The significance of changes in the red/farred ratio, associated with either neighbour plants or twihght, for tillering in Lolium multiflorum Lam.
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1 New Phytol (990), 6, The significance of changes in the red/farred ratio, associated with either neighbour plants or twihght, for tillering in Lolium multiflorum Lam. BYJ.J. CASAL, R. A. SANCHEZ and DIANA GIBSON Departamento de Ecologia Facultad de Agronomta, Universidad de Buenos Aires, 47 Buenos Aires, Argentina {Received 2 June 990; accepted 3 September 990) SUMMARY Lolium multiflorum Lam. plants were used to investigate whether phytochromemediated tillering responses, anticipatory to competition: (a), are potentially disturbed by the twilight drop in the red to farred ratio (R:FR) of sunlight (caused by atmospheric factors), and {b), occur in denselysown (> 280 plants m~^) grass canopies, where competition is quickly established. Isolated plants grown under sunlight received natural low R: FR during twilight, but supplementary R provided simultaneously did not increase tillering. When a wide range of R: FR was provided at the end of natural or fluorescent light photoperiods, tillering was reduced only by very low R:FR (lower than natural twilight R:FR). Leaf sheath length followed a similar pattern of response. Single plants were grown in pots placed at various densities. High densities reduced the R:FR at plant bases and the number of tillers per plant before changes in dry weight and leaf number were found. Both very low R:FR provided at the end of the photoperiod, and increasing plant densities, caused more erectophile shoots. In denselysown canopies of Lolium multiflorum both R:FR signals caused by neighbours, and tillering responses occur well before strong competition is established. Tillering is not obviously affected by the twilight drop in R:FR. Key words: Lolium multiflorum Lam, photomorphogenesis, phytochrome, tillering. INTRODUCTION Under natural conditions photomorphogenic responses mediated by phytochrome provide green plants with a sensitive mechanism for adaptation to the changing light environment in plant stands (Smith, 982; Casal & Smith, 9896). Tillering in grasses is affected by changes in the red: farred (R: FR) of the light perceived by phytochrome (Deregibus, Sanchez & Casal, 983; Casal, Deregibus & Sanchez, 985; Deregibus etal., 985; Kasperbauer & Karlen, 986; Barreiro, Beltrano & Montaldi, 989). We have proposed that, in natural growing grass canopies, this response may occur before intense competition for light is established, inducing a redirection of growth before photoassimilates become scant (Casal, Sanchez & Deregibus, 986; 987). This idea is based on the following observations, {a) Tillering rate can he reduced as a result of small reductions in the R: FR of the light below the values provided by sunlight, even if R: FR reductions are restricted to the base of the shoots, i.e. the part of the plant more likely to become shaded first in growing canopies (Casal et al, 987). {b) Relatively low plant densities, which reduce the daily amount of PAR by less than 5 % compared to that received by isolated plants, may cause a strong reduction of tillering in grass plants grown in pots (Casal et al,, 986). (<:) This density effect is fully reversed by the addition of low amounts of R directed towards the base of the plants, a treatment that does not increase tillering of isolated plants (Casal et al, 986). Similarly, the rate of stem extension growth in dicotyledonous plants is enhanced by the light reflected by nonshading neighbouring plants, sug 392
