+ All Categories
Home > Documents > Factors affecting the direction of growth of tree roots · Factors affecting the direction of...

Factors affecting the direction of growth of tree roots · Factors affecting the direction of...

Date post: 04-May-2018
Category:
Upload: lamkhanh
View: 217 times
Download: 1 times
Share this document with a friend
12
HAL Id: hal-00882555 https://hal.archives-ouvertes.fr/hal-00882555 Submitted on 1 Jan 1989 HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci- entific research documents, whether they are pub- lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés. Factors affecting the direction of growth of tree roots M.P. Coutts To cite this version: M.P. Coutts. Factors affecting the direction of growth of tree roots. Annales des sciences forestières, INRA/EDP Sciences, 1989, 46 (Suppl), pp.277s-287s. <hal-00882555>
Transcript

HAL Id: hal-00882555https://hal.archives-ouvertes.fr/hal-00882555

Submitted on 1 Jan 1989

HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.

Factors affecting the direction of growth of tree rootsM.P. Coutts

To cite this version:M.P. Coutts. Factors affecting the direction of growth of tree roots. Annales des sciences forestières,INRA/EDP Sciences, 1989, 46 (Suppl), pp.277s-287s. <hal-00882555>

Factors affecting the direction of growth of tree roots

M.P. Coutts

Forestry Commission, Northern Research Station, Roslin, Midlothian, EH25 9SY, Scotland, U.K.

Introduction

The direction of growth of the main rootsof a tree is an important determinant of theform of the root system. It affects the waythe system exploits the soil (Karizumi,1957) and has practical significance for

the design of containers and for cultivationsystems which can influence tree growthand anchorage. This review discusses theway in which root orientation is esta-

blished and how it is modified by the envi-ronment.

The form of tree root systems can beclassified in many ways but the common-est type in boreal forests is dominated byhorizontally spreading lateral roots withinabout 20 cm of the ground surface (Fayle,1975; Strong and La Roi, 1983). A verticaltaproot may persist or may disappearduring development. Sinker roots are

more or less vertical roots which growdown from the horizontal laterals. Theyare believed to be important for anchorageand for supplying water during dry peri-ods. Roots which descend obliquely fromthe tap or lateral roots are also presentand the distinction between these and

sinkers is a matter of definition. Dif-

ferences in root form could arise from dif-ferences in root direction or from differen-tial growth and survival of roots which

were originally growing in many directions.In practice, both the direction of growthand differential development contribute tothe final form.

There is scant information about the

principal controls over the orientation of

tree roots. Most studies deal with herba-ceous species, and even for them experi-mental work and reviews have generallybeen confined to geotropism of the seed-ling radicle. The direction sensing appara-tus lies in the root cap (Wilkins, 1975).The structure of the root cap is variable,but there is no essential difference be-tween those of herbaceous species andtrees. Work on herbaceous species there-fore has a strong relevance for trees, butcertain differences must be noted. For

example, any correlative effects betweenthe taproot and laterals may be modifiedin trees by the size, age and complexity oftheir root systems. Furthermore, the rootsof herbs, and especially of annuals, mayhave evolved optimal responses to sea-sonal conditions, whereas the young treemust build a root system to support it phy-sically and physiologically for many years.An example of response to temporaryinfluences is given by soybean, in which

the lateral roots grow out 45 cm horizon-

tally from the taproot, then turn down verti-cally during the summer (Raper and Bar-ber, 1970), possibly in response to

drought or high temperature (Mitchell andRussell, 1971 ). A forest tree could not sur-vive on a root system so restricted lateral-ly.

Orthogeotropic roots

In both herbs and trees the seedlingtaproot (or radicle) is usually positivelygeotropic. If the root is displaced from itsvertical (orthogeotropic) position, the tipbends downwards. The signal for thedirection of the vector of gravity is given bythe sedimentation of starch grains onto thefloor of statocytes in the central tissues ofthe root cap. This signal results, in an

unexplained way, in the production andredistribution of growth regulators, in-

cluding indole-3-acetic acid and abscisicacid (ABA), which become unevenlydistributed in the upper and lower parts ofthe root. Unequal growth rates then occurin the upper and lower sides of the zone of

extension, resulting in corrective curva-

ture. There are many reviews of geotrop-ism (Juniper, 1976; Firn and Digby, 1980;Jackson and Barlow, 1981; Pickard, 1985)and the mechanism will not be discussedfurther here.

