morphogenetic effects of the gibberellins

J.L.S.B. LVI] MORPHOOENETIC EFFECTS OF THE GIBBERELLINS 237

Morphogenetic effects of the gibberellins. By P. W. BRIAN, Akers Research Laboratories, Imperial Chemical Industries Ltd., Welwyn, Hertfordshire

INTRODUCTION The discovery of the gibberellins dates from 1926. While investigating a disease of rice caused by Gibberellafujikuroi (Saw.) Wr. [imperfect state Fusarium moniliforme Sheld.], a characteristic symptom of which is lengthening of stems and leaves of infected plants, Kurosawa (1926) found that the treatment of rice seedlings with cell-free filtrates from cultures of the fungus would induce these same abnormal growth symptoms. Yabuta & Hayashi (1939a) isolated small quantities of a highly active crystalline material from such culture filtrates. They called this ‘gibberellin A’ and proposed for it the molecular formula C22H2,0,. In an unsuccessful attempt to prepare this substance, Curtis & Cross (1954) isolated instead a pure compound, with similar physiological activity, but clearly distinct chemically from ‘ gibberellin A’. They called this new substance gibberellic acid C,,H,O,) and it has since (Cross, Grove, MacMillan, Moffatt, Mulholland, Seaton & Sheppard, 1959) been shown to have the following structure :

HO

COOH

Three other pure gibberellins have since been isolated, via. gibberellin A, (C19H2406), a dihydro derivative of gibberellic acid in which the double bond in ring A is reduced (Takahashi et al. 1957a; Grove, Jeffs & Mullholland, 1958); gibberellin A$ (C,,H,,O,) (Takahashi et al. 1957a) and gibberellin A4 (C,,H,,O, or C,&I,O,) (Takahashi et al. 1957 6). The nature of the original ‘gibberellin A’ is obscure; Japanese workers have recently concluded that it was a mixture, but we cannot now be sure which of the known pure gibberellins it contained. Gibberellins A,, A, and A4, and gibberellic acid, seem to have qualitatively similar physiological activity, though gibberellic acid is most active (Bukovac & Wittwer, 1958). Because of this similarity, in the rest of this paper the precise compound or mixture used in experimental work is not usually specified, the more general term gibberellin being in many ways more convenient.

As is shown later a characteristic feature of the gibberellins is that they induce abnormally great extension of shoot structures of many plant species when applied exogenously, but the response is greatest from genetic dwarfs. They also induce flowering of many biennials and long-day plants kept in non-inductive conditions of photoperiod and temperature. The significance of these observations has been much increased by the discovery of v gibberellin-like' substances in many plant tissues, that is substances capable of inducing physiological responses of the kind just mentioned. Such responses cannot in general be elicited by application of indolylacetic acid or other natural auxins. v gibberellin-like' substances have been found in shoots and roots of peas, in many seeds, in inflorescences of Brassim and in coconut milk (Biinsow, Penner & Harder, 1958; Lang, Sandoval & Bedri, 1957; Lona, 1957; McComb & Carr, 1958; Murakami, 1957; Phinney, West, Ritzel & Neely, 1957; Radley, 1956,1958; Radley & Dear, 1958; West & Phinney, 1956). The v gibberellin-like ’ substance demonstrated in seeds of runner-beans (Phaseolus muZti$orus Willd.) by Radley (1958) has been isolated by MacMillan & Suter (1958) and shown to be gibberellin A,. Gibberellin A, has also been found in seeds of french bean (P. vulgaris L.) (West & Murashige, 1958). Thus the gibberellins, or at least some of them, are natural plant hormones, which we must in future consider in any discussion of control of morphogenesis in plants.

238 P. W. BRIAN: [J.L.s.B. LVI

In this paper I propose to describe some of the effects of exogenously applied gibberellin on the development of plants, and then to discuss the significance of these observations in the light of the discovery that the gibberellins are natural plant hormones. I shall not attempt to cover the whole rapidly expanding literature ; more complete bibliographies will be found in the reviews of Stowe & Yamaki (1957) and Brian (1959).

