV). The GLM

revealed a significant influence of salinity level on

both HWCD and maximum conduit diameter, and

an effect of organ type (i.e. fine or coarse root) on

Figure 1. Box plots of specific conductivities (k,) of fine roots (a; diameter d�2 mm), coarse roots (b; d¼ 2–10 mm) and branches (c; d¼6–

8 mm) of three Olea europaea varieties under freshwater (Control; 1.2 dS m71), moderately saline (4.2 dS m71) and highly saline (7.5 dS

m71) irrigation. Box plots represents the median (horizontal line), 25 and 75% percentiles (box limits), and 5 and 95% percentiles (bars).

Outliers are plotted as triangles (~) and far outliers (‘‘high conductivity roots’’) are plotted as plus (þ) symbols (see statistical analyses for

definitions). Log-transformed (log10) y-axes were chosen due to presentability. See Table II for sample sizes and statistics.

16 B. Rewald et al.


maximum conduit diameter (Table IV). The

HWCD and the maximum conduit diameter

increased significantly in high conductivity fine

roots (Figure 2), and in coarse roots of Barnea

variety under severe salinity.

Proportion of conduit diameter classes on theoretical

hydraulic conductivity

In consequence of observed differences in conduit

diameters (data not shown), theoretical conductiv-

ities (khtheo) were distributed to different conduit size

classes in the three varieties and under the different

salt treatments (Table V). Fine roots of Barnea

variety covered 46–49% of khtheo with conduits of

5–15 mm in diameter under moderate or severe salt

stress, whereas the proportion of 5–15 mm conduits

on conductivity was 30 and 35% in Arbequina and

Proline varieties under salt stress, respectively.

Medium-sized vessels (d¼ 15–25 mm) in Proline

roots contributed more to the conductivity under

moderate salt stress than under freshwater irrigation

(Table V); however, this was only marginally

significant (P5 0.1). In contrast, the proportion of

medium-sized conduits on root khtheo decreased

significantly in var. Arbequina under moderate salt

stress, and in highly salt-stressed Barnea trees. The

theoretical conductivity of var. Barnea high con-

ductivity fine roots (7.5 dS m71) was significantly

based on conduits4 25 mm in diameter (Figure 2).

Discussion

The above-average salt tolerance of var. Barnea, and

the moderate salt tolerance of Arbequina, were

previously indicated by stem perimeter and yield

obtained under saline irrigation up to 4.2 dS m71

(Weissbein et al. 2008); 6 dS m71 is considered to be

the upper limit of tolerable salt stress for olive trees

(FAO 1985).

Our data on stem growth and photosynthetic

assimilation rates (Anet) confirm the salinity tolerance

of both Barnea (under saline irrigation up to 7.5 dS

m71) and Arbequina (Table I). By contrast, Proline

trees were found to be less salt tolerant than the other

two varieties, as evidenced by significantly reduced

stem growth and Anet under moderate salinity.

Thus, we ranked the olive varieties according to

their salt tolerance as follows: Barnea (highly salt

resistant)4Arbequina (salt resistant)�Proline (salt

sensitive).

Roots of non-halophytic plants, including different

olive cultivars, are usually thought to be less sensitive

to salinity than shoots (Munns & Termaat 1986;

Perica et al. 2008). However, this study revealed

significantly altered axial conductivities (ks) in salt-

stressed roots, but not branches, of mature olive trees

(Figure 1, Tables II and III), indicating a rather

insensitive above-ground hydraulic system. Un-

changed conductivities in salt-stressed olive branches

are in contrast to significantly modified conductiv-

ities under water stress (Bacelar et al. 2007),

suggesting that NaCl stress affects the xylem of

branches in a different way as compared with water

deficit, the latter merely due to an increased water

potential gradient between soil and leaves.

The unaltered or increased axial conductivities in

olive roots are in contrast to previous studies showing

lower root conductivities under salt stress in herbac-

eous plant species (Munns & Passioura 1984; Joly

1989). It remains to be established whether reduced

root conductivity is a significant factor necessary for

salt tolerance (Shannon et al. 1994) or if more salt-

tolerant species have higher root hydraulic conduc-

tivities (An et al. 2003). Increasing axial conductiv-

ities may balance increasing radial resistances, or

may have a ‘‘compensatory effect’’ (West 1978) with

regard to decreasing root system size under salinity.

