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Root System Architecture and Gravitropism in the Oil Palm

C H R I S T O P H E J O U R D A N *{, N I C O L E M I C H A U X - F E R R I E RE{ and GE R A L D P E R B A L}

{Departement des Cultures Perennes, Centre de Cooperation Internationale en Recherche Agronomique pour le

Developpement (C.I.R.A.D.), TA 80/01, Avenue Agropolis, F-34398 Montpellier cedex 05, France,

{Laboratoire d'Histo-Cytologie (BIOTROP), Centre de Cooperation Internationale en Recherche Agronomique pour

le Developpement (C.I.R.A.D.), TA 40/03, Avenue Agropolis, F-34398 Montpellier cedex 05, France and

}Universite Pierre et Marie Curie, Laboratoire CEMV, 4 place Jussieu, F-75252 Paris cedex 05, France

Received: 4 November 1999 Returned for revision: 26 January 2000 Accepted: 27 February 2000

The oil palm (Elaeis guineensis Jacq.) has a root system consisting of primary (or order 1) roots, which are eitherorthogravitropic (R1 VD, with positive gravitropism) or diagravitropic (R1 H). Their statenchyma have very similarcharacteristics (mainly vacuolated, large cells). However, their statoliths sediment along the longitudinal wall in R1 H

and along the distal wall in R1 VD (furthest cell wall from the apical meristem, opposite the proximal wall). Order2 roots may have vertical upward (R2 VU) or downward growth (R2 VD) or even horizontal growth (R2 H). In allcases, the statoliths are located near the lower wall of the statocyte (distal in R2 VD, proximal in R2 VU andlongitudinal in R2 H). Order 3 roots are usually agravitropic. When they grow upwards, R3 VU, their amyloplasts arelocated near the proximal wall. Likewise, the growth direction of R4 varies, but they have little or no statolithsedimentation. Roots with marked gravitropism (positive or negative) have amyloplasts that can sediment alongdierent walls. But, irrespective of amyloplast position in the statocytes, the direction of root growth may be stable.The relation between the dierent reactions of roots and dierent sensitivity to auxin or to a curvature-halting signalis discussed. # 2000 Annals of Botany Company

Key words: Elaeis guineensis Jacq., gravitropism, oil palm, root architecture, statoliths.

I N T R O D U C T I O N

The architecture of a plant's root system has a direct

inuence on numerous functions carried out by the roots.

Many authors have shown a close relationship between root

architecture, especially the branching pattern, and anchor-

ing in the soil (Coutts, 1983; Fitter, 1986; Ennos et al., 1993;

Stokes et al., 1996), and also between root architecture and

the acquisition of water and mineral resources from the soil

(Barley, 1970; Bosc and Maertens, 1981; Hamblin and

Tennant, 1987; Habib et al., 1991; Sattelmacher et al., 1993).

Several dierentiation levels exist within root systems and,

based on this concept of heterorhizy, introduced rst by

Tschirch (1905) for herbaceous species and applied soon

after to woody species (Noelle, 1910), many authors have

categorized roots according to (1) their function, i.e.

`anchorage roots' and `feeding roots' (Kubikova, 1967);

(2) their size, i.e. `long roots' and `short roots' (Wilcox,

1964); or (3) their anatomical characteristics, i.e. `woody

roots' and `non-woody roots' (Lyford and Wilson, 1964).

These classications emphasized two dierent types of

roots: thick polyarch roots with potential for longitudinal

and radial growth called `macrorhizae' and thin diarch

roots of determined longitudinal and radial growth called

`brachyrhizae' (Jenik and Sen, 1964). Macrorhizae are either

orthotropic or plagiotropic (Kahn, 1977) and are specialized

in conduction (Lyford and Wilson, 1964; Kubikova, 1967)

whereas brachyrhizae are essentially plagiotropic (Kahn,

1977) and are specialized in uptake (Lyford and Wilson,1964; Kubikova, 1967).

The root architecture of plants can be then understood

using architectural analysis developed for the aerial part of

tropical trees (Halle and Oldeman, 1970), which is based on

studying how the meristems of each axis function (growth

and branching processes, direction of growth, deciduous-

ness, diameter, growth rate, etc.) and how hierarchical

relations are established between these axes. Such an

analysis can be used to categorize roots with a similar

structure and behaviour, especially those having the same

direction of growth. Analysis of the oil palm (Elaeis

guineensis Jacq.) root system was carried out using this

method (Jourdan and Rey, 1997). It revealed the existence

of four branching orders and eight root types: two types of

primary roots, three types of secondary roots, two types of

tertiary roots and one type of quaternary root. Primary and

secondary roots could be considered as macrorhizae

whereas tertiary and quaternary roots could be considered

as brachyrhizae (Jourdan and Rey, 1997).