Since I have drawn most of my examples from recently published work, I may appear to underestimate the Japanese work published between the discovery of growth-promoting activity in culture filtrates of Gibberella fujikuroi in 1926 and the awakening of interest outside Japan some 4 or 5 years ago. I should like to dispel any such impression immediately. The isolation of ' gibberellin A ', the demonstration that it affected growth of most plants, and the description of the general nature of its effects on shoot and root growth were primarily Japanese contributions to our knowledge and it is regrettable that their work received so little attention in other countries for so long.

STEM GROWTH

(a) Day-neutral herbaceous plants In non-branching plants the most striking effect of gibberellin treatment is increase in internode length without any great increase in internode number; this is exemplified by the response of the garden pea. In branching plants, for example, Cupid sweet pea or dwarf bean (Phuseolus vulgaris), the internode extension is increased but in addition branching is inhibited and the main axis continues to elongate so that a higher proportion of the internodes formed are to be found in the main axis. The general habit of the plant is thus markedly changed, The increase in internode length is due to a more rapid extension; the time during which extension of any one internode takes place is in fact slightly reduced, thus the more rapid extension results in longer internodes in spite of more rapid ageing of the cells (Brian & Hemming, 1955; Brian, Hemming & Lowe, 1958, 1959).

Though application of gibberellin usually enhances apical dominance when applied to intact plants, it does not always do so and branching may actually be encouraged, for example, in Pinto bean (Gray, 1957). Gibberellin does not directly inhibit lateral buds as indolylacetic acid does (Kato, 1953) ; neither does it directly encourage development of normally inhibited lateral buds (Wickson & Thimann, 1958). It appears that it prolongs the activity of apical buds if applied while they are still active, thus enhancing correlative inhibition, but encourages development of lateral buds if the apical buds have declined in activity, whether naturally or as a consequence of treatment with such substances as maleic hydrazide (Brian & Hemming, 1957).

Increase in internode length may be due mainly or entirely to increased cell extension, as in the garden pea (Brian & Hemming, 1955), but increase in the number of cell divisions may also be involved, as in P . vulgaris (Feucht, 1958; Greulach & Haesloop, 1958).

The magnitude of the response to gibberellin varies from species to species and from variety to variety within a species, The response is most marked in genetic dwarfs, as has been demonstrated in the garden pea (Brian & Hemming, 1955), maize (Phinney, 1956), rye-grass (Lolium perenne L.) (Cooper, 1958) and cotton (Ergle, 1957). As a result of treatment with gibberellin the dwarf assumes the appearance of the tall phenotype. Tall varieties of the same Bpecies respond only slightly or not at all.

(b) Herbaceous plants sensitive to phtoperiod The stem growth of most herbaceous plants is profoundly in0uenced by day-length.

Such plants typically produce short internodes in short-day photoperiods and long- internodes in long-day photoperiods ; the number of internodes may be greater in long- day conditions. The extreme case is found in those plants which grow in a rosette form in short-day photoperiods, with negligible formation of visible internodes, but develop

J.L.S.B. LVI] MORZHOGENETIC EFFECTS OX" THE GIBBERELLINS 239

long leafy stalks in long-day photoperiods. It should be noted that this general association of vigorous shoot growth with long-day photoperiods holds good irrespective of the flowering behaviour of the plants-plants in which flowering is induced by exposure to long-days and those which are induced to flower only in short-day photoperiods, all usually show maximum stern-development in long-day photoperiods.

Gibberellin treatment of plants kept in short-day conditions leads to vegetative developments similar to those induced by exposure to longer days. This has been shown for such long-day plants (in their flowering response) as species of Adonis, Anethum, Grepis, Lactuca, Lapsana, Petunia, Polemonium, Raphanus, Rudbeckia, Samolus, Silene, Scccbiosa and Spinucia (Bunsow & Harder, 1956, 1957; Chaylakhian, 1957; Chouard, 1958a; Lang, 1957; Wittwer & Bukovac, 1957a). The short-day plant Kalanchoe bloss- feldianu Poelln. also produces greatly enlarged vegetative shoots when treated with gibberellin, though flowering is inhibited, as also occurs if this plant is exposed to long-day conditions.

Thus, generally speaking, in such plants growing under short-day conditions, gibberellin induces vegetative developments characteristic of their development in long-day conditions. If it is applied to plants growing in long-day conditions the effects are usually smaller, suggesting that the effects of exogenous gibberellin and exposure to long-day photoperiods are essentially similar. Some exceptions to this generalization are mentioned in the next section.