2 gesting that the R:FR could be an initial signal anticipatinjg competition for light (Ballare et al., 987; 988; Ballare, Scopel & Sanchez, 989; 990; Casal & Smith, 989 b; Smith, Casal & Jackson, 990). However, at least two questions remain on the occurrence and significance of early tillering responses to R: FR before competition is established in grass canopies. {a) Are these responses distorted by the twilight drop in R:FR caused by atmospheric factors and affected by latitude, sky conditions and time of the year (Holmes & Smith, 977; Hughes et al., 984)? Tillering is reduced both by *endofday', 'pure' FR pulses and by small reductions of the R:FR during the photoperiod (Deregibus et al., 983; Casal et al., 985; 987). If the high sensitivity to daytime changes in R: FR were also found for endofday R:FR changes, it might be expected that nonshaded plants respond to the twilight drop in R:FR as if it were a neighbour signal. Physiological experiments suggest that plants could distinguish between the reductions in R:FR that occur during daytime (i.e. related to the presence of neighbours) and at the end of the photoperiod (i.e. not caused by the presence of neighbours) (Casal & Smith, 988; 989 a, b). However, those experiments were conducted with only one dicotyledonous species {Sinapis alba) and were restricted to stem extensiongrowth observations after a single continuous white lightdark transition. {b) In denselysown grass canopies, where competition for light is quickly established, is the R: FR signal anticipatory or virtually overlapping with competition? Implicit in the concept of an anticipatory signal is the idea that in a growing grass canopy the reductions of R: FR should be perceived early enough so as to allow plastic responses to occur by the time PAR becomes limiting. In our previous density experiments (Casal et al., 986), supplementary R provided by lightemitting diodes was effective at low plant densities ( < 40 plants m~^), but not at plant densities either high or very low (i.e. isolated plants). In other words, tillering was increased by R only when the time elapsed before competition was established was considerably long. This question is of importance, for high seedling densities (> 00 seedlings m~^) frequently occur in grasslands, especially soon after the period in which seed germination takes place (Deregibus, Casal & Simone, 986). The aim of this work is to investigate whether Lolium multifiorum (Lam.) plants respond to twilight changes in R: FR, and whether mutualplant shading effects occur on both R:FR and tillering before intense competition for light is established in densely sown canopies. Changes in shoot angle (a novel response) and leafsheath length were recorded in addition to tillering responses, and are reported here. MATERIALS AND METHODS Growth room experiments with endofday irradiations Single Lolium multiflorum Lam. plants were obtained from seed and grown in 67 cm^ pots containing a soilsand mixture in a growth room with the temperature set at 20 C during day (0 h) and night (4 h). PAR of 60/*mol m~^ s~^ was provided by fluorescent lamps (Philips TLF 40 W, spectral emission is shown in Casal et al., 987). Treatments began when the first leaf was fully expanded and at that time PAR was increased to 230 /*mol m~^ s~^ (other conditions remained unchanged). Treatments consisted of 5 min endofday saturating irradiations, giving calculated phytochrome photoequilibria (Pfr/P) = O75 (40/<mol m'si provided by red light fluorescent tubes. Philips TLF 40W/5 ; Pfr/P = 029 (40/^mol m~^ s~^ provided by an incandescent 50 W internal reflector lamp filtered through 5 cm water and two red acetate sheets); Pfr/P = 07 (7/*mol m~^ s"^ provided by an incandescent 50 W internal reflector lamp filtered through 5 cm water, two red and one clear blue acetate sheets); and Pfr/P = 003 (70 /tmol m^^ s"^ provided by a 2000 W quartz halogen incandescent lamp filtered through 0 cm water, two red acetate sheets and three blue acrylic [Paolini 203, Argentina] sheets). Spectral emission of light sources Fig. ) was measured with an ISCO SR spectroradiometer calibrated against an ISCO SR calibrator. The Pfr/P values were calculated as described previously (Casal et al., 987). They are not regarded as the true Pfr/P values established in the tissues where the light signals are perceived, but are used for comparisons among our own experiments (Mancinelli & Lim, 989). In these experiments (0 U C a> _3 0 C o o x: 5 05 (0 +^ ov a CO 0 > ilati cc ft I / ' / /'I // ' V \ ' * > 'l / // / /,' * y' : (/ / / / ' / / ; t Wavelength (nm) Figure. The relative spectral photon fluence rates of the sources used for R/FR irradiations, Pfr/P = 0 03 (i.e. FR);, Pfr/P = 07;, Pfr/P = 0 29;, Pfr/P = 075 (i.e. R). ' / y...