In olive, a strong decrease of root biomass under salt

stress was found in the salt-sensitive var. Proline,

while highly salt-resistant Barnea trees retained

Figure 2. Light microscope-micrographs of a standard (a) and a

high conductivity (b) fine root of Olea europaea var. Barnea under

severe salt stress (7.5 dS m71). Scale bars¼250 mm.



higher root biomasses (Rewald et al. 2010). The

importance of compensating increased resistances in

smaller-sized root systems, like in Proline, becomes

apparent by an observed correlation between root

hydraulic conductance and leaf surface area in olives

(Nardini et al. 2006), and the reduced water uptake

Table III. Within-population variability (Relative Distance Variability Index, RDVI), and between-treatment plasticity (Relative Distance

Plasticity Index, RDPI) of the specific conductivity (ks) of fine roots, coarse roots, and branches of three Olea europaea varieties under

freshwater (control; 1.2 dS m71), moderately saline (4.2 dS m71) and highly saline (7.5 dS m71) irrigation.

RDVI RDPI

Control Moderate salinity High salinity Control/moderate salinity Control/high salinity

Fine roots

Barnea 0.48aAB 0.58 abA 0.67 bA 0.52 abA 0.59 bA

Arbequina 0.47 aA 0.51 acA n.d. 0.48 aA n.d.

Proline 0.61 bcA 0.42 aA n.d. 0.55 abA n.d.

Coarse roots

Barnea 0.58 acA 0.48 bA 0.66 cA 0.53 abA 0.62 bA

Arbequina 0.44 abA 0.47 abcA n.d. 0.54 aA n.d.

Proline 0.45 bB 0.20 dB n.d. 0.46 aB n.d.

Branches

Barnea 0.29 aB 0.22 aB 0.22 aB 0.24 aB 0.26 aB

Arbequina 0.18 aB 0.12 aB n.d. 0.14 aB n.d.

Proline 0.14 aC 0.22 aB n.d. 0.19 aC n.d.

GLM results RDVI: salinity effect, F¼144.61, P50.0001, variety effect, F¼ 121.33, P5 0.0001, organ effect, F¼586.94, P5 0.0001.

GLM results of RDPI: salinity effect, F¼47.55, P5 0.0001, variety effect, F¼33.66, P5 0.0001, organ effect, F¼305.34, P5 0.001.

Significant differences of either RDVI or RDPI within organs (fine roots, coarse roots, and branches) are indicated by different lowercase

letters, and significant differences between organs within a certain variety and salinity treatment by different capital letters (Scheffe test,

P5 0.05; mean values; n.d.¼not determined; see Table II for sample sizes).

Table II. Specific conductivity (ks) and degree of embolism in fine roots, coarse roots and branches of three Olea europaea varieties under


Olive variety Treatment n ks (1074 m2 s71 MPa71) Embolism (%)

Fine roots

Barnea Control 14 0.9+0.4 aA 24.8+ 8.1abA

Moderate salinity 11 1.0+0.3 aA 21.2+ 11.2 aA

High salinity 21 0.6+0.1 aA 23.0+ 6.1 abA

Barnea HC* High salinity 5 156.3+12.3 b 18.2+ 4.8 ab

Arbequina Control 18 1.0+0.3 aA 18.2+ 4.7 abA

Moderate salinity 16 1.3+0.3 aA 33.0+ 7.6 bcA

Proline Control 20 3.0+0.9 acA 36.3+ 6.2 cA

Moderate salinity 22 3.7+0.7 cA 22.3+ 4.8 abA

Coarse roots

Barnea Control 29 6.2+1.1 abB 39.5+ 4.6aB

Moderate salinity 33 4.9+0.6 acB 26.6+ 3.1bB

High salinity 22 5.6+1.4 abB 36.6+ 7.0abA

Barnea HC* High salinity 1 230.3 5.9

Arbequina Control 11 2.2+0.4 aB 12.3+ 4.1 cdeA

Moderate salinity 8 8.4+2.3 bdB 23.0+ 11.5 bdA

Proline Control 22 5.2+0.8 bcB 33.1+ 5.4 abA

Moderate salinity 14 12.2+1.1 dB 25.9+ 6.8 beAB

Branches

Barnea Control 11 6.2+1.1 abcB 10.5+ 2.1 abA

Moderate salinity 11 5.2+0.5 acB 11.2+ 2.2 aA

High salinity 11 6.4+0.7 adB 18.7+ 3.7 bdA

Arbequina Control 11 7.1+0.7 bdC 32.8+ 3.7 cB

Moderate salinity 11 7.1+0.5 bdB 26.3+ 3.8 cdA

Proline Control 11 3.8+0.3 ceAB 29.5+ 4.9 cA

Moderate salinity 11 6.8+2.3 aeC 35.5+ 6.8 cB

*High conductivity roots (see statistics section for selection criteria). Barnea roots grown under highly saline irrigation are separated into

‘‘standard’’ and high conductivity (HC). Significant differences between varieties and salinity treatments within organs (fine roots, coarse

roots and branches) are indicated by different lowercase letters, and significant differences between organs of the same variety and salinity

treatment by different capital letters (Mann–Whitney U test, P50.05; mean+SE, n¼ sample size).