The response to gibberellin may be considerably greater than the natural response to long-days. This depends to a great extent on the dose of gibberellin applied or on the frequency of application of doses. Sometimes quite novel developments are induced, a particularly interesting case being that of Ramondia pyrenaica Rich. This plant produces no leafy stem in nature, the flowers being borne on a leafless scape and all leaves borne in a basal rosette. If treated with gibberellin a leafy stem is produced (Chouard, 1958a).

(c) Herbaceous plants which require vernalization for complete development

Many long-day plants require exposure to low temperature for a critical period before maximum vegetative development takes place. Typical plants of this class are the biennials, which only pass from the rosette stage to formation of a leafy stalk when they are vernalized by low temperature treatment and subsequently exposed to long-day photoperiods. Lang (1956a, b, c ) showed that gibberellin treatment would replace vernalization in Hyoscyamus and, since then, many other biennials have been shown to respond similarly, including species of Apium, Brassica, Centaurium, Cichorium, Daucus, Digitalis, Euphorbia, Petroaelinum and Scrophuluria (Bukovac & Wittwer, 1957 ; Carr, McComb & Osborne, 1957; Chouard, 1958a; Wittwer & Bukovac, 19576).

Gibberellin will usually replace vernalization and allow development to proceed normally in plants kept in long-day photoperiods. It often has a much smaller effect in plants kept in short days, so that it appears that it will not always replace the effects of vernalization and long-day photoperiods; this has been shown in Hyoscyamus (Lang, 1956a, b) and Centaurium minus Moench. (Carr et al. 1957). This may only be a matter of finding the right magnitude and frequency of gibberellin dosage. Indeed, it is probably significant that large doses of gibberellin are needed to simulate vernalization. To induce marked shoot development in day-neutral dwarfs and in long-day plants doses of the order of a microgram of gibberellin per plant are usually sufficient, but to induce shoot formation in biennials doses nearer a milligram per plant are usually needed. Indeed, some vernalization-requiring species, notably Reseda luteola L., a t first appeared not to respond at all to repeated doses of gibberellin (Chouard, 1958a) but eventually it was found that a stalk formed after a sufficiently large dose had been applied (Chouard, 1958 b). Nevertheless, vernalization-dependent stem development of biennials and perennials can usually be induced by treatment with gibberellin.


(d) Woody plants The pronounced seasonal character of growth in woody shrubs and trees is essentially

a response to photo-period (Nitsch, 1957a; Wareing, 1956). Cessation of growth, dormancy of buds and leaf fall in deciduous plants are usually a response to the onset of shorter days in the autumn. This dormant condition is terminated in the spring by the return to longer days; in some cases exposure to low temperatures is also necessary. These stimuli, as in the examples of herbaceous plants discussed above, can in some cases be replaced by treatment with gibberellin; this has been demonstrated in Ace?', CamelZia, Elberta peach, Paeonia and some species of Pinus (Barton & Chandler, 1957 ; Bourdeau, 1958; Donoho & Walker, 1957; Lockhart & Bonner, 1957; Lona & Borghi, 1957; Nitsch, 1957 b ; Wareing, 1958). Three points of special interest have emerged from these investi- gations. (i) In some species, the similarity between the effects of gibberellin and exposure to long-day photoperiods is emphasized by the observation that growth is stimulated by exogenous gibberellin in plants kept in short days, but the already more rapid growth of plants transferred to long-day photoperiods is not further accelerated by exogenous gibberellin (Bourdeau, 1958). In other species the differential effect is less marked but the response to gibberellin is, nevertheless, greater in short-day photoperiods (Nitsch, 1957 b). (ii) In Acer pseudoplatanus L. cambial activity of dormant shoots is only slightly stimulated by exogenous gibberellin and the new tissue formed consists of small unligni- fied cells. If indolylacetic acid is applied with gibberellin a wide zone of fully differen- tiated wood is formed, though indolylacetic acid alone has little effect (Wareing, 1958). (iii) No response to gibberellin of plants kept in short-day photoperiods has been detected with several woody species (Lockhart & Bonner, 1957 ; Nitsch, 1957 b ) . It is possible that combinations of gibberellin and indolylacetic acid would have been effective, a8 in Ace? pseudoplatanus.

