Annals of Botany 85: 861868, 2000 doi:10.1006/anbo.2000.1148, available online at http://www.idealibrary.

com on

Root System Architecture and Gravitropism in the Oil Palm

R E { and G E RALD PERBAL} C H R IS TO P HE JO U R D A N * {, N I CO L E MI C H A U X - F E R R I E {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 either orthogravitropic (R1 VD, with positive gravitropism) or diagravitropic (R1 H). Their statenchyma have very similar characteristics (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). Order 2 roots may have vertical upward (R2 VU) or downward growth (R2 VD) or even horizontal growth (R2 H). In all cases, the statoliths are located near the lower wall of the statocyte (distal in R2 VD, proximal in R2 VU and longitudinal in R2 H). Order 3 roots are usually agravitropic. When they grow upwards, R3 VU, their amyloplasts are located near the proximal wall. Likewise, the growth direction of R4 varies, but they have little or no statolith sedimentation. Roots with marked gravitropism ( positive or negative) have amyloplasts that can sediment along dierent 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 signal # 2000 Annals of Botany Company is discussed. Key words: Elaeis guineensis Jacq., gravitropism, oil palm, root architecture, statoliths.

I N T RO 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 anchoring 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)
* For correspondence. Fax 33 467616590, e-mail jourdan@cirad.fr

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 and Oldeman, 1970), which is based on tropical trees (Halle studying how the meristems of each axis function (growth and branching processes, direction of growth, deciduousness, 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, irrespective of topological order. Given these characteristics, this root system has a highly specic spatial distribution that aords # 2000 Annals of Botany Company

0305-7364/00/060861+08 $35.00/00

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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 `dynamic analysis'. 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 plagiotropic 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) in nursery 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.

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 less determined 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 environmental conditions, such as light (Lake and Slack, 1961; Mandoli et al., 1984; Horwitz and Zur, 1991), temperature (Mosher and Miller, 1972; Pahlavanian and Silk, 1988; Horwitz and Zur, 1991), pH (Gabella and Pilet, 1978), oxygen availability (Rufelt, 1957; Bejaoui and Pilet, 1977), and soil matric potential or structure (Coutts, 1989). The direction of root growth in the soil thus results from the combined eects of various environmental factors, one of which is gravity. The site of gravity perception is located in the centre of the 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 large amyloplasts (statoliths) which are able to move under the inuence of gravity (Audus, 1962; Perbal, 1971; Sievers and Volkmann, 1979; Sack, 1991). These organelles may act by creating 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 starchfree plastids, are still able to respond to a gravitropic stimulus (Caspar and Pickard, 1989; Kiss et al., 1989). It might therefore be that the whole protoplasm directly activates the ion channels, or acts on integrins (Wayne et al., 1992). The mechanism of gravitropic reaction has been extensively studied on the primary roots of simple models such as young seedlings, and it now seems necessary to analyse more complex models, such as root systems where roots show a range of gravitropic behaviours, and to examine their statolith apparatus at the same time. In fact, the very simple models which have usually been used have provided an incomplete understanding of the reality of gravitropic behaviour (Firn and Digby, 1997). In this article, after presenting results of the architectural analysis for the oil palm root system, we characterize the statenchyma which were observed in the various roots of this perennial monocotyledon in order to determine how statoliths inuence the direction of root growth. M AT 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 the C1001F `family' (Jourdan, 1995) commonly used in estate plantings. Our eld investigations were carried out at the La experimental research station in south-eastern Co Me te d'Ivoire. The humid subtropical climate with marked seasons is characterized by (1) average annual rainfall of 1400 mm with a 380 mm year 1 water decit; (2) average temperatures of between 24 and 288C; and (3) around

Architectural analysis approach Our study was based on the concepts developed in aerial and Oldeman, 1970; Edelin, 1977, plant architecture (Halle et al., 1978; Barthe le my et al., 1989, 1991). 1984; Halle 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 hierarchical relationship; 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 nursery has been analysed previously (Jourdan and Rey, 1997), and is not discussed here.

