PHYLLOTAXIS OF KNIPHOFIA AND LILIUM CANDID UM

PHYLLOTAXIS OF KNIPHOFIA AND LILIUM CANDID UM BY R. SNOW Felloiv of Magdalen College, Oxford [Received 12 March 1957) (With Plate i and 8 figures in the text) KNIPHOFIA According to Berger (1908) the leaves in most species of Kniphofia are arranged in four ranks. In a few species they are arranged in three or five ranks and in one, K. northiae, spirally. But he figures only a section taken far above the stem apex through four ranks of leaves in iv, iivaria (syn. aloides). Troll (1937) figures a section of a bud of K. iivaria, taken only a little way above the stem apex, and from this section also it appears that the leaves in this species are in four ranks, and further that they form pairs of opposite members, the pairs being successively at right angles. It also appears that the leaves in each pair differ in size. But for certainty and for a more exact description one needs transections through the stem apex and the insertions of the youngest leaves. Since four-ranked phyllotaxis is uncommon in monocotyledons, it seemed of interest to study further the phyllotaxis of Kniphofia in sections of buds of various species. Most of the buds examined have been the terminal buds of seedlings from seed of K. uvaria and K. piimila, and the others were lateral buds growing out from the base of older plants of various species in early May. The genetic nature of the seedlings is uncertain, since Kniphofias hybridize readily, but no differences were noticed between the buds of those attributed to the two different species. Some sections were cut free-hand after embedding in collodion, including those shown in Figs. 1,5,6 and some, for which I am indebted to my wife, with a microtome after embedding in paraffin, I am also much indebted to Dr. F. A. L. Clowes for the micro-photographs. The seedlings are all at first distichous. Sections of a young distichous seedling of K. uvaria, about 2 months old, are shown in Fig. i, a and b. Each leaf forms a complete sheath round the apex, as is usual in the Aloinae, and in Fig. 1,6, it can be seen that the youngest leaf has already done so before the end of the plastochron. The sheaf of this leaf was not indeed yet free for the apex, but it could be clearly recognized from the cell pattern, its cells being clearly distinct from those of the stem apex. The parts of the sheaths on the far side of the apex or axis are at first very thin, only 2 or 3 cells thick, and they remain for some time very low, so that the sheaths of the youngest leaves are often seen complete in a few sections only. Fig, 2, a and b, shows a seedling of K. pitmila about three months old. The original distichy, still shown by leaves 5 to 8, has changed abruptly to the mature four-ranked arrangement, or tetrastichy, at leaf 4. A photograph of this apex is shown in Plate 2, a. A lateral bud from the base of an old plant, probably of K. itvaria, with leaves in four ranks is shown in Fig. 3, At this stage of the plastochron, leaf i has nearly, but not quite, formed a sheath round the apex. Leaves 2 to 4 are cut above their sheaths, and outside leaf 4 the section has passed into the axis, which in buds of old plants is bowl-shaped, 160

Phyllotaxis of Kniphofia and Lilium candidum 3a Fig. I, a, b. A young seedling of Kniphofia iwaria, ax4 Fig. 2, a, b. An older seedling of K. pumila, a X 19, b X4 Fig. 3, a, c. Lateral bud of an old plant of K. uvaria, X 45. B N.P.

i62 R. SNOW A photograph is shown in Plate 2, b. In these buds, as in all the tetrastichous buds sanctioned, the leaves of each pair differ clearly in size and in level of insertion, and so presumably in age. In the bud shown in Fig. 3 the pairs are not quite at right angles. The seedlings do not all change directly from distichy to tetrastichy. In two seedlings of K. pitmila the early distichy was followed by an irregular spiral. Sections of the spiral part of one of these are shown in Fig. 4, a, b. The divergence angles in degrees from leaf 9 to leaf I (the youngest) were 170, 148, 134, 135, 137, 170, ioi. In the other seedling the angles from leaf 7 to leaf i were 163, 122, 129, 136, 152, 106. These two seedhngs were perhaps just turning to the normal tetrastichy with the youngest two leaves. An interesting point is that in tetrastichy the orientations of successive pairs of leaves may change in either of two ways. With one arrangement a line drawn through the centres of all the older leaves of each pair, or of all the younger ones, would form a spiral round the axis, as in Fig. 6, a, b, K. titbergeniana. With the other arrangement such a line would reverse its direction at each step, since all the older leaves of each pair are in two ranks on one side of the axis, and all the younger ones on the other side, as in Fig. 5, a, b, K. tysoni. This last arrangement was found in all the buds of K. uvaria and K. pttmila also, including the seedlings. The same two arrangements are well known it! the formation of other members, for instance lateral buds in some species with decussate phyllotaxis. The leaves of each pair in Kniphofia differ less in size, and presumably in age, than do the second leaf of a pair and the first leaf of the next. This is brought out clearly if one measures the radii from the centre of the apex or axis to a convenient point on each successive leaf, such as the centre of its outer or abaxial surface, and then calculates the ratios of every successive two radii. For example, in the bud of A', tvsoni shown in Fig. 5, these ratios, starting with that ofthe radii to the two youngest leaves, are the following: 0.47, 0.89, 0.57, 0.88, 0.72, 0.96, 0.72. The second, fourth and sixth of these ratios are those of the radii to the leaves of a pair, and they are much closer to unity than the others. In the spiral part of the seedling of K. pumila shown in Fig. 4, from leaf 3 to leaf 7, the successive ratios are more nearly equal, being 0.71, 0.83, 0.77, 0.71. The use of such ratios has been advocated by Richards (1948), who calls them 'plastochrone ratios'. He measures the radii to the morphological centres of leaves, but these in Kniphofia are not very sharply defitied. The outstanding peculiarity in the phyllotaxis of these species of Kniphofia is that the plane in which the leaves arise changes by a right angle after every second leaf, so that distichy is converted into tetrastichy. Troll (1937, p. 430) supposes that the apex twists through 90" after the formation of alternate leaves owing to an internal inherited cause. But this would surely be revealed by distortions of the apical cell pattern, and actually no such distortions are to be seen. Also in order to account for the two arrangements of successive leaf pairs described above, it would be necessary to suppose that in some species or some buds of Kniphofia the apex twists repeatedly in the same direction, and in other species in a direction that reverses every time. It seems to the writer improbable that there is any such difference between species or buds within one genus due directly to an inherited cause, and more probable that the difference between the two arrangements is brought about in some more itidirect way. As an alternative to Troll's theory, the following explanation may be suggested. In most species with apices that are elliptic in cross section when the new leaves are about