The detection of and response to gravityare rapid. The presentation time for theseedling radicle of Picea abies L. is only8-10 min (Hestnes and Iversen, 1978)and curvature is often completed in a mat-ter of hours. Orthogeotropic taproots retaintheir response to gravity indefinitely,although 2 m long roots of Quercus robur(L.) responded more slowly to displace-ment and had a longer radius of curvaturethan shorter, younger roots (Riedacker etal., 1982).

Plagiogeotropic and diageotropic roots

First order lateral roots (1 ° L) grow fromthe taproot horizontally (diageotropic) or

are inclined at an angle (plagiogeotropic).The angle bei:ween the lateral root and theplumb line is called the liminal angle, andis known to vary with species (Sachs,1874). Billan et al. (1978) even found dif-ferences in the liminal angles between twoprovenances of Pinus taeda L.: the pro-venance from the driest site had the small-est angle (i.e., the most downwardly di-rected lateral roots). They also found thatthe liminal angle of the upper laterals wasabout twice that of those lower on the

taproot, a finding in general agreementwith Sachs’ (1874) observations on herbs.

The responses of plagiotropic roots togravity have been demonstrated by reo-rienting either entire plants growing in

containers (S;achs, 1874; Rufelt, 1965), orindividual roots (Wilson, 1971 When Wil-son (1971) displaced horizontal Acerrubrum L. roots to angles above the hori-zontal, the roots bent downwards. Whendisplaced below the horizontal, the rootsdid not curve, they continued to grow in

the direction in which they had been

placed. Such roots are described as beingweakly plagi!otropic (Riedacker et al.,1982). However, some species show anupward curvai:ure of downwardly displacedroots (strong plagiotropism). In his review,Rufelt (1965) concluded that the liminal

angle is determined by a balance betweenpositive geotropism and a tendency to

grow upwards, e.g., a negative geotro-pism.

Certain correlative effects between the

tip of the taproot and the growth andorientation of 1 L L have been described. InTheobroma cacao L., if the taproot is ex-cised below very young laterals, some ofthem will bend downwards, increase insize and vigour, and become positivelygeotropic replacement roots, i.e., roots

which replace the radicle. However, if the

taproot is cut below laterals more than 7 dold, they do not change in growth rate or

orientation; their behaviour has becomefixed (Dynat-Nejad, 1970; Dynat-Nejadand Neville, 1972). Experiments by theseworkers, which included decapitation of

the taproot tip and blocking its growth bycoating it with plaster, showed that the

progressive development of a ratherstable plagiotropism by the lateral roots

was related to the growth rate of the

taproot, but not to that of the lateral rootsthemselves. Experiments on C7. robur in-dicated that the behaviour of the lateral

roots in that species is determined evenearlier than in T. cacao, at the primordialstage (Champagnat et al., 1974). Riedac-ker et al. (1982) largely confirmed thiswork. They found that if the tip of the

taproot was blocked rather than cut, thegrowth of new laterals above the blockagewas enhanced and they became weaklyorthogeotropic. However, it took time forthe roots to acquire this response and, inQ. suber L., the lateral roots grew20-30 cm and developed thicker tips be-fore turning downwards. It is not entirelyclear whether such a response was alsoinduced in lateral roots already present atthe time the taproot tip was blocked.

When the tip of a main vertical or hori-zontal root is injured, replacement rootsare free from apical dominance effectsand curve forwards, to become parallel tothe main root, instead of growing at theusual liminal angle, or angle with respectto the mother root (Horsley, 1971 ). In thisway, the direction of growth of the mainroot axes is maintained, both outwards,away from the tree, and in the vertical

plane.

The way in which the direction of root

growth with respect to gravity becomesfixed, or programmed, has not been stu-died. Although gravity is sensed by thecap, the programme must lie elsewhere,because the cap dies when the rootbecomes dormant (Wilcox, 1954; John-

son-Flanagan and Owens, 1985), yet thedirection of growth can remain unalteredover repeated cycles of growth and dor-mancy. Furthermore, loss of the entire root

tip generally gives rise to replacementroots which have the same gravitropic re-sponses as the mother root, indicating thatthe programme lies in the subapical por-tion. Work on the acquisition of the plagio-geotropic growth habit by lateral roots

requires further development and exten-sion to other species. Plagiogeotropism iseven less well understood than geotro-pism of the radicle, on which much morework has been done, but the experimentson correlative control indicate that in the

developed tree root system, it is unlikelythat the vertical roots influence the orienta-tion of existing plagiogeotropic laterals.

