Photo- and Thermoperiodic Effects in Plant Growth

Photo- and Thermoperiodic Effects in Plant Growth

F. W, WENT

Missouri Botanical Garden, St. Louis, Missouri

To establish the significance of a particular factor in the physiology of an organism, it is necessary to make it limiting, and to vary it at will. Today I have to discuss periodicities in plant growth. Until recently, all experiments on plant growth were carried out either with seedlings under apparently constant conditions of temperature and light for short periods, or with older plants under less controlled conditions. These usually involved natural light, or if artificial, the light was still supplied on a 24-hour cycle. But even under the best controlled conditions the plants were subjected to a 24-hour rhythm of air pollution, even in the countryside, where the air is oxidizing during day and reducing during night. The latter external cycle can be removed by passing all air through activated carbon filters. I t is therefore not surprising that the 24-hour rhythm was not conceived as an important or essential factor in normal growth of a plant. Circadian rhythms were discovered in plants only in connection with responses which were rhythmic and free swinging under constant conditions, such as nyctinastic movements.

For about 100 years we have had significant informa- tion on temperature effects on plant growth. Sachs [1] showed that for the growth of plants a minimum, optimum, and maximum temperature could be established. These same cardinal temperatures could be established for all partial processes, and soon the trend toward analysis caused the temperature characteristics of photosynthesis, respiration, transpiration, etc., to ')ecomc well known. In all those cases the optimal ;emperature was high, well above 30~ Below the optimum the temperature effect was exponential and followed more or less van 't Hoff's rule with a Qlo some, where between 2 and 3. Therefore, there is very little doubt in the mind of biologists that the basic plant processes are controlled by, or are themselves, chemical processes. And above the optimal temperature, injurious effects, such as protein denaturation, reduce the reaction rates.

When the optimal temperature of the growth process was determined, this behaved like any other individual physiological process, except when growth of the intact plant was studied. Then much lower optima were found, for the first time by Blaauw and collaborators for bulbous plants. And now we know that for the majority of plants investigated the optimal temperature lies somewhere between 10 and 20~ [2]. There- fore, the processes which integrate the different plant

parts into an organism must themselves have a low temperature optimum, or they must limit the rate of chemical processes above 10-20~

A third attribute of the temperature response of the plant as a whole is its periodicity. When the optimal growing conditions of a plant such as a tomato are investigated, then it is found almost invariably that the night temperature has to be kept well below the day temperature. For tropical plants this day-night temperature differential should be about 3-6 ~ for temperate region plants about 5-7 ~ and for desert plants 10~ or more. For a long time I explained this behavior on the basis that the light processes during day, such as photosynthesis, had a higher optimal temperature than the dark processes, such as sugar translocation. This tied thermoperiodicity in closely with photoperiodism, which made it difficult to separate the two. Yet in many plants, such as the tomato, which do not specifically respond to photoperiod, thermoperiodicity has been established. And I now believe that thermoperiodicity is more commonly controlling plant behavior than photoperiodism.

There are many different plant growth processes which are controlled or influenced by light, directly and indirectly. Let us only mention photosynthesis, phototropism, photoperiodism, pigment formation, and many growth processes. Each of these processes has its own spectral sensitivity range, and most of these ranges are specifically different as far as the different processes are concerned, but similar for the same process in different plants. It is interesting that the plant as a whole also has light requirements beyond those of its individual processes, very much like the temperature requirement. And even in a third respect the light response resembles the temperature response. This is its periodicity. In many plants only a succession of light and darkness leads to normal growth, and the propor- tion between light and dark periods determines the plant response in many cases. This is termed photoperiodism.

The periodic aspect of photo- and thermoperiodicity is a very important attribute of these phenomena, and recently the full significance of this aspect is becoming known. It is really most remarkable that Garner and Allard [3] immediately recognized this significance in the selection of the name for photoperiodism, which is the more remarkable since for almost 40 years the in-

221

222 WENT

vestigators of this phenomenon disregarded almost completely its periodic aspect.

