Leaf Growth in Dactylis glomerata following Defoliation J. L. DAVIDSON' AND F. L. MILTHORPE
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1 Leaf Growth in Dactylis glomerata following Defoliation BY J. L. DAVIDSON' AND F. L. MILTHORPE Unwertity of Nottingham School of Agriculture, Sutton Bonmgton, Loughborovgh ABSTRACT Defoliation to a height of 2-5 cm considerably reduced the increase in leaf area in young Dactylis glomerata (cocksfoot) plants compared with that of intact plants, the reduction in the rate of appearance of new leaves being relatively greater than the reduction in expansion of existing leaves. The growth of those expanding leaves which were cut during defoliation accounted for 94 per cent of the total increase in leaf area during the first four days after defoliation. In such a leaf, expanding cells were confined to a basal section which was well below the ligule of the enclosing fully expanded leaf. There was a positive relationship between rate of leaf expansion and total soluble carbohydrate content of the stubble when the carbohydrate content was varied by placing the plants in the dark, but not when it was varied by defoliation and subsequent growth. These and other results suggest that the concentration of soluble carbohydrate in the bases of expanding leaves was a factor controlling leaf expansion following defoliation, and that the concentration in any one leaf depended on the photosynthetic contribution from its exposed portion. When the external nutrient supply was high, removal of the laminae of fully expanded leaves, which comprised about two-thirds of the total leaf area, did not reduce leaf expansion. When the nutrient status was low, these leaves were of primary importance, presumably because of their role as a source of labile nutrients. INTRODUCTION ONE of the more controversial topics in grassland agronomy is the question of the significance of soluble carbohydrate 'reserves' in regrowth which follows defoliation. Field studies have shown that growth after defoliation is generally associated with a decline in the soluble carbohydrate content of both roots and stubble (e.g. Graber et al., 1927; Weinmann, 1948). These changes led to the belief that after defoliation carbohydrate reserves are converted to structural components of new and expanding cells and may control the rate of regrowth. Weinmann (1952) argued from these concepts that the aim of pasture management must be to maintain an adequate level of reserves in the desirable species of the sward. The significance of the soluble carbohydrates in growth generally was questioned when Archbold (1945) showed that accumulated sugars and fructosans in the stem of barley contributed little to subsequent grain development. More recently, the arguments have been reviewed by May (i960) who concluded 1 C.S.I.R.O. Division of Plant Industry, Deniliquin, N.S.W., Australia. [Annals of Botany, N.S. Vol. 30, No. 118, 1966.]
2 174 Davidson and Milthorpe Leaf Growth in Dactylis that the role of accumulated soluble carbohydrates in regrowth of grass has yet to be established. Growth following defoliation depends first of all on the development of a photosynthetic surface. It seems reasonable to expect that the factors most important in determining rates of regrowth will be those upon which leaf growth after defoliation is primarily dependent. The series of experiments described here was an attempt to examine the influence of some of the most likely factors to be concerned during the period immediately following defoliation. DEVELOPMENT OF THE LEAF SURFACE Measurements were made of the relative contributions of leaves cut by the defoliation treatment and of younger leaves to the developing leaf surface. Experimental Procedures In this and subsequent experiments reported here, the cultural techniques employed to grow plants of S37 cocksfoot {Dactylis glomerata L.) were the same as previously reported (Davidson and Milthorpe, 1965). Plants were grown in sand culture with standard Long Ashton nutrient solution (Hewitt, 1952) at 22 0 C with a 16-hour day of 2-90 cal visible radiation/cm 2 /hr. When the plants were five weeks old all exposed laminae were removed and each tiller was cut to a height of 2-5 cm. The areas of cut and uncut leaves were measured 2, 4, 8, and 16 days later, five plants being taken at each harvest. Results Growth measurements on uncut plants of the same age and size grown under the same conditions were reported previously (Davidson and Milthorpe, 1965). Comparison with these show that defoliation to 2-5 cm caused marked reductions in the rate of leaf appearance and leaf-area increase (Table 1). TABLE I Mean increases in leaf area and leaf number of intact and defoliated plants under otherwise similar conditions Treatment Intact plants Defoliated to a a height of 2-5 cm. Onginal leaf area (cm 1 ) (before defoliation) Increase in leaf area (cm 1 ) Increase in leaf number Tune interval (days) 7 8 Increase in leaf number was reduced relatively more than increase in leaf area. Indeed, immediately following defoliation, leaf expansion was almost entirely dependent on the expansion of the older expanding leaves which