3 Effect of red/farred ratio on tillering in Lolium 567 planttoplant light reflection was minimal as very young seedlings were used. Glasshouse experiments with irradiations at the end of the photoperiod Single plants were obtained from seed and grown in 240 cm^ pots filled with a soilsand mixture in a heated glasshouse (min. temperature > 4 C). Experiments were conducted in autumn, winter and spring and photoperiod ranged from 0 to 4 h, and PAR at midday from 200 to 500/*mol m'^ s~^ (cloudy winter days and clear spring days respectively). Treatments began when the first leaf was expanding and consisted of 90 min irradiations which started 30 min before sunset. Different R:FR were obtained by using a series of light sources with emission spectra similar to those described for growth room experiments. These sources were placed above the plants and, in order to obtain intermediate R: FR some of the plants were placed at intermediate positions between two different light sources, thus receiving a mixture of light from both of them. As a result of solar angle the shade of light sources was not projected over the plants. In different experiments and positions the irradiance provided by the sources at plant position ranged from to 8 /tmol m~^ s~^. No obvious effects were found as a result of these differences. Moreover the irradiance of the R:FR treatments reaching the plants was not systematically correlated to the R: FR as different light source combinations were used in different experiments. Plant density experiments Single plants were grown from seed in a heated glasshouse in 300 or 67 cm^ pots (different experiments) filled with a soilsand mixture. Light and temperature conditions were as described above. The R and FR (650 and 725 nm) quantum fluxes were measured with the I SCO spectroradiometer. The cosinecorrected head of the remote probe was located on a horizontal planar surface either above or within the canopy at the height of plant bases by temporarily removing a central plant pot from each of the experimental arrays. In order to determine above and below ground biomass, the material was oven dried at 70 C and weighed. Site filling (i.e. the rate of tiller production per unit leaf production) was calculated according to Davies & Thomas (983). Measurements of shoot zenith angle Shoot zenith angle (i.e. the angle with respect to the vertical) was measured with a protractor by considering an imaginary straight line touching the base of the shoot, the ligule of the last expanded leaf and the middle length of the longest leaf in expansion (a diagrammatic representation is shown at the top of Fig. 6). Leaf lamina zenith angle was measured by considering an imaginary straight line fitting the average position of the entire lamina. In density experiments, shoot and leaf lamina zenith angles were measured without taking the plants out of the canopy. Statistics Tiller and leaf number data were square roottransformed, and dry weight per plant was log^transformed, to obtain homogeneity of variance for the analysis of variance. Means were back transformed to be shown in figures and, for this reason, deviation estimates are indicated in the legends. RESULTS Tiller number and leafsheath length responses to R: FR at the end of the photoperiod To investigate whether tillering is affected by the twilight drop in R:FR, isolated plants of L. multiflorum were exposed to supplementary R or FR during twilight, or remained as nonirradiated controls. The R:FR during twilight (e.g. 09, 30 min after sunset) was lower than during daytime ('2). Supplementary R increased R: FR above twilight values, but caused no effects on tillering (Table ). Supplementary, 'pure' FR reduced tillering (Table ) indicating that plants were able to respond to the R:FR at the end of the photoperiod though, presumably, not within the range between twilight and twilight plus R. To test this interpretation, plants were exposed to a series of R: FR at the end of the photoperiod either under natural radiation or under light and temperaturecontrolled conditions. Leaf sheath length responses are also shown. Neither Table. Tillering of Lolium multiflorum plants as affected by supplementary R or FR at the end of natural daylight photoperiods Light treatment Control + R IFR Number of tillers per plant 55a 45 a 3Ob Data are means of 79 plants. Different lower case letters shown at the right side of the means indicate differences {P < 005). The SE of square roottransformed data are < 7 % of the means.