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Histology Samples corresponding to all types of roots identied by the architectural analysis were xed in the eld in a 2 % glutaraldehyde and 2 % paraformaldehyde solution in a phosphate buer (0.2 M, pH 7.2), to which 1 % caeine was added to precipitate the oxidated polyphenols in situ. After gradual dehydration by passing through alcohol baths of increasing concentration, up to absolute alcohol, then embedding in Technovit 7100 resin (Labonord), they were cut 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, which specically 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 on 15 sections for each root (ten roots for each root type) using computer assisted image analysis (Optilab, Graftec). R E S U LT S Root architecture analysis The characteristics of the root architecture unit in the adult oil palm (Jourdan and Rey, 1997) are summarized in Table 1 and illustrated in Fig. 1. Two types of order 1 roots can be found: R1 VD with vertical downward growth and R1 H with horizontal growth, both with a mean diameter of 57 mm and a length of up to several metres. R1 VD bear order 2 roots around their circumference, all of which grow horizontally (R2 H). As for R1 H, they bear either ascending (R2 VU) or descending (R2 VD) order 2 roots. These two specic secondary root growth directions give the 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 if the direction of growth of R1 H is modied, they resume their 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 little branching and have radial symmetry. They maintain a generally horizontal direction of growth, although it is not
sR3 R2 VU

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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 and nutrients. 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 consider the performance of statoliths in each dierent case.

Ground R1 H

R2 H

R4

dR3 R1 VD R2 VD

F I G . 1. Diagram of an adult oil palm root system showing the dierent types of roots observed. R1 VD, Primary roots with downward vertical growth; R1 H, primary roots with horizontal growth; R2 VD, secondary roots with downward vertical growth; R2 VU, secondary roots with upward vertical growth; R2 H, secondary roots with generally horizontal growth; sR3, supercial tertiary roots; dR3, deeplying tertiary roots; R4, quaternary roots.

T A B L E 1. Oil-palm root architecture unit

Root type R1 VD R1 H R2 VU R2 VD R2 H sR3 dR3 R4 Woody axis W W W W W NW NW NW Gravitropism $ 3 4 % $ 3 4 Mean diameter (mm) 5.3 + 0.7 6.3 + 1.0 1.8 + 0.5 2.3 + 0.8 1.5 + 0.4 1.0 + 0.3 1.0 + 0.3 0.5 + 0.1 (n (n (n (n (n (n (n (n 91) 94) 98) 96) 95) 36) 36) 43) Growth I I I I D D D D Maximum length (m) 6.0* 25.0 2.0 6.0* 0.5 0.2 0.1 0.015 Symmetry R B R R R R R R

* * *

W, Woody; NW, non-woody; $, positive orthogravitropic; 3 4, diagravitropic; %, negative orthogravitropic; *, agravitropic; n, number of observed roots; I, indenite growth; D, denite growth; *, maximum observed value; R, radial symmetry; B, bilateral symmetry.

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Anatomical analysis

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Figure 2 species the terms used in the statenchyma study. Figures 3 and 4 illustrate the cytological aspect of the statenchyma and the position of the statoliths for each root type. A morphometric analysis of the statenchyma is shown in Table 2, which also indicates the percentage of vacuolation, the mean area of the statocytes, the mean number of statoliths per statocyte and the mean diameter of the statoliths. If the dimensions and cytological characteristics of the statocytes were considered, oil palm roots could be grouped into three categories: (1) The rst comprised R1 VD and R1 H, whose statocytes were very large and highly vacuolated. On average, they contained from nine to 13 statoliths in section. For R1 VD (Fig 3A and B), growth (G) was in the direction of gravity (g) and the statoliths were located near the distal wall. The nuclei of the statocytes contained very marked nucleoli and were located near the proximal wall. The R1 H (Fig. 3C and D) grew horizontally, hence at 908 to gravity. The statoliths accumulated along the longitudinal wall, whereas the nucleus was located towards the proximal wall. This sedimentation was total in the well-dierentiated cells of the statenchyma. It occurred gradually in the ten or so cell layers occurring between the meristem and the statenchyma. (2) R2 VD, along with the R2 VU and sR3 (VU) formed a second category. The statenchyma cells had a surface area half that of the rst category, with little vacuolation. The number of statoliths, amounting to six seven per cell on average in section, was smaller. For R2 VD (Fig. 3E and F), the direction of growth was in line with the direction of gravity and, as for R1 VD, the statoliths 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 a direction of growth (G) opposite to that of gravitropism (g). In both these types of roots, the statoliths and also the nucleus were near the proximal wall. (3) Quaternary roots (R4) made up the third category (Fig. 4E). These roots had the same characteristics as juvenile R2 (Fig. 4F), which are unbranched R2, observed exclusively on young oil palms in the nursery and are morphologically identical to R4. The statenchyma cells were very small with very little vacuolation; they contained two to four statoliths on average, which

g n am c statocyte s

Proximal cell wall Longitudinal cell wall Distal cell wall

F I G . 2. Location of statocytes in the root and denition of the terms used. am, Apical meristem; c, root cap; g, direction of gravity; n, nucleus; s, statolith.