Field observations showed that roots could grow

vertically, either upwards or downwards, horizontally, or

without any specic direction in relation to gravity. In the

oil palm root system, all root types maintain the same

direction of growth throughout their life span, and

branching angles are always very close to 908, irrespectiveof topological order. Given these characteristics, this root

system has a highly specic spatial distribution that aords

Annals of Botany 85: 861868, 2000

doi:10.1006/anbo.2000.1148, available online at http://www.idealibrary.com on

0305-7364/00/060861+08 $35.00/00 # 2000 Annals of Botany Company

* For correspondence. Fax 33 467616590, e-mail [email protected]


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it colonization of the soil horizons between 0 and 6 m deep(Jourdan, 1995).

In some cases, the direction of root growth is more or lessdetermined at the time of emergence, e.g. the plagiotropic

lateral roots of the cocoa tree (Dyanat-Nejad and Neville,1972a, b), however, it can also be modied by environmen-

tal conditions, such as light (Lake and Slack, 1961; Mandoliet al., 1984; Horwitz and Zur, 1991), temperature (Mosherand Miller, 1972; Pahlavanian and Silk, 1988; Horwitz andZur, 1991), pH (Gabella and Pilet, 1978), oxygen avail-

ability (Rufelt, 1957; Bejaoui and Pilet, 1977), and soilmatric potential or structure (Coutts, 1989). The directionof root growth in the soil thus results from the combined

eects of various environmental factors, one of which isgravity.

The site of gravity perception is located in the centre ofthe root cap (Gibbons and Wilkins, 1970; Volkmann and

Sievers, 1979; Jackson and Barlow, 1981; Moore and Evans,1986). The cells responsible for graviperception form the

statenchyma and are called statocytes. They possess largeamyloplasts (statoliths) which are able to move under theinuence of gravity (Audus, 1962; Perbal, 1971; Sievers and

Volkmann, 1979; Sack, 1991). These organelles may act bycreating tensions within the actin network of the statocytes(Sievers et al., 1991; Volkmann et al., 1991; Perbal et al.,1997), which may then activate stretch ion channels (Pickard

and Ding, 1992).However, mutants of Arabidopsis thaliana, with starch-

free plastids, are still able to respond to a gravitropicstimulus (Caspar and Pickard, 1989; Kiss et al., 1989). It

might therefore be that the whole protoplasm directlyactivates the ion channels, or acts on integrins (Wayne et al.,

1992).The mechanism of gravitropic reaction has been exten-

sively studied on the primary roots of simple models such asyoung seedlings, and it now seems necessary to analyse

more complex models, such as root systems where rootsshow a range of gravitropic behaviours, and to examinetheir statolith apparatus at the same time. In fact, the verysimple models which have usually been used have provided

an incomplete understanding of the reality of gravitropicbehaviour (Firn and Digby, 1997).

In this article, after presenting results of the architecturalanalysis for the oil palm root system, we characterize the

statenchyma which were observed in the various roots ofthis perennial monocotyledon in order to determine howstatoliths inuence the direction of root growth.

M A T E R I A L S A N D M E T H O D S

Material, study site and terminology

The plant material used in this study belonged to theC1001F `family' (Jourdan, 1995) commonly used in estateplantings. Our eld investigations were carried out at the La

Me experimental research station in south-eastern Co ted'Ivoire. The humid subtropical climate with marked

seasons is characterized by (1) average annual rainfall of1400 mm with a 380 mm year1 water decit; (2) averagetemperatures of between 24 and 288C; and (3) around

1800 h of sunshine per year. The soil, made of loamy-sand

detrital formations dominated by coarse sand (Hartmann,

1991), is quite deep and uniform with neither apparent

interruptions nor constraints to a depth of at least 6 m.

The study techniques are based on partial or total root

system excavations for the `static analysis' and on miniature

root-growth chambers or `eld rhizotrons' for the `dynamicanalysis'. See Jourdan and Rey (1997) for further details.

The oil palm root system is of the fasciculate type, or the

adventitious type VII (centralized uniformal root system)

according to Cannon's (1949) classication, or the plagio-

tropic secondary type as dened by Kahn (1977, 1983).

Jenik (1978) classied it in the category of `root system with

axes lacking secondary thickening', which is a dominant

characteristic of monocotyledon plant roots. The primary

root aborts shortly after emerging from the seed and the

entire root system is considered an adventitious system

(Clowes, 1961).