3 Davidson and Milthorpe Leaf Growth in Dactylis 175 were actually cut during defoliation (Fig. 1). The younger uncut leaves accounted for 2, 6, 20, and 65 per cent of the total increase in leaf area at 2, 4, 8, and 16 days after defoliation respectively; their contribution was significant only after eight days, by which time expansion of the older cut leaves had apparently ceased DUncut leaves Leaves uncut during' defoliation ISO 50 A Days after defoliation FIG. 1. Expansion of cut and uncut leaves following defoliation of the plant to a height of 3-5 an. These results suggest that immediately following defoliation growth is controlled by those factors which limit the rate of expansion of the older expanding leaves. INFLUENCE OF SOLUBLE CARBOHYDRATE LEVEL The effect of total soluble carbohydrate content on leaf growth after defoliation was explored on plants of different initial carbohydrate status, achieved by dark treatment, and defoliated at intervals during regrowth. Experimental Procedures Six weeks after emergence plants were divided into two groups: (1) those with a high initial status of carbohydrates were grown throughout in sand culture at 25 0 C and 16-hour daylength of 778 cal visible radiation/cm 2 /hr, and (2) those with low carbohydrate status were transferred from the above conditions to complete darkness at 25 0 C for the 48 hours preceding defoliation.
4 176 Davidson and Milthorpe Leaf Growth in Dactylis The plants were defoliated by removing all exposed laminae and were then returned to the lighted growth room. Defoliation was repeated at two-day intervals for eight days. One sub-group of six plants of initially high carbohydrate status was kept in complete darkness for these eight days. At each defoliation three replicates of the treatments other than that in continuous darkness were preserved for carbohydrate determinations. Results Treatment in the dark for 48 hours resulted in a low initial content of soluble carbohydrate in both tops and roots (Fig. 2A). Following the initial 10 J \ v lo ROOTS Days after initial defoliation I 30 L20 s 10 I I initial carbohydrate Iffl Low initial carbohydrate High initial carbohydratecontinual dark Days after initial defoliation FIG. 3. (A) Total soluble carbohydrate content of plants subjected to lamina removal at twoday intervals. Plants of high and low initial carbohydrate status are denoted by circles and crosses respectively. Closed circles denote plants kept in continual darkness, (B) Leaf expansion in two days following the successive defoliation of plants with different initial soluble carbohydrate levels. Vertical lines represent least significant differences (P = 0-05). defoliation there was a marked carbohydrate decline in the tops for four to six days followed by a rise, with the two initially different treatments converging. In roots of high initial carbohydrate status the level fell for four days before reaching a stable level; in roots of initially low carbohydrate status the content varied little with time. Over the two days following the first defoliation, leaf expansion was greater in plants of high initial carbohydrate level than in plants with a low initial level; it was no less in complete darkness than under lights when the initial carbohydrate levels were similar (Fig. 2B). Despite this apparent relationship between leaf expansion during the first two days after defoliation and initial carbohydrate level, there was no evidence of such a relationship with sub-
5 Davidson and Milthorpe Leaf Growth in Dactylis 177 sequent defoliation. For instance, in plants initially of high carbohydrate status, although the initial total soluble carbohydrate content in both tops and roots was approximately double that at subsequent defoliations, leaf expansion was scarcely altered. Also, over the two days following the second and subsequent defoliations, leaf expansion in plants of low initial carbohydrate status was greater than it was after the first defoliation even though the soluble carbohydrate content was then lower. A reduction in soluble carbohydrate content brought about by growth following defoliation did not lead to reduced leaf expansion; a similar reduction resulting from dark treatment was associated with a significant reduction in leaf expansion following defoliation. After eight days in complete darkness, when the rate of leaf expansion was very low compared with other treatments, the soluble carbohydrate content of the tops was approximately half that of the other treatments. This supports the conclusion of Albert (1927) that growth in complete darkness stops when considerable carbohydrate remains, and suggests that not all of the total soluble carbohydrate is available for leaf expansion or can be used in it. THE SITE OF LEAF EXPANSION Experimental Procedures Measurements to determine the location of expanding cells within laminae and leaf sheaths were confined to leaves on the main tiller. After having been grown forfiveweeks at 22 C and 3-2 cal visible radiation/cm*/hr with a 16-hour daylength, plants were selected for uniformity of length of main tiller. 