The Power of Movement in Plants

by Charles Darwin; Sir Francis Darwin

SENSITIVENESS OF THE TIP OF THE RADICLE TO MOIST AIR.

Sachs made the interesting discovery, a few years ago, that the radicles of many seedling plants bend towards an adjoining damp surface.[^[9]] We shall here endeavour to show that this peculiar form of sensitiveness resides in their tips. The movement is directly the reverse of that excited by the irritants hitherto considered, which cause the growing part of the radicle to bend away from the source of irritation. In our experiments we followed Sachs’ plan, and sieves with seeds germinating in damp sawdust were suspended so that the bottom was generally inclined at 40° with the horizon. If the radicles had been acted on solely by geotropism, they would have grown out of the bottom of the sieve perpendicularly downwards; but as they were attracted by the adjoining damp surface they bent towards it and were deflected 50° from the perpendicular. For the sake of ascertaining whether the tip or the whole growing part of the radicle was sensitive to the moist air, a length of from 1 to 2 mm. was coated in a certain number of cases with a mixture of olive-oil and lamp-black. This mixture was made in order to give consistence to the oil, so that a thick layer could be applied, which would exclude, at least to a large extent, the moist air, and would be easily visible. A greater number of experiments than those which were actually tried would have been necessary, had not it been clearly established that the tip of the radicle is the part which is sensitive to various other irritants.

[9] ‘Arbeiten des Bot. Institut., in Würzburg,’ vol. i. 1872, p. 209.

Phaseolus multiflorus.—Twenty-nine radicles, to which nothing had been done, growing out of a sieve, were observed at the same time with those which had their tips greased, and for an equal length of time. Of the 29, 24 curved themselves so as to come into close contact with the bottom of the sieve. The place of chief curvature was generally at a distance of 5 or 6 mm. from the apex. Eight radicles had their tips greased for a length of 2 mm., and two others for a length of 1½ mm.; they were kept at a temperature of 15°–16° C. After intervals of from 19 h. to 24 h. all were still vertically or almost vertically dependent, for some of them had moved towards the adjoining damp surface by about 10°. They had therefore not been acted on, or only slightly acted on, by the damper air on one side, although the whole upper part was freely exposed. After 48 h. three of these radicles became considerably curved towards the sieve; and the absence of curvature in some of the others might perhaps be accounted for by their not having grown very well. But it should be observed that during the first 19 h. to 24 h. all grew well; two of them having increased 2 and 3 mm. in length in 11 h.; five others increased 5 to 8 mm. in 19 h.; and two, which had been at first 4 and 6 mm. in length, increased in 24 h. to 15 and 20 mm.

The tips of 10 radicles, which likewise grew well, were coated with the grease for a length of only 1 mm., and now the result was somewhat different; for of these 4 curved themselves to the sieve in from 21 h. to 24h., whilst 6 did not do so. Five of the latter were observed for an additional day, and now all excepting one became curved to the sieve.

The tips of 5 radicles were cauterised with nitrate of silver, and about 1 mm. in length was thus destroyed. They were observed for periods varying between 11 h. and 24h., and were found to have grown well. One of them had curved until it came into contact with the sieve; another was curving towards it; whilst the remaining three were still vertically dependent. Of 7 not cauterised radicles observed at the same time, all had come into contact with the sieve.

The tips of 11 radicles were protected by moistened gold-beaters’ skin, which adheres closely, for a length varying from 1½ to 2½ mm. After 22 h. to 24 h., 6 of these radicles were clearly bent towards or had come into contact with the sieve; 2 were slightly curved in this direction, and 3 not at all. All had grown well. Of 14 control specimens observed at the same time, all excepting one had closely approached the sieve. It appears from these cases that a cap of goldbeaters’ skin checks, though only to a slight degree, the bending of the radicles to an adjoining damp surface. Whether an extremely thin sheet of this substance when moistened allows moisture from the air to pass through it, we do not know. One case indicated that the caps were sometimes more efficient than appears from the above results; for a radicle, which after 23 h. had only slightly approached the sieve, had its cap (1½ mm. in length) removed, and during the next 15½ h. it curved itself abruptly towards the source of moisture, the chief seat of curvature being at a distance of 2 to 3 mm. from the apex.

Vicia faba.—The tips of 13 radicles were coated with the grease for a length of 2 mm.; and it should be remembered that with these radicles the seat of chief curvature is about 4 or 5 mm. from the apex. Four of them were examined after 22h., three after 26 h., and six after 36 h., and none had been attracted towards the damp lower surface of the sieve. In another trial 7 radicles were similarly treated, and 5 of them still pointed perpendicularly downwards after 11 h., whilst 2 were a little curved towards the sieve; by an accident they were not subsequently observed. In both these trials the radicles grew well; 7 of them, which were at first