After the transient juvenile phase (approx. 1 year long) innursery bags, palms were transplanted directly in the soil

where many new roots were emitted on the periphery of the

root-soil plate. In adult palms (10 years old), several

thousand roots emerge from the bole located beneath the

stem. These roots are categorized as primary roots (Purvis,

1956; Ruer, 1967, 1968), and are roots of order 1. By

convention, we shall call them R1. They branch, and the

roots borne by them are order 2 roots, called R2. These

bear order 3 roots, or tertiary roots, called R3. They in turn

bear quaternary roots, called R4, which do not branch.

Architectural analysis approach

Our study was based on the concepts developed in aerial

plant architecture (Halle and Oldeman, 1970; Edelin, 1977,

1984; Halle et al., 1978; Barthe le my et al., 1989, 1991).

The principle of root system architectural analysis is

based on observing and characterizing the methods of

growth, branching and morphological dierentiation in the

dierent axes at dierent stages of development (Atger,

1992). Architectural analysis involves three basic phases: (1)

identication and characterization of the dierent elements

making up the system; (2) characterization of the relative

layout of the dierent axes, along with their hierarchicalrelationship; and (3) characterization of the sequence in

which the dierent components of the system appear, along

with how they develop.

However, several types of roots belonging to the same

branching order have been identied in the oil palm (Purvis,

1956; Ruer, 1968). Thus, it proved necessary to have a root

typology, in order to characterize as clearly as possible the

dierent groups of roots making up the root system. The

typology is based on morphological criteria: shape, length,

diameter, axis colour, branching pattern, edication

sequence over time, branching angle and spatial layout.

Juvenile root architecture of young palms in a nurseryhas been analysed previously (Jourdan and Rey, 1997), and

is not discussed here.

862 Jourdan et al.Root Architecture and Gravitropism


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Histology

Samples corresponding to all types of roots identied bythe architectural analysis were xed in the eld in a 2 %glutaraldehyde and 2 % paraformaldehyde solution in aphosphate buer (0.2 M, pH 7.2), to which 1 % caeinewas added to precipitate the oxidated polyphenols in situ.

After gradual dehydration by passing through alcohol bathsof increasing concentration, up to absolute alcohol, thenembedding in Technovit 7100 resin (Labonord), they werecut in 3 mm sections with a LKB Historange microtome.

The sections were successively stained with PAS reagent( periodic acid Schi), which stained polysaccharides red(walls and starch), and with naphthol blue-black, whichspecically coloured soluble and non-soluble proteins blue

(Fisher, 1968).The measurements and counts carried out on the

statenchyma of the dierent root types were performed on15 sections for each root (ten roots for each root type) using

computer assisted image analysis (Optilab, Graftec).

R E SU L T S

Root architecture analysis

The characteristics of the root architecture unit in the adult

oil palm (Jourdan and Rey, 1997) are summarized inTable 1 and illustrated in Fig. 1. Two types of order 1 rootscan be found: R1 VD with vertical downward growth andR1 H with horizontal growth, both with a mean diameter

of 57 mm and a length of up to several metres. R1 VDbear order 2 roots around their circumference, all of which

grow horizontally (R2 H). As for R1 H, they bear eitherascending (R2 VU) or descending (R2 VD) order 2 roots.These two specic secondary root growth directions givethe R1 H a bilateral symmetry. Such horizontally growing

plagiotropic axes can be qualied as diagravitropic axes(Larsen, 1962). Spot observations in the eld showed that ifthe direction of growth of R1 H is modied, they resumetheir original direction of growth, irrespective of the type or

direction of the deviation.R2 H, which are short (under 50 cm), with denite

growth, have a mean diameter of 1.5 mm, show littlebranching and have radial symmetry. They maintain agenerally horizontal direction of growth, although it is not

as strict as that of R1 H; they are diagravitropic. R2 VD and

VU have a mean diameter of 2 mm, indenite growth

and are both orthogravitropic (either positive or negative,

respectively). Some R2 VU can change direction when they

reach the surface, assuming horizontal growth. R2 VU are

more branched than R2 VD probably because they grow in

the topsoil horizon, known to be rich in organic matter andnutrients.

Order 3 roots located deep down (dR3) show little

branching, whereas those formed near the surface (sR3) are

highly branched. These two types of R3 have radial

symmetry, a small mean diameter (1 mm), are very short

(10 to 20 cm) and have denite growth, though there is no

predominant direction of growth; they are agravitropic.

Order 3 roots all bear identical order 4 roots which have

a small diameter (0.5 mm) and are very short (1.5 cm) with

denite and agravitropic growth.