1. The lamina. All visible laminae (sections above ligules) on the main tiller were marked with Indian ink at four or five equal intervals. The lengths and median widths of each section were measured at the time of marking and again after 24 hours. 2. The leaf base. When the young plants are defoliated by the removal of all laminae, the remaining stubble consists of the sheaths of the older leaves with ligules exposed (which will be referred to as 'outer' leaves) and all parts of younger leaves enclosed by these sheaths (referred to as 'inner' leaves). This stubble, with laminae still attached, was marked to denote four measured sections by length the basal 1 cm (Section d), and the remainder divided into three equal parts (Sections c, b, and a, respectively, reading from the base). At the top of each section a fine needle was pushed horizontally through the centre of the tiller. After 24 hours the length of each section was measured on all marked leaves. Using the method of Wright (1961) cell numbers were estimated in each section of expanding and fully expanded leaves. Results There was no measurable change in the dimensions of exposed laminae over the 24-hour period. This confirms the conclusions of Sharman (1942), Esau (1943), and Begg and Wright (1962) that the exposed parts of grass leaves
6 178 Davidson and Milthorpe Leaf Growth in Dactylis are fully expanded, as are those leaves with exposed ligules. Measurements of lamina expansion can therefore be confined to those leaves whose ligules are not yet exposed. TABLE 2 The extension in 24 hours, initial cell number, and carbohydrate content of successive sections of inner and outer leaf bases Distance Initial total soluble from tiller Extension Cell number carbohydrate content Section base (cm) (cm) (io'/g fresh weight) (per cent dry weight) Inner Outer Inner Outer Inner Outer a o b o o c I- S io d o-i-o i-o o S.E... ± ±1-42 ±0-08 The piercing technique employed on the stubble did result in reduced leaf extension 3-2^0-14 and 2-5^0-14 cm/day in normal and pierced plants, respectively perhaps by damaging vascular tissue and thereby reducing substrate flow to expanding cells. However, the technique served to indicate that cell extension was confined to the basal Sections c and d which consisted of small densely packed cells (Table 2). The zone of extension did not extend into Section b in any replicate and, therefore, was probably limited to the lowest 3 cm of the stubble. THE EXTENT OF CARBOHYDRATE REDUCTION IN DIFFERENT LEAVES Measurements were made of the reduction in the soluble carbohydrate content of expanding and fully expanded leaves brought about by treatment in the dark and growth following defoliation. Experimental Procedures Plants were grown at 25 0 C and 7-78 cal visible radiation/cm 2 /hr for 16 hours per day for six weeks after emergence. One group was then defoliated by removing all laminae and kept under the same conditions (defoliation treatment); another was put into continuous darkness at a similar temperature (dark treatment), and a third group was grown without disturbance (normal treatment). After two days in these conditions the plants were stripped of all exposed laminae, and the bases of expanding and fully expanded leaves separated. These portions were then analysed for soluble carbohydrates. Results In each of the treatments 74 per cent of the dry matter of the stubble was accounted for by the sheaths of outer fully expanded leaves and 36 per cent by the younger expanding leaves. Total soluble carbohydrates comprised 10-3, 6-5, and 4-8 per cent of the dry matter in the normal, defoliation, and dark
7 Davidson and Milthorpe Leaf Growth in Dactylis 179 treatments, respectively. In the younger expanding leaves the total soluble carbohydrate concentration was almost double that of the outer, older, fully expanded leaves (Table 3). TABLE 3 The soluble carbohydrate contents of the bases of expanding and fully expanded leaves in plants subjected to dark and defoliation treatments for 2 days Carbohydrate content Treatment Normal Defoliation Dark S.E. Leaves Expanding Fully expanded Expanding Fully expanded Expanding Fully expanded (per cent dry matter) Alcohol-soluble IO-I 'I ±049 Fructosan IO-I i'i ±O-I9 Total soluble ±0-52 Reduction of towi as per cent of normal values The dark treatment led to the same relative reduction of carbohydrate concentration in expanding as in fully expanded leaves, whereas, with the defoliation treatment, the relative reduction in the expanding leaves was only half of that of the older fully expanded leaves which comprised three-quarters of the total dry weight. The results suggest that only that soluble carbohydrate held in the base of an expanding leaf is used for subsequent expansion of that leaf; the much greater quantity of soluble carbohydrate in the bases of older fully expanded leaves may have little direct influence on leaf expansion but may well be used by roots and tiller buds. INFLUENCE OF LEVEL OF DEFOLIATION ON LEAF GROWTH The effect of varying the height of cutting on the subsequent rate of leaf expansion was investigated. Experimental Procedures Plants were grown under the conditions described in the section on leaf expansion above for five weeks and the tillers were then marked to delineate Sections a, b, c, and d, as described on p All laminae were removed and the stubble was cut off at the top of Sections a, b, c, and d. Leaf expansion was measured after 24 hours. Results The removal of all laminae led to a 44 per cent reduction in leaf extension (Table 4). Further removal of Section a, the top one-third of the stubble S3 55
