Root tissue structure is linked to ecological strategies of grasses

RESEARCH New Phytol. (2000), 148, 459–471

Root tissue structure is linked to ecological

strategies of grasses

STEFAN WAHL PETER RYSER*

Geobotanisches Institut ETH, Gladbachstr. 114, 8044 ZuX rich, Switzerland

Received 10 March 2000; accepted 14 July 2000

The present study investigated to what extent there is a link between root tissue structure and ecological strategies

of plant species; such a link is known for leaf tissue structure. We investigated experimentally root tissue mass

density, root diameter and several characteristics of root anatomy in the axile roots of 19 perennial grass species

from different habitats and related these parameters to the ecological behaviour of the species. Root characteristics

were assessed in new roots produced by mature plants grown under standardized conditions. The ecological

behaviour was characterized in terms of relative growth rate (RGR), plant height at maturity and ecological

indicator values for nutrients, light and tolerance to mowing according to Ellenberg. We found a striking

dichotomy between root anatomical characteristics associated with interspecific variation in RGR and those

associated with variation in plant height. RGR correlated with anatomical characteristics that contribute to root

robustness, whereas plant height correlated with characteristics associated with axile root hydraulic conductance.

RGR correlated negatively with tissue mass density (TMDr) in roots. Interspecific variation in TMD

rwas

explained by the proportion of stele in the cross-sectional area (CSA) of the axile root and the proportion of cell

wall in the CSA of the stele. For a given root diameter, slow growing species had smaller, albeit more numerous,

xylem vessels, indicating a higher resistance to cavitation and protection against embolisms. Plant height

correlated positively with root CSA, total xylem CSA and mean xylem vessel CSA, indicating a need for a high

transport capacity in roots of species that attain a large size at maturity. TMDrcorrelated positively with dry

matter content in leaves. The results emphasize the close relationship between tissue structure and growth

characteristics at the whole-plant level.

Keywords: axile roots, interspecific variation, Poaceae, relative growth rate, root anatomy, root tissue mass

density, species height, tissue structure.

Trade-offs between characteristics of plants pro-

moting resource capture and rapid growth, and those

promoting resource conservation and stress tol-

erance, are crucial in determining the ecological

behaviour of a species. This conclusion is based on

numerous studies dealing with the physiological,

chemical and morphological traits of plant species

with contrasting inherent relative growth rates

(RGR; Grime et al., 1997; Reich et al., 1997;

Lambers et al., 1998). Plant tissue structure is one of

the traits strongly affecting such trade-offs. Low

tissue mass density in leaves is associated with a high

specific leaf area, large total leaf area and fast growth,

on the one hand (Garnier, 1992; Ryser & Lambers,

1995; Meerts & Garnier, 1996; Ryser & Aeschli-

mann, 1999), and with short life span and high

resource losses on the other (Schla$ pfer & Ryser,

1996; Ryser & Urbas, 2000). Leaf toughness and

*Author for correspondence (tel41 1 632 44 80; fax41 1 261

0595; e-mail ryser!geobot.umnw.ethz.ch).

high tensile strength are associated with slow growth

and also with a high degree of mechanical stability of

the leaves, which tend to be well protected against

environmental hazards such as herbivory (Coley,

1983; Reich et al., 1991; Cornelissen et al., 1999).

Hence, tissue mass density is an effective means of

predicting the performance of plants along gradients

of resource availability (Wilson et al., 1999); a low

tissue mass density is characteristic of plants of

productive habitats, a high tissue mass density is

typical in plants of unproductive environments

Studies on the ecological significance of tissue

structure have mostly been restricted to above-

ground organs, especially leaves. However, con-

siderations of both above-ground and below-ground

traits are essential when trade-offs with respect to

resource balance are discussed, as fast growth

requires good resource-acquisition capacity both

above- and below-ground, and resource losses are

caused by turnover of both leaves and roots. One of

the main arguments for the importance of tissue

structure for resource capture is, in fact, that a plant

with low tissue mass density can simultaneously

460 RESEARCH S. Wahl and P. Ryser

Table 1. The 19 grass species studied, their indicator values for nutrients (N-value), light (L-value), and mowing

tolerance (M-value) according to Ellenberg et al. (1992) and Briemle & Ellenberg (1994), seedling relative growth

rate (RGR), seedling relative leaf dry matter content (DM}FM"), mean plant height at maturity and

characteristic habitat

Species N-value L-value M-value

RGR

(g g−" d−")

DM}FM"

(g g−")

Plant height at

maturity (m) Characteristic habitat

Agropyron repens (L.)

Beauv.

7 7 7 0.214 0.138 0.61 Arable land, road verges

Anthoxanthumodoratum L.

— — 7 0.205 0.173 0.19 Wide range of grasslands

Arrhenatherum elatius(L.) J. & C. Presl

7 8 6 0.158 0.175 0.95 Meadows, road verges

Brachypodiumpinnatum (L.) Beauv.

4 6 3 0.089 0.278 0.48 Undermanaged grasslands

Briza media L. 2 8 4 0.100 0.230 0.17 Nutrient-poor grasslands

Bromus erectusHudson

3 8 5 0.093 0.257 0.24 Limestone grasslands

Dactylis glomerata L. 6 7 8 0.178 0.194 0.51 Productive grasslands, road

verges

Deschampsia caespitosa(L.) Beauv.

3 6 5 0.209 0.191 0.18 Grasslands on poorly

drained soils

Festuca ovina L. 1 7 6 0.099 0.267 0.13 Nutrient-poor grasslands

Helictotrichonpubescens (Hudson)

Pilger

4 5 5 0.124 0.265 0.18 Unproductive grasslands

Holcus lanatus L. 5 7 6 — — 0.24 Moist to dry grasslands

Lolium perenne L. 7 8 8 0.189 0.137 0.25 Pastures and meadows

Melica nutans L. 3 4 — 0.034 0.198 0.26 Dry woodlands

Milium effusum L. 5 4 — 0.058 0.226 0.22 Moist woodland

Poa angustifolia L. 3 7 8 0.099 0.230 0.13 Dry grasslands

Poa nemoralis L. 4 5 — 0.166 0.178 0.37 Deciduous woodlands

Poa pratensis L. 6 6 9 0.179 0.227 0.30 Productive grassland

Poa trivialis L. 7 6 8 0.168 0.156 0.11 Moist productive grasslands

Trisetum flavescens(L.) Beauv.