For some time the deleterious effect of continuous light on the development of some plants was known. I t was probably Hanson and Highkin [4] who first tied this in with a 24-hour rhythm when they found that a fight-dark cycle of 6-6 or 24-24 hours was almost more injurious than continuous light. Later I-Iillman [5] established clearly that the injury to tomato plants caused by continuous light (chlorosis, decreased growth) could be prevented by subjecting the plants either to a light-dark cycle on a 24-hour basis or to a temperature cycle with a sufficient temperature differential, also on a 24-hour cycle. I found that in peas constancy of temperature and light causes another phenomenon, namely sharply increased variability [6]. This variability is equally relieved by introducing temperature and/or light cycles, and combining a light with a temperature cycle does not further reduce variability. There are several other cases where temperature cycles can at least partially replace light cycles (in the flowering of Xanthium and of peas). We come, therefore, to the conclusion that

1). For normal or optimal development of a number of plants there must be a 24-hour rhythm in the plant environment,

2). This cycle can be either in the nature of a temperature or of a light cycle,

3). This implies that both in tomatoes and peas at least part of the growth process has an internal circadian rhythm which has to be synchronized by an external rhythm of a 24-hour period to proceed normally,

4). This internal clock can be set or synchronized by light, but it is not directly linked with a pigment system, because a temperature cycle is equally effective.

We are therefore dealing here with an internal clock mechanism which does not have any direct external manifestation (except perhaps leaf-angle as suggested by Biinning), but which can be established primarily only by abnormalities which appear in the absence of an external synchronizing signal. I believe that in this respect the phenomenon is analogous with the flowering response of plants, which Dr. Hamner will discuss, and which does not proceed properly unless an external signal on a 24-hour cycle is applied.

Before entering further into the nature of the clock itself, I want to discuss a few individual processes leading to growth and their dependence on rhythms. First, photosynthesis. This is in the plant definitely periodic, and it might even have an autonomous rhythm, but most likely it is tied in with the periodic behavior of the plant as a whole (stomatal opening, e.g.). When we probe the capacity of the plant at different times of its daily cycle to convert fight energy into chemical energy, then we find remarkable differ-

ences, which are understandable on the basis of Biin- ning's photophil and scotophil phases. By exposing plants to sub-saturating light intensities, photosynthesis can be measured by the amount of dry matter produced. When this light is supplied on a daily basis for a one or two week period, the increase in dry weight becomes very considerable and can be measured accurately. By dividing the daily light period into two 4-hour periods, the same increase in dry weight is obtained as with a single 8-hour light period only when the second light exposure falls within the photophil period of the plant set up by the first light period [2, 6]. Therefore, only light interruptions of 2 and 4 hours produce maximal dry weight, and dry weight increase is substantially decreased with 6 and 8 hour interruptions. In the latter case, the situation is the same as in a 12-hour light-dark cycle.

In super-saturating light the situation is more complicated because the plant is able to use a higher light intensity after a dark period, and therefore the light utilization becomes a periodic function of the time separation between light periods; first an increase, then a decrease.

This type of experiment, like those of Hillman and Hanson and Highkin, suggested experiments with other cycle lengths. This was actually done for about two years in the Earhart Laboratory to the extent that equipment was available. Growing plants in rhythms differing from the 24-hour one is only possible with proper sources of artificial light under which the plants can be grown normally.

E X P E R I M E N T A L

These experiments were carried out in a number of sliding-top cabinets like those Bonde [7] had used for his studies of cycle length effects (see Fig. 1). They are light-tight, and four of them are placed in a row under a bank of fluorescent lights. Their tops can either be open or closed so as to expose the plants in them to light or to darkness. The sliding tops are operated by air cylinders and pistons, into which compressed air is admitted by solenoid valves, activated by time clocks. The cabinets themselves each have a fan which blows room air into the base, past the plants, and which escapes near the top through a light trap. Thus the air temperature inside the cabinets remains constant whether the lids are closed or open.

