LEAF RESISTANCE IN A GLASSHOUSE TOMATO CROP IN RELATION TO LEAF POSITION AND SOLAR RADIATION
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1 New Phytol. (1969) 68, LEAF RESISTANCE IN A GLASSHOUSE TOMATO CROP IN RELATION TO LEAF POSITION AND SOLAR RADIATION BY R. G. HURD Glasshouse Crops Research Institute, Littlehampton, Sussex {Received 4 November 1968) SUMMARY Leaf resistances were measured in a glasshouse tomato crop, using a mass flow porometer. With plants of different age the sixth to eleventh leaf from the top of the plant had the lowest leaf resistance, both within the stand and at its perimeter. Full leaf expansion occurred at the twelfth to fourteenth leaf. Older leaves had high leaf resistances, especially within the crop. Raising the COj concentration of the glasshouse to approximately 1000 vpm tended to increase leaf resistance but this increase was seldom significant and was sometimes not observed at all. On sunny days, leaf resistances were higher for much of the day than resistances on dull days. This was believed to be due to a form of the midday stomatal closure observed in some plants under high insolation. INTRODUCTION Whilst there is a considerable amount of information on stomatal movements in plants, relatively little refers to plants growing as a crop. This is particularly true of glasshouse crops although, because of the measure of environmental control possible, studies of this sort should be easier to interpret than those in an outdoor crop. Field studies have recently been made easier by the development of a portable porometer which gives measurements quickly and hence provides sufficient information to overcome the variability usually encountered in field material (Alvim, 1964; Bierhuizen, Slatyer and Rose, 1965; Shimshi, 1967). The original version was used in the present project to investigate effects of solar radiation, CO 2 concentration and leaf position on leaf resistance in a tomato crop. METHODS Tomato plants {Lycopersicon esculentum Mill.) sown in mid-november were grown at approximately 20 C day 18 C night, although the temperatures varied slightly between years within the range C depending on treatment. The plants were spaced 30 cm apart with a metre wide path between alternate rows. Selected plants were either well within the block of plants or, where specified, were guard plants on the east or west boundary of the block. Surrounding the whole block was a path with a row of plants on the outside against the glass. The plants were 1-2 m high when the measurements were taken (March-June). They were supplied with water and nutrients by means of a trickle irrigation system and in hot weather were sprayed before midday. When houses were given additional COj this was supplied from a liquid CO2 source via perforated layhat 265
2 266 R. G. HURD polythene tubing to ensure uniform distribution. COj concentrations between 800 and 1500 vpm (volumes per million), depending on wind speed, were achieved during the hours of daylight from a standard rate of injection. CO2 analysis was originally made with an infra-red gas analyser but for spot checks during these experiments a simple semi-quantitative volumetric method of assay was used. A mass flow porometer (Alvim, 1964) was used to measure leaf resistance (R^), calculated after Bierhuizen et al. (1965), assuming a mean air pressure difference across the leaf of 7 cm mercury. In early experiments the time taken for a given pressure drop was recorded, requiring no log transformation to obtain mean values, but later the pressure drop over 15 seconds was determined since it enabled measurements to be made quickly even at high leaf resistances. As glasshouse tomato leaves are delicate it is necessary to squash the leaf tissue to make an airtight seal between the leaf and porometer, incidentally preventing lateral air movement. By taking repeated measurements close together on the same leaflet it was found with this technique that approximately 2 minutes elapsed before stomatal closure began. During this 2 minute period the log pressure fell linearly with time. Shimshi (1967) found a similar time before stomatal reaction following application of the porometer in three different crops. The temporary increase in leaf resistance he found in some species ('Ivanov' effect) immediately after applying the porometer was not observed. All the leaflets of a leaf had resistances of the same order, with two exceptions. Only the distal more expanded leaflets of leaves less than about 5 cm long had low resistances and the terminal leaflets of old leaves usually had high resistances, possibly because they were either often curled under or were the oldest expanded part of the leaf. Middle leaflets were selected for most measurements and were only measured once; no leaf was recorded more frequently than every 2 hours. Considerable variability within and between leaves of the same age (coeflicients of variation of the order of 100%) necessitated as much replication as could be conveniently achieved. Leaf resistance and stomatal dimensions were recorded simultaneously on 27 June 1967 for the tenth leaf (counting leaves > i cm long from the top of the plant) of tomato plants cv. J14. Stomatal measurements close to the porometer cup were taken from leaf impressions obtained with dental plastic (Sampson, 1961). Log i?^ was found to be highly correlated inversely with log pore width. Jarvis, Rose and Begg (1967) established a theoretical relationship between i?l ^n.<i l^^f anatomical dimensions. Their equation 8 was simplifled for the present data based on several leaves since stomatal dimensions were the same on the upper and lower surface for any one leaf, stomatal depth was assumed constant, and stomatal frequency was found to be approximately the same for all the leaves used. Pooling the resulting constants in their equation gives the relation where i?; is the internal leaf resistance, b and w are stomatal length and width respectively and C is the coefhcient of slip. A highly signiflcant straight line relation was obtained between i?l ^nd ^/w^b [w + bq; R^ was calculated to be 3.0 x 10* g cm"^ sec"^ Jarvis et al. (1967) calculated R^ for young cotton leaves, from anatomical dimensions, to be 1.2 X 10* g cm"^ sec"^ Since R^ was usually much greater than this (3.0 x 10* to 200 X io"^ g cm"^ sec"^) it is largely the result of stomatal resistance. To distinguish resistances higher than 200x10* g cm~^ sec~^ would have required a porometer of much smaller air capacity than the 225 ml volume of the instrument used here.
3 Leaf resistance in a tomato crop 267 Solar radiation was measured outside the glasshouse with a Kipp solarimeter operating a potentiometric recorder. Approximately 60% of the outdoor radiation is received inside glassbouses of tbe type used here (Edwards, 1963). RESULTS Variation with leaf position The leaf resistance {Ri) of five 3-montb old plants cv. Ware Cross within a block of plants was recorded at four intervals during the day. The plants were i m high and had twenty-two leaves longer than i cm. Tbe outdoor radiation receipt for this rather dull 12 hour day (23 March 1965) was 185 cal cm~^ total radiation. (a) _ (b). (c) - o o - o [ome xlo'tg 1] I [older leoves removed] c-') Fig I. Mean leaf resistance during the day for successive leaves, (a) Plants with twenty-two leaves (o) and thirty-four leaves (D) growing within the stand; (b) edge plants, all leaves; (c) edge plants, unshaded leaves. Arrows indicate first mature (fully expanded) leat. i?l varied with leaf position in a well-defined pattern, wbich was also obtained in other experiments witb plants of this age (Fig. la, plants with twenty-two leaves). The top few leaves had high resistances which decreased progressively down to the seventh to ninth leaf. R^ then increased again in the next five leaves and stayed high m the remaining leaves, the gas volume in the porometer being too large to detect any pressure drop in these leaves within 1.5 minutes. A month later, when these plants had thirtyfour leaves (recorded on 23 April 1965, with total radiation 217 cal cm" ), the pattern of R, with leaf position was very similar to that found previously (Fig. la), although on the later date three or four more leaves had low resistances and the zone of lowest resistance was between leaves nine and eleven. Measurements of illumination made with a photocell showed that the top six or seven leaves were exposed to almost full illumination whilst the leaves with lowest i?l were in a zone some 30 cm from the top of the crop where leaf shading was appreciable.