( e ) Other examples of shoot dormancy The dormancy of potato-tubers is not related to photoperiod or any requirement for

vernalization, but disappears gradually after the tubers are harvested. This type of dormancy too is broken by gibberellin treatment of the tubers. If growing plants are sprayed with gibberellin the buds on the tubers do not become dormant, so that highly deformed, branched tubers are produced (Brian, Hemming & Radley, 1955; Lippert, Rappaport & Timm, 1958; Rappaport, Lippert & Timm, 1957).

A dormant condition of shoots and fruits of Marglobe tom&oes, induced by too high a proportion of far-red in the incident light, can be relieved by spraying the plants with gibberellin solutions (Liverman & Johnson, 1957).

LEAF GROWTH

Effects of gibberellin on leaf-growth are available. Leaf size is unaffected in some plants, for example, in the garden pea. In others, for example, Phaseolus (Gray, 1957), Cupid sweet pea (Brian, Hemming & Lowe, 1959) and wheat (Brian, Elson, Hemming & Radley, 1954) leaf size may be considerably increased. In Phaseolw this is merely an accelera- tion of development, final leaf size being unaffected (Humphries, 1958) but in the Cupid sweet pea and wheat final leaf size is also increased.

Gibberellin induces expansion of discs cut from etiolated Phaseolus leaves and of sections of etiolated cereal leaves (Hayashi & Murakami, 1954; Radley, 1958). Natural gibberellins may therefore be of importance in control of mesophyll growth.

ROOT QROWTH

Gibberellin has little effect on root growth. High concentrations may slightly inhibit root extension (Brian et al. 1954, 1955; Sumiki, 1952; Yabuta & Hayashi, 1939b). Stimulation of root growth of intact plants has not been recorded, and of root sections

J.L.S.B. LVI] MORPHOGENETIC EFFECTS OF THE GIBBERELLINS 241

only once (Whaley & Kephart, 1957). Root sections from dwarf peas which respond markedly to gibberellins in shoot growth show no response to gibberellin over a wide range of concentrations (Brian & Hemming, unpublished results). This apparent lack of effect of gibberellins on root growth is surprising, but further investigation may modify this picture.

Formation of adventitious roots on cuttings is strongly inhibited (Brian, Hemming & Radley, 1955). It has been suggested (Brian, 1957) that this might be a secondary effect caused by diversion of nutrients to the apex of the cutting, since gibberellin-treated stem cuttings may extend considerably. Further work has shown that this explanation is incorrect, and that there is a direct inhibition of the cell-divisions which would lead to the formation of the adventitious root initials.

FLOWERING

Gibberellin has little effect on the flowering of day-neutral plants, except to delay slightly or to accelerate the appearance of flowers. Its most clear cut effect is in induction of flowering of long-day plants kept in non-inductive short-day photoperiods or in replacing low-temperature exposure as a necessary pre-requisite t o flowering of some biennials. In nature, flowering of such plants is associated with increased vegetative development, notably in production of a leafy stalk. Most of those species which respond to gibberellin vegetatively (see the section on stem growth above) also flower as a result of treatment. However, a minority of plants which respond vegetatively have not yet been induced to flower ; these include Petkus rye (Lang, 1957), Scrophularia vernalis, Iberis intermedia, ~ u ~ h o r ~ i a lathyrus L. (Chouard, 1958a) and winter wheat (Krekule & Martinovska, 1958).

Short-day plants have been less extensively investigated. Gibberellin treatment of Kalanchoe blossfeldiana kept in inductive short-day photoperiods leads to extensive vegetative development but flowering is inhibited. In fact the plant develops just as if it were exposed to long-day photoperiods (Harder & Bunsow, 1958).

Sexuality of flowers. Nelson & Rossman (1958) have shown that treatment of some lines of inbred maize with rather high concentrations of gibberellin applied as a plant spray, leads to a very high incidence of male sterility. Plack (1958) has shown that the effect of emasculation of Clechoma hederacea L. flowers (reduction of size of corolla as in natural female flowers) can be reversed by treatment with gibberellin.

DEVELOPMENT OF FRUITS AND SEEDS

Pollen-tube growth. Gibberellin might indirectly affect fruiting by its effects on pollen- tube growth. In some species pollen-tube growth is accelerated and percentage germination in defined media increased by gibberellin (Chandler, 1957; Kato, 1955; Sumiki, 1955 ; Wada, 1949). In other species pollen-tubes are stunted and distorted by gibberellin (Chandler, 1957).