Inside the cabinets, which open in front with a light- tight door, there are three shelves which can individ- ually be adjusted to any height. Thus plants can be grown in these cabinets at three different light intensities, and usually 500, 1000, and 1500, or 600 and L200 ft.c. were used. Before the light panels were separated from the sliding-top cabinets by glass or plastic, temperature differences of up to 5~ were observed

PHOTO-THERMOPERIODIC EFFECTS IN PLANT GROWTH 223

FIGURE 1. Sliding top cabinet. Door (D) is normally closed. Inside are shelves (S) on which plants are placed. A perforated double bottom (B) allows the air supplied by the fan (F) to be distributed evenly through cabinet. A steel arm (A), hinged at the bottom and spring-loaded, can be moved by the piston of a compressed air-operated cylinder (C), thus sliding the top (T) forward through the grooves (G) and exposing the plants to light from the fluorescent tube panel (P). A 3-way magnetic valve (V) admits air from the compressed air line to open the top, and releases this air slowly in the off-position.

between cabinets under the same light panel, due to eddy currents passing over the fluorescent lamps in the light panels.

A set of four sliding-top cabinets was constructed in each of three constant temperature rooms so that at three different temperatures, 15 ~ 21 ~ and 30 ~ plants could be subjected to four different cycle lengths each, and the temperature dependence of the optimal cycle length could be determined. To make all experiments strictly comparable, all cycles were equally divided in half light and half dark periods, e.g., 12 hours light-12 hours dark, or 15 hours light-15 hours dark.

Most experiments with young tomato plants lasted two weeks; the length measurements indicate that in general the response to differences in cycle length started to appear as early as four days after the begin- ning of the treatment. The results after 14 days were only more pronounced than those after seven days but did not change in character, as might have been expected if adaptation to abnormal cycle lengths had occurred. Experiments with Saintpaulia lasted much longer, usually several months, since these plants respond only very slowly to changed conditions.

RESULTS

About ten separate experiments were run with tomato plants using in individual experiments eight plants each for 4-7 different cycle lengths, three temperatures, and two light intensities. The overall behavior of the plants was the same in the different light intensities, but, according to the temperature, they behaved very differently in the different cycle lengths. Figure 2 shows the appearance of plants which, from July 7 to July 18, had been in cycle lengths of 18, 24, 30, and 36 hours. I t is clear that at 15~ the plants grown in cycle lengths of 30 hours, closely followed by those at 36 hours, were tallest and heaviest, whereas those at 24 hours were shortest. At 20 ~ fastest development occurred at 30 and 24 hour cycle lengths with an opti- real at 28 hours, whereas at 30 ~ the optimal length was 18 hours. I t is interesting that at this high temperature a secondary optimum seems to occur at 36 hours (2 • 18). Hamner (see this symposium) and many others found that multiples of the basic cycle length (24 hours at their experimental temperatures) were as effective in producing (or inhibiting) flowering as the basic cycle length.

Many other experiments were conducted to deter- mine more precisely the optimal cycle length for tomato plants (see Fig. 3). At optimal temperatures (20~ there was less effect on growth by aberrant cycle length than at sub- or supra-optimal temperatures.

This is seen in Fig. 4, which gives the average stem elongation of tomato plants in 6-8 individual experiments, where there is little effect of cycle length at 20-21 ~ .

Among the experiments carried out at 15 ~ with cycle lengths of 24, 27, 30, and 33 hours, we find that in six cases optimal growth occurred at 27 hours and in two cases, at 30 hours. When averaging all eight experiments, an optimal cycle length of about 27.5 hours is found (see Fig. 4). This figure shows the superiority at 15~ of a 27-hour cycle length over a 24-hour one, as indicated in Fig. 3, which presents an individual experiment.

At 30 ~ the average of six experiments shows an optimal cycle length of 20 hours or slightly less (see Fig. 4). The same can be seen in Fig. 3. Therefore all experiments show the same response. Recently this behavior was confirmed by Ketellapper (1960).

If not plant length or growth rate, but wet or dry weight or leaf length is used as a measure, the same optimal cycle lengths are found, indicating that not one terminal developmental process is influenced by cycle length, but that in the tomato all growth processes are affected, placing the circadian rhythm mechanism at a very basic focal point for development, ahead of the response mechanism.

