Factors Affecting the Direction of Growth of Tree Roots

8/10/2019 Factors Affecting the Direction of Growth of Tree Roots

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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 forthe 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 aremore 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 andsinkers 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 oftree roots. Most studies deal with herba-ceous species, and even for them experi-mental work and reviews have generally

been 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

taprootand laterals

maybe modified

in 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 whichthe lateral roots

growout 45 cm horizon-

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


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drought or high temperature (Mitchell andRussell, 1971 ). Aforest 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 anunexplained 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

varywith

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 incontainers (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 roots

did not curve, they continued to grow inthe direction in which they had beenplaced. 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 liminalangle is determined by a balance betweenpositive geotropism and a tendency to

grow upwards, e.g.,a

negative geotro-pism.

Certain correlative effects between thetip of the taproot and the growth andorientation of 1L 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., rootswhich replace the radicle. However, if thetaproot is cut below laterals more than 7 dold, they do not change in growth rate or


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orientation; their behaviour has becomefixed (Dynat-Nejad, 1970; Dynat-Nejadand Neville, 1972). Experiments by theseworkers, which included decapitation ofthe taproot tip and blocking its growth bycoating it with plaster, showed that theprogressive development of a ratherstable plagiotropism by the lateral rootswas related to the growth rate of thetaproot, but not to that of the lateral rootsthemselves. Experiments on C7. robur in-dicated that the behaviour of the lateralroots 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 thetaproot 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

growingat the

usual 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 verticalplane.

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 roottip 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 rootsrequires 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

gravityis sensed

bythe sedimentation of the amyloplasts inthe 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 withincreased 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.


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The orientation of root initials

Root orientation is determined first by thedirection in which the root initial is facingbefore it emerges from the parent rootand, subsequently, by curvature. The 1 LLmaintain a direction of growth away fromthe plant, an obvious advantage for soilexploration and for providing a frameworkfor anchorage. Noll (1894) termed thisgrowth habit of roots exotropy. The lateralsare initiated in vertical files related to the

position of the vascular strands in thetaproot. The taproot of Q. robur, forexample, 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 primaryxylem line, is vertical,roots will emerge pointing only upwardsand downwards (Fig. 1 a). This verticalorientation is present in the 1 L at itsjunction 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) in

A. rubrum, therefore twisting of the rootapex 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 the

initiation of horizontal roots. As the roottwists, 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


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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 eachtype 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 areweakly 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:lateral

roots from them emerge almost horizontal-ly, but then turn sharply downwards(Fayle, 1975).


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Surface roots

Many 1 L curve gently downwards with

distance 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

bythe 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 has

been growing, and impenetrable objects inthe soil. Downwardly directed roots candeflect 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 at45 into compacted but penetrable layersdid not deflect. Wilson

(1967)found that

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


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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 turndownwards 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 whitelight (Coutts and Nicholl, unpublished).Such responses indicate that care must beexercised when using root boxes withtransparent 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 influencedby temperature. At soil temperaturesabove and below 17C, 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 rootdevelopment (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, andregeneration takes place when it falls

during drier periods. Such periodic deathand regrowth produce the well-knownshaving 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 0-45from the vertical did not deflect when

approaching a water table maintained26 cm below the surface (Coutts andNicholl, 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-

sarilymean

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

Little is known about the response ofplagiotropic 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-drained

soil. The proliferation of the surface rootsof trees on wet sites may be a result ofcompensatory growth rather than achange in orientation.


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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 Zobels(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 diageotropicbut the

roots of three other species did notrespond 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 positive

geotropism oftree

roots is difficultto

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 surfaceof the

peat. 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 invarious orientations. In most plants tested,including Pinus, no consistent curvaturetowards the wet soil occurred. In specieswhich gave a positive result, the 1

L wereunaffected,

onlythe 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 Ewans 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 itwas concluded that the cap sensed ahumidity gradient.

These results have implications for thebehaviour of tree roots at the soil surfaceand where horizontally growing roots


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Factors Affecting the Direction of Growth of Tree Roots

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