8 180 Davidson and Milthorpe Leaf Growth in Dactylis length, caused no further reduction, but removal of Sections b and c led to reductions of 62 and 91 per cent respectively in leaf extension compared with uncut plants. The effects on leaf-area increase were essentially the same. TABLE 4 Leaf growth in the first 24 hours after defoliation from main tillers cut to different heights Level of defoliation to the top of section Intact plants a b c d S.E. Stubble length (cm) i-o ±0-73 Leaf extension (cm) 3-2 i-8 19 I '2 o-3 ±0-15 Leaf area increase (cm 1 ) I'l O-2 ±O-2I Reduced leaf expansion which follows the removal of all tissue above the limit of cell expansion is presumably the result of depleted substrate (and possibly hormone) supply. The drastic effect of removing all but 1 cm of stubble involves the added consequence of removing part of the reservoir of cells upon which leaf expansion depends. INFLUENCE OF NUTRIENT SUPPLY ON LEAF GROWTH AFTER DEFOLIATION The effects of leaf removal were examined under conditions of continuous and restricted nutrient supply. Experimental Procedures Plants were grown at 22 0 C under a 16-hour day of 3-2 cal visible radiation/ cm 2 /hr for six weeks after emergence with the normal nutrient supply. Half the number of pots were then leached with standard and half with onetenth standard Long Ashton nutrient solution. Two days later, plants in each group were subjected to one of the following defoliation treatments: (1) undefoliated; (2) laminae of fully expanded leaves removed; (3) visible laminae of expanding leaves removed; (4) all visible laminae removed. Leaf expansion of the main tiller was measured after 29 hours. Results At each nutrient level 63 per cent of the total leaf area was removed with the fully expanded leaves and 37 per cent with the younger expanding leaves. The effect of reducing the nutrient supply on leaf growth was rapid. Within two days the low nutrient supply led to a significant reduction in leaf growth (Table 5). At both nutrient levels complete lamina removal reduced leaf extension to the same value. At the high (normal) level of nutrient supply the removal of all fully expanded leaves, i.e. two-thirds of the total leaf area,
9 Davidson and MiUhorpe Leaf Growth in Dactylis 181 did not reduce the rate of leaf extension. However, this was reduced significantly by removing the exposed laminae of the expanding leaves. This supports the concept already developed that under the conditions of continuous nutrient supply maintained in these experiments, leaf expansion depended TABLE 5 Leaf extension from the main tiller of plants subjected to different defoliation treatments at two levels of the external nutrient supply Leaf extension (cm) High nutrient Low nutrient Laminae removed supply supply None 43 3'3 Fully expanded Expanding All s S.E... ±026 ±026 primarily on the photosynthesis of the expanding leaves themselves. When these exposed laminae were removed, photosynthate from the older, fully expanded leaves was presumably drawn upon since their removal led to a further reduction in extension. At low nutrient status the results were not conclusive. Following the removal of all fully expanded leaves, leaf extension was similar to that when all leaves were removed and significantly less than when only expanding leaves were removed; yet the removal of either category of leaf resulted in extension not significantly different from that of the uncut plants. In order to test these responses further, plants were grown as before except that no nutrients were added from two weeks prior to defoliation in order to deplete further the nutrient status of the plants. Leaf extension was then measured four days after defoliation and was II-I, io-o, and 8-6^0-^2 cm from the three treatments, uncut, expanding leaves removed, and fully expanded leaves removed, respectively. These further results indicate that, under conditions of limiting nutrient status, the removal of fully expanded leaves caused a significant reduction in leaf extension, whereas the removal of the younger, expanding leaves had no significant effect. The results suggest that there may be an interaction of nutrient and carbohydrate limitations on leaf growth following defoliation. The fully expanded leaves were presumably a reservoir of labile nutrients, and their removal, when the nutrient status was low, led to reduced leaf extension; further, these older leaves possibly supply to the roots carbohydrate required for continued uptake of nutrients. When the nutrient supply was high, leaf extension was apparently controlled by the carbohydrate concentration in the base of the expanding leaves, and was influenced primarily by the photosynthate produced by the exposed laminae of these leaves.