The other plants investigated in the same way as to their growth response to different cycle lengths be-

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FIGURE 2. Wet weight (broken lines), stem elongation during cycle treatment (drawn lines), and length of 6th leaf (stippled lines) of tomato plants, grown for a week at 15 ~ (single), 20 ~ (double), and 30~ (triple line) at 500-600 ft.c. in different cycle lengths (abscissa, in hours). At each cycle length the plants were subjected to light for exactly half the period (e.g., 11 hours light and 11 hours dark on a 22-hour cycle).

haved very much in the same manner. Two photo- graphs show the behavior of Baeria chrysostoma (Fig. 5), and of Saintpaulia ionantha (Fig. 6). They are very different in their general temperature characteristics: Baeria dies when kept at a constant temperature of 26~ (Lewis and Went [8], Loo [9]) and grows well at lower temperatures, whereas Saintpaulia dies at a constant 10 ~ temperature. Yet their optimal cycle lengths are about the same at the same temperature. I t is obvious that the best Baeria plants developed at 14 ~ at a 33-hour cycle length, and that at a 24-hour cycle length at 30 ~ they hardly grew and ultimately died. Yet the 30~ could be supported on a 20-hour

cycle length. In Saintpaulia optimal growth occurred at 21 ~ , but both higher and lower temperatures could be very well supported at respectively shorter and longer cycle lengths. In one experiment [6] Saintpaulia plants, dying at 10 ~ on a 24-hour cycle, developed well on a 32-hour cycle, and in another case Begonia semper- florens plants behaved in the same way [10].

DISCUSSION

In Fig. 7 all data discussed in this paper have been brought together. The optimal cycle length for the growth of different plants, and for the nyctinastic leaf movements of Phaseolus, is plotted here as a function


of the temperature. It is quite obvious, like in the curves already published [11, 6], that the cyclic processes of higher plants of which the cycle length has been studied in relation to temperature, behave similarly, and have a Qi0 of 1.2 to 1.3.

We might proceed with the discussion by trying to harmonize these results with the temperature independence of biological clocks in other organisms, on which basis Biinning [12] and Pittendrigh [13] develop their arguments as to the nature of these clocks. It seems better for the present to consider only the rhythms of higher plants. Later a synthesis of the views reached with the different classes of organisms can be attempted. I f the clock mechanisms in different organisms were different, only confusion can result from applying arguments and principles holding for one group to the behavior of other groups. And the difference between the temperature dependence of the biological clock in higher plants, and the temperature independence of such clocks in animals and lower plants (see for review Biinning 1958 [12]), is an important argument to consider the rhythms of higher plants by themselves.

Biinning considers Leinweber's [14] results indicating temperature independence of the Phaseolus clock more significant than his own earlier ones. As mentioned earlier [6], my own experiments confirm Btinning's original results (1934)., with no indication of a transient temperature effect, and therefore Bfinning's arguments against his own experiments seem invalid. The second case of a 24-hour temperature-independent rhythm, in higher plants, which Biinning [12] cites, is the work of Ball and Dyke [15] with Arena coleoptiles, which shows a clear-cut 24-hour rhythm in growth. In view of the results of Hull, Went, and Yamada [16] the rhythm in Arena coleoptile growth can be explained through the interference of air pollution with the normal growth process. The latter has a typical grand period with an increasing growth rate during the third day, and a declining rate on tile fourth or fifth day. By depressing the growth once every 24 hours due to air pollution at midday, a multi-topped growth curve must result, in which only a 24-hour period (or slightly longer or shorter, depending on which phase of the grand period the growth depression occurs) can be discovered, which obviously must be temperature independent. For these

FIGVRE 3. Tomato plants, photographed Jan. 24, 1958, after 2 weeks growing in 7 different cycle lengths (indicated in hours above each group of plants) and 3 different temperatures (upper row 30 ~ middle row 20 ~ lower row 14~ at a 500 ft.c. light intensity.

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FIGURE 4. Average stem elongation of tomato plants grown for a week at different temperatures at 500-600 ft.c. in different cycle lengths (abscissa in hours). At each cycle length the plants were subjected to light for exactly half the period.

reasons the published evidence for temperature-independence of the Biinning cycle in higher plants must be considered insufficient and does not contradict the evidence for a Q10 of 1.2-1.3 in the present paper.