Lateral roots of second and higherorders of branching and diminishing dia-meter become successively less responsi-ve to gravity. Since gravity is sensed bythe sedimentation of the amyloplasts in

the root cap, higher order roots may havecaps too small to enable a geotropic re-sponse. Support for this idea comes fromwork on Ricinus. The first order lateralroots grow 15-20 mm horizontally fromthe taproot, then turn vertically down-wards. Moore and Pasieniuk (1984) foundthat the development of this positive re-

sponse to gravity was associated with

increased size of the root cap. The gra-dual development of a gravitropic re-

sponse in laterals of Q. suber might alsobe associated with growth of the root cap.The ectomycorrhizal roots of conifers,which are ageotropic, have poorly de-

veloped caps and the cap cells appear tobe digested by the fungal partner (Clowes,1954). Whether there are importantanatomical differences between the root

caps of the larger, first order plagiotropiclateral roots of trees, and the caps of

taproots and sinkers, has not been de-termined.

The orientation of root initials

Root orientation is determined first by thedirection in which the root initial is facingbefore it emerges from the parent root

and, subsequently, by curvature. The 1 L Lmaintain a direction of growth away fromthe plant, an obvious advantage for soil

exploration and for providing a frameworkfor anchorage. Noll (1894) termed this

growth habit of roots exotropy. The lateralsare initiated in vertical files related to the

position of the vascular strands in the

taproot. The taproot of Q. robur, for

example, has 4-5 strands (Champagnatet al., 1974), and the existence of 4-5 filesof laterals ensures that the tree will haveroots well distributed around it. In conifers,the taproot is usually triarch or tetrarch,whereas the laterals are mostly diarch,e.g., Pseudotsuga menzesii (Mirb.) Franco(Bogar and Smith, 1965), Pinus contorta(Douglas ex Louden) (Preston, 1943). Insome species, the files of laterals are aug-mented by adventitious roots from thestem base and trees produce additionalmain roots by branching near the base ofthe 1 ° L (see Coutts, 1987).The diarch condition of most of the la-

teral roots of conifers restricts branches of

the next order to positions opposite thetwo primary xylem strands. Thus, if a linedrawn through these strands in transversesection, the ’primary xylem line’, is vertical,roots will emerge pointing only upwardsand downwards (Fig. 1 a). This verticalorientation is present in the 1 L at its

junction with the taproot (Fig. 1b). In prac-tice, many branches on 1 L at a distancefrom the tree :are produced in the horizon-tal plane, as observed by Wilson (1964) inA. rubrum, therefore twisting of the root

apex must occur. Wilson noted a clock-wise twisting (looking away from the tree)in A. rubrum. Twisting is also common inPicea sitchensis (Bong.) Carr. Many rootswhich were sectioned showed partial rota-tion of the axis, followed by correctionsin the opposite direction (Coutts,unpublished). Examination of 24 roots,2-5 m long, showed that the primaryxylem line was more commonly orientedhorizontally than vertically, favouring theinitiation of horizontal roots. As the root

twists, the next order laterals can arise inany direction.

The angle of initiation may account forthe production of sinker roots fromlaterals. In an unpublished study on P. sitchensis, sinkers were defined as roots

growing downwards at angles of less than45° to the vertical 12-15 cm from their

point of origin, while roots at angles within45° of the horizontal were called sideroots. An examination of 50 roots of each

type on 10 yr old trees showed that theangle of growth was strongly related to theangle of initiation, and thus to the angle ofthe primary xylem line (Fig. 2).

Sinkers and side roots were predomi-nantly initiated in a downward and ina horizontal direction, respectively. Rootsof both types tended to curve sligh-tly downwards after they emerged fromthe 1 ° L. Some species, e.g., Abies, ha-

ve sinker roots with a stricter verti-cal orientation than those of Picea, andthey may therefore originate in a differentway.

It is not known whether sinker roots are

weakly plagiotropic, their direction beingmainly a matter of the direction of initia-

tion, or whether the tip becomes positivelygeotropic, perhaps by some process ofhabituation. Observations on Pinus resi-nosa Ait. indicate that the sinkers mayhave special geotropic properties: lateralroots from them emerge almost horizontal-

ly, but then turn sharply downwards

(Fayle, 1975).