In oil palm, the direction of root growth is a major root

typological criterion. It is therefore important to considerthe performance of statoliths in each dierent case.

R2 H

R1 VD R2 VD

R4

dR3

R1 H

Ground

sR3 R2VU

F IG . 1. Diagram of an adult oil palm root system showing the dierenttypes of roots observed. R1 VD, Primary roots with downward verticalgrowth; R1 H, primary roots with horizontal growth; R2 VD,secondary roots with downward vertical growth; R2 VU, secondaryroots with upward vertical growth; R2 H, secondary roots withgenerally horizontal growth; sR3, supercial tertiary roots; dR3, deep-

lying tertiary roots; R4, quaternary roots.

TA B L E 1. Oil-palm root architecture unit

Root type Woody axis Gravitropism Mean diameter (mm) Growth Maximum length (m) Symmetry

R1 VD W $ 5.3 + 0.7 (n 91) I 6.0* RR1 H W 34 6.3 + 1.0 (n 94) I 25.0 BR2 VU W % 1.8 + 0.5 (n 98) I 2.0 RR2 VD W $ 2.3 + 0.8 (n 96) I 6.0* RR2 H W 34 1.5 + 0.4 (n 95) D 0.5 RsR3 NW * 1.0 + 0.3 (n 36) D 0.2 RdR3 NW * 1.0 + 0.3 (n 36) D 0.1 RR4 NW * 0.5 + 0.1 (n 43) D 0.015 R

W, Woody; NW, non-woody;$, positive orthogravitropic; 34, diagravitropic;%, negative orthogravitropic; *, agravitropic; n, number ofobserved roots; I, indenite growth; D, denite growth; *, maximum observed value; R, radial symmetry; B, bilateral symmetry.

Jourdan et al.Root Architecture and Gravitropism 863


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Anatomical analysis

Figure 2 species the terms used in the statenchyma study.Figures 3 and 4 illustrate the cytological aspect of thestatenchyma and the position of the statoliths for each roottype. A morphometric analysis of the statenchyma is shownin Table 2, which also indicates the percentage of vacuo-

lation, the mean area of the statocytes, the mean number ofstatoliths per statocyte and the mean diameter of thestatoliths.

If the dimensions and cytological characteristics of the

statocytes were considered, oil palm roots could be groupedinto three categories:

(1) The rst comprised R1 VD and R1 H, whose statocyteswere very large and highly vacuolated. On average, theycontained from nine to 13 statoliths in section. For R1VD (Fig 3A and B), growth (G) was in the direction of

gravity (g) and the statoliths were located near the distalwall. The nuclei of the statocytes contained very

marked nucleoli and were located near the proximalwall. The R1 H (Fig. 3C and D) grew horizontally,hence at 908 to gravity. The statoliths accumulated

along the longitudinal wall, whereas the nucleus waslocated towards the proximal wall. This sedimentationwas total in the well-dierentiated cells of the statench-

yma. It occurred gradually in the ten or so cell layersoccurring between the meristem and the statenchyma.

(2) R2 VD, along with the R2 VU and sR3 (VU) formed asecond category. The statenchyma cells had a surface

area half that of the rst category, with little vacuo-lation. The number of statoliths, amounting to six

seven per cell on average in section, was smaller. For R2VD (Fig. 3E and F), the direction of growth was in linewith the direction of gravity and, as for R1 VD, thestatoliths accumulated along the distal wall, and as

usual the nucleus was near the proximal wall. R2 VU(Fig. 4A and B) and sR3 (VU) (Fig. 4C and D) had adirection of growth (G) opposite to that of gravitropism(g). In both these types of roots, the statoliths and alsothe nucleus were near the proximal wall.

(3) Quaternary roots (R4) made up the third category(Fig. 4E). These roots had the same characteristics asjuvenile R2 (Fig. 4F), which are unbranched R2,observed exclusively on young oil palms in the nursery

and are morphologically identical to R4. The statench-yma cells were very small with very little vacuolation;they contained two to four statoliths on average, which

did not show any preferential position. The diameter of

statoliths observed in the statenchyma of the variousroot types was almost constant (Table 2) at between 2

and 3 mm, except in juvenile R2, which were stilldeveloping.

Thus, in oil palm, the horizontal roots and those withmarked ( positive or negative) gravitropism have amylo-plasts that always sediment under the eect of gravity. Aconsistent direction of growth with respect to gravity can be

obtained irrespective of the position of the amyloplasts inthe statocytes. They accumulate against the distal wall in R1VD and R2 VD, against the longitudinal wall in R1 H andagainst the proximal wall in R2 VU and sR3 (VU).