4 568. J. Casal, R. A. Sanchez and D. Gibson 0 (a) R:FR A ' A ; its) c a> 0 08 o X "/' o A 3 JS 06 ft/^ / 03 (D CD B CO Hermg o % a a> Q. en <i> > ^ (D E.S 3 z (b) \ 3 x: len A A H <D n Calculated Pfr/P Figure 2. Number of tillers (a), and length of the third fully expanded leaf sheath (i), in Lolium multiflorum plants, as affected by the calculated Pfr/P provided at the end of natural daylight photoperiods. Treatments began when the first leaf was in expansion and data correspond to 2435 d of treatment. Different symbols correspond to different experiments. Each point is the mean of 67 plants. The SE of square roottransformed rate of tillering ranged from 5 to 26% of the means (largely below 2%). Tillering rate of high Pfr/P treated plants varied from 0 to 037 tillers per day among different experiments, and was set at unity. tillering, nor leafsheath length responded significantly to R:FR that established calculated Pfr/P between 03 and 075, but steep responses were revealed below Pfr/P = 0203 (i.e. R:FR < 0 3) (Figs 2, 3). The shape of the Pfr/Presponse relationships was similar for different dates (data not shown). Tiller, leaf, and dry matter production as affected by plant density To investigate whether R:FR signals and tillering responses occur before intense competition for light is established in actively growing canopies, single plants of L. multifiorum were grown in pots placed at high densities. Plants at lower densities were used as controls. The R:FR at plant bases and the number of tillers per plant were periodically recorded. Changes in leaf or dry matter production were Calculated Pfr/P Figure 3. Number of tillers (a, O), number of unfolded leaves (a, #), and first to second leaf interligule distance (b) in Lolium multiflorum plants, as affected by the calculated Pfr/P provided at the end of fluorescent whitelight photoperiods under constant temperature (20 C). The interligule distance equals the length of the second leaf sheath minus the length of the first leaf sheath, the latter was fully expanded when treatments started. Tiller data correspond to 6 d of treatment in order to show the effects on the appearance of the first tiller. Each value is the mean of 3739 plants. The SE of the square roottransformed rate of tillering is 34% of the means. Different lowercase letters given next to the symbols indicate significant (P < 005) differences. Bars indicate + SE. monitored as both variables are strongly affected by PAR (Hunt & Halligam, 98; Davies & Thomas, 983; Hunt & Thomas, 985). Leafsheath length was not measured. In a first experiment, the number of tillers per plant and the site filling rate decreased significantly at the highest density after c. 26 d (Fig. 4a). The production of leaves was unaffected (Fig. 46). Changes in R: FR at plant bases occurred before the tillering responses, being significant by day 5 of the experiment (Fig. 4c). In a second experiment, the number of tillers per plant decreased in highdensity stands after 40 d (Fig. 5 a). This response occurred before any effects on dry matter per plant or relative growth rate took place (Fig. 5 b). The shoot.root ratio was also unaffected (data not shown). Changes in R:FR at plant bases occurred before tillering responses (Fig. 5 a, inset).
5 Effect of red/farred ratio on tillering in Lolium ^ ling r lea ** a Site Hers lant a a CO tillei 0 8 'o 6 umbe LH'P I Vi I I I Days of treatment Figure 4. Timecourse of plant density effects on the number of tillers per plant {a), the average site filling rate between 20 and 33 d (a, inset), the number of leaves on the main shoot {b), and the R: FR at the base of the canopy at midday (c)., 280 plants m^^; g, 76 plants m^^; ^, 8 plants m"^. Treatments began when the first two leaves were fully expanded. Each value is the mean of 6 plants + SE. The SE of square roottransformed data is < 3 % of the mean. The R: FR of plants grown at the lowest density was equal to the R: FR of unfiltered sunlight. Different lowercase letters shown next to the symbols indicate significant differences (P < 005) for a given date or period (inset). Other experiments showed that, at later stages of canopy development, both leaf number and dry matter production become affected by the range of plant densities used above (data not shown). Effects of plant density and different R: ER irradiations on shoot zenith angle Increasing plant densities reduced shoot zenith angle of L. multifiorum plants, but did not affect the position of leaf lamina (Fig. 6). The effect of plant density on shoot position was already present after 32 d of treatment, i.e. before any density effect on leaf production was noticed, but after plant density had reduced the R:FR reaching plant bases (see Fig. 4). Similarly, very low R:FR of the irradiation provided during twilight caused more erectophile shoots (i.e. reduced shoot zenith angle) (Fig. 7) c 03 _to a S. 02 I Days of treatment Figure 5. Timecourse of plant density effects on tiller number (a), and dry matter per plant (b) in Lolium multifiorum. Data are means of (a) 25 or (b) 4 5 plants. The inset shows the effects of plant density on R: FR measured at the base of the plants at midday, 3 d after the beginning of treatments (the R:FR of unfiltered sunlight is 2). #, 670 plants m'^;, 400 plants m^^; A, 300 plants m^ Different lowercase letters shown next to the symbols or to the bars indicate significant differences (P < 0*05). The SE of square root (a) or log (b) transformed data were < 5 % (after 20 d) and < 2 % of the means respectively. DISCUSSION Tillering of L. multiflorum plants is unaffected by the twilight changes in R: ER caused by atmospheric factors The R:FR of the light was lower during twilight than during daytime. However, supplementary R during twilight did not increase tillering. Tiller number was reduced only by very low twilight R:FR. No significant responses to twilight changes of Pfr/P in the range between Pfr/P = 03 and 075, i.e. R:FR > 02 took place. This range of R:FR comprises sunlight R: FR values reaching the surface of the earth during daytime and twilight (Holmes & Smith, 977; Hughes et al., 984). Therefore, present data indicate that the twilight drop in R: FR
6 570 y.j. Casal, R. A. Sanchez and D, Gibson (deg rees) nith angle a> N k ////////// Vi ^ Shoot zenith angle /////////////////// Leaf lamina *"*N.,^ Shoot Density (plants m ) Figure 6. Effect of plant density on shoot (O) and leaf lamina {%) zenith angle oi Lolium multifiorum plants. Data are means of 0 plants (five shoots and five leaflamina subsamples were taken per plant). Bars indicate +SE. The diagram shown at the top of the figure defines shoot zenith angles. (0 H C3) c CD c N R:FR Calculated Pfr/P Figure 7. Main shoot zenith angle in Lolium multiflorum plants as affected by the calculated Pfr/P provided at the end of natural daylight photoperiods. Different symbols correspond to different experiments. Data are means of 2 (, A) or 8 (#) plants. Data were recorded after 2837 d of treatment. Bars indicate SE. 06 I is unlikely to affect tillering and disturb early neighbour detection. Small reductions of the R:FR below the values provided by daytime sunlight reduce tillering when applied throughout the photoperiod (Casal et al., 987), but not when restricted to the end of the photoperiod. There are several differences between R: FR treatments applied during or at the end of the day that could theoretically account for the different sensitivity. These include the duration of the differences in Pfr/P (day and night vs. night alone), and the presence or absence of blue light, phytochromeabsorbable radiation and PAR while the plants have different Pfr/P. The shift in sensitivity cannot be attributed to different temperatures as these were the same (20 C) during daytime (Casal et al., 987) and night time (Fig. 3) under controlled conditions. However, under natural conditions temperature changes may play a role in reducing the relative importance of twilight changes in R: FR (Morgan & Smith, 978; KadmanZahavi, 980). Very low R: FR increased leafsheath length and reduced shoot zenith angle. Both responses showed a range of sensitivity to R: FR similar to that observed for tillering responses. More erectophile leaves as a result of low Pfr/P had been reported for several dicotyledonous species (e.g. Sinningia speciosa, Satter & Wetherell, 968). This report shows the first indications for a comparable response in grass shoots. Evidence for R: FR as an anticipatory signal of impending competition in grass canopies At high plant densities (> 280 plants m~^) both the R: FR within the canopy, and the rate of tillering of L. multifiorum plants decreased (compared to control values in sparser canopies) before any indication of competition for light. Leaf number or plant biomass production, both known to be strongly affected by changes in PAR (Hunt & Halligam, 98; Davies & Thomas, 983; Hunt & Thomas, 985), showed no effects (within the duration of present experiments), even