Surface roots

Many 1 ° L curve gently downwards withdistance from the tree (Stein, 1978; Eis,1978), but some, which may originatefrom the upper part of the taproot andtherefore have the largest liminal angles,grow at the soil surface, in or beneath thelitter. Many surface roots are 2° L and 3° L(Lyford, 1975; Eis, 1978). Surface rootsgrow up steep slopes as well as downhill(McMinn, 1963). Presumably they are pro-grammed to grow diageotropically, buttheir orientation is modified by the environ-ment. The remainder of this review dealswith environmental effects.

Mechanical barriers

Barriers which affect root orientation in-clude soil layers with greater mechanicalimpedance than that in which the root hasbeen growing, and impenetrable objects inthe soil. Downwardly directed roots can

deflect upwards to a horizontal position onencountering compacted subsoil, but turndown if they enter a crack of hole (Dexter,1986). Horizontal roots or A. rubrumdeflected upwards when they encountered

a zone of compacted vermiculite (Wilson,1971), but roots growing downwards at

45° into compacted but penetrable layersdid not deflect. Wilson (1967) found thatwhen horizontal roots of A. rubrumencountered vertical barriers, they de-flected along them, sometimes with theroot tip distorted laterally towards the bar-rier (Fig. 3a). On passing the barrier, theroots deflecteci back towards the originalangle. The correction angle varied with theinitial angle of incidence between root andbarrier, and with barrier length. Barrier

length in the range 1-7 cm had only asmall effect on correction angle. Riedacker(1978) obtained similar results with theroots of Populus cuttings and barriers upto 7 cm long. With barriers 10-12 cm long,nearly half of the roots continued growth inthe direction of the barrier. Roots made todeflect downwards at barriers inclined tothe vertical, made upward corrective cur-vature; they were slightly less influencedby barrier length than horizontal roots.

Orthogeotropic: taproots of Q. robur seed-lings deflected past a series of 2 cm longbarriers, maintaining a remarkably verticalorientation overall (Fig. 3b). Replacementtaproots formed after injury appeared tobe insensitive t:o barrier length.The mechanism by which roots make

corrective curvatures after passing bar-riers is not known. Large variation in cor-rection angles has been reported, and it is

possible that barrier length is less impor-tant than the time for which the root hasbeen forced to deflect. The mechanism isan important one for maintaining exotropicgrowth.

Light and temperature

Light from any direction can increase thegraviresponsiveness of the radicle andlateral roots of some herbaceous species(Lake and Slac:k, 1961 Light is sensed by

the root cap (Tepfer and Bonnet, 1972).Wavelengths which elicit a response varywith plant species, e.g., Zea (Feldman andBriggs, 1987) and Convolvulus (Tepferand Bonnett, 1972) respond to red lightand show some reversal in far red, where-as the plagiotropic roots of Vanilla turn

downwards only in blue light (Irvine andFreyre, 1961). ).There is little information on trees. Iver-

sen and Siegel (1976) found that when P.abies seedlings were lain horizontally inthe light, subsequent growth of the radiclein darkness was reduced, but curvaturewas unaffected. Lateral roots of P. sitchensis showed reduced growth anddownward curvature in low levels of white

light (Coutts and Nicholl, unpublished).Such responses indicate that care must beexercised when using root boxes with

transparent windows for studies on thedirection of growth. In the field, light mayhelp regulate the orientation of surfaceroots, just as it does for Aegeopodium rhi-zomes, which respond to a 30 s exposureby turning downwards into the soil (Ben-net-Clark and Ball, 1951 ).The growth of corn roots is influenced

by temperature. At soil temperaturesabove and below 17°C, plagiotropic prima-ry roots become angled more steeplydownwards (Onderdonk and Ketcheson,1973). No information is available fortrees.

Waterlogging and the soil atmosphere

Waterlogging has a drastic effect on soilaeration and consequently on tree root

development (Kozlowski, 1982). Waterlog-ged soils are characterised by a lack ofoxygen, increased levels of carbon dioxideand ethylene, together with many otherchemical changes (Armstrong, 1982). The

tips of growing taproots and sinkers arekilled when the water table rises, and

regeneration takes place when it falls

during drier periods. Such periodic deathand regrowth produce the well-known

’shaving brush’ roots on many tree spe-cies. In spite of poor soil aeration, the tipsof taproots and sinkers maintain a gen-erally downward orientation. This could bebecause periods of growth coincide withperiods when the soil is aerated. However,in an experiment on P. sitchensis grownout of doors in large containers of peat,main roots which grew down at 0-45°

from the vertical did not deflect when

approaching a water table maintained26 cm below the surface (Coutts and

Nicholl, unpublished). The roots pene-trated 1-5 cm into the waterlogged soiland then stopped growing. This behaviourcontrasts with certain herbaceous species.Guhman (1924) found that the taprootsand laterals of sunflower grew diageotropi-cally in waterlogged soil, and Wiersum