5 7 7 0.147 0.204 0.41 Meadows

The indicator values are expressed on a scale from 1 (low requirements for nutrients, light or low mowing tolerance) to

9 (high requirements, high tolerance). To determine RGR and DM}FM"27 plants were harvested 2–6 wk after planting.

Parameter values were calculated for the plant dry mass of 19 mg. Plant height was determined by image analysis of two

garden-grown plants per species.

have a large leaf area and an extensive root system.

Unlike biomass allocation, tissue mass densities

above- and below-ground do not directly constrain

each other (Ryser & Lambers, 1995).

Both root-system length and leaf area are con-

strained by negative consequences of low tissue mass

density and small organ diameter (Ryser, 1998). The

limits of maximizing root length by reducing tissue

mass density and root diameter are set by the low

hydraulic capacity (Mapfumo et al., 1993), the low

tensile strength (Easson et al., 1995) and the short

life span (Ryser, 1996; Schla$ pfer & Ryser, 1996) of

thin roots with a low tissue mass density. As root-

system length is closely associated with acquisition

capacity for below-ground resources (Ryser, 1998),

the already mentioned constraints are likely to

influence the ecological characteristics of a species.

Furthermore, these constraints are probably also

reflected in root anatomy. In leaves, there is an

association between tissue mass density and pro-

portion of sclerenchyma (Garnier & Laurent, 1994;

Van Arendonk & Poorter, 1994), and in roots

diameter is associated with cell size in the cortex and

with thickness of secondary walls in the exodermis

(Eissenstat & Achor, 1999). However, the ecological

significance of interspecific variation in root anatomy

with respect to plant growth strategies is still largely

unknown.

The main aim of this study was to assess the extent

to which structural characteristics that constrain root

length, tissue mass density and diameter of axile

roots, for example, can be related to ecological

characteristics of a species. We investigated root

tissue structure and root anatomy of axile roots

among 19 ecologically contrasting perennial grass

species. Axile roots, although forming a small

proportion of the total root length, contain a large

part of the biomass allocated below ground (Boot &

Mensink, 1990). One may assume that interspecific

differences in characteristics of axile roots reflect

those of lateral roots as well, as grass roots lack

secondary growth. Among grasses, turnover rate of

axile roots seems to be comparable to that of the finer

laterals (Ryser, 1998).

RESEARCH Interspecific variation in root tissue structure 461

In addition, we investigated which anatomical

traits of roots underlie the interspecific variation in

tissue mass density, and how relations in these traits

are reflected in variation in root diameter. We related

the anatomical data to ecological behaviour of the

various species. The ecological parameters used were

the ecological indicator values for nutrient and light

requirements (Ellenberg et al., 1992), tolerance to

mowing (Briemle & Ellenberg, 1994), and measured

values of relative growth rate (RGR) and plant

height. Plant height and RGR are frequently con-

sidered to be independent key traits defining adaptive

strategies of plant species (Grime & Hunt, 1975;

Chapin et al., 1996; Westoby, 1998). For example, a

high RGR is generally associated with species from

productive and disturbed habitats, whereas tallness

is associated with productive and relatively un-

disturbed habitats. There are indications that both of

these ecologically important characteristics are re-

lated to aspects of root structure; RGR with tissue

mass density, and height with hydraulic conductance

and root diameter (Ryser, 1998). Our study was

restricted to grasses that display a wide variation in

ecological behaviour with respect to nutrients and

disturbance, despite a comparatively uniform growth

form. Lack of secondary growth in grasses further

facilitates comparisons of root anatomy.

Tissue mass density and anatomy of grass roots

We investigated the tissue mass density and root

anatomy of 19 perennial grass species of contrasting

habitats in terms of nutrient availability and light

conditions (Table 1). Species names follow Lauber

& Wagner (1996). Seeds were collected from popu-

lations in the Swiss Mittelland and were sown on

perlite in a glasshouse. After germination, seedlings

were planted on 20 July 1996 in 1-l pots (diameter 10

cm, height 12 cm) containing quartz sand of 0.1–0.7

mm grain size. Every week, during the growing

season, each plant received 200 ml of diluted

Hoagland solution containing the following nu-

trients ; 41 µmol KH#PO

%, 136 µmol KNO

$, 65 µmol

Ca(NO$)#, 37 µmol MgSO

%, 0.017 µmol

CuSO%[5H

#O, 0.0070 µmol ZnSO

%[7H

#O, 0.17

µmol MnCl#[4H

#O, 0.42 µmol H

$BO

$, 0.0045 µmol

Na#MoO

%[2H

#O, 0.02 µmol FeCl

$[6H

#O and 0.02

µmol tartaric acid. Plants were watered with tap

water.

On 23 April 1997, after one season of growth in the

glasshouse, the plants were transferred into a garden

in 2.6-l pots (diameter 10 cm, height 30 cm)

containing quartz sand of 0.1–0.7 mm grain size.

The intact root-balls were carefully transferred from

the small pots into the large ones and separated from

the new substrate by a wide-meshed polyethylene

net (1 cm mesh size). This allowed us to distinguish

Co

St

EnMX

(a)

Co

St

En

MX

(b)

Co

St

En

MX

(c)

Fig. 1. Digital images showing segments of root cross-

sections stained with Toluidine Blue of three grass species,

(a) Dactylis glomerata, (b) Milium effusum and (c) Helicto-trichon pubescens. Co, cortex; En, endodermis; MX, large

meta xylem vessel ; St, stele. Bar, 50 µm.

the roots grown during the second growing season,

which were needed for the anatomical investigations.