Normal development in the tomato depends on a rhythm in light-dark or high temperature-low temperature sequences with a 24-hour period [5]. In constant temperature and continuous illumination, tomato plants become chlorotic and have a strongly reduced growth rate. Therefore, normal development depends on an internal process which has to be synchronized by a light or a temperature cycle in the environment. But this guidance is only possible at a 24-hour period. The

present paper adds two important points to this state- ment:

a) There is a continuous entrainment between the external cycle and the internal autonomous cycle. When these two processes are out of period, with a difference as small as 10%, development is impaired, and the effect is the same during the first few days as in the succeeding weeks. There is no adaptation cor- recting the lack of entrainment. The continuing growth retardation indicates a continuing stress due to the internal and external rhythm being out of phase; the degree to which they are out of phase determines the degree of growth retardation.


b) The Q10 of 1.2-1.3 for the clock mechanism sug- gests that the internal rhythm depends on a diffusion- type process. Therefore, the mechanism suggested by Galston (1959) based on adaptive enzyme production cannot be used, since this will presumably be influenced by temperature like any chemical system, with a Q~0 of 2-3. We can now try to fit these facts into a general picture which accounts for the phenomena known to occur in higher plants.

1) A response mechanism exists which has an autonomous 24-hour rhythm (nyctinastic leaf movements; mitoses: Btinning [17]; flower movements: Overland [18]). I t continues under completely cue-less conditions, and therefore depends on an internal clock mechanism, located at the site of the response mechanism. A more

complicated hypothesis assumes a separate clock mechanism which entrains the response mechanism [13]; this requires for even the most elementary periodic phenomena an entrainment mechanism, involving a periodic signal emanating from the clock and being picked up by the response mechanism. Since, e.g., mitosis has an inherent periodicity, not induced by external stimuli, the simplest assumption is that the response mechanism is inherently periodical.

2) The perception of many stimuli is periodic as well. This is evidenced by the need for a 24-hour rhythm of light and darkness or temperature fluctuations for normal growth of tomatoes, or for flowering of photoperiodic plants (Hamner, this symposium). Since we know that the perception and response mechanisms of

FIGURE 5. Baeria chrysostoma plants after 2 months' growth at 500 ft.c. light. Plants arranged as in Fig. 3.

FIGURE 6. Saintpaulia ionantha plants after 2 months' growth at 500 ft.c. light. Plants arranged as in Fig. 3 and 5.

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FIGURE 7. Optimal cycle length in hours (ordinate) at different temperatures (abscissa, in degrees C.) for Baeria (circles) and tomato (plusses, data from this paper), for the movements of the primary leaves of Phaseolus (crosses, data of Biinning 1934, triangles, data of Went 1958), and Saintpaulia (squares, data of Went 1958). Two lines, indicating Q10 values of 1.2 and 1.3, are drawn in for comparison.

at least photoperiodism are spatially separated, the same clock mechanism controlling the response cannot be involved in the perception. We therefore are forced to assume that the photoperiodic perception mechanism is periodic as well, and sets in motion a train of periodic phenomena.

3) This train of periodic reactions, starting with the perception mechanism, must become enmeshed with the periodic response mechanism, through a periodic transmission process, which apparently accurately follows the cycle of the perception and entrains the response mechanism.

The simplest set of assumptions which will fit the above experimental facts are:

A periodic change in the environment, of an ap- proximately 24-hour cycle length, is perceived by a process, which derives its period from the environment. This sets in motion a periodic transmission process, again with the period impressed upon it by the periodic perception. This periodic transmission then gets enmeshed (or clashes) with the reaction mechanism which has an autonomous 24-hour clock mechanism. I t is the latter clock mechanism which has a Q10 of 1.2-1.3.

The more the period lengths of transmission and response differ, the poorer the entrainment, and the poorer the process depending upon the clock mechanism proceeds.