(1967) observed that Brassica and potatoroots grew upwards towards better aer-ated zones. The finest roots of trees mayalso grow upwards from waterlogged soils,as found for Melaleuca quinquenerva(Cav.) Blake by Sena Gomes and Koz-lowski (1980), and for flooded Salix (seeGill, 1970). However, the emergence ofroots above flooded soil does not neces-

sarily mean that the roots have changeddirection, they may have been growingupwards prior to flooding.

Little is known about the response of

plagiotropic roots to waterlogging. Arm-strong and Boatman (1967) consideredthat the shallow horizontal root growth ofMolinia in bogs was a response to water-logged conditions, but did not presentobservations on growth in well-drainedsoil. The proliferation of the surface rootsof trees on wet sites may be a result of

compensatory growth rather than a

change in orientation.

The direction of growth of plant organsis influenced by C02. For example, thediageotropic rhizomes of Aegeopodiumdeflect upwards in the presence of 5%

C02 (Bennet-Clark and Ball, 1951), andthis response has been supposed to helpmaintain their position near the soil sur-

face. Ycas and Zobel (1983) measuredthe deflection of the plagiotropic radicle ofcorn exposed to various concentrations of02, C02 and ethylene. Substantial effectson the direction of growth were obtainedonly with C02. Roots in normal air grew atan angle of 49° to the vertical, whereas in11 % C02 they deflected upwards to anangle of 72°. The minimum concentrationof C02 required to cause measurabledeflection was 2%. Concentrations of2-11% C02 are above those found in well-drained soils but, in poorly draining, for-ested soils, Pyatt and Smith (1983) fre-

quently found 5-10% C02 at depths of35-50 cm. However, concentrations were

usually less than 5% at a depth of 20 cmand would presumably have been lowerstill nearer the surface, where most of theroots were present. In Ycas and Zobel’s

(1983) experiments, ethylene at non-toxicconcentrations had little effect on thedirection of corn root growth, and onlysmall effects on corn had been found byBucher and Pilet (1982). In another study,orthogeotropic pea roots responded to

ethylene by becoming diageotropic but theroots of three other species did not

respond in this way (Goeschl and Kays,1975).

It appears as though the downwardlygrowing roots of trees do not deflect onencountering waterlogged soil. This failureto deflect is consistent with the conclusionof Riedacker et al. (1982) that the positivegeotropism of tree roots is difficult to alter.There is not enough information on plagio-geotropic roots to say whether soil aera-tion affects their orientation.

Dessication

The curvature of roots towards moisture iscalled hydrotropism. Little work has beendone on it and Rufelt (1969) questionedwhether the phenomenon exists. Sachs

(1872) grew various species in a sieve ofmoist peat, hanging inclined at an angle ina dark cupboard. When the seedling rootsemerged into water-saturated air, theygrew downwards at normal angles, but indrier air they curved up through the small-est angle towards the moist surface of thepeat. Sachs concluded that they wereresponding to a humidity gradient. Loomisand Ewan (1935) tested 29 genera, in-

cluding Pinus, by germinating seeds be-tween layers of wet and dry soil held in

various orientations. In most plants tested,including Pinus, no consistent curvaturetowards the wet soil occurred. In specieswhich gave a positive result, the 1 ° L were

unaffected, only the radicle responded.Some of the non-responsive species hadresponded in Sachs’ system, an anomalywhich may be explained by problems ofmethodology. The containers of wet anddry soils in Loomis and Ewan’s experi-ments were placed in a moist chamberand the vapour pressure of the soil atmo-

sphere may well have equilibrated duringthe course of the experiment.