4 268 R. G. HuRD Determinations of leaf maturity from thirty-six plants grown under similar conditions the previous year showed that in plants with twenty-four and thirty-three leaves, the twelfth and fourteenth leaves respectively were the youngest 'mature' leaves (showing no further increase in length for i week). Thus the least resistance to mass flow of air was found in leaves three or four nodes above the first fully expanded leaf. Measurements were made on five guard plants of cv. Minibelle (total forty-six leaves) on the west face of a block throughout a sunny day (2 June 1965: 524 cal cm ^) for comparison with plants grown within the crop. The records taken between and hours GMT shown in Fig. i (b and c) demonstrate that stomata of even the 08, Fig. 2. Variation in leaf resistance on a dull and a bright day. Upper graph shows radiation receipt on 26 April 1967 ( ) and ii April 1967 ( ), and the lower graph the leaf resistance of leaf eight (o) and leaf nine (D) on 26 April 1967 and leaf eight ( ) and leaf nine ( ) on 11 April lower leaves were open to a variable extent, although only the upper leaves had consistently low resistances. This was true whether the comparison was made between all the measurements (Fig. ib) or when only those from fully exposed leaves were compared (Fig. ic). The higher i?l of the lower leaves compared with those in the top of the plant may still be due to the lower radiation towards the bottom of the plant even in guard rows, hut it seems likely that an increase in i?l 'with leaf age exists. On the previous day, when radiation of 344 cal cm ~ ^ was recorded, leaves below about the twelfth leaf of eastfacing guard plants had very high resistances throughout the day. Earlier in the year (25 and 26 March 1965) plants next to the glass and therefore fully exposed to the sun
5 Leaf resistance in a tomato crop 269 had shown the same pattern of high R^ in leaves below about the twelfth (from a total of twenty-two leaves). These records were taken in the early afternoon on well-watered plants. It is concluded that normally, and certainly within the crop, most leaves below the top fifteen or so have a high i?l. Variation with solar radiation The change in i?l of younger leaves over the day was followed on several occasions in plants of cv. GCR93 and compared with outdoor records of solar radiation. On dull days i?l diminished to values as low as x 10* g cm"^ sec~^ by hours GMT, increasing slowly again after about hours. In sunny weather i?l ^^s low in the morning, although seldom as low as on dull days and gradually increased with time (Fig. 2). Thus on average between hours and hours the leaves had a higher resistance to viscous flow of air on bright than on dull days. The consistency of this effect is demonstrated in Table i: the average 2?L on three dull days was only 15 x 10* g cm" ^ sec" * Table 1. Mean total radiation outside the glasshouse and leaf resistance between and hours GMT on three dull and three bright days Date II April April April 1967 Mean Leaf no j9 \ CO2 enriched (X Mean leaf resistance 10* g cm"^ sec"') II.I II.I Mean radiation (cal cm"^ mi: April April April 1967 Mean II O I.os I Leaf resistances are the mean of eight replicated determinations repeated at approximately hourly intervals over the period. over the midday period, whereas on sunny days with much higher radiation levels R^ averaged 47x10** g cm'^ sec"^ Spraying the foliage with water, which is normal commercial practice in hot weather, usually increased the resistance to viscous flow considerably for about half-an-hour, apparently due to liquid water either in or on the leaf. When this surplus water had evaporated the leaves did not have a lower resistance than before spraying. Watering the plants during a sunny day (Fig. 2) decreased the ninth leaf resistance, but it did not drop to that of plants exposed to low radiation; the eighth leaf resistance was not decreased by watering. Changes in i?l with leaf position were also compared at different times during the day. i?l was determined at six leaf positions between leaf five and twenty at four times during the day on eight replicate plants. The morning was dull becoming fine in the afternoon (10 April 1967). Free hand curves through the mean values of R^ for each leaf position show (Fig. 3) that the pattern of leaf resistance was unaltered throughout
6 270 R. G. HuRD fffu\o'^g cm-2sec-l) 250 Fig. 3. Variation in leaf resistance at different leaf positions at the four times shown. RL based on eight replicates for each of six leaf positions. o_ S 0 8 a ' p *- o o- 0-4 o _ <J o ^^ o I io.oo J Time (GMT) Fig. 4. Leaf resistance at approximately 1000 vpm CO2 (O) or approximately 350 vpm CO2 (D) in relation to the radiation receipt on 13 April i?l based on eight replicate determinations from leaves nine or ten.