did not show any preferential position. The diameter of statoliths observed in the statenchyma of the various root types was almost constant (Table 2) at between 2 and 3 mm, except in juvenile R2, which were still developing. Thus, in oil palm, the horizontal roots and those with marked ( positive or negative) gravitropism have amyloplasts that always sediment under the eect of gravity. A consistent direction of growth with respect to gravity can be obtained irrespective of the position of the amyloplasts in the statocytes. They accumulate against the distal wall in R1 VD and R2 VD, against the longitudinal wall in R1 H and against the proximal wall in R2 VU and sR3 (VU). DISCUSSION The macrorhizae of the oil palm (R1, R2) are either orthogravitropic (growth in the direction of gravity) or strongly diagravitropic (growth perpendicular to gravity). All these graviresponsive roots, irrespective of their direction of growth, have a statenchyma with statoliths sedimenting under the eect of gravity, whereas the agravitropic R4 roots do not. These results are in agreement with the statolith theory (Volkmann and Sievers, 1979). A stable direction of growth can be established either downward, upward or horizontally 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. Our morphometric analysis of the statocytes shows that there is a relation between the number of statoliths (the volume of

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

R1 VD % Vacuolation of statenchyma Statocyte mean length (mm) Statocyte mean width (mm) Statocyte mean area (mm2) Mean number of statoliths/statocyte Statoliths mean diameter (mm) 37.6 + 4.30 30.9 + 5.40 21.5 + 4.11 670 + 200 9.2 + 4.79 2.8 + 0.77 R1 H 32.9 + 3.78 30.9 + 3.28 24.1 + 3.05 747 + 128 13.1 + 4.72 2.9 + 0.66 R2 VD 15.2 + 1.49 22.1 + 2.92 16.8 + 2.18 367 + 36.6 7.0 + 3.24 2.6 + 0.40 R2 VU 13.9 + 1.36 23.7 + 1.92 15.7 + 3.05 373 + 81.0 7.3 + 2.80 2.9 + 0.47 sR3 (VU)* 9.5 + 0.78 19.3 + 4.59 12.8 + 1.77 248 + 75.3 6.2 + 2.62 2.3 + 0.41 R4 6.3 + 0.45 11.5 + 3.84 8.3 + 1.98 102 + 62.3 3.8 + 2.02 1.8 + 0.40 Juvenile R2 3.3 + 0.24 8.7 + 1.76 6.2 + 1.41 56 + 21.2 1.7 + 0.71 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 root observed in situ was upwardly oriented; although it is agravitropic, we noted it sR3 (VU).

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F I G . 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).

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 possess very 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 not therefore depend upon the perception mechanism, but could be linked to a dierent sensitivity to auxin which,

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F I 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).

through dierential redistribution, causes curvature (Dolan, 1998; Pilet, 1998). Roots with negative gravitropism (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 rst would seem to be of internal origin and inherent to each of the root types within which each root has a xed initial

Jourdan et al.Root Architecture and Gravitropism

direction of growth (Dyanat-Nejad and Neville, 1972b). The second would seem to be more of external origin, linked to environmental conditions in the vicinity of the roots. For instance, in the case of supercial lateral roots of the sitka spruce or lodgepole pine, Coutts and Nicoll (1991) showed that they were diagravitropic, with initial upward growth, but as these roots approached the soil surface they responded to some signal from the environment ( probably light), that caused a downward deection, and thus roots tended to grow horizontally. A similar hypothesis has been proposed by Firn and Digby (1997) which states that organs possess a mechanism which allows them to attain a stable gravitropic position at a given angle and that each organ has a characteristic gravitropic set-point angle (GSA). But the GSA can be developmentally changed or regulated by environmental factors. In their recent review, Hemmersbach et al. (1999) showed that in view of the physical nature of gravity, the stimulus must 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 later amplied. 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 preferentially located along certain walls, stable horizontal growth (e.g. R1 H roots) could be linked to an absence of sensors along the longitudinal wall of the statocyte, whilst vertical growth (e.g. R2 VD, R2 VU) could be linked to an absence of sensors along the transversal walls ( proximal or distal). The GSA, therefore, should be determined by the location of the gravisensors along (or on) the plasma membrane, and the stable direction of growth should be attained when the statoliths or the cell can no longer exert an action on these gravisensors. This hypothesis is consistent with the fact that gravisensitivity is mostly located at both ends of the characean internodal cells (Wayne and Staves, 1996). Molecular characterization would make it possible to locate these receptors and thus validate this hypothesis. The fact that environmental factors can change the GSA may be because they aect the distribution of receptors within the cell. AC K N OW L E D GE M E N T S We thank the Centre National de Recherche Agronomique , Ivory (CNRA) for access to the eld experiments at La Me Coast. Travel expenses and nancial support for this work were covered by the Tree Crop Department of the Centre de ration Internationale en Recherche Agronomique Coope veloppement (CIRAD). pour le De L I T E R AT U R E C I T E D
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