when short periods of time were considered. Decreases in R: FR may appear before any detectable reduction in photosynthate availability takes place, firstly because light reflection by neighbours is wavelength selective and may modify the light environment of fully illuminated plants (Ballare et al., 987; Smith et al., 990), and secondly, because the first part of the grass plant to be shaded is its base, which is composed mainly of sheaths, which are less active photosynthetically (Thorne, 959; Parsons et al., 983). In dicotyledonous canopies, changes in R:FR can be detected earlier if we measure the light propagated horizontally instead of vertically (Ballare et al., 987; Smith et al., 990). Since grass shoots are not completely vertical we chose a conservative approach and measured the R:FR of the light reaching a horizontal, cosine
7 Effect of red/farred ratio on tillering in Lolium 57 corrected, planar sensor. Thus, it is very likely that, R:FR signals were present even earlier than shown here. The observations (a), that in the present experiments the reductions of the R:FR received by a plant took place prior to tillering reduction, and {b), that tillering is known to be affected by daytime changes in the R:FR of the magnitude observed here, without causing alterations in leaf number or dry matter production (Casal et al., 985; 987), are strong indications that the reductions in R:FR caused by the presence of neighbours were, at least in part, the cause of tillering responses anticipatory to competition. Sensu stricto, the involvement of other environmental factors, or even changes in a particular pool of photoassimilates with little impact in total biomass cannot be ruled out. It is doubtful that changes in soil temperature have played an important role in causing the efifects observed in the experiments reported here. The optimutn temperature for tillering is lower than for leaf growth (Harris, Forde & Hardacre, 98; Thomas & Norris, 98), and no differences in aboveground biomass were found. Moreover, in a wide range, temperature does not modify site filling rate (Davies & Thomas, 983; Hunt & Thomas, 985). CONCLUDING REMARKS We previously proposed the hypothesis that in grass canopies phytochromemediated tillering responses to changes in R:FR anticipate competition (Casal et al., 986). Here, we show: (a) that tiller number, leafsheath length and shoot angle in ryegrass plants are not affected by twilight changes in R: FR (within the range found in natural conditions); and {b) that both R: FR and tillering rate decrease before intense competition is established in densely sown grass swards. These observations strongly suggest that early neighbour detection in grass canopies is unlikely to be disturbed by the twilight drop in R:FR, and has sufficient time to occur even in densely sown swards. Therefore, the observations are in agreement with the proposed hypothesis. They also suggest that R: FR effects on shoot angle (a novel response) could be another early response in growing grass canopies. ACKNOWLEDGEMENTS We thank Professor V. A. Deregibus for his suggestions at various phases of this project, and Dr O. E. Sala for helpful comments on the manuscript. This work was financially supported by CONICET (Argentina). REFERENCES BALLARE, C. L., SANCHEZ, R. A., SCOPEL, A. L., CASAL, J. J. & GHERSA, C. M. (987). Early detection of neighbour plants by phytochrome perception of changes in reflected sunlight. Plcmt, Cell and Environment 0, BALLAHE, C. L., SANCHEZ, R. A., SCOPEL, A. L. & GHERSA, G. M. (988). Morphological responses of Datura ferox seedlings to the presence of neighbours. Their relationship with canopy microclimate. Oecologia 76, BALLARE, C. L., SCOPEL, A. L. & SANCHEZ, R. A. (989). Photomodulation of axis extension in sparse canopies. Role of the stem in the perception of lightquality signals of stand density. Plant Physiology 89, BALLARE, C. L., SCOPEL, A. L. & SANCHEZ, R. A. (990). Farred radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247, BARREIRO, R., BELTRANO, J. & MONTALDI, E. R. (989). Relacidn entre cantidad y calidad de luz con la arquitectura del canopeo de Paspalum dilatatum Poir. X Reunion de la Sociedad Latinoamericana de Fisiologia Vegetal, Puerto Iguazu, Argentina. Book of abstracts, p. 23. CASAL, J. J., DEREGIBUS, V. A. & SANCHEZ, R. A. (985). Variation in tiller dynamics and morphology in Lolium multiflorum Lam. Vegetative and reproductive plants as aftected by differences in red/farred