Plants were arranged in a randomized block design,

with one replicate per species in each of the eight

blocks. Plants received the same amount of nutrients

during their second season as they received in the

glasshouse during the first season. Pots were placed


Table 2. Correlations between ecological, structural and anatomical characteristics among the studied 19 grass

species. Pearson correlation coefficients (R) and significance levels are shown, except for correlations with indicator

values for nutrients (N), light (L), and mowing tolerance (M), for which Spearman’s rank correlation coefficients

are shown ; correlations of relative growth rate (RGR) and axile root tissue density (TMDr) with root anatomical

traits are conducted with (a) and without (b) Milium effusum and Helictotrichon pubescens

Seedling RGR Height at

maturity

Axile root tissue

mass density (TMDr)

Root cross-

sectional

area

Plant traits a b a a b a

RGR — 0.23 ®0.68** ®0.03

TMDr

®0.68** 0.01 — 0.16

Leaf dry matter content ®0.66** ®0.25 0.74*** 0.16

Root CSA ®0.03 0.58** 0.16 —

Proportion of cell wall in stele CSA ®0.00 0.04 ®0.12 0.52* 0.49* ®0.01

Stele CSA ®0.38 ®0.47 0.52* 0.31 0.55* 0.78***

Stele cell size ®0.07 ®0.15 0.55* ®0.03 0.13 0.65**

Stele cell number ®0.44 ®0.54* 0.40 0.47* 0.76*** 0.60**

Proportion of stele in root CSA ®0.58* ®0.72** 0.31 0.37 0.71** 0.24

Total xylem CSA ®0.19 ®0.28 0.63** 0.19 0.44 0.83***

Mean xylem vessel CSA 0.20 0.43 0.52* ®0.04 ®0.32 0.55*

No. of xylem vessels ®0.41 ®0.63** 0.31 0.28 0.69** 0.57*

Proportion of total xylem in root CSA ®0.30 ®0.43 0.48* 0.19 0.52* 0.53*

Mean xylem vessel CSA relative to

root CSA

0.27 0.56* 0.02 ®0.30 ®0.66** ®0.23

No. of xylem vessels per unit root

CSA

®0.43 ®0.70** ®0.02 0.19 0.64** ®0.14

N-value 0.57* 0.50* ®0.55* 0.04

L-value 0.24 0.11 ®0.40 0.28

M-value 0.45 0.05 ®0.69** ®0.48

Significance levels : ***, P !0.001; **, P !0.01; *, P !0.05. The following data points are missing: RGR for Holcuslanatus, N-value and L-value for Anthoxanthum odoratum and M-value for Melica nutans, M. effusum and Poa nemoralis.CSA, cross-sectional area.

in shallow trays filled with water to 1–2 cm depth,

which kept the substrate moist and prevented

drought stress during the experiment.

Plants were harvested on 12 October 1997 and

separated into above-ground biomass and roots.

Only roots produced during the second growing

season (i.e. those which had grown through the net)

were used for further examinations. One axile root

per plant was randomly selected. We cut one piece of

c. 5 cm length at the proximal end of the root, c. 10

cm from the point of attachment at the node and

stored it in 70% ethanol. One half of this sample was

used for the anatomical studies, the other half for

determination of tissue mass density. For this

purpose, root diameter was measured using a light

microscope and the volume of the root piece was

calculated by assuming a cylindrical form and

multiplying the cross-sectional area by the length.

The root pieces were dried at 70°C for at least 24 h

and their dry mass was determined to a precision of

³2 µg using an analytical balance (MT 5 Mettler

Toledo GmbH, Greifensee, Switzerland). Root

tissue mass density was then calculated as dry mass

per volume (mg mm−$).

The root samples for anatomical examinations

were embedded in 2-hydroxyethylmethacrylate

(HEMA) also known as GMA (Igersheim &

Cichocki, 1996). Slices (4-µm thick) were cut with a

microtome. To contrast cell walls against the

background, the specimens were stained with Tol-

uidine Blue, which stains lignin blue-green and

cellulose purple or red-violet (Gerlach, 1984). Digi-

tal images of the cuts were obtained by light

microscopy at ¬100 and ¬200 using a video camera

(JVC TK 1280; Victory Company of Japan Ltd,

Yokohama, Japan) connected to a computer.

Image analysis on the computer allowed us to

determine the CSA of the whole root, as well as the

CSA of the stele, endodermis, cortex and individual

large xylem vessels (Fig. 1). These areas were

assessed by tracing the outlines of the structures with

a cursor.

Based on these measurements we calculated the

relative amounts of various tissues and structures per

total root CSA; the proportion of stele CSA, the

proportion of total xylem CSA, the mean CSA of

xylem vessels relative to root CSA and the number of

xylem vessels per unit CSA of the root (n mm−#).

Additionally, the proportion of cell wall in the

CSA of stele and endodermis was determined. As

cell walls generally contain less water than cyto-

plasm, this parameter can be assumed to be closely

related to the mass density of these tissues. For this

purpose segments of stele or endodermis were

randomly chosen (c. 10% of total CSA), avoiding

xylem elements which were measured separately.


0.3

0.2

0.1

00 0.1 0.2 0.3

Root CSA (mm2)

TM

Dr (

mg

mm

–3) (e) 0.3

0.2

0.1

00 0.1 0.2 0.3

TMDr (mg mm–3)

DM

/FM

l (g

g–1

)

(f)

1

0.10 0.1 0.2 0.3

TMDr (mg mm–3)

Hei

gh

t (m

)

(c) 1

0.10 0.1 0.2 0.3

Root CSA (mm2)

Hei

gh

t (m

)(d)

0.3

0.2

0.1

00 0.1 0.2 0.3

TMDr (mg mm–3)

RG

R (

g g

–1 d

–1)

(a) 0.3

0.2

0.1

00 0.1 0.2 0.3

Root CSA (mm2)

RG

R (

g g

–1 d

–1)

(b)

Fig. 2. Relationships between axile root tissue mass density

(TMDr), cross-sectional area (CSA) of axile roots and

ecologically important plant traits among the grass species

studied. (a) Relative growth rate (RGR) and TMDr, (b)

RGR and axile root CSA, (c) plant height at maturity (log-

transformed) and TMDr, (d) plant height at maturity (log-

transformed) and axile root CSA, (e) TMDr

and axile

root CSA and (f) dry mass: fresh mass ratio in leaves

(DM}FMl) and TMD

r. n¯19 (c,d,e) and n¯18 (a,b,f).