Jaffe et al. (1985) studied hydrotropismin the pea mutant, ’Ageotropum’, whichhas roots not normally responsive to gravi-ty. Upwardly growing roots which emergedfrom the soil surface continued to growupwards in a saturated atmosphere but, atrelative humidities of 75-82%, they bentdownwards to the soil. No response took

place if the root cap was removed and it

was concluded that the cap sensed a

humidity gradient.These results have implications for the

behaviour of tree roots at the soil surfaceand where horizontally growing roots

encounter the sides of drains. For

example, when P. sifchensis roots growfrom the side of a furrow made by spaced-furrow ploughing, they turn downwards onemerging into litter or overarching vegeta-tion. Experiments to investigate this be-haviour shewed that horizontal roots which

emerged from moist peat into air at a rela-tive humidity of 99% grew without de-

flecting, but at 95% they deflected down-wards to the peat (Coutts and Nicholl,unpublished). This behaviour could havebeen a hydrotropic response, but roots

which grew out from the peat at anglesabove the horizontal into air at 95% humi-

dity, also turned downwards, rather thanupwards towards the nearest moist sur-face. This suggests that localised waterstress at the root tip had induced a posi-tive geotropic response. It is relevant to

note that water stress induces the forma-tion of ABA in root tips (Lachno and Baker,1986; Zhang and Davies, 1987), and ABAhas been implicated in geotropism. Anexplanation of geotropism induced bywater stress could also apply to the down-ward curvature of otherwise ageotropicroots already mentioned, but not to

upward curvatures in Sachs’ experiments.It is in any case unlikely that roots growingin soil exhibit hydrotropism because thevapour pressure difference, even betweenmoist soil and soil too dry to support rootgrowth, is so small (Marshall and Holmes,1979) that roots would be unlikely to

detect it. A positive geotropic response byroots in dry soil would be likely to directthem to moister layers lower down.

Conclusions

The seedling radicle, and roots which

replace it after injury, are usually positivelygeotropic. Sinker roots, at least in one

species, appear to originate from root pri-mordia which happen to be angled down-wards. Their georesponsiveness is un-

known. The gravitropism of taproots is a

stable feature and the vertical roots oftrees do not seem to deflect from water-

logged soil layers, unlike the roots of cer-tain herbs. They have been made to

deflect only on encountering impenetrablebarriers.

The direction of growth of first order

laterals around the tree in the horizontal

plane is set by the position of the initials

on the taproot. The direction of growth ismaintained away from the tree by correc-tive curvatures, when the root is made todeflect by obstacles in the soil. If the tip iskilled, replacement roots also curve andcontinue growth in the direction of the

main axis. In the vertical plane, geotropicresponses of the laterals are subject for ashort period to correlative control by the tipof the taproot. Work on broadleaved spe-cies indicates that during that period, thelateral root apex becomes programmed togrow at a particular angle to the vertical.This angle can be modified by the environ-ment: temperature, light and humidity canalter the graviresponsiveness of lateralroots. It is not certain whether hydrotropicresponses occur nor whether the lateralroots of trees respond to soil aeration or

deflect from waterlogged soil. The way inwhich the growth of main lateral roots is

maintained near the soil surface, even inroots growing uphill, is not properlyunderstood. Thin roots of more than first

order, including mycorrhizas, have smallroots caps and do not appear to respondto gravity.

Acknowledgment

I thank Dr. J.J. Philipson for his helpful com-ments on the manuscript.

References

Armstrong W. (1982) Waterlogged soils. in:Environment and Plant Ecology (EtheringtonJ.R., ed.), John Wiley, Chichester, pp. 290-330Armstrong W. & Boatman D.J. (1967) Somefield observations relating the growth of bogplants to conditions of soil aeration. J. Ecol. 55,101-110 0

Bennet-Clark T.A. & Ball N.G. (1951) The dia-geotropic behaviour of rhizomes. J. Exp. Bot. 2,169-203

Bilan M.V., Leach J.H. & Davies G. (1978) Rootdevelopment in loblolly pine (Pinus taeda L.)from two Texas seed sources. In: Root Form ofPlanted Trees (van Eerden E. & Kinghorn J.M.,eds.), British Columbia Ministry of Fo-rests/Canadian Forestry Service, Joint Reportno. 8, pp. 17-22

Bogar G.D. & Smith F.H. (1965) Anatomy ofseedling roots of Pseudotsuga menziesii. Am.J. Bot. 52, 720-729Bucher D. & Pilet P. (1982) Ethylene effects ongrowing and gravireacting maize root seg-ments. Physiol. Plant. 55, 1-4Champagnat M., Baba J. & Delaunay M. (1974)Correlations entre le pivot et ses ramificationsdans le systbme racinaire de jeunes ch6nescultiv6s sous un brouillard nutritif. Rev. Cytol.Biol. V6g. 37, 407-418 8