D I S C U S S I O N

The macrorhizae of the oil palm (R1, R2) are eitherorthogravitropic (growth in the direction of gravity) orstrongly diagravitropic (growth perpendicular to gravity).

All these graviresponsive roots, irrespective of their directionof growth, have a statenchyma with statoliths sedimentingunder the eect of gravity, whereas the agravitropic R4 rootsdo not. These results are in agreement with the statolith

theory (Volkmann and Sievers, 1979). A stable direction ofgrowth can be established either downward, upward orhorizontally with the amyloplasts sedimenting on the distal,proximal or longitudinal cell walls. This could be because

amyloplasts act as ballasts (Wayne and Staves, 1996) and

their sedimentation has no physiological eect. Ourmorphometric analysis of the statocytes shows that there isa relation between the number of statoliths (the volume of

Proximalcell wall

Longitudinal

cell wall

Distalcell wall

g

statocytec

am s

n

F I G . 2. Location of statocytes in the root and denition of the termsused. am, Apical meristem; c, root cap; g, direction of gravity;

n, nucleus; s, statolith.

TA B L E 2. Anatomical characteristics of the statenchyma in dierent types of oil palm roots

R1 VD R1 H R2 VD R2 VU sR3 (VU)* R4 Juvenile R2

% Vacuolation of statenchyma 37.6 + 4.30 32.9 + 3.78 15.2 + 1.49 13.9 + 1.36 9.5 + 0.78 6.3 + 0.45 3.3 + 0.24Statocyte mean length (mm) 30.9 + 5.40 30.9 + 3.28 22.1 + 2.92 23.7 + 1.92 19.3 + 4.59 11.5 + 3.84 8.7 + 1.76Statocyte mean width (mm) 21.5 + 4.11 24.1 + 3.05 16.8 + 2.18 15.7 + 3.05 12.8 + 1.77 8.3 + 1.98 6.2 + 1.41Statocyte mean area (mm2) 670 + 200 747 + 128 367 + 36.6 373 + 81.0 248 + 75.3 102 + 62.3 56 + 21.2Mean number of statoliths/statocyte 9.2 + 4.79 13.1 + 4.72 7.0 + 3.24 7.3 + 2.80 6.2 + 2.62 3.8 + 2.02 1.7 + 0.71Statoliths mean diameter (mm) 2.8 + 0.77 2.9 + 0.66 2.6 + 0.40 2.9 + 0.47 2.3 + 0.41 1.8 + 0.40 0.6 + 0.08

Values are means + s.e.; n 10 to 47. Measurements were made on several sections (in 2 dimensions) of each root type. *, The sR3 rootobserved in situ was upwardly oriented; although it is agravitropic, we noted it sR3 (VU).



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which is nearly constant) in the statocytes and their ability to

perceive gravity. In R1, the statocytes possess nine13

amyloplasts whereas those of the R2 or R3 have fewer

statoliths (sixseven). R4 which are agravitropic possessvery few statoliths which do not sediment. In these roots, the

protoplast and the amyloplasts may not be suciently heavy

to induce a gravistimulus. In any case, our results show

that the direction of growth cannot be determined by the

direction of movement of amyloplasts.

A negative or a positive response of the roots may nottherefore depend upon the perception mechanism, but

could be linked to a dierent sensitivity to auxin which,

F IG . 3. Histology of the statenchyma in dierent types of oil palm roots. g, Direction of gravity; G, direction of growth; n, nucleus; s, statolith.A, C, E: 1 cm 25 mm; B, D, F: 1 cm 10 mm. A and B, Root with downward vertical growth, of order 1 (R1 VD); C and D, root with

horizontal growth, order 1 (R1 H); E and F, root with downward vertical growth, of order 2 (R2 VD).



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through dierential redistribution, causes curvature

(Dolan, 1998; Pilet, 1998). Roots with negative gravitrop-ism (R2 VU) could therefore react like stems or coleoptiles

(Cosgrove, 1997; Edelmann, 1997).

The stability in the direction of growth for any type of

root could result from a combination of two eects. The rstwould seem to be of internal origin and inherent to each of

the root types within which each root has a xed initial

FI G . 4. Histology of the statenchyma in some oil palm root types. g, Direction of gravity; G, direction of growth; n, nucleus; s, statolith. A and C:1 cm 25mm; B, D, E, F: 1 cm 10mm. A and B, Root with upward vertical growth, of order 2 (R2 VU); C and D, surface root with upward

vertical growth, of order 3 (sR3 VU); E, order 4 root (R4); F, juvenile order 2 root (R2 Y).