Significant correlations (P !0.05) are shown with a

regression line.

The lumen of the cells was outlined and subtracted

from the total area of the segment. Area and

proportion of cell wall in stele and endodermis were

determined separately, but for further analysis we

used an average of these parameters, weighted with

their relative proportions in CSA. Although the

endodermis belongs ontogenetically to the cortex

(Von Guttenberg, 1968), it was treated as belonging

structurally to the stele. The number and the area of

individual stele cells were estimated from the chosen

segments. The proportion of cell wall in the cortex

was not determined because cell walls in the cortex

were too thin to be measured by light microscopy.

Image analysis was performed on a Macintosh

computer using the public domain NIH Image

program version 1.62 (developed at the US National

Institutes of Health, and available on the Internet).

Species’ height at maturity

Species’ height at maturity was determined on plants

grown in a garden for one full growing season. Seeds

of the species studied were sown on perlite on 16

March 1999. After germination in the last week of

March and the first week of April, the seedlings were

grown in 0.4-l pots on potting soil in a glasshouse

until 3 May when they were transferred to garden

beds outside in five randomized blocks, one replicate

plant per species in each block. The distance between

plants was 45 cm. To enhance growth, 3.5 g of slow-

release fertilizer (Osmocote Plus, Hauert Du$ nger,

Grossaffoltern, Switzerland) with 15% (of mass)

NH%NO

$, 11% P

#O

&, 13% K

#O, 2% MgO and trace

elements were added to the soil before planting. The

beds were weeded to reduce competition by other

plants and watered during dry periods.

An index of plant height was determined by image

analysis. On 19 August 1999, two plants of each

species were photographed from a distance of 1.5 m

using a digital camera (Dimage EX, Minolta Co.

Ltd, Osaka, Japan) against a white background with

a scale. A binary image of the whole plant was made

and plant height was defined as the height at which

95% of the pixels were summarized. To achieve a

normal distribution, the values were log-transformed

for the analysis.

Species’ RGR and leaf tissue mass density

Root anatomical characteristics of the species studied

were compared with seedling RGR, as this trait is

commonly assumed to reflect the ecological be-

haviour of a species with respect to resource avail-

ability and disturbance rate (Grime & Hunt, 1975;

Poorter & Garnier, 1999). Seeds were sown on

perlite in April 1999. Seedlings were planted be-

tween 29 April and 17 May in the garden in 1-l pots

(diameter 10 cm, height 12 cm) containing quartz

sand (0.1–0.7 mm grain size). Hoagland nutrient

solution (5 ml), diluted to 100 ml, was added twice a

week. The RGR was determined by logarithmic

regression using data of 27 plants per species

harvested in six harvests at intervals of 2 d starting

on 28 May. Size effect was taken into account by

calculating the RGR for all species at a plant size of

19 mg dry mass. Leaf tissue mass density was

expressed as leaf dry mass : fresh mass ratio. Leaf

fresh mass was measured after the plants had been

saturated overnight between wet paper towels in a

refrigerator. Dry mass was determined after drying

plants for at least 48 h at 70°C. As with RGR, leaf

tissue density was calculated for a plant size of 19

mg. Holcus lanatus was not included in this ex-

periment.

Statistical analysis

For the statistical analysis we used JMP version

3.2.2 (SAS Institute Inc. 1995, Cary, NC, USA).

The correlations between the various root char-

acteristics, and between root characteristics and the

ecological parameters RGR and species height, were

tested using Pearson correlation. Plant height was


0.3

0.2

0.1

00 0.6 1.2

Proportion of total xylemin root CSA (%)

TM

Dr (

mg

mm

–3)

(g)

1.8 0 0.2 0.4Mean xylem vessel CSArelative to root CSA(%)

(h)

0.6 0 10 20No. of xylem vessels

per unit CSA

(i)

300.8

MeHp

MeHpHp

Me

0.3

0.2

0.1

00 1200 2400Total xylem vessel CSA (µm2)

(d)

3600 0 500 1000Mean xylem vessel CSA (µm2)

(e)

0 2 4No. of xylem vessels

(f)

61500

Me

HpMe

HpHpMe

0.3

0.2

0.1

00 0.05

Stele CSA (mm2)

(a)

0.1 0 10 20Proportion of cell wall in stele

CSA (%)

(b)

0 50 60Proportion of stele in root

CSA (%)

(c)

7030

MeHpMe

HpHpMe

80

8

Fig. 3. Relationships between root tissue mass density (TMDr) and root anatomical traits among the 19 grass

species studied. TMDris plotted against (a) stele cross-sectional area (CSA), (b) proportion of stele in root

CSA, (c) proportion of cell wall in stele CSA, (d) total xylem CSA, (e) mean xylem vessel CSA, (f) number of

xylem vessels, (g) proportion of total xylem in root CSA, (h) mean xylem vessel area relative to root CSA and

(i) number of xylem vessels per unit root CSA. Significant correlations (P !0.05) are shown with a regression

line. For correlations which were significant only when Helictotrichon pubescens (Hp) and Milium effusum (Me)were omitted, nonsignificant regressions including these two species are shown with dashed lines and the two

species are indicated with open symbols.

log-transformed to obtain normal distribution of the

data. The relationships between root characteristics

and indicator values were tested with the non-

parameteric Spearman rank correlation test, as the

indicator values are categorical data.

