Crop Production and Environment (1960) 140-148
R. O. Whyte
PHASIC DEVELOPMENT PDF
Visible and Invisible Phases
The Russian plant physiologists support the theory of phasic development proposed by Lysenko (see p. 36). Most of the current experiments are based on this hypothesis and use the appropriate terminology such as thermo-phase, photo-phase and so on. On the basis of the fact that the rate of growth and the rate of development may be quite different, it is assumed that the thermo-phase may be passed while the plant is still a slowly growing seed, and the photo-phase while it is still only a young seedling provided it has a chlorophyll mechanism capable of photosynthesis. There is no reference to the number-of-leaves statement of Gregory and Purvis (p. 31). Presumably subsequent phases of development are also considered as able to proceed while the plant is still in an early growth stage. Whether or not these various invisible phases, which are stated to be always in a strict sequence, have been passed in any given plant will not become evident until later; if they have, the plant will flower.
The alternative view held by investigators outside Russia is based on a combination of invisible and visible (morphological) phases. It appears from the literature that the inward state or condition of ripeness to flower represents a first phase, which is not at the time manifested by external appearance of the plant. Subsequent phases, however, are based upon external appearance, even if micro-dissection may be necessary to diagnose the first of them. These phases or stages are generally regarded as the formation of flower primordia at the growing point (to be found by micro-dissection), the formation of flowers, flowering, the formation of viable male and female gametes (gametogenesis), and so on.
The exposure of slowly growing seeds to requisite low temperature (vernalization) and of plants of a certain age to requisite daylength (photoperiodic induction) is accepted in most physiological circles as able to influence subsequent development of plants towards reproduction, even if the plants being treated are, after exposure to the required temperature and daylength, transferred to conditions that do not favour development as such. Some authors talk of photothermal induction, suggesting that early treatment with temperature and appropriate daylength are necessary. This approaches very near to the Russian phasic outlook, although the dogmatic statement characteristic of Soviet articles that there are separable and distinct phases dependent for completion on different factors would not be supported by non-Russian investigators.
It may well be that winter varieties may be induced to flower under artificial conditions by exposure first to the required low temperature and then to the required length of day. It is, however, doubtful whether a winter variety sown in the autumn and growing under natural conditions first responds only to low temperature until the thermo-phase is completed, when it clicks over into the photo-phase and begins to respond to daylength (combined with a high temperature).
Some investigators appear to consider that exposure to optimal daylength without any previous exposure, intentional or accidental, to low temperature, will cause plants to flower. Others are beginning to consider that temperature is the controlling factor throughout, overriding the effects of photoperiod, nutrition, etc.
A reviewer approaching this problem from the agricultural point of view feels that no definite conclusion can yet be made. The application of this research in agricultural and horticultural practice is, however, important; an understanding of the relation between development and the environment will make it possible to control growth and reproduction according to the crop concerned, whether it be a lettuce or cabbage (growth), a herbage plant at its most nutritive stage (just before shooting), or a cereal (development to reproduction, i.e. grain formation).
Extreme Phasic Interpretations
It will now be appropriate to indicate some extreme interpretations of development put forward by supporters of phasic development in the Russian sense. These theories and results of experiments should, however, be accepted with great caution, as the evidence is not yet in any way conclusive.
Phase or Phases Preceding Thermo-Phase
Some Russian work on Brassica spp. has shown that it is not possible to obtain any response to vernalization of seed of these species when treated in the usual way (partial germination and exposure to low temperature). Vernalization is effective, however, if applied to young seedlings. It is therefore concluded that this inability of the germinating seed to respond to temperature indicates that the thermo-phase does not begin until late, and that therefore there must be a pre-vernalization phase with special environmental requirements that are not yet known.
Following on the studies of the germination behaviour of seeds before they are ripe, made by Noguchi on rice (1929), Harlan and Pope on barley (1922, 1926), Nutman on winter rye (1939, 1941), Culpepper and Moon on maize (1941), Modilevskii (1943) has postulated the existence of three stages of development of the embryo up to ripening and harvesting of the grain. A characteristic of the first stage is that the unripe grain is completely devoid of the capacity to germinate, no matter how favourable the conditions. Modilevskii states that this period has been determined as 9 days in spring wheat, while Nutman found it to be 5 days in winter rye.
|FIGURE 36 Diagrammatic representation of phases before and subsequent to seed dormancy, according to Modilevskii (1943)|
With the beginning of Modilevskii's second stage, the capacity to germinate is acquired, although to make it effective a definite preparatory period (18 to 20 days in spring wheat) is necessary. This is thought to be due to the need for conversion of certain 'raw' chemical substances into substances which are necessary both to stimulate the development of the embryo and for its nutrition and growth.