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direction of growth (Dyanat-Nejad and Neville, 1972b). Thesecond would seem to be more of external origin, linked toenvironmental conditions in the vicinity of the roots. Forinstance, in the case of supercial lateral roots of the sitka

spruce or lodgepole pine, Coutts and Nicoll (1991) showedthat they were diagravitropic, with initial upward growth,

but as these roots approached the soil surface theyresponded to some signal from the environment (probablylight), that caused a downward deection, and thus rootstended to grow horizontally. A similar hypothesis has been

proposed by Firn and Digby (1997) which states that organspossess a mechanism which allows them to attain a stablegravitropic position at a given angle and that each organ has

a characteristic gravitropic set-point angle (GSA). But theGSA can be developmentally changed or regulated byenvironmental factors.

In their recent review, Hemmersbach et al. (1999) showed

that in view of the physical nature of gravity, the stimulusmust interact with the mass (by inducing a primary physical

reaction such as sedimentation). As gravity is a weak force,such physical energy must be used by a receptor and lateramplied. The nature of the mechanoreceptor is unknown

but could be stretch ion channels (Pickard and Ding, 1992)or integrins (Wayne et al., 1992).

If one assumes that gravireceptors are preferentiallylocated along certain walls, stable horizontal growth

(e.g. R1 H roots) could be linked to an absence of sensorsalong the longitudinal wall of the statocyte, whilst verticalgrowth (e.g. R2 VD, R2 VU) could be linked to an absenceof sensors along the transversal walls (proximal or distal).

The GSA, therefore, should be determined by the locationof the gravisensors along (or on) the plasma membrane,

and the stable direction of growth should be attained whenthe statoliths or the cell can no longer exert an action onthese gravisensors. This hypothesis is consistent with thefact that gravisensitivity is mostly located at both ends of

the characean internodal cells (Wayne and Staves, 1996).Molecular characterization would make it possible to locatethese receptors and thus validate this hypothesis. The factthat environmental factors can change the GSA may be

because they aect the distribution of receptors within thecell.

A C K N O W L E D G E M E N T SWe thank the Centre National de Recherche Agronomique(CNRA) for access to the eld experiments at La Me , IvoryCoast. Travel expenses and nancial support for this work

were covered by the Tree Crop Department of the Centre deCoope ration Internationale en Recherche Agronomiquepour le De veloppement (CIRAD).

L I T E R A T U R E C I T E D

Atger C. 1992. Essai sur l'architecture racinaire des arbres. PhD Thesis.Universite Montpellier II, France.

Audus LJ. 1962. The mechanism of the perception of gravity by plants.

Symposium of the Society for Experimental Biology 16: 197226.Barley KP. 1970. The conguration of the root system in relation to

nutrient uptake. Advanced Agronomy 22: 159201.

Barthe le my D, Edelin C, Halle F. 1989. Architectural concepts fortropical trees. In: Holm-Nielsen LB, Nielsen I, Baslev H, eds.Tropical forests: botanical dynamics, speciation and diversity.London: Academic Press, 89100.

Barthe le my D, Edelin C, Halle F. 1991. Canopy architecture. In:Raghavendra AS, ed. Physiology of trees. New York: Wiley &Sons Inc., 120.

Bejaoui M, Pilet PE. 1977. Oxygen uptake of growing and geo-stimulated roots. Plant Science Letters 8: 223226.

Bosc M, Maertens C. 1981. Ro le de l'accroissement du syste meracinaire dans l'absorption de divers e tats du potassium du sol.Agrochemica 25: 18.

Cannon WA. 1949. A tentative classication of root systems. Ecology30: 542548.

Caspar T, Pickard BG. 1989. Gravitropism in a starchless mutant ofArabidobsis. Planta 177: 185197.

Clowes FAL. 1961. Apical meristems. Oxford: Blackwell.

Cosgrove DJ. 1997. Cellular mechanism underlying growth asymmetryduring stem gravitropism. Planta 203: 130135.

Coutts MP. 1983. Root architecture and tree stability. Plant and Soil71: 171188.

Coutts MP. 1989. Factors aecting the direction of growth of treeroots. In: Dreyer E, Aussenac G, Bonnet-Masimbert M,

Dizengremel P, Favre JM, Garrec JP, Le Tacon F, Martin F,eds. Forest tree physiology. Paris: Elsevier, 227287.

Coutts MP, Nicoll BC. 1991. Orientation of lateral roots of trees. I.Upward growth of surface roots and de ection near the soilsurface. New Phytologist 119: 227234.

Dolan L. 1998. Pointing roots in the right direction: the role of auxintransport in response to gravity. Genes and Development 12:20912095.