Root tissue mass density, root cross-sectional area

and species ecology

Both of the two measured ecological traits, RGR and

height at maturity, correlated with Ellenberg N

indicator values (Table 2). However, there was no

significant correlation between RGR and height at

maturity for the species studied, indicating an

independence of these two characteristics among

grasses. Furthermore, these two ecological charac-

teristics were themselves correlated with different

root traits. RGR correlated negatively with TMDr,

but not with root CSA (Fig. 2a,b, Table 2). Plant

height did not correlate with TMDr, but correlated

positively with root CSA (Fig. 2c,d). The root traits

TMDr

and CSA did not correlate with each other

(Fig. 2e). The TMDrcorrelated positively with the

corresponding above-ground parameter, the relative


Table 3. Multiple regression between tissue mass density of roots (TMDr)

as dependent variable and proportion of stele in total root cross-sectional

area (CSA) and proportion of cell wall in stele CSA as independent

variables

Standard regression coefficient

for independent variables

Dependent variable n

Proportion of

stele in root

CSA

Proportion of

cell wall in

stele CSA R#

1. TMD#

19 0.46* 0.59** 0.42**

2. TMDr

17 0.72*** 0.50** 0.73***

Standardized regression coefficients, coefficients of determination (R#) and

levels of significance are given. 1. Regression with all species (n¯19), 2.

Regression without H. pubescens and M. effusum (n¯17). Significance levels :

***, P !0.001; **, P !0.01; *, P !0.05.

dry matter content of leaves (DM}FMl) (Fig. 2f,

Table 2). TMDr

correlated negatively with the

indicator values for nutrients and for tolerance to

mowing, but not with the indicator value for light.

Root CSA did not significantly correlate with any of

the indicator values (Table 2). However, there was a

tendency to a negative correlation between root CSA

and tolerance to mowing (P¯0.057).

Anatomical characteristics underlying root tissue

mass density

The tissue mass density of a root is determined by

the amount of dry matter per unit volume of the

different tissue types in the root, and by the relative

proportions of those various tissue types. For the

species studied, TMDrcorrelated positively with the

proportion of cell wall in the stele (Fig. 3), a

parameter that can be assumed to contribute to

variation in the tissue density in the stele. The

proportion of cell wall in the stele did not correlate

with cell size in the stele (R#¯0.016, P¯0.60, n¯19), indicating that its interspecific variation is

caused by variation in cell wall thickness.

There was a tendency to a positive relationship

between the proportion of stele in root CSA and

TMDr, but the correlation was not significant due to

two outlying species, Helictotrichon pubescens and

Milium effusum. These species had very high tissue

mass densities for their relatively small proportions

of stele (Fig. 3, Table 2), which could be explained

in terms of dense cortex; in particular H. pubescens

had very thick cortex cell walls and also thick cell

walls in the stele (Fig. 1). These two species were

consistently outliers in all correlations that included

stele dimensions. As there was a seemingly close

relationship between tissue density and stele dimen-

sions among the other 17 species, we conducted the

statistical analyses twice, with and without H.

pubescens and M. effusum.

Table 4. Coefficient of variation (CV) in root tissue

mass density (TMDr), proportion of cell wall in stele

cross-sectional area (CSA) and proportion of stele in

total root CSA; (1) CV calculated with all species

(N¯19), (2) CV calculated without Helictotrichon

pubescens and Milium effusum (n¯17)

Root traits n CV(%)

TMDr(1) 19 24.2

TMDr(2) 17 21.0

Prop. cell wall in stele CSA (1) 19 7.3

Prop. cell wall in stele CSA (2) 17 7.2

Proportion stele in root CSA (1) 19 29.4

Proportion stele in root CSA (2) 17 28.4

In a multiple regression both the proportion of cell

wall in the stele and proportion of stele in root CSA

were significantly associated with TMDr

and to-

gether they explained 42% of the variation in this

correlation. If H. pubescens and M. effusum were

excluded from the calculation the regression ex-

plained 73% of the variation (Table 3). The

coefficient of variation for the proportion of stele in

root CSA was similar to that for TMDr, whereas the

amount of interspecific variation in the proportion of

cell wall in the stele CSA was clearly less (Table 4).

A high TMDr

was associated with a large stele

CSA and a large number of stele cells, H. pubescens

and M. effusum also being outliers in these relation-

ships. By contrast, size of stele cells was not

associated with TMDr

(Table 2). Similar relation-

ships could also be seen in the correlation of TMDr

with xylem traits. Although TMDrcorrelated posi-

tively with the number of xylem vessels, it did not

correlate with total xylem area or with mean xylem

vessel area. However, if the xylem characteristics

were expressed per unit root CSA, they correlated

with root tissue mass density: the total xylem CSA

and the number of xylem vessels positively, and the

466

RESEA

RC

HS

.W

ahland

P.R

yser

Table 5. Root anatomical characteristics for the 19 grass species studied, mean values and standard errors are given in parentheses

Species n

Root tissue

mass

density

(mg mm−$)

Root cross-

sectional

area

(mm#)

Cell wall

in stele

CSA (%)

Stele

CSA

(mm#)

Stele cell

size

(µm#)

Stele cell

number

(n)

Stele CSA

in total

root CSA

(%)

Total

xylem

CSA

(µm#)

Mean

xylem

vessel CSA

(µm#)

No.

xylem

vessels

(n)

Total

xylem in

root CSA

(%)

Mean xylem

vessel CSA

relative to

root CSA (%)

No. xylem

vessels per

unit root CSA

(n mm−#)

AR 8 0.125 0.21 58.7 0.024 77.7 167 11.7 1733 1022 2.00 0.77 0.51 12.13

(0.004) (0.04) (1.82) (0.004) (6.60) (27.3) (0.87) (385) (175.0) (0.42) (0.05) (0.09) (4.50)

AO 9 0.131 0.11 60.6 0.016 77.4 125 14.9 659 479 1.44 0.61 0.46 13.82

(0.003) (0.01) (1.79) (0.002) (5.86) (9.99) (0.74) (102) (50.1) (0.24) (0.05) (0.05) (2.55)

AE 8 0.137 0.23 57.7 0.037 112.5 186 16.3 2472 869 2.88 1.11 0.43 13.25

(0.004) (0.03) (2.63) (0.005) (10.6) (19.9) (0.73) (350) (90.0) (0.40) (0.06) (0.06) (1.16)