18 B. Rewald et al.


in salt-stressed olive trees, resulting in limitation of

photosynthesis (Table I; Loreto et al. 2003). At any

rate, although fine and coarse roots of var. Proline

possess the highest specific conductivities, this

variety was also found to be most vulnerable to salt

stress (Table I). Thus, high axial root conductivities

might constitute an important means to partially

compensate lower root biomass or increased xylem

sap viscosities, but seem not to be a premise for salt

tolerance.

While there were only minor differences in the

plasticity (RDPI) of root-specific conductivities in

the three olive varieties, the intra-environmental

phenotypic variability (RDVI) of root ks was found

to differ significantly between varieties (Table III).

Significantly higher phenotypic variabilities of root ks

were found in salt-stressed Barnea and Arbequina

varieties (Figure 1a and b; Table III). Plasticity is

thought to be most favourable when environmental

factors vary on the same spatial scale, when the plant

can respond faster than changes in the factors occur,

and when environmental variation is highly, but not

completely, predictable (Alpert & Simms 2002).

Heterogeneous but spatially and temporally

Table IV. Hydraulically weighted xylem conduit diameters (HWCD) and maximum conduit diameters (maximum CD) in fine roots and

coarse roots of three Olea europaea varieties grown under freshwater (control; 1.2 dS m71), moderately saline (4.2 dS m71) and highly saline

(7.5 dS m71) irrigation.

Olive variety Treatment n HWCD (mm) Maximum CD (mm)

Fine roots

Barnea Control 8 8.2+0.7 aA 27.8+ 3.0 aA


High salinity 6 9.1+4.2 aA 31.1+ 14.7 aA

Barnea HC* High salinity 4 33.5+4.6 b 92.4+ 16.9 b

Arbequina Control 8 10.7+0.8 aA 34.4+ 3.2 aA


Proline Control 8 9.2+1.2 aA 28.8+ 4.0 aA


Coarse roots

Barnea Control 8 11.8+1.1 aB 42.4+ 4.2 aB

Moderate salinity 11 12.1+0.8 aB 42.8+ 3.8 aB

High salinity 8 16.3+3.1 aA 49.4+ 7.3 bA

Arbequina Control 8 12.8+1.0 aA 44.3+ 3.4 aA


Proline Control 8 12.9+1.3 aA 43.0+ 4.6 aA


*High conductivity roots (see statistics section for selection criteria). GLM results of HWCD: salinity effect, F¼12.86, P5 0.0001, variety

effect, F¼ 0.33, P¼ 0.72, organ effect, F¼ 2.67, P¼0.11. GLM results of maximum CD: salinity effect, F¼7.78, P¼0.0007, variety effect,

F¼0.12, P¼ 0.88, organ effect, F¼ 6.89, P¼0.01. Barnea roots grown under high saline irrigation are separated into ‘‘standard’’ and high

conductivity (HC) roots. Significant differences within organs (fine roots and coarse roots) are indicated by different lowercase letters, and

significant differences between organs of the same variety and salinity treatment by different capital letters (Scheffe, P50.05; mean+SE,

n¼ sample size).

Table V. Proportion of conduit diameter classes on theoretical hydraulic conductivity of fine roots of three Olea europaea varieties under


Olive variety Treatment n

Proportion of conduit diameter classes on theoretical hydraulic

conductivity (%)

5–15 mm 15–25 mm 425 mm

Barnea Control 8 47.6+8.6 a 38.7+ 4.6 a 13.7+ 5.9 ab

Moderate salinity 8 45.0+9.4 a 46.5+ 7.2 a 8.5+ 3.8 a

High salinity 6 48.7+13.9 a 27.4+ 4.6 b 23.9+ 11.1 b

Barnea HC* High salinity 4 0.1+0.1 b 0.4+ 0.2 c 99.5+ 0.2 c

Arbequina Control 8 17.6+2.7 a 58.4+ 6.4 a 24.0+ 1.8 a

Moderate salinity 8 30.3+8.5 a 44.8+ 7.6 b 28.8+ 11.6 a

Proline Control 8 44.2+11.7 a 34.4+ 5.7 a 21.4+ 9.3 a

Moderate salinity 8 35.0+10.0 a 48.1+ 6.8 b 16.9+ 7.4 a

*High conductivity roots (see statistics section for selection criteria). Barnea roots grown under highly saline irrigation are separated into

‘‘standard’’ and high conductivity (HC) roots. Significant differences between salinity treatments within varieties are indicated by different

lower case letters (Mann–Whitney U test, P5 0.1; mean+SE, n¼ sample size).



predictable environments, such as drip-irrigated

orchards (Oron et al. 1999), may rather favour

species or varieties with a broad phenotypic varia-

bility in modular subunits (i.e. individual roots) than

different whole-plant reaction norms (de Kroon et al.