Clowes F.A.L. (1954) The root cap of ectotro-phic mycorrhizas. New Phytol. 53, 525-529Coutts M.P. (1987) Developmental processes intree root systems. Can. J. For. Res. 17, 761-767

Dexter A.R. (1986) Model experiments on thebehaviour of roots at the interface between atilled seed-bed and a compacted sub-soil.Plant Soil 95, 149-161Dynat-Nejad H. (1970) Contr61e de la plagiotro-pie des racines lat6rales chez Theobromacacao L. Bull. Soc. Bot. Fr. 117, 183-192Dynat-Nejad H. & Neville P. (1972) Sur le moded’action du méristème radical orthotrope sur lecontr6le de la plagiotropie des racines latdraleschez Theobroma cacao L. Rev. Gen. Bot. 79,319-340

Eis S. (1978) Natural root forms of westernconifers. In: Root Form of Planted Trees (vanEerden E. & Kinghorn J.M., eds.), BritishColumbia Ministry of Forests/Canadian ForestryService, Joint Report no. 8, pp. 23-27Fayle D.C.F. (1975) Extension and longitudinalgrowth during the development of red pine rootsystems. Can. J. For. Res. 5, 109-121

Feldman L.J. & Etriggs W.R. (1987) Light-regu-lated gravitropism in seedling roots of maize.Plant Physiol. 53, 241-243Firn R.D. & Digby J. (1980) The establishmentof tropic curvatures in plants. Annu. Rev. PlantPhysioL 31, 131-148Gill C.J. (1970) The flooding tolerance of woodyspecies - a review. For. Abstr. 31, 671-688Goeschl J.D. & Kays S.J. (1975) Concentrationdependencies of some effects of ethylene onetiolated pea, peanut, bean and cotton seed-lings. Plant Physiol. 55, 670-677Guhman H. (1924.) Variations in the root systemof the common everlasting (Gnaphalium polycephalum). Ohio ,I. Sci. 24, 199-208Hestnes A. & Ive!rsen T. (1978) Movement ofcell organelles and the geotropic curvature inroots of Norway spruce (Picea abies). Physiol.Plant. 42, 406-41 41

Horsley S.B. (1971) Root tip injury and develop-ment of the paper birch root system. For. Sci.17, 341-348Irvine J.E. & Freyre R.H. (1961) Diageotropismin Vanilla roots. Science 134, 56-57

Iversen T. & Siegel K. (1976) The geotropic cur-vature in roots of Norway spruce (Picea abies)containing anthocyanins. Physiol. Plant. 37,283-287

Jackson M.B. & E3arlow P.W. (1981) Root geo-tropism and the role of growth regulators fromthe cap: a re-examination. Plant Cell Environ. 4,107-123

Jaffe M.J., Takahashi H. & Biro R.L. (1985) Apea mutant for the study of hydrotropism inroots. Science 230, 445-447

Johnson-Flanagan A.M. & Owens J.N. (1985)Development of white spruce (Picea glauca)seedling roots. Can. J. Bot 63, 456-462

Juniper B.E. (1976) Geotropism. Annu. Rev.Plant Physiol. 27, 385-406Karizumi N. (1957) Studies on the form and dis-tribution habit of the tree root. Bull. For. Exp.Sta. Meguro, Tokyo no. 94, pp. 205 (in Japan-ese)Kozlowski T.T. (1982) Water supply and treegrowth. Part 2, Flooding. For. Abstr. 43, 145-161

Lachno D.R. & Baker D.A. (1986) Stressinduction of abscisic acid in maize roots. Physiol. Plant. 68, 215-221

Lake J.V. & Slack G. (1961) Dependence onlight of geotropism in plant roots. Nature 191,300-302

Loomis W.E. & Ewan L.M. (1935) Hydrotropicresponses of roots in soil. Bot Gaz. 97, 728-743

Lyford W.H. (1975) Rhizography of non-woodyroots of trees in the forest floor. In: The De-

velopment and Function of Roots. (Torrey J.G.& Clarkson D.T., eds.), Academic Press,London, pp. 179-196

Marshall J.J. & Holmes J.W. (1979) In: SoilPhysics. Cambridge University Press, Cam-bridge, pp. 345McMinn R.G. (1963) Characteristics of Douglasfir root systems. Can. J. Bot. 41, 105-122