Flower dehiscence. Seed production by Cupid sweet peas is considerably enhanced by systemic treatment with gibberellin, a result mainly due to prevention of premature abscission of flowers (Brian et al. 1959).

Parthenocarpy. Parthenocarpic development of tomato fruit as a result of spraying the trusses with gibberellin solutions was first described by Wittwer, Bukovac, Sell & Weller (1957). Using a male-sterile Earlypak tomato, Persson & Rappaport (1958) have shown that the effect is systemic, parthenocarpic fruit-set being increased even where gibberellin is applied to the roots by soil-treatment, or applied to expanded leaves or the stem apex.

Fruit swelling. Liverman & Johnson (1957) showed that swelling of ‘dormant’ tomato fruits was enhanced by gibberellin treatment. More recently, remarkable enlargement of berries of two varieties of seedless grape has been shown to follow gibberellin


treatment (Weaver, 1958). Fruit swelling has for some time been known to be associated with auxin production by the immature seeds in the fruit. Weaver has pointed out that it now seems possible that gibberellins may also be involved, since immature seeds are known to be particularly rich sources of these hormones (Phinney et al. 1957; Radley, 1958). Indeed, in an investigation of growth-promoting substances in bean (Phaseolus vulgaris) seeds a t various stages in the development of the seed, Nitsch & Nitsch (1955) detected two growth-promoters present a t maximum concentration in the immature seed, declining in concentration as the seed matured. One of these was identified as indolylacetic acid; the other substance, judging by its behaviour on chromatograms, could well be gibberellin A,, which has since been identified as a constituent of Phaseolus seeds (see Introduction).

SEED QERMINATION

Gibberellin overcomes seed-dormancy in many cases. This includes the dormancy of light- requiring seeds, such as lettuce (Kahn, Goss & Smith, 1957; Lona, 1956) and Kalanchoe (Biinsow & von Bredow, 1958) and of seeds normally requiring low-temperature treatment, e.g. certain species of Malus (Barton, 1956). These effects are in line with light- simulating and vernalization-simulating effects described in earlier sections of this paper. But seed dormancy is undoubtedly biochemically complex. Thus, Skinner & Shive (1958) have demonstrated synergistic effects between gibberellin and kinetin in stimulation of lettuce seed germination, and Pollock (1958) found that dormant barley grain responded to gibberellin, kinetin and hydrogen sulphide, with a particularly striking synergism between hydrogen sulphide and gibberellin with some samples of grain.

DEVELOPMENT or LOWER PLANTS

Though little work has yet been reported, it is clear that gibberellin may have profound effects on the development of lower green plants, though fungi are unaffected. Among effects observed are promotion of elongation of the filaments of germlings of the Alga Ulva lactucu (Provasoli, 1957) and of moss protonemata (von Maltzahn L MacQuarrie, 1958); in the latter case increases of both cell multiplication and cell elongation are involved. A particularly interesting observation concerns the elongation of the dormant sporogonial setae of the liverwort Pellia epiphylla L. The sporogonium is fully differen- tiated early in the winter but elongation of the setae does not take place until February or March onwards; this is apparently a photoperiodic response. The dormant setae extend immediately if the plants are sprayed with gibberellin (Asprey, Benson-Evans & Lyon, 1958). Wardlaw & Mitra (1958) have demonstrated formative effects of gibberellin on shoot apices of the fern Dyopteris austriaca (Jacq.) Waynar.

DISCUSSION (a ) Interrelations of gibberellins and indole-auxins

It will be clear from the foregoing account of the physiological responses to exogenous gibberellin that the gibberellins have properties in many ways distinct from those of indolylacetic acid and other indole-auxins, and there is much further evidence for this view (Brian, 1958; Brian & Hemming, 1958; Brian et al., 1955; Kato, 1953,1958). Brian & Hemming (1958) have presented evidence that, in its effects on extension of pea internodes, gibberellin is dependent on the presence of indolylacetic acid. A similar dependence on the presence of indolylacetic acid has been demonstrated by Kuse (1958), using a technique based on extension of petioles of Ipomoea batatas Poir., by Asprey et al. (1958) using isolated sporogonia of Pellia epiphylla and by Wareing (1958) in his work on cambial activity in Acer pseudoplatanus. Thus where gibberellin has an eflect on vegetative

J.L.S.B. LVI] MORPHOGENETIC EBFECTS O F THE GIBBERELLINS 243

growth when applied alone we may assume that sufficient endogenous indole-auxin is already present ; this view is supported by the work of Purves & Hillman (1958) using pea sections at various distances from the apex, thus containing varying concentrations of endogenous auxin, and by similar work of Radley (1958) with sections of the first true leaf of wheat seedlings.