The autonomous clock mechanism is not only some- what temperature dependent, but it also does not keep absolute time. That is to say that the lack of complete entrainment resets the clock, so that when, e.g., a 24- hour cycle is supplied while the clock runs on a 20-hour period, there arc no spurts of growth every five days, when an absolute clock would be synchronous again, very much like Dr. Lobban's results with water excre- tion in man. The experiments reported by Went ([2], Fig. 66, [6], Fig. 1) allow another conclusion as to the nature of the clock mechanism. When the total amount of light applied daily to tomatoes at an optimal temperature is split up into two or three periods interrupted by darkness, the growth response and the wet and dry weight production is not decreased as long as the last of the two or three light periods does not fall within the scotophil phase (as indicated by the angle the leaf stalk makes with the stem). Therefore Bfinning's concept [12] of a tension developing inside the system on a 24-


hour cycle which can be released or built up by light according to the phase of the system (his original photophil or seotophil phase) comes closest to an ac- ceptable interpretation of the facts. But since a temperature cycle can substitute for a light-dark cycle, it would be better to talk about a relaxor and a tensor phase, as Btinning is doing now.

We come now to a consideration of the low Q~0 of the clock mechanism. This can be envisaged in several different ways.

1) One can assume that basically this clock has a Q10 of 2 to 3, like most chemical pcocesses occurring in the cell. In addition, one assumes the existence of an inhibitory process with a Q~0 slightly lower than that of the clock. This would result in an overall Q~0 of 1.2 to 1.3. This seems to be in the minds of many persons since they call the low Q~0 a temperature-compensating mechanism. There are several objections to this interpretation of the Q~0 of 1.2-1.3 in higher plants, a) Con- trol of a process by two opposing mechanisms leads inevitably to a high variability, whereas under optima] growing conditions the variability of plant growth is remarkably small [19]. b) A whole range of different Q~0's for the different plant clocks could be expected, depending upon the degree of temperature compensation between the promotive and inhibitory mechanisms. c) Through adaptation the temperature compensation should be adjustable. But it is most likely that the reason that tropical plants, such as Saintpaulia and Begonia, cannot live at lower temperatures (around 10 ~ ) is that their circadian rhythm is synchronized with the 24-hour external cycle at a high temperature, whereas temperate-region plants (such as Baeria and Bellis) have their clocks adjusted to 24 hours at a low temperature. Since there is no temperature adjustment I assume that basically the Q~0 of 1.2-1.3 is non-adjustable, and therefore is not temperature-compensated.

2) The second possibility to explain temperature independence is the assumption of Dr. Brown that an unknown periodic external stimulus with a 24-hour period is perceived by the plant and, without or with phase shifts, synchronizes the auto-phasing of its development. This had been generally assumed to be the case in the periodic leaf movements of plants, until the experiments of Btinning [20] and Kleinhoonte [21] seemed to rule out an external signal as synchronizing agent. In the case of tomato growth it is certain that this external signal is insufficient to be perceived by the plant as indicated by its poor growth under constant light and temperature. Therefore, we cannot use this external signal for the explanation of the circadian rhythm under conditions of strong light or temperature signals.

3) The explanation which, to me, seems most likely is the assumption that the circadian clock mechanism in higher plants depends on a diffusion process rather than on a chemical process. Chemical processes involve the

activation of molecules. Depending on the amount of energy required for their activation, the Q10 of chemical processes ranges upwards of 2. At lower activation energies the process proceeds spontaneously and no Qlo can be measured.

If, on the other hand, a diffusion process is involved, on the average all molecules of a species are equally speeded up by temperature with a Ql0 of 1.2. A diffusion process is non-compensatable and, unless semiperme- able membranes are involved, cannot be much influenced by physical factors other than temperature.

Since small molecules diffuse very rapidly over short distances, such as encountered in cells or meristems, diffusion could provide a basis for timing only if macro- molecules are involved, since diffusion equilibrium is reached within seconds or minutes with small molecules. I therefore suggest that a diffusion process, involving the cytoplasm and the nucleus of meristems, is involved in circadian rhythms. The exact nature of this diffusion process has to be established, but it is interesting that :

1) Only organisms with well-established nuclei exhibit circadian rhythms.

2) The cell dimensions of meristematic cells are all of the same order of magnitude, whether the plant is large or small.

Tile above considerations do not apply to circadian rhythms of animals, and therefore they do not con- tribute to a unitarian viewpoint, but, as mentioned earlier, there arc no compelling reasons to assume that a circadian rhythm developed curly in the evolution of organisms. Therefore, let us consider separately the circadian rhythms of plants, all with the same, small, temperature dependence, and let us try to find their underlying cause.