Dyanat-Nejad H, Neville P. 1972a. Etude expe rimentale de l'initiationet de la croissance des racines late rales pre coces du cacaoyer(Theobroma cacao L.). Annales des Sciences Naturelles, Botanique13: 211246.

Dyanat-Nejad H, Neville P. 1972b. Sur le mode d'action du me riste meradical orthotrope sur le contro le de la plagiotropie des racineslate rales chez Theobroma cacao L. Revue Generale de Botanique 79:

319340.Edelin C. 1977. Images de l'architecture des coniferes. PhD Thesis.

Universite Montpellier II, France.

Edelin C. 1984. L'architecture monopodiale: l'exemple de quelquesarbres d'Asie tropicale. The se d'Etat. Universite Montpellier II,France.

Edelmann HG. 1997. Gravistimulated asymmetrics in the outerepidermal cell walls of graviresponding coleoptiles. Planta 203:123129.

Ennos AR, Crook MJ, Grimshaw C. 1993. The anchorage mechanics ofmaize, Zea mays. Journal of Experimental Botany 44: 147153.

Firn RD, Digby J. 1997. Solving the puzzle of gravitropismhas a lostpiece been found?. Planta 203: S159S163.

Fisher DB. 1968. Protein staining of ribboned epon section for lightmicroscopy. Histochemie 16: 9296.

Fitter AH. 1986. The topology and geometry of plant root systems:inuence of watering rate on root system topology in Trifoliumpratense. Annals of Botany 58: 91101.

Gabella M, Pilet PE. 1978. Eects of pH on georeaction andelongation of maize root segments. Physiologia Plantarum 44:157160.

Gibbons GSB, Wilkins MB. 1970. Growth inhibitor production by rootcaps in relation to geotropic responses. Nature 226: 558559.

Habib R, Page s L, Jordan MO, Simonneau T, Se billotte M. 1991.Approche a l'e chelle du syste me racinaire de l'absorption hydro-mine rale. Conse quences en matie re de mode lisation. Agronomie11: 623643.

Halle F, Oldeman RAA. 1970. Essai sur l'architecture des arbres et ladynamique de croissance des arbres tropicaux. Paris: Masson.

Halle F, Oldeman RAA, Tomlinson PB. 1978. Tropical trees and forests.An architectural analysis. Berlin: Springer-Verlag.

Hamblin A, Tennant D. 1987. Root length density and water uptake incereals and grain legumes: How well are they correlated?.Australian Journal of Agriculture Research 38: 513527.



8/8

Hartmann C. 1991. Evolution et comportement hydrique des sols sablo-argileux ferrallitiques sous culture de palmiers a huile. Cas de la

plantation R. Michaux a Dabou (Cote d'Ivoire). PhD Thesis.Universite Paris VI, France.

Hemmersbach R, Volkmann D, Ha der DP. 1999. Graviorientation inprotists and plants. Journal of Plant Physiology 154: 115.

Horwitz BA, Zur B. 1991. Gravitropic response of primary maizerootlets as inuenced by light and temperature. Plant, Cell andEnvironment 14: 619623.

Jackson MB, Barlow PW. 1981. Root geotropism and the role ofgrowth regulators from the cap: a re-examination. Plant, Cell andEnvironment 4: 107123.

Jenik J. 1978. Roots and root systems in tropical trees: morphologicand ecologic aspects. In: Tomlinson PB, Zimmermann MH, eds.Tropical trees as living systems. Cambridge: Cambridge UniversityPress, 323349.

Jenik J, Sen DN. 1964. Morphology of root systems in trees: aproposal for terminology. Tenth International Botanical Congress,Edinburgh. Abstracts, 393394.

Jourdan C. 1995. Modelisation de l'architecture et du developpement dusysteme racinaire du palmier a huile. PhD Thesis. UniversiteMontpellier II, France.

Jourdan C, Rey H. 1997. Architecture and development of the oil-palm

(Elaeis guineensis Jacq.) root system. Plant and Soil 189: 3348.Kahn F. 1977. Analyse structurale des syste mes racinaires des plantesligneuses de la foret tropicale dense humide. Candollea 32:321358.

Kahn F. 1983. Architecture comparee des forets tropicales humides etdynamique de la rhizosphere. The se d'Etat, Universite MontpellierII, France.

Kiss JZ, Hertel R, Sack FD. 1989. Amyloplasts are necessary for fullgravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177:198206.

Kubikova J. 1967. Contribution to the classication of root systems ofwoody plants. Preslia Prague 39: 236243.

Lake JV, Slack G. 1961. Dependence on light of geotropism in plantroots. Nature 191: 300302.