It is not improbable therefore, that in other effects on plant development, gibberellin acts in association with the indole auxins. This view is supported by what little we know of its distribution in plant tissues. Naturally occurring gibberellin-like materials are particularly abundant in young developing seeds, as also are the indole-auxins, and their concentration declines as the seeds mature, just as indole-auxins also decline in concentration. Radley (unpublished results) has found gibberellin-like substances particularly abundant in young leaves of Phaseolus, declining in concentration as the leaves expand, which is very similar to the distribution of indole-auxins in seedling leaves.

(b) Role of gibberellins in responses to photoperiod

The responses of plants to exogenous gibberellin, reviewed in earlier sections of this paper, enable us to make some assessment of the probable role of the gibberellin-like hormones now known to be present in plants. Here I propose particularly to discuss responses of plants to photoperiod and vernalization, dealing first with vegetative responses, and then with flowering responses.

The data presented above reveal a remarkable parallelism between the egects of exogenous gibberellin and the effects of exposure to long-day photoperiods. This is particularly true of vegetative responses, of both herbaceous and woody higher plants, and of the extension of sporogonial setae of the liverwort Pellia epiphylh. There is also a striking similarity between the vegetative effects of exogenous gibberellin and those of exposure to low temperature in such plants as biennials. A hypothesis that would satisfactorily explain most, if not all, vegetative responses to photoperiod would be that gibberellins are formed in plant tissues in light and reversibly decay to an inactive precursor in darkness so that the longer the photoperiod the greater the concentration reached (Brian, 1958, 1959). Similarly, the vegetative responses to vernalization could be interpreted as the result of activation of gibberellin-synthesizing systems. These hypotheses are strongly but indirectly supported by what we know of the effects of exogenous applications of gibberellin, but no direct evidence, from measurements of endogenous gibberellin levels, is yet available.

There are some experimental observations which may appear to be at variance with the hypothesis, and which therefore need further consideration. Some biennials have failed to respond to gibberellin as they do to vernalization; the dormant shoots of some woody plants in short-day photoperiods have also failed to respond to gibberellin. It seems to me highly probable that such cases will be found to respond if the gibberellin dosage is adjusted, as was found to be the case with Reseda luteola (Chouard, 1958a, b) , or if gibberellin is used in combination with an indole auxin, as was found to be effective in inducing cambial activity in dormant Acer twigs (Wareing, 1958). Thus vegetative responses to photoperiod and to vernalization can be plausibly explained in terms of gibberellin synthesis, bearing in mind that here, as in simpler growth responses to gibberellin, an interaction with the effects of indole auxins is also probably involved,

Flowering responses cannot be satisfactorily explained on so simple a basis, though the frequent association between vegetative growth and flowering in long-day plants, whether induced by long-day photoperiods or by exogenous gibberellin, points to a related mechanism.

Considering first of all long-day plants, we find that most of them, if treated with gibberellin, will form a flower stalk and flowers even if kept in short day photoperiods. Similarly, exogenous gibberellin treatment in most cases will induce flowering of


biennials, without vernalization, though less regularly than such a treatment induces formation of a stalk. Thus in general outline the flowering response of long-day plants to exogenous gibberellin is parallel to the vegetative response. However, there are some divergent observations that require explanation :

(i) Some biennial long-day plants will flower if treated with gibberellin and kept in long-day photoperiods, but not if kept in short-day photoperiods, e.g. Hyoscyamus niger L. (Lang, 1956b). This is not always the case, and it seems to me likely as I have already suggested, that a suitable gibberellin dosage regime will be found to induce flowering in such cases.