BP 6 0.237 0.21 63.9 0.042 62.1 426 20.4 3479 731 4.83 1.61 0.38 24.04

(0.012) (0.03) (2.07) (0.006) (6.46) (58.4) (1.45) (787) (100.5) (0.79) (0.15) (0.06) (4.50)

BM 8 0.190 0.14 64.3 0.023 71.8 197 16.9 1123 361 3.38 0.77 0.28 24.10

(0.031) (0.02) (1.86) (0.002) (4.74) (19.6) (0.54) (261) (70.5) (0.65) (0.10) (0.07) (4.52)

BE 8 0.172 0.27 55.5 0.058 109.8 363 21.9 3491 509 6.63 1.25 0.18 26.37

(0.022) (0.03) (2.30) (0.006) (11.04) (31.4) (1.31) (605) (75.6) (0.50) (0.11) (0.02) (2.50)

DG 8 0.154 0.26 56.7 0.039 94.7 267 15.1 3371 860 3.75 1.23 0.30 14.85

(0.020) (0.05) (2.46) (0.007) (8.42) (40.6) (0.58) (893) (104.7) (0.65) (0.09) (0.05) (1.59)

DC 8 0.155 0.20 68.1 0.019 64.4 154 9.6 1181 728 1.75 0.61 0.43 9.66

(0.012) (0.03) (2.36) (0.003) (9.03) (22.7) (0.64) (331) (83.0) (0.53) (0.07) (0.07) (2.21)

FO 8 0.168 0.17 63.2 0.025 82.0 206 15.0 1159 370 3.38 0.63 0.23 22.4

(0.006) (0.031) (2.18) (0.004) (10.2) (32.6) (0.67) (381) (127.5) (0.46) (0.05) (0.05) (2.93)

HL 8 0.126 0.176 52.3 0.018 55.8 190 11.7 1362 960 1.50 0.85 0.65 12.1

(0.008) (0.053) (2.18) (0.004) (5.29) (37.4) (1.10) (312) (225.3) (0.27) (0.06) (0.09) (2.04)

HP 7 0.230 0.180 67.0 0.015 55.9 141 8.6 653 646 1.14 0.35 0.34 10.1

(0.011) (0.041) (1.53) (0.003) (5.30) (27.0) (0.79) (151) (154.7) (0.14) (0.03) (0.06) (4.02)

LP 9 0.118 0.160 61.3 0.019 78.7 162 12.0 952 891 1.22 0.57 0.53 8.63

(0.007) (0.018) (3.63) (0.003) (4.81) (18.1) (1.0) (167) (183.3) (0.22) (0.05) (0.09) (1.77)

MN 8 0.185 0.157 57.5 0.040 85.9 284 25.7 1942 502 4.38 1.33 0.38 29.9

(0.004) (0.023) (1.73) (0.005) (7.87) (42.8) (1.23) (298) (96.0) (0.60) (0.10) (0.10) (4.08)

ME 7 0.245 0.157 60.8 0.023 70.2 184 15.3 1197 999 1.14 0.72 0.64 9.46

(0.017) (0.030) (1.89) (0.004) (8.79) (34.0) (0.8) (305) (167.3) (0.14) (0.06) (0.07) (2.39)

PA 8 0.151 0.109 61.1 0.012 60.7 114 11.6 516 399 1.50 0.50 0.36 16.8

(0.009) (0.015) (2.50) (0.001) (5.42) (10.4) (1.0) (98) (78.4) (0.38) (0.07) (0.05) (5.04)

PN 7 0.160 0.164 59.3 0.027 68.1 252 17.0 2090 559 3.86 1.33 0.35 26.2

(0.023) (0.021) (2.51) (0.003) (8.21) (22.8) (1.38) (340) (80.5) (0.55) (0.15) (0.05) (5.55)

PP 8 0.156 0.092 61.3 0.013 62.6 115 13.5 628 323 1.88 0.62 0.35 27.2

(0.005) (0.021) (3.16) (0.003) (6.34) (17.1) (0.66) (204) (69.7) (0.23) (0.06) (0.05) (6.22)

PT 8 0.113 0.072 51.6 0.008 44.0 125 11.5 523 374 1.38 0.70 0.57 20.2

(0.006) (0.011) (3.37) (0.001) (4.79) (29.8) (0.76) (122) (59.3) (0.26) (0.07) (0.11) (2.43)

TF 7 0.207 0.157 62.9 0.032 86.9 282 21.0 1252 431 3.43 0.82 0.28 22.7

(0.034) (0.015) (2.64) (0.002) (11.48) (60.1) (2.32) (124) (89.4) (0.53) (0.05) (0.05) (3.85)

AR, Agropyron repens ; AO, Anthoxanthum odoratum ; AE, Arrenatherum elatius ; BP, Brachypodium pinnatum ; BM, Briza media ; BE, Bromus erectus ; DG, Dactylis glomerata ; DC,

Deschampsia caespitosa ; FO, Festuca ovina ; HL, Holcus lanatus ; HP, Helictotrichon pubescens ; LP, Lolium perenne ; MN, Melica nutans ; ME, Milium effusum ; PA, Poa angustifolia ;

PN, Poa nemoralis ; PP, Poa pratensis ; PT, Poa trivialis ; TF, Trisetum flavescens.


0.3

0.2

0.1

00 0.6 1.2


RG

R (

g g

–1 d

–1)

(g)


(h)


per unit CSA

(i)

300.8

Me

Hp

Me

HpHp

Me

0.3

0.2

0.1

00 1200 2400Total xylem vessel CSA (µm2)

(d)


(e)


(f)

61500

Me

Hp

Me

HpHp

Me

0.3

0.2

0.1

00 0.05

Stele CSA (mm2)

(a)


CSA (%)

(b)


CSA (%)

(c)

7030

Me

Hp

Me

HpHp

Me

80

8

Fig. 4. Relative growth rate (RGR) and root anatomical traits among 18 grass species. RGR is plotted against

(a) stele cross-sectional area (CSA), (b) proportion of stele in root CSA, (c) proportion of cell wall in stele CSA,

(d) total xylem CSA, (e) mean xylem vessel CSA, (f) number of xylem vessels, (g) proportion of total xylem

in root CSA, (h) mean xylem vessel CSA relative to root CSA and (i) number of xylem vessels per unit root

CSA. Significant correlations (P !0.05) are shown with a regression line. For correlations which were

significant only when Helictotrichon pubescens (Hp) and Milium effusum (Me) were omitted, nonsignificant

regressions including these two species are shown with dashed lines and the two species are indicated with open

symbols.

mean vessel CSA negatively (Fig. 3, Table 2). These

relationships were significant (P !0.05) only if

H. pubescens and M. effusum were excluded from

the analysis (Fig. 3, Table 2). These two species had

exceptionally few vessels in relation to their high

TMDr(Table 5).