10 182 Davidson and Milthorpe Leaf Growth in Dactytis DISCUSSION In cocksfoot, as in other grasses, the leaves which are still expanding are those emerging vertically from the enclosing sheaths; leaves which are fully expanded are those with fully exposed ligules from which the laminae bend back. In the experiments, these visible expanding leaves were mainly responsible for the initial increase in leaf area after defoliation. In the first four days after cutting to a height of 2-5 cm, only 6 per cent of the increase in leaf area could be attributed to expanding leaves too small to be cut by the treatment imposed. Some confusion is evident in publications concerning the zone of leaf expansion. Sampson (1952) and Stoddart and Smith (1955) stated that the growing region of grasses is concentrated at the base of the blade and the base of sheath. Sharman (1942) concluded from measurements of epidermal cells of maize leaves that cell extension stopped when the tissue emerged from the sheath. Begg and Wright (1962), working with Phalaris anmdmacea, agreed with this view and suggested that the sudden cessation of cell expansion upon emergence from the sheath was associated with phytochrome; however, they found that their measurements of epidermal cell lengths were too variable to determine when cell expansion stopped. In the present study measurements of leaf extension indicate that cell expansion was restricted to regions well within the surrounding sheaths and had ceased before the tissue emerged from them. The observation of a higher concentration of soluble carbohydrates in expanding compared with fully expanded leaves and the apparent increase in concentration towards the leaf base is compatible with the account of leaf development presented by Sharman (1942) from a detailed morphological examination. He showed that, in fully expanded leaves, differentiated vascular elements are linked directly with those of the roots. He also found that vascular differentiation began at the leaf tip and extended down towards the leaf base, so that the lowest region of expanding leaves is without differentiated vascular tissue. Presumably, for carbohydrates to move out of an expanding leaf, they must traverse by diffusion this basal densely packed region of dividing cells; this could result in a build-up of carbohydrate above this zone. If this is the explanation of carbohydrate build-up in the base of an expanding leaf, then the carbohydrate there would be derived from photosynthesis of the exposed blade of the expanding leaf itself. In this respect, autoradiographic studies by Williams (1964) showed very little export of carbohydrate from young leaves; export only commenced when laminae were almost fully expanded. A positive relationship between the rate of leaf expansion and total soluble carbohydrate content of the stubble existed when the carbohydrate content was varied by dark treatment, but not when it was varied by growth following defoliation. The results indicate that the carbohydrate of primary importance in developing the leaf surface is that present above the zone of
11 Davidson and Milthorpe Leaf Growth in Dactytis 183 expansion of expanding leaves (and possibly in roots of those grasses in which carbohydrates accumulate in roots). An originally small but increasing supply to these zones following defoliation will normally result from photosynthesis of the upper sections as the leaves grow. There is no such source in darkness or for older leaves which are fully expanded when cut; the soluble carbohydrate concentration in fully expanded leaves, which comprise the greater Days after defoliation 30 3S FIG. 3. New growth made by plants of low (broken lines) and high (solid lines) carbohydrate status after defoliation to leave two (closed circles) and no (open circles) leaves. (Data of Ward and Blaser, 1061, fig. 3.) proportion of stubble dry weight, is reduced more during normal regrowth than is that of expanding leaves. This reduction probably represents respiratory losses from these tissues and may also include some export to the roots. When the external nutrient status is high the prime effect of defoliation is the sudden depletion of the source of