Larsen P. 1962. Geotropism an introduction. In: Rudhland W, ed.Encyclopdia of plant physiology, Vol. 17. Berlin: Springer Verlag,

3473.Lyford WH, Wilson BF. 1964. Development of the root system of Acer

rubrum L. Harvard Forest Paper 10: 117.Mandoli DF, Tepperman J, Huala E, Briggs WR. 1984. Photobiology

of diagravitropic maize roots. Plant Physiology 75: 359363.Moore R, Evans ML. 1986. How roots perceive and respond to gravity.

American Journal of Botany 73: 574587.Mosher PN, Miller MH. 1972. Inuence of soil temperature on the

geotropic response of corn roots (Zea mays L.). Agronomy Journal64: 459462.

Noelle W. 1910. Studien zur vergleichenden Anatomie und Morpho-logie der Koniferenwurzeln mit Ru cksicht die Systematik.Botanische Zeitung 68: 169266.

Pahlavanian AM, Silk WK. 1988. Eect of temperature on spatial andtemporal aspects of growth in the primary maize root. Plant

Physiology 87: 529532.Perbal G. 1971. Action de la pesanteur sur la re partition des organitesdans les cellules axiales centrales (statenchyme) de la coie du

Lens caulinaris L. Comptes Rendus de l'Academie des Sciences,Serie D 273: 789792.

Perbal G, Driss-Ecole D, Tewinkel M, Volkmann D. 1997. Statocytepolarity and gravisensitivity in seedling roots grown in micro-gravity. Planta 203: S57S62.

Pickard BG, Ding JP. 1992. Gravity sensing in higher plants. Advancesin Compartmental and Environmental Physiology 10: 81110.

Pilet PE. 1998. Applied indol-3yl-acetic acid on the cap and auxinmovements in gravireacting maize roots. Journal of PlantPhysiology 152: 135138.

Purvis C. 1956. The root system of the oil palm: its distribution,morphology and anatomy. Journal of West African Institute of OilPalm Research 1: 6082.

Ruer P. 1967. Morphologie et anatomie du syste me radiculaire dupalmier a huile. Oleagineux 22: 595599.

Ruer P. 1968. Contribution a l'etude du systeme racinaire du palmier ahuile. The se Docteur Inge nieur I.R.H.O. Faculte des Sciences deParis, France.

Rufelt H. 1957. Inuence of the composition of the nutrient solutionon the geotropic reactions of wheat roots. Physiologia Plantarum10: 373396.

Sack FD. 1991. Plant gravity sensing. International Review of Cytology127: 193252.

Sattelmacher B, Gerendas J, Thoms K, Bruck H, Bagdady NH. 1993.Interaction between root growth and mineral nutrition. Environ-mental and Experimental Botany 33: 6373.

Sievers A, Volkmann D. 1979. Gravitropism in single cells. In: HauptW, Feinleib ME, eds. Encyclopedia of plant physiology. New series,vol. 7, Physiology of movements. Berlin: Springer-Verlag, 567572.

Sievers A, Buchen B, Volkmann D, Hejnowicz Z. 1991. Role ofcytoskeleton in gravity perception. In: Lloyd CW, ed. The cyto-skeletal basis of plant growth and form. London: Academic Press,169182.

Stokes A, Ball J, Fitter AH, Brain P, Coutts MP. 1996. An experi-mental investigation of the resistance of model root systems touprooting. Annals of Botany 78: 415421.

Tschirch A. 1905. U ber die heterorhizie bei Dikotyleden. Flora 94:6878.

Volkmann D, Buchen B, Hejnowicz Z, Tewinkel T, Sievers A. 1991.Oriented movement of statoliths studied in a reduced gravita-tional eld during parabolic ights of rockets. Planta 185:153161.

Volkmann D, Sievers A. 1979. Graviperception in multicellular organs.In: Haupt W, Feinleib ME, eds. Encyclopedia of plant physiology.New series, vol. 7, Physiology of movements. Berlin: Springer-Verlag, 573600.

Wayne R, Staves MP. 1996. A down to earth model of gravisensing orNewton's law of gravitation from the apple's perspectives.Physiologia Plantarum 98: 917921.

Wayne R, Staves MP, Leopold AC. 1992. The contribution of theextracellular matrix to gravisensing in characean cells. Journal ofCell Science 101: 611623.

Wilcox HE. 1964. Xylem in the roots of Pinus resinosa Ait. in relation

to heterorhizy and growth activity. In: Zimmermann MH, ed. Theformation of wood in forest trees. New York: Academic Press,459478.


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