7 Leaf resistance in a tomato crop 271 the day. Minor changes in R^ affecting upper and lower leaves rather differently were not consistently obtained. Variation with CO 2 concentration The effect of CO 2 enrichment on i?^ was studied by comparing plants in similar adjacent glasshouses maintained at the same temperatures. The comparison was made on 13 April 1967 when the plants were 5 months old and had forty-three leaves. Three spot checks of CO2 concentration at 10.00, and hours showed that at each of these times the CO2 concentration in the enriched house was approximately 1000 vpm whilst that in the control house was 350 vpm. Total radiation was 169 cal cm"^ for a 13.3 hour day; for a period in the afternoon with some sunshine, intermittent ventilation would have temporarily diminished the level of enrichment. Frequent determinations of i?l showed that at no time were there any effects of CO2 on i?l (Fig. 4). The pattern of i?l in both houses was remarkably similar and corresponded to those previously depicted (Fig. 2) for a dull day. However, increases in i?l in C02-enriched houses were obtained in March 1966 in November-sown plants having thirty leaves and also grown in similarly treated glasshouses. On two succeeding days, both with a total outdoor radiation of 210 cal cm"^ and approximately 12.5 hour days, significantly higher i?l in the sixth and ninth leaf were obtained with CO 2 enrichment, the differences diminishing on older leaves with higher resistances. DISCUSSION The seventh to twelfth leaves from the top of the plant (occupying the top 5-40 cm of the canopy) normally had the lowest R^^, whilst leaves below fourteen to sixteen had high resistances, particularly so in plants growing within the crop. It seems unlikely that these differences in i?l are entirely due to variation in radiation. In fact, the relation between R^ and radiation was not close: older fully exposed leaves usually had high resistances, plants on dull days often had lower resistances than on bright days, and the zone of lowest i?l was about 30 cm from the top of the plant where self shading was beginning to reduce the intensity of radiation. On the other hand there is probably a relation with leaf age since the leaves with lowest resistance are those expanding from half to full size, at which time photosynthesis is maximal on a leaf area basis (Hopkinson, 1964; Hardwick, Wood and Woolhouse, 1968). This high rate of photosynthesis may result in the lowest concentrations of CO 2 in the substomatal cavities and hence the widest stomatal aperture. Alternatively, photosynthesis is higher in these leaves because the guard cells open more readily, allowing a greater influx of CO2. MacDowall (1963) found diminishing stomatal apertures in tobacco once leaves reached full size. The most unexpected result has been the lower i?l found on dull days compared with bright ones (Table i). The values of i?l for the two occasions diverge as the day progresses and this may be related to the observation that on sunny afternoons the tops of glasshouse tomatoes sometimes wilt even when soil water is adequate, suggestmg an increasing leaf water deficit. Such an increase in water deficit and associated stomatal closure was obtained even in well-watered outdoor chrysanthemums by Yemm and Willis (1954).,. It seems likely therefore that an increase in R^ with time on days with high insolation is a constant feature of the tomato crop, regardless of the watering regime. The phenomenon could be a form of the frequently observed midday closure of stomata usually
8 272 R. G. HURD attributed to high leaf temperature and water stress (Heath, 1959). It is thought that this results in a high respiration rate and lower photosynthesis (Gates, 1965) thereby increasing the internal CO 2 concentration and inducing the stomata to close. It is also possible that the increase in i?l on sunny days is not entirely due to a change in stomatal resistance. Gale and PoljakoflF-Mayber (1967) found that internal leaf resistance in beans increased without a change in stomatal diffusion resistance as relative humidity was reduced. In the present experiments atmospheric humidity would have been lower on sunny than