RGR and anatomical traits

RGR correlated only with those anatomical traits

which also correlated with TMDr. With the ex-

ception of the total number of xylem vessels and the

number of cells in the stele, RGR only correlated

with traits expressed per unit root CSA (Fig. 4).

RGR correlated negatively with the proportion of

stele in root CSA, mean xylem vessel CSA relative to

root CSA and the number of xylem vessels per unit

root CSA, but was independent of the proportion of

cell wall in the stele CSA, stele CSA, mean xylem

vessel CSA and total xylem CSA. However, RGR

did not correlate with the proportion of xylem in root

CSA. Species with a high RGR had fewer cells in the

stele and also fewer xylem vessels. Once again M.

effusum was an outlier in these relationships and

three of the correlations were significant only if this

species was removed from the dataset. The total


1

0.10 0.6 1.2


Hei

gh

t (m

)

(g)


(h)


per unit CSA

(i)

300.8

1

0.10 1200 2400Total xylem vessel CSA (µm2)

(d)


(e)


(f)

61500

1

0.10 0.05

Stele CSA (mm2)

(a)


CSA (%)

(b)


CSA (%)

(c)

7030 80

8

Fig. 5. Relationships between plant height at maturity and root anatomical traits among 19 grass species. Plant

height at maturity (log-transformed) is plotted against (a) stele cross-sectional area (CSA), (b) proportion of

stele in root CSA, (c) proportion of cell wall in stele CSA, (d) total xylem CSA, (e) mean xylem vessel CSA,

(f) number of xylem vessels, (g) proportion of total xylem in root CSA, (h) mean xylem vessel area relative to

root CSA and (i) number of xylem vessels per unit root CSA. Significant correlations (P !0.05) are shown with

a regression line.

xylem CSA and the mean xylem vessel CSA were

not significantly correlated with RGR (Fig. 4,

Table 2).

Anatomical characteristics associated with axile root

cross-sectional area

As shown in Table 2, root CSA correlated with the

CSA of the stele, but not with the proportion of stele

in the root CSA or with the proportion of cell wall in

the stele CSA. Root CSA was positively correlated

with the size and number of stele cells and with the

total xylem CSA, mean xylem vessel CSA, and

number of xylem vessels. The only proportional trait

related to root CSA was the proportion of xylem

(Table 2).

Plant height and root characteristics

Plant height was not correlated with any traits that

correlated significantly with RGR (Figs 4, 5, Table

2) and also, in most cases, not with traits that

correlated with TMDr. The significant anatomical

correlations that plant height manifested were simi-

lar to those for the CSA of axile roots (Table 2).

Plant height correlated positively with the stele

CSA, stele cell size, total xylem CSA and mean

xylem vessel CSA (Fig. 5). The only proportional

parameter plant height was significantly correlated


with was the proportion of xylem in root CSA. Plant

height was not correlated with the proportion of cell

wall in the stele, with the proportion of stele in root

CSA, with mean xylem vessel CSA relative to root

CSA or with the number of xylem vessels (Fig. 5,

Table 2).

Root tissue mass density and plant ecology

The results show the close relationship between

below-ground and above-ground tissue structure

and the species’ ecology. Interspecific variation in

TMDrof axile roots among ecologically contrasting

grasses is associated with the growth behaviour of

these species, and correlates with variation in

proportional leaf dry matter content (DM}FMl), an

estimator for tissue mass density of leaves. A

relationship between leaf tissue mass density and

species’ growth behaviour and ecology has already

been shown (Garnier, 1992; Ryser, 1996; Wilson et

al., 1999). In species with a low tissue mass density

the low costs of dry matter for construction of a unit

volume of leaves and roots enable the simultaneous

development of a large leaf area and an extensive root

system, resulting in high acquisition capacities both

for above-ground and below-ground resources. Low

root tissue mass density is thus a characteristic of

fast-growing species from nutrient-rich habitats, as

is also low leaf tissue mass density.

Root tissue mass density did not show any

significant correlations with plant height, indicating

that this trait is subject to a different set of constraints

from those influencing seedling RGR. Even among

herbaceous species, tall plants have to invest more

than small plants in supporting structures with a

higher proportion of lignified tissue in their stems

(Givnish, 1995; Niklas, 1995). However this in-

vestment is not reflected in tissue mass density of

roots or in the proportion of stele in root CSA.

Anatomical traits underlying TMDr

Of the anatomical traits measured, only the pro-

portion of cell wall in the stele CSA explained a

significant proportion of the interspecific variation in

root tissue mass density among all species studied.

This was not a result of variation in cell size, but only

of variation in cell wall thickness. We have no

general data about cell wall thickness in the cortex,

but the fact that H. pubescens had both a high root

tissue mass density and thick cortex cell walls

suggests that the cell wall thickness in the cortex also

contributes to the interspecific variation in root

tissue mass density. However, this contribution

might be reduced because of the lower density of the

cell walls themselves. Nagahashi et al. (1994)

discovered that the density of cortex cell walls is

lower than that of stelar cell walls for corn, carrot

and pea. It remains an open question whether

interspecific variation in cell wall density contributes

to the variation in TMDr.

Variation in the proportion of tissues with dif-

ferent densities has been found to contribute to

interspecific variation in leaf tissue mass density or

specific leaf mass (Garnier & Laurent, 1994; Van

Arendonk & Poorter, 1994). This was also the case

for root tissue mass density among most of the

species studied, a high proportion of stele being

associated with a high root tissue mass density.