(ii) Whereas vernalization of biennial long-day plants kept in long-day photoperiods leads to a more or less simultaneous differentiation of a stalk and flower primordia, gibberellin treatment sometimes (but not in all species) leads to a separation in time between these two effects, so that a considerable development of stalk takes place before flower primordia are formed, e.g. in Hyoscyamas (Lang, 1957; Sarkar, 1958), and Sarkar (1958) has in consequence concluded that the hypothetical hormone ' vernalin ' postu- lated by Melchers (1939) to be formed as a result of vernalization, cannot be identical with gibberellin. I do not think this conclusion is really warranted; it seems to me unlikely that application of exogenous gibberellin need necessarily exactly simulate the effects of endogenously produced glibberellin-like hormone, since the precise responses must depend on concentration levels and concentration gradients within the plant, difficult to achieve by exogenous application. Lang (1957) has suggested that the partial separation of the vegetative response of Hyoscyamus to gibberellin from its flowering response, indicates that the effect on flowering may be indirect. Indeed, there is experimental evidence that vegetative and flowering responses of long-day plants to photoperiod or to vernalization are separable. For example, Parker, Hendricks & Borthwick (1950) showed that increasing the number of long-day photocycles in induction of flowering of Hyoscyamus to levels in excess of that required to induce a complete flowering response, resulted in increased stem extension. Murneek (1940) showed that if Budbeckia bicolor Nutt. is grown in long-day photoperiods throughout its life, it produces flowers on long-stems; if after the necessary critical period for induction of flowering it is returned to short-dBy conditions, flowering proceeds normally but stem extension is much reduced. In other words, the flowering response has a relatively short critical induction period, characteristic of the species, but vegetative growth is quantitatively related to the number of long-day photoperiods to which the plant is exposed with no clear-cut critical period.

Thus it seems to me that the flowering response of long-day plants to photoperiod can be brought into line with the explanation offered above for the vegetative response by supposing that gibberellin is produced in the plant as a response to light, vegetative growth being proportional to the amount of gibberellin formed and hence to the total length of the light exposure, but that the flowering response is induced as a result of maintenance of certain critical levels of the gibberellin in the plant for a critical period. This explains the possibility of experimental separation of the two effects. Responses to vernalization can be similarly explained.

This view enables us to explain the responses of short-day plants with little further elaboration. Long-day photoperiods stimulate vegetative development of short-day plants but inhibit flowering, The little experimental evidence at present available indicates that gibberellin has a similar effect. Here we must assume that the induction of flowering only takes place if levels of gibberellin are maintained for a critical period below a certain critical level, a level which would be exceeded if the plant were exposed to long- days.

Thus, to summarize, I am suggesting that vegetative responses to photoperiod are governed directly by the influence of gibberellins, or similar substances, formed in the plant as a result of exposure to light, whereas flowering is governed by a further reaction

J.L.S.B. LVI] MORPHOGENETIC EFFECTS OF THE GIBBERELLINS 245

which is itself influenced by the endogenous gibberellin level. More concretely, supposing that a flowering hormone, ‘florigen’, common to short-day and long-day plants, does really exist, then in long-day plants its formation is dependent on maintenance of relatively high endogenous gibberellin levels for a critical period, and in short-day plants it is dependent on the maintenance of relatively low endogenous gibberellin levels for a critical period.

This is all frankly speculative, but is in good agreement with all we know of the effects of exogenous gibberellin on vegetative development and flowering. It is a t least a reason- ably useful hypothesis on which to base further experimental work.

( c ) Genetic dwarf.. The relationship between genetic dwarfs and their tall counterparts is in some ways

analogous to the relationship between photoperiodically sensitive plants growing in short- and long-day photoperiods respectively. I have tentatively explained the latter relationship in terms of gibberellin metabolism, biosynthesis being more active in long- day conditions. Similarly, genetic dwarfs, particularly since they assume the appearance of a tall phenotype if treated with gibberellin, could be interpreted as having a genetic failure in gibberellin metabolism. Indeed, some such reasoning as this was behind the successful search for gibberellin-like hormones in higer plants. However, Radley ( 1958) has failed to find any great difference in content of gibberellin-like hormones between dwarf and tall peas. This may be due to imperfections in extraction technique, but the result does emphasize the need for direct evidence for the explanation of responses to photoperiod proposed above.

However, while caution is necessary, the general impression obtained from the mass of experimental information on physiological effects of gibberellin now accumulating, is that we may be very near to a much closer understanding of the biochemical control of development of higher plants than we were before the discovery that the gibberellins are natural plant constituents.

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