Phyllolaxis of Kniphofia and Lilium candidum 163 6a Fig. 4, a, b. A spiral bud of A', pumiln, a : ig, b x 55. Fig. 5, a, b. K. tysoni, a 22, b <55. Fig. 6, a, b. K. tubergeniana, a ^ 21, b >:5i.

164 R. SNOW to arise, these leaves arise at the narrow ends of the ellipse, as for instance in most decussate apices. In tetrastichous apices of Kniphofia when the last leaf formed has been the second leaf of a pair, the apex is very narrow in the plane in which the last two leaves have been formed, and much broader in the plane at right angles, as can be seen in Figs. 2 and 3, K. uvaria and K. pitmila. But when such an apex is forming the first leaf of a pair, it seems that it is broadest in the plane through the centre of this leaf (Figs. 5 and 6, K. tysoni and K. tubergeniana). In the early distichous phase, it seems that the apex is more nearly circular (Fig. 1). So it may be that in the tetrastichous apices the new leaves encroach on the apex so much that after the formation of each pair the apex is left very narrow in the plane through their centres, and consequently the next pair is formed from the narrow ends of the roughly elliptic apex in the plane at right angles. Weisse (1894, p. 285) considered that a similar periodic change of shape helps to regularize the phyllotaxis of decussate apices. But the present problem does not arise with regard to decussates, since they are at no time distichous, their leaf insertions being too small. It is of interest that the phyllotaxis can be spiral in Kniphofia, as also it is in palms (Henri, 1955) in/?/iofo (Snow, M., i95i)andin various other plants in which the youngest leaves form complete sheaths. This seems at first a difficulty for a space-filling theory of phyllotaxis, such as the writer has taken part in supporting (1931, 1955). For on such a theory the spirals and other regular systems are due to a process in which the new leaves are fitted into the depressions between the central parts of the existing leaves round the stem apex. But there is some evidence that the bases of encircling leaf sheaths to some degree conform to the contour line formed by the oldest leaves below them, rising closer to the tip of the stem apex above the higher central parts of the leaves below, and sinking further away from it elsewhere. Such evidence has been found in Dipsacus (Snow, R., 1951, p. 306) and in Rhoeo (Snow, M., 1957, p. 57). When the leaf sheaths develop in this way they will not prevent the central parts of the new leaves from fitting into depressions of the contour line round the stem apex. Concerning the three-ranked and four-ranked phyllotaxis systems reported by Berger in Kniphofia, it will be wise to wait until their existence has been confirmed in bud sections LiLIUM CANDIDUM Lilium candidum is the first of the species upon which a new theory of phyllotaxis has been founded (Plantefol, 1946-47). The theory, which the writer has discussed elsewhere (1955) is in brief the following. It is supposed that a number of leaf-generating centres travel in parallel ascending helices round the stem apex, leaving behind them continuous paths consisting of the bases of the leaves which they have formed at regular intervals of time. These paths, or the infiuences forming them, are called foliar helices, and are often the same as what were previously called parastichies, being one of the two sets of parastichies that wind round the apex in opposite directions. The foliar helices are supposed to be usually three in monocotyledons, and their rhythmic leaf-forming activities are supposed to be co-ordinated by a cetitre at the tip of the stem apex. The phyllotaxis of Lilium candidum is considered to support this theory for the following reason. If on the mature stem one tries to trace a regular genetic spiral that is, a spiral through the leaf bases in their order of age - it is claimed that one cannot do so: for if one chooses leaves at about equal angular divergences round the stem, one finds that one is sometimes taking a higher leaf before a lower one. On the other hand, it is