However, this relationship was not general for all

species owing to the outlying position of two of the

species, H. pubescens and M. effusum. These two

species had a high tissue mass density but only a low

proportion of stele. Several other anatomical charac-

teristics in these species, such as stele CSA, stele cell

number, number of xylem vessels, proportion of

xylem in root CSA and mean xylem vessel CSA

relative to root CSA were similar to species with a

low tissue mass density. The behaviour of these two

species shows that there can be more than one

explanation for high tissue mass density, but it is not

clear whether the special character combination in

these two species has the same functional reasons for

both of them. There is no obvious ecological or

phylogenetic similarity between these two species.

The extent of interspecific variation in the pro-

portion of stele was similar to that in root tissue mass

density, but variability in the proportion of stele cell

walls was considerably less. This indicates that the

proportion of stele might better explain the range of

interspecific variation in root tissue mass density

than the proportion of cell wall in the stele, even

though the latter showed a more consistent re-

lationship among the species studied.

The ecological importance of anatomical traits

The dichotomy in the association of root anatomical

traits with the ecological characteristics of the species

was striking. The anatomical traits were either

associated with the RGR or with the plant height.

This dichotomy supports the postulate of Ryser

(1998) that root length is constrained by tissue mass

density when interspecific variation with respect to

RGR is taken into account, and by root diameter

when interspecific variation with respect to plant

height is considered. Root characteristics associated

with plant height are those related to the CSA,

important for the hydraulic conductance of axile

roots. Large plants have thicker axile roots with large

cells and a large stele CSA, large total xylem CSA

and large mean xylem vessel CSA. In particular

xylem vessel area has a major influence on hydraulic

conductance of mature roots as, according to the law

of Hagen-Poiseuille, the transport capacity of a pipe

increases with the fourth power of the pipe diameter.


Mean vessel CSA correlates with root diameter, as

has been demonstrated for intraspecific variation, for

example, in maize (Varney et al., 1991). Our data

show that root diameter is also in an interspecific

comparison related to potential hydraulic conduc-

tance.

Interspecific variation in RGR is generally related

to resource availability in characteristic habitats of

species, the slow growth of a stress-tolerant plant

being a result of investments in robust tissue with a

long life span. This was also reflected in root

anatomy. The anatomical traits which correlated

with RGR are those which are generally assumed to

be associated with robustness and resistance against

environmental hazards, but not with respect to

hydraulic conductance. However, relative to root

CSA, fast-growing species had a larger mean vessel

CSA than the slow-growing ones, indicating a need

for a high transport capacity in these species relative

to their size. This confirms findings for stems of

woody species (Castro-Dı!ez et al., 1998). Fast-

growing species had fewer vessels than slow-growing

ones, but CSA of the vessels is more important for

hydraulic conductance than their number (McCully

& Canny, 1988).

The higher number of vessels with a relatively

smaller diameter per vessel per root CSA in slow-

growing species might reflect a higher protection of

the vessel functioning. Narrow vessels have a lower

volume : surface ratio, which is known to be

associated with a lower probability for embolisms,

induced by freezing and thawing and pathogens.

The significance of conduit CSA for the probability

of embolism caused by drought stress has been

questioned (Sperry, 1995), but indications of a

higher cavitation frequency for xylem conduits of

large diameter have been found (Salleo & Logullo,

1986; Linton et al., 1998). It has also been shown

that narrow vessels refill more rapidly than wide

ones and thus spend less time empty (McCully et al.,

1998).

The exceptional trait combination in M. effusum of

slow growth and a low number of large vessels might

be related to the environmental conditions in its

characteristic habitat, which is woodland on rela-

tively moist soils. Under such conditions drought

stress is unlikely to occur, but productivity is limited

by shadiness.

The high proportion of stele in the roots of slow-

growing species is an expression of the robustness of

such roots. The concentration of the dense, scler-

enchymatic stele in the centre of the root results in a

high tensile strength. Stele and cortex together build

a composite material and ensure optimal biomech-

anical stability (Haberlandt, 1918). Thus the higher

proportion of stele in slow-growing species might

result in a more rigid single root cord for a given

diameter, protecting the root against mechanical

hazards.

What is the ecological significance of the large

proportion of cortex in the fast-growing species? A

larger cortex might ensure a better supply to the root

of oxygen via intercellular air spaces and aerenchyma

(Jackson & Armstrong, 1999) as well as provide a

larger store for minerals, proteins or lipids (Von

Guttenberg, 1968; Chino, 1981; Luxova, 1992). It

has also been suggested that the cortex is important

for recycling of phosphorus (Robinson, 1990).

However, an association between interspecific vari-

ation in these functions and in RGR is unknown.

Cortical tissue is also important as an interface

between arbuscular mycorrhizal fungi and plant

(Smith & Smith, 1997), but general differences

between fast-growing and slow-growing species with

respect to relative importance of mycorrhizal sym-

biosis have so far not been shown (Koide, 1991;

Smith & Smith, 1996). The function of the relatively

larger cortex in fast-growing species might simply be

to increase the root surface area and absorption rate

per root length.

In conclusion, our data clearly show that ana-

tomical characteristics of plant roots are an important

aspect of the trade-offs which determine plant

characteristics at the whole-plant level and the

ecological behaviour of a species. Anatomical struc-

tures which protect root functioning result in high

tissue density and constrain RGR, whereas ana-

tomical structures related to hydraulic conductance

are associated with plant height. Although clear

relationships between plant traits at the anatomical

and whole-plant levels can be found, individual

species might attain a similar higher-level trait

through different lower-level characteristics.

We thank Anton Igersheim and Peter Endress from

University of Zu$ rich for advice in anatomical work and for

facilities, Felix Wa$ ckers for use of equipment; Peter J.

Edwards, Johannes Kollmann, Dieter Ramseier, Cathy

Bayliss, David Robinson and an anonymous reviewer for

critical comments on earlier versions of the manuscript.

Stefan Wahl was financially supported by the Swiss

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Root tissue structure is linked to ecological strategies of grasses

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