REFERENCES

1. SACHS, J. 1860. Physiologische Untersuchungen iiber die Abh~ngigkeit der Keimung vonder Temperatur. Jahrb. wiss. Bot., 2: (repr. in Ges. Abh. 1: 49-83, 1892).

2. WENT, F. W. 1957. The Experimental Control of Plant Growth. Waltham, Mass.: Chronica Botanica Co.

3. GARNER, W. W., and H. A. ALLARD. 1920. Flowering and fruiting of plants as controlled by the length of day. Yearbook of the U. S. Dept. of Agrie.: 377- 400.

4. HANSON, J. B., and H. R. HIGHKIN. 1954. Possible interaction between light-dark cycles and endogenous daily rhythms on the growth of tomato plants. Plant Physiol., 29: 301-302.

5. HILLMAN, W. S. 1956. Injury of tomato plants by continuous light and unfavorable photoperiodic cycles. Am. J. Botany, 4i3: 89-96.

6. WENT, F. W. 1959. The periodic aspect of photoperiodism and thermoperiodicity, pp. 551-564. Photoperiodism and Related Phenomena in Plants and Animals, ed. Withrow. Washington: A.A.A.S.

7. BONDE, E. K. 1955. The effect of various cycles of light and darkness on the growth of tomato and cocklebur plants. Physiol. Plant., 8: 913-923.

230 WENT

8. LEWIS, H., and F. W. WENT. 1945. Plant growth under controlled conditions, IV. Response of Cali- fornia annuals to photoperiod and temperature. Amer. Jour. Bot., 82: 1-12.

9. Loo, S. W. 1946. Preliminary experiment on the cul- tivation of Baeria chrysostoma under sterile conditions. Amer. Jour. Bot., 38: 382-389.

10. WENT, F. W. 1957. Some theoretical aspects of effects of temperature on plants, pp. 163-174. Influence of Temperature on Biological Systems.

11. - - . 1957. Periodic aspects of photoperiodism and thermoperiodicity. Publ. No. 34, Ser. B. de l 'U.J.S.B.--Colloque International sur le Photo- thermoperiodism. Parma. 131-139.

12. BIJNNING, E. 1958. Die physiologische Uhr. Berlin: Springer-Verlag.

13. PITTENDRIGH, C. S., and V. G. BRUCE. 1959. Daily rhythms as coupled oscillator systems and their relation to thermoperiodism and photoperiodism. pp. 475-505. Photoperiodism and Related Phe- nomena in Plants and Animals, ed. Withrow. Wash- ington : A.A.A.S.

14. LEINWEBER, F. J. 1956. ()ber die Temperaturabh~ing-

igkeit der Periodenliinge bei der endogenen Tages- rhythmik von Phaseolus. Z. Botan., 64: 337-364.

15. BALL, N. G., and J. J. DYKE. 1957. The effects of decapitation, lack of oxygen, and low temperature on the endogenous 24-hour rhythm in the growth rate of the Avena-coleoptile. J. Exp. Bot., 8: 323- 338.

16. HULL, H. M., F. W. WENT, and N. YAMADA. 1954. Fluctuations in sensitivity of the Arena test due to air pollutants. Plant Physiol., 29: 182-187.

17. Bi]NNING, E. 1952. Uber den Tagesrhythmus der Mi- tosehs in Pilanzen. Z. Botan., 60: 193-199.

18. OVERLAND, L. 1960. Endogenous rhythm in opening and odor of flowers of Cestrum nocturnum. Amer. Jour. Bot., 47: 378-382.

19. WENT, F. W. 1953. The effect of temperature on plant growth. Ann. Review Plant Physiol., 6: 347-362.

20. BL'NNING, E. 1932. Untersuchungen fiber die autonomen tagesperiodischen Bewegungen der Primi~r- bli~tter von Phaseolus multiflorus. Jahrb. Wiss. Botan., 75: 439-480.

21. KLEINHOONTE, A. 1932. Untersuchungen fiber die autonomen Bewegungen der Prim~trbl~tter von Canavalia ensiformis. Jb. Wiss. Bot., 75: 679-725.

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Photo- and Thermoperiodic Effects in Plant Growth