Mitchell R.L. & Russell W.J. (1971) Root de-velopment and rooting patterns of soybean(Glycine max (L.) Merill) evaluated under fieldconditions. Agron. J. 64, 313-316 6Moore R. & Pasieniuk J. (1984) Gravirespon-siveness and cap dimensions of primary andsecondary roots of Ricinus communis (Euphor-biaceae). Can. J. Bot. 62, 1767-1769Noll F. (1894) Ueber eine neue eigenschaft deswurzelsystems. In: Sitzungsbericht Niederrheinschen Gesellschaft Fur Natur-und Heil-kunde. Springer-Verlag, Bonn, pp. 34-36Onderdonk J.J. & Ketcheson J.W. (1973) Effectof soil temperature on direction of corn root

growth. Plant Soil 37, 177-186

Pickard B.G. (1985) Roles of hormones, pro-tons and calcium in geotropism. In: Encyclo-pedia of Plant Physiology, New Series, 2 (Pir-son A. & Zimmermann M.H., eds.), Springer-Verlag, Berlin, pp. 193-265Preston R.J. (1943) Anatomical studies of theroot of juvenile lodgepole pine. Bot. Gaz. 104,443-448

Pyatt D.G. & Smith K.A. (1983) Water and oxy-gen regimes of four soil types at NewcastletonForest, south Scotland. J. Soil Sci. 34, 465-482

Raper C.D. & Barber S.A. (1970) Rooting sys-tems of soybeans. I. Differences in root mor-

phology among varieties. Agron. J. 62, 581-584Riedacker A. (1978) Etude de la d6viation desracines horizontales ou obliques issues de bou-tures de peuplier qui rencontre un obstacle:applications pour la conception de conteneurs.Ann. Sci. For. 35, 1-18 8

Riedacker A., Dexheimer J., Tavakol R. &Alaoui H. (1982) Modifications exp6rimentalesde la morphog6n6se et des g6otropismes dansle syst6me racinaire de jeunes ch6nes. Can. J.Bot. 60, 765-778

Rufelt H. (1965) Plagiogeotropism in roots. In:

Encyclopedia of Plant Physiology 17. (RuhlandW., ed.), Springer, Berlin, pp. 322-343Rufert H. (1969) Geo- and hydrotropic re-

sponses of roots. In: Root Growth. (WhittingtonW.J., ed.), Butterworths, London, pp. 54-64Sachs J. (1872) Ablenkung der wurzeln vonihrer normalen wachsthumsrichtung durchfeuchte korper. Arb. Bot. lnst. Wurzburg 1, 209-222

Sachs J. (1874) Ueber das wachsthum der

haupt-und nebenwurzeln. Arb. Bot. Inst Wurz-burg 1, 584-634Sena Gomes A.R. & Kozlowski T.T. (1980) Re-sponses of Melaleuca quinquenervia seedlingsto flooding. Physiol. Plant 49, 373-377Stein W.I. (1978) Naturally developing seedingroots of five western conifers. In: Root Form ofPlanted Trees. (van Eerden E. & Kinghorn J.M.,eds.), British Columbia Ministry of Forests/Canadian Forestry Service, Joint Report no. 8,pp. 28-35

Strong W.L. & La Roi G.H. (1983) Root systemmorphology of common boreal forest trees inAlberta, Canada. Can. J. For. Res. 13, 1164-1173

Tepfer D.A. & Bonnett H.T. (1972) The role ofphytochrome in the geotropic behaviour of rootsof Convolvulus arvensis. Planta 106, 311-324

Wiersum L.K. (1967) Presumed aerotropicgrowth of roots of certain species. Naturwis-senschaften 8, 203-204

Wilcox H. (1954) Primary organization of activeand dormant roots of noble fir, Abies procera.Am. J. Bot. 41, 812-821

Wilkins M.B. (1975) The role of the root cap ingeotropism. Curr. Adv. Plant Sci. 6, 317-328Wilson B.F. (1964) Structure and growth of

woody roots of Acer rubrum L. Harv. For. Pap.11, pp. 14 4Wilson B.F. (1967) Root growth around barriers.Bot. Gaz. 128, 79-82

Wilson B.F. (1971) Vertical orientation of red

maple (Acer rubrum L.) roots. Can. J. For. Res.1, 147-150Ycas J.W. & Zobel R.W. (1983) The re-

sponse of maize radicle orientation to soilsolution and soil atmosphere. Plant Soil 70,27-35

Zhang J. & Davies W.J. (1987) Increased syn-thesis of ABA in partially dehydrated root tipsand ABA transport from roots to leaves. J. Exp.Bot. 38, 2015-2023


Recommended