carbohydrate for leaf growth. The removal of the photosynthetic part of expanding leaves caused a marked reduction in leaf expansion, but removal of the laminae of fully expanded leaves, which comprised two-thirds of the total leaf area, had no effect. When the external nutrient supply is low nutrient availability may override carbohydrate depletion in limiting regrowth, and hence, removal of the laminae of fully expanded leaves, which are a source of labile nutrients, had the major effect. This study has concentrated on leaf growth during the first few days after defoliation because it is argued that subsequent growth-rates will depend on this initial development of the leaf surface. Ward and Blaser (1961) concluded from defoliation studies with cocksfoot, in which leaf area was reduced to two amounts and soluble carbohydrate concentrations were varied by dark treatment, that carbohydrate food reserves were influential in stimulating regrowth up to 25 days after plants were completely or partially defoliated. After this,
12 184 Davidson and Milthorpe Leaf Growth in Dactylis regrowth rates were dependent on leaf area (cf. their fig. 3). If, however, these results are plotted on a logarithmic scale, so that the slope between two points is the measure of relative growth-rate (Fig. 3), it is clear that the advantage attributed to a higher leaf area existed from the first harvest, and the influence associated with carbohydrate status was confined to the early growth phase. Their results in fact suggest that some factor associated with carbohydrate status influences leaf expansion immediately after defoliation, with early differences in leaf area resulting in subsequent differences in absolute growth-rates. Results from the study reported here indicate that this factor is the soluble carbohydrate level within the bases of expanding leaves. The first effects of defoliation on growth may be explained largely in terms of effects on the supply of carbohydrate to leaves capable of expansion. Growth substances may also have an important influence, but their role at this stage must remain a matter for speculation. ACKNOWLEDGEMENTS An Overseas Studentship awarded by the Commonwealth Scientific and Industrial Research Organization enabled one of us (J. L. D.) to take part in this work which was included in a thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy. LITERATURE CITED ALBERT, W. B., Studies on the growth of alfalfa and some perennial grasses. J. Am. Soc. Agron. 19, ARCHBOLD, H. K., Some factors concerned in the process of starch storage in the barley grain. Nature, Lond. 156, BEGG, J. E., and WRIGHT, M. J., Growth and development of leaves from intercalary meristems in Phalarii arundinacea L. Ibid. 194, DAVIDSON, J. L., and MILTHORPE, F. L., The effect of temperature on the growth of cocksfoot (Dactylis glomerata L.). Ann. Bot. 29, ESAU, K., Ontogeny of the vascular bundle in Zea mays. Hilgardia, 15, GRABER, L. F., NELSON, N. T., LEUKBL, W. A., and ALBERT, W. B., Organic food reserves in relation to the growth of alfalfa and other perennial herbaceous plants. Bull. Wis. agric. Exp. Stn. 80, HEWITT, E. J., Sand and water culture methods used in the study of plant nutrition. Tech. Commun. Commonw. Bur. Hort. Plantn Crops No. 22. MAY, L. H., i960. The utilization of carbohydrate reserves in pasture plants after defoliation. Herb. Abstr. 30, SAMPSON, A. W., Range Management. Principles and Practices. Wiley, New York. SHARMAN, B. C, Developmental anatomy of the shoot of Zea mays L. Ann. Bot. 6, STODDART, L. A, and SMITH, A. W., Range Management. McGraw-Hill, New York. WARD, C. Y., and BLASER, R. E., Carbohydrate food reserves and leaf area in regrowth of orchard grass. Crop Set. 1, WETNMANN, H., Underground development and reserves of grasses. J. Br. Grassld Soc. 3, Carbohydrate reserves in grasses. Proc. 6th Int. Grassld Congr. 1, WILLIAMS, R. D., Assimilation and translocation in perennial grasses. Ann. Bot. 28, WRIGHT, S. T. C, Growth and cellular differentiation in the wheat coleoptile (Triticum vulgare L.). I. Estimation of cell number, cell volume and certain nitrogenous constituents. J. exp. Bot. 12,
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