The second stage of development of the embryo thus begins when the capacity to germinate first becomes apparent, and continues until a definite and 'sudden' change occurs. According to Modilevskii, the grains and their embryos are more ripe at the end of the second stage, but they then seem to require a longer period in the moist chamber before they can germinate. The length of the second stage is defined as the period between the time when the capacity to germinate is first acquired (end of first stage), and when the preparatory period required for considerably older developing grain to germinate begins to lengthen again. In spring wheat, Melanopus 069, the duration of the first stage is 9 days, and of the second stage about 21 days.
The third stage is characterized by further chemical changes in the ripening grain and finally by its drying into the ripe grain of commerce. The two parts of this stage may be separated at some point by actual harvesting. This third stage of development of embryo and grain is not essential to the development of the embryo into a new plant, being no more than an adaptation to certain ecological conditions. Embryos germinated at the end of the second stage may produce normal plants and yield (see Gregory and Purvis, p. 152).
Modilevskii accepts the results of experiments on observations on vernalization before seed dormancy, but states that vernalization does not begin until the end of his second stage. It has been indicated in Chapter V that an embryo can begin to react to the temperature of the environment at the end of the first stage postulated by Modilevskii.
Phases Following Thermo-Phase
Several exponents of phasic development have attempted to improve upon Lysenko's hypothesis or to explain discrepancies that have arisen by postulating new phases before or in the vicinity of the photo-phase. For example, the Ukrainian investigator, Eremenko (1936, 1938) round that for the first 12 to 15 days after the germination of vernalized winter wheat seed, the length of the subsequent vegetative period did not depend upon daylength during this time, that is that the photo-phase did not begin (no reaction to light) until 12 to 15 days after vernalization. From a number of experiments only one will be quoted, a pot experiment with the late-ripening spring wheat Hordeiforme 0802. The results given in Table 19 show that during the first 12 days after sprouting, the plants did not react at all; from the 12th to the 20th day they reacted only weakly to daylength by a change in the time of earing. The change of daylength from the 20th to the 35th day after sprouting had a marked effect on time of earing, but this became weaker from the 35th day after sprouting, when the plants had a well-developed stem. The unvernalized plants again reacted somewhat later than the vernalized ones to the change in daylength, the interpretation again being that part of the thermo-phase had still to be completed under natural conditions before the daylength could begin to act.
Eremenko's main conclusions are therefore that: (a) there is in wheat a biologically important transitional stage of development between the thermo- and the photo-phase; (b) this phase does not require the long days essential for the photo-phase; (c) lack of differentiation of the rudimentary spike is a typical anatomical character of this period; (d) when wheat plants have passed this transitional phase and enter the light or photo-phase, they require continuous illumination or long day in addition to other factors, a short day retarding earing; (e) the beginning of the photo-phase is characterized by increased long-day requirement and differentiation of the rudimentary spike; (f) the end of the photo-phase corresponds with the beginning of stem formation when the differentiation of the main elements of the ear seems to be achieved; (g) at the end of the photo-phase, the requirement for long days appears to become reduced.
Influence of light regime on the rate of earing in wheat Hordeiforme 0802 (Pot experiment 1937) (Eremenko 1936, 1938.
|From sprouting||Short 10-hour days||Short day through-
out the experiment
|Number of days from
sprouting to earing
|From sprouting||Natural Days||Natural day
out the experiment
|Number of days from
sprouting to earing
|PLATE 17. Inhibiting influence of leaves on photoperiodic response of Nobel spinach (see p. 155). Photo: Withrow, Withrow and Biebel, 1943.|
|PLATE 18. After grafting of a leaf of Agate soybean on to a Biloxi plant, the latter has been induced to flower. Photo: Bureau of Plant Industry, Soils and Agricultural Engineering, U.S.D.A.|
By utilizing the data obtained in experiments described in this and earlier chapters, Oljhovikov (Whyte and Oljhovikov, 1939) developed a theory based upon a succession of phases considerably more hypothetical than those put forward by the phasic development school. Reference is made to the concept that long-day plants may at a certain stage of their development require a short day (Wanser, 1922), and vice versa. The conclusion is therefore made that there is an identical sequence of phases in both long- and short-day plants, namely:
→ thermo-phase → dark phase → light phase.