irradiation. Annals of Botany 56, CASAL, J. J., SANCHEZ, R. A. & DEREGIBUS, V. A. (986). Effects of plant density on tillering: the relationship with the R/FR and the proportion of radiation intercepted per plant. Environmental and Experimental Botany 26, CASAL, J. J., SANCHEZ, R. A. & DEREGIBUS, V. A. (987). Tillering responses of L. multiflorum plants to changes of red/farred ratios typical of sparse canopies. Journal of Experimental Botany 38, CASAL, J. J. & SMITH, H. (988). The loci of perception for phytochrome control of internode growth in lightgrown mustard. Promotion by low phytochrome photoequiiibria in the internodes is enhanced by blue light reaching the leaves. Planta 76, llll'&l. CASAL, J. J. & SMITH, H. (989a). The 'endofday' phytochrome control of internode elongation in mustard. Kinetics, interaction with the previous fluence rate and ecological implications. Plant, Cell and Environment 2, CASAL, J. J. & SMITH, H. (9896). The function, action and adaptive significance of phytochrome in lightgrown plants. Plant, Cell and Environment 2, DAVIES, A. & THOMAS, H. (983). Rates of leaf and tiller production in young spaced perennial ryegrass plants in relation to soil temperature and solar radiation. Annals of Botany 57, DEREGIBUS, V. A., CASAL, J. J. & SIMONE, F. (986). Heavy grazing effects in tamed pastures invaded by Cynodon dactylon. ' Revista Argentina de Produccion Animal 6, DEREGIBUS, V. A., SANCHEZ, R. A. & CASAL, J. J. (983). Light quality effects on tiller production in Lolium spp. Plant Physiology 72, DEREGIBUS, V. A., SANCHEZ, R. A., CASAL, J. J. & TRLICA, M. J. (985). Tillering responses to enrichment of red light beneath the canopy in a humid natural grassland. Journal of Applied Ecology 22, HARRIS, W., FORDE, B. J. & HARDACRE, A. K. (98). Temperature and cutting effects on the growth and competitive interaction of ryegrass and paspalum. I. Dry matter production tiller numbers, and light interception. New Zealand Journal of Agricultural Research 24, HOLMES, M. G. & SMITH, H. (977). The function of phytochrome in the natural environment. I. Characterization of daylight for studies in photomorphogenesis and photoperiodism. Photochemistry and Photobiology 25, HUGHES, J. E., MORGAN, D. C, LAMBTON, P. A., BLACK, C. R. & SMITH, H. (984). Photoperiodic timesignals during twilight. Plant, Cell and Environment 7, HUNT, W. F. & HALLIGAM, G. (98). Growth and developmental responses of perennial ryegrass grown at constant temperature. I. Influence of light and temperature on growth and net assimilation. Australian Journal of Plant Physiology 8, 890. HUNT, W. F. & THOMAS, V. J. (985). Growth and developmental responses of perennial ryegrass grown at constant temperature. II. Influence of light and temperature on leaf tiller and root appearance. Australian Journal of Plant Physiology 2, KADMANZAHAVI, A. (980). 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8 572. Casal, R. A. Sanchez and D. Gibson Photoreeeptors and Plant Development (Ed. by De Greef), pp Antwerpen University Press, Belgiiun. KASPERBAUER, M. J. & KARLEN, D. L. (986). Lightmediated bioregulation and photosynthate partitioning in wheat. Physiologia Plantarum 66, MANCINELLI, A. L. & LIM, J. (989). Light perception by phytochrome in vivo. Photochemistry and Photobiology 50, MORGAN, D. C. & SMITH, H. (978). The relationship between phytochrome photoequilibrium and development in light grown Chenopodium album L. Planta 42, PARSONS, A. J., LEAF, E. L., COLLET, B. & STILES, W. (983). The physiology of grass production under grazing.. Characteristics of leaf and canopy photosynthesis of continuouslygrazed swards. Journal of Applied Ecology 20, 726. SATTER, R. L. & WETHERELL, D. F. (968). Photomorphogenesis in Sinningia speciosa cv Queen Victoria. II. Stem elongation: interaction of phytochrome controlled process and a redrequiring reaction. Plant Physiology 43, SMITH, H. (982). Light quality, photoperception a.id plant strategy. Annual Review of Plant Physiology 33, SMITH, H., CASAL, J. J. & JACKSON, G. M. (990). Reflection signals and the perception by phytochrome of the proximity of neighbouring vegetation. Plant, Cell and Environment 3, THOMAS, H. & NORRIS, I. D. (98). The influence of light and temperature during winter on growth and death of simulated swards of Lolium perenne. Grass and Forage Science 36,076. THORNE, G. N. (959). Photosynthesis of lamina and sheath of barley leaves. Annals of Botany 23,
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