2005; Pierret et al. 2007), subsequently causing

higher water availabilities in leaves (for different olive

varieties see Fernandez et al. 2008).

The existence of functional groups, i.e. roots

specialised in nutrient or water uptake, within root

systems can have major benefits for uptake pro-

cesses. Different parts of root systems have been

previously found to respond independently to

salinity and water availability (Shani et al. 1993;

Pierret et al. 2007). As outlined by Tattini and

Traversi (2009; references therein), the overall salt

tolerance in Mediterranean evergreens, including

olives, depends largely on the ability to reduce

water uptake and transpiration during the summer,

and a fast recovery in carbon acquisition when

water with lower salt concentrations becomes

available (e.g. after salt leaching). High conductivity

roots of Barnea variety (Figures 1a and 2) could

thus highly contribute to water uptake if either

placed in less salt-affected soil regions (e.g. close to

the dripper) or during times of higher soil water

potentials (e.g. after salt leaching events).

However, not only functional differences between

individuals roots but also in terms of the xylem

anatomy may change the water uptake ability of olive

varieties. Previous studies found both higher vessel

densities and declining vessel dimensions in stem,

branch and root xylem under water or salt stress

(Bacelar et al. 2007; Sobrado 2007), which are

associated with an increased hydraulic safety (Lo

Gullo et al. 1995; Eshel et al. 2000). In this study,

neither the maximum nor the hydraulically weighted

conduit diameter (HWCD) of roots were found to be

significantly different under moderate saline irriga-

tion (Table IV). Small conduit diameters may be a

common adaptation to an increased tension of the

water column in the conducting system (e.g. Baas

et al. 1983). However, they cannot explain the

differences in salt resistance between the three

studied olive varieties, although Barnea trees meet

a higher proportion of their root conductivity with

small-diameter vessels (Table V). The discrepancy

with previous studies may be caused by the already

remarkably small root conduits of olive under fresh-

water irrigation, compared to other Mediterranean

species (Martınez-Vilalta et al. 2002) or by changes

in xylem anatomy masked by an increased dimorphic

vessel distribution (i.e. in Arbequina under moderate

and in Barnea under high salinity; Table V).

Dimorphic vascular systems with both narrow (safe)

and large (efficient) conduits are thought to

possess increased water use efficiencies (Mauseth &

Stevenson 2004), especially under temporarily

variable water availability and evaporative demand,

which may explain its frequent occurrence in the

flora of arid regions (Baas et al. 1983) and in

mangrove trees (Schmitz et al. 2006). However, our

statistical evidence for a more bimodal conduit

distribution in salt-resistant olive varieties is still

scarce, likely caused by the high variability in fine

roots conductivities.

While studies on the influence of below-ground

processes on salt tolerance of woody species are still

scarce, it has been previously demonstrated that

differences in salt resistance can be caused by

differences in root system traits (Lin & Sternberg

1994; Gucci et al. 1997). Although roots were, for a

long time, treated as coherent masses (Pregitzer

2002), our study begins to highlight the importance

of intra-environmental variability within the root

hydraulic system in heterogeneous saline environ-

ments, in contrast to a less variable and plastic

above-ground hydraulic system. Tattini and Traversi

(2009) pointed out that even severe restrictions of

water uptake in saline soils may have only minor

significance in olive, which can tolerate declines in

leaf water potential without permanent damages to

the photosynthetic apparatus. However, we suggest

that phenotypic variability of the root xylem in

response to heterogeneous environmental signals,

coming to full effect in high conductivity roots, is of

major importance for the growth potential of the

three olive varieties under salt stress, improving the

functional adjustment of Barnea and Arbequina

varieties to spatial and temporal soil conditions,

and subsequently increasing the amount, and the

reliability, of the water supply (Rewald et al. 2010).

The positive outcome of this strategy is evidenced by

the significantly lower degree of embolism in

branches of var. Barnea, and the unaffected stem

growth and net photosynthetic rates of salt-stressed

Barnea and Arbequina trees.

Future studies on stress tolerance should address

the functional differentiation within root systems in

order to improve our mechanistic understanding of

water acquisition in spatially and temporally hetero-

geneous environments.

Acknowledgements

The authors thank Prof. Y. Waisel for his critical

comments on an early version of the manuscript, and

Prof. M. Silberbush and S. Weissbein for fruitful

discussion and excellent support in the field. The

first author was financially supported by the Dryland

Research Specific Support Action (DR-SSA) of the

European Union (FP6). This project was developed

within the COST E38 action ‘‘Woody Root

Processes’’.

20 B. Rewald et al.


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Influence of salinity on root hydraulic properties of three olive varieties

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