This hypothesis is thought to explain the different requirements of long- and short-day plants noted in the previous chapter, namely, continuous light for long-day plants, continuous darkness for short-day plants. It is assumed that the long dark phase characteristic of short-day plants becomes reduced when one studies plants of longer-day latitudes, while the light phase becomes proportionately longer in the same direction, that is as one approaches the true long-day latitudes. Long-day and short-day plants are therefore seen merely as extreme variants in the same series, with the possibility of all manner of intermediate forms between them, as the two phases governed by darkness and light compensate one another.
The results obtained in experiments made by Wort (1941) are claimed to support a rigid distinction into phases, the existence of a dark phase before the photo-phase, and the division of the photo-phase into two parts.
The Formation of Gametes
This is a visible phase and is probably the most important from an immediate practical point of view, being the essential preliminary to the formation of fruit. It is therefore very desirable to know to what extent the environment affects this phase in the progress of a plant towards ultimate reproduction.
It has already been noted that there is a tendency among some workers to divide the light-responsive phase into two parts. The Russian investigators Kraevoi and Kiricenko (1935) consider that there is a phase subsequent to the photo-phase during which the pollen grains and female germ cells are formed. It is not clear, however, what the decisive factors for this phase are supposed to be.
The only recent Russian work found dealing with development after the photo-phase is that by Samohina and Ziherman (1941), who studied the effect of temperature on the rate of development of spring wheat after it had passed through the light phase. Plants were kept at: (1) 17 to 22°C. throughout the interval between the shooting (light phase) and ear-forming stages; (2) at 17 to 22°C. for 50 days and then at 5 to 8°C.; (3) at 17 to 22°C. for 32 days (10 days after shooting) and at 5 to 8°C. thereafter; (4) at 17 to 22°C. for 27 days (5 days after shooting) and at 5 to 8°C. thereafter; and (5) at 5 to 8°C. throughout. The daylength was maintained at 18 hours.
The rate of development was highest in (I); ear formation occurred in 53 and 103 days in (1) and (5) respectively. The slowing down of ear formation occurred principally after the stage of shooting (light phase) had been passed. The retardation of ear formation at low temperatures was not due to a reduction in the rate of growth but to the inhibition of development. Studying the changes at the growing point, these investigators found that for 16 days there were no appreciable differences among the five groups of plants, but these became obvious to an ever-increasing degree after shooting had taken place. Pollen sacs were fully developed in variant (1) in 70 days and in (5) in 50 days after shooting. Differentiation of the ear was therefore more rapid at the higher than at the lower temperatures, and actually ceased altogether in other experiments where the range of temperatures was 0 to 5°C.
There have been several studies in North America on the relation between the environment and the formation and viability of pollen. The experiments of Nielsen (1942) on Biloxi soybeans may be taken as an example. Three experimental series of plants were given photo-inductive treatments of from two to ten cycles, each consisting of 8 hours of natural daylight followed by 16 hours of darkness, that is the short days required by this variety for flowering. After induction, Series I and II were placed in cycles of long photoperiods consisting of 21 hours of light and 3 hours of darkness, and Series III in cycles of 16 hours of light and 8 hours of darkness. Floral buds from control plants and from the experimental series were collected progressively to obtain the various stages in development.
Among the control plants, those under short and natural photoperiods flowered normally and the reduction division preliminary to pollen formation occurred, but no flowers were formed on those kept in long photoperiods. In the plants of the three experimental groups, floral structures developed normally until differentiation of the pollen grains in the anthers, after which there were abnormalities in meiosis associated with the photo-inductive treatment. In those plants that were given five or less photo-inductive cycles, reduction divisions in the anthers began, but the nucleus disintegrated in the prophase. In those plants given six or more cycles, the reduction division proceeded to a later stage before degeneration, in some cases as far as the formation of the resting nucleus of the tetraspores, while in a few instances pollen grains that were normal in morphology were formed (see Plates 14 and 15). Nos. 1 to 9 in Plate 14 are normal stages in the production of the pollen tetrads seen in No. 9, and the normal microspores in No. 10, Plate 15. Varying degrees of vacuolation and degeneration of microsporocytes and ultimately microspores are seen in Nos. 11 to 19 (Nielsen, 1942).
The number of photo-inductive cycles thus influences the degree and stage to which normal development of pollen grains may proceed. In addition, the length of the photoperiod following induction appears to be an important factor affecting the degree of sterility of the plants in these experiments, if they are compared with the results obtained by Borthwick and Parker (1938), who used the natural photoperiod following the photo-inductive treatments. These results seem to indicate that the visible phase or stage of the formation of male and female gametes (gametogenesis) has environmental requirements of light and probably also temperature that differ from those governing flowering as such. Flower formation can be induced by a given photoperiodic treatment, but these flowers will be sterile until the subsequent requirements of gametogenesis are also provided.