Phyllotaxis of Kniphofia and Lilium candidum 165 8 Figs. 7 and 8. Main buds of two bulbs of Lilium candidum, a, 64, b 'C 56.

i66 R. SNOW claimed that one can trace three fairly regular foliar helices, which in this species must be supposed not to be so co-ordinated exactly. But though this is a theory of the origin of leaves, their early positions in this species have not been observed, but only inferred from their later positions on the mature stem, a method which often leads to error. So in order to see the early positions, the writer has now cut sections of the buds. Bulbs of Lilium candidtun were started into growth in autumn, and when the shoots were about 1.5 cm. long to the tip of the stem, the terminal buds of four of them were flxed, embedded in collodion and sectioned freehand. Transections of two of them at the level of the youngest leaf, drawn under a projecting microscope, are illustrated in Figs, i and 2. The leaves are numbered along the genetic spiral. The bud shown in Fig. i has a very regular Fibonacci spiral phyllotaxis with contacts 3, 5 and 8, the contact 3 being only just reached. The leaves follow steadily along the genetic spiral, and the first ten divergence angles, from leaf o to leaf io, are 135, 136, 132, 136, 137, 137, 138, 134, 134, 136. The regularity of the pattern can also be appreciated by following the two conspicuous sets of intersecting curved parastichies, the five with leaf numbers differing by five, and the eight with numbers differing by eight. The bud shown in Fig. 2 has developed a little further, having a stem 1.71; cm. long, though it has not begun to form axillary flower-buds; and it has a higher phyllotaxis, the contacts being 8 and 13. It also is regular, except that it appears to be slightly eccentric, the leaves older than leaf six having grown a little more strongly on the right-hand half of the bud than on the left. The two sets of parastichies, the set of eight and the set of 13, run quite regularly, and the mean of the divergence angles from leaf i to leaf 35 is 137.2, or from 2 to 36, 137.4. The other two buds sectioned had also regular Fibonacci spirals with contacts five and eight. It may be noted that in three of the four buds sectioned the young leaves did not make contact along the three curves with leaf-numbers differing by three, although according to Plantefol (1948, pp. 154, 194) it is an essential point that leaves are formed in contact along the foliar helices. An appearance of such contact on the mature stem may be due to later lateral extension of the leaf bases. Several other bulbs of the same batch were left to grow on and flower, and it was confirmed that they were indeed L. candidum. Naturally it remains possible that in some other race of this species the phyllotaxis of the young leaves of the bud may be irregular, but this is now very improbable, and unless it can be directly demonstrated, there are no grounds for supposing it. As to the nature of the irregularities described on the mature stem, these seem to be similar, though slighter, to those described by Schoute (1922) in various species, and called by him 'growth whorls'. He concluded that they were secondary irregularities in the levels of the leaves caused by unequal elongations of diflerent sectors of the stem. REFERENCES BERCER, otrcer, A. (iqos). (IC)OS). Aloinae. fpanzeiireich, Pflanzeiireich, 4, 38. HENRI, M. P. (1955). Organisation foliaur chez le piilmier palmier hiule. Rev, Gen, Bot,, 62, 127. PLANTEFOL, L. (1946-47). La Theorie dos Helices Foliariss Multiples. Ann. Sci. Nat. Bot. 7 and 8. (Also separately, Paris, Masson, 1948.') ' RICHARDS, F. J. (1948). The geometry of phyllotaxis. Symp. Soc, EX/T. Biol 2, 217 SCHOUTE, J. C. (1922). Growth Whorls. Rec, trav. bot. Neerl., 19, 184. SNOW, M. (1951). Experiments on spirodistichous shoot apices. Phil. Tram. Roy. Soc. Lond., B, 235, SNOW, M. (1955). Spirodistichy re-interpreted. Ibid., 239, 43.

PLATE I THE NEW PHYTOLOGIST, 57, 2 &^^^s^s SNOW W/17./,O7'.-JA7.S' Of' KNIPHOFIA LI MUM CANDIDUM cinri p. 167)

Phyllotaxis of Kniphofia and Lilium candidum 167 SNOW, M. B., SNOW, R. (1931). Experiments on phyllotaxis, part i. Ibid., 221, i. SNOW, R. (1951). Experiments on bijugate apices. Ibid., 235, 291. SNOW, R. (1955). Problems of phyllotaxis and leaf determination. Endeavour, 14, 190. TROLL, W. (1937). Vergleichende Morphologie der Hoheren Pflanzen, i. WEISSE, A. (1894). Neus Beitrage zur mechanischen Blattstellungslehre. Jahrb. wiss. Bot., 26, 236. LEGEND TO PLATE i Plate I, a. Same bud of Kniphofia pumila as text-fig. 2, x 102. b. Same bud of Kniphofia uvaria as text-fig. 3, X102.