on dull days, although raising humidity by leaf spraying in fine weather did not reduce i?l to the value observed on days with less radiation. A final explanation of this difference in i?l with radiation intensity will require simultaneous measurements of the leaf water status and components of leaf resistance on bright and dull days, whilst a direct assessment of its practical significance could be obtained from photosynthesis measurements. Plants which had been grown in atmospheres normally enriched with CO2 during the day sometimes had higher values of i?l than control plants although this was not consistent. On one occasion small increases in resistance were consistently found, on another, apparently similar day the following year, no such differences were observed. Reductions in stomatal aperture have been obtained at above ambient CO2 concentrations in some species but not others (Holmgren, Jarvis and Jarvis, 1965; Ford and Thorne, 1967). Pallas (1965) found that tomato stomata were the least sensitive to changes in CO2 concentration of the five species he used, transpiration rates being nearly constant between 400 and 3000 ppm CO2 concentration. From a practical point of view these small reductions in stomatal aperture appear to be of little consequence since CO2 enrichment is widely found to increase yield through increased photosynthesis and in some plants increasing dry weight production has been obtained at concentrations as high as 30,000 vpm CO2 (Imazu, Yabuki and Oda, 1967). ACKNOWLEDGMENT The assistance of Mr R. Hemsley in collecting and transforming the 1967 data is gratefuly acknowledged. REFERENCES ALVIM, P. DE T. (1964). A new type of porometer for measuring stomatal opening and its use in irrigation studies. Arid Zone Res., 25, 325. BiERHUizEN, J. F., SLATYER, R. O. & ROSE, C. W. (1965). A porometer for laboratory and field operation. y. exp. Bot., 16, 182. EDWARDS, R. L (1963). Transmission of solar radiation by glasshouses. Exp. Hort., g, i. FORD, M. A. & THORNE, G. N. (1967). Effect of CO2 concentration on growth of sugar-beet, barley, kale and maize. Ann. Bot. N.S., 31, 629. GALE, J. & POLJAKOFF-MAYBER, A. (1967). Resistance to gas flow through the leaf and its significance to measurements made with viscous fiow and diffusion porometers. Israel J. Bot., 16, 205. GATES, D. M. (1965). Energy, plants and ecology. Ecology, 46, i. HARDWICK, K., WOOD, M. & WOOLHOUSE, H. W. (1968). Photosynthesis and respiration in relation to leaf age in Perilla frutescens (L.) Britt. Neiv Phytol., 67, 79. HEATH, O. V. S. (1959). The water relations of stomatal cells and the mechanisms of stomatal movement. In: Plant Physiology, Vol. II (Ed. by E. C. Steward). Academic Press, New York. HOLMGREN, P., JARVIS, P. G. & JARVIS, M. S. (1965). Resistances to carbon dioxide and water vapour transfer in leaves of different plant species. Physiologia PL, 18, 557. HoPKiNSON, J. M. (1964). Studies on the expansion of the leaf surface. IV. The carbon and phosphorus economy of a leaf. j. exp. Bot., 15, 125. IMAZU, T., YABUKI, K. & ODA, Y. (1967). Studies on the carbon dioxide environment for plant growth. I. Effects of carbon dioxide concentration on the growth of Swiss chard {Beta vulgaris L. var. flavescens D.C.). y. yap. Soc. hort. Sci., 36, 179.
9 Leaf resistance in a tomato crop 273 JARVIS, P. G., ROSE, C. W. & BEGG, J. E. (1967). An experimental and theoretical comparison of viscous and diffusive resistances to gas flow through amphistomatous leaves. Agric. MeteoroL, 4, 103. MACDOWALL, F. D. H. (1963). Midday closure of stomata in ageing tobacco leaves. Can. J. Bot., 41, PALLAS, J. E. JR (1965). Transpiration and stomatal opening with changes in CO^ content of the air. Science, N.Y., 147, 171. SAMPSON, K. (1961). A method of replicating dry or moist surfaces for examination by light microscopy. Nature, Lond., 191, 932. SHIMSHI, D. (1967). Some aspects of stomatal behaviour, as observed by means of an improved pressuredrop porometer. Israel jf. Bot., 16, 19. YEMM, E. W. & WILLIS, A. J. (1954). Stomatal movements and changes of carbohydrate in leaves of Chrysanthemuin maximum. New PhytoL, 53, 375.
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