Further study of this stage in plant development has great practical significance. Investigations such as those of Poole (1932) and Sexsmith and Fryer (1943) show the relationship between the production of good and bad pollen throughout the flowering period and the degree of seed setting. Poole's conclusion is that fluctuation in the percentages of good and bad pollen in pure species is probably not influenced by external factors 'but by the physiological adjustments made to flowering and senescence'. Sexsmith and Fryer find no significant difference in pollen viability throughout the season on any one plant, but differences between plants may be highly significant. Their conclusion is that the seasonal variation in pod-setting cannot be due to changes in pollen viability. It would be interesting to know whether the wide variation in pollen viability between plants may be due to the fact that many plants are out of harmony with their environment as far as the gametogenic phase is concerned. It would also be desirable to know the relation between abnormal ovule development and the seasonal variation in pod setting.
Reference has already been made (p. 46) to the effects of developing reproductive organs as vegetative growth. That research shifts the emphasis from the type of vegetative growth that is conducive to flower and fruit formation to the converse question, the effect of the complex processes associated with formation of gametes on the growth behaviour of the same plant.
CybeRose note: It seems possible that the light phase and dark phase are not strictly sequential, but are rival processes that function in parallel. MacDougal (1903) observed that Cypripedium montanum Dougl. grown under normal conditions of alternating dark and light produces two types of trichomes: pointed and glandular. But when a plant was raised in complete darkness, the pointed hairs were absent while the glandular trichomes were larger than normal. It is doubtful that the glandular trichomes would be produced first under normal conditions, followed by the pointed hairs. It would be interesting to learn whether the same species, grown under continuous light, would produce only pointed trichomes.
MacDougal was studying only the effect of darkness on plants, without regards to temperature. So, it remains to be seen whether temperature (or "thermo-phase") might override so-called "photoperiodism" as it does in the growth of some plants. E.g., Heide, 2008 (Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Scientia Horticulturae. 2008;115:309–314.) found that "P. cerasus L. and P. insititia L. (two cultivars each), and P. avium L. were insensitive to photoperiod at high temperature and maintained continuous growth in both 10 and 24-h photoperiods at 21°C. At lower temperatures, however, growth was controlled by the interaction of photoperiod and temperature, the species and cultivars varying somewhat in their responses." This suggests that the thermoperiod may also operate in parallel with the dark- and light-phases, though under normal conditions the phases are likely to be sequential.
In many cases, the actions of the various periods must be strictly sequential because they act on different stages of development. Some strains of winter wheat require heat to initiate flowering while others respond to photoperiod. In both cases flowering cannot occur until vernalization is completed.
Similarly, conditions suitable to flowering will have no effect until after floral initiation and development have been completed, where the required conditions are different. As Went (1948) explained:
"In some cases the low temperatures may have no other effect than supplying a stimulus, so that a definite time after being subjected to a sudden drop in temperature, irrespective of the duration of this lower temperature, development occurs. The flower buds of the orchid Dendrobium crumenatum offer a clear-cut example. Nine days after a sufficiently rapid drop in temperature (usually associated with a heavy rainfall) the flowers of this orchid open, causing a sudden burst of flowering over a wide area. Some other orchids seem to behave in the same way, and probably other plants as well (gregarious flowering of Coffea liberica). In these cases the flower buds develop gradually up to a certain point, beyond which no growth is possible under the prevailing temperature conditions. The longer the temperature drop is delayed, the more flower buds will have reached the critical size, and the more abundant the flowering is after the temperature drop."
The same delayed response is seen in Fragaria vesca, except that in this case floral induction occurs at low temperatures and short days.
"Figure 5 shows the main events in this seasonal calendar. Flower initiation in late August/early September is induced by cool temperatures and shortening photoperiods. Initiation continues until autumn temperatures become too cool to sustain growth. From September the plants start to enter dormancy so that by late October it is at a maximum. Winter chilling has two principal effects: it removes dormancy, so that when warm conditions return in the spring the plants have renewed vegetative vigour. Second, it switches off flower initiation. Chilled plants appear to be insensitive to inductive conditions after chilling, offering an explanation for the failure of plants to initiate flowers during the spring. The autumn-initiated flowers emerge in the spring, and after anthesis in May, the fruiting period is accompanied and followed by runner production, a response to long days. During August as daylength shortens, branch crown formation takes over from runner production; branch crowns form new growth axes within the parent plant, and represent an alternative strategy of vegetative reproduction. Branch crown production is a photoperiod-induced response, and has the effect of maximizing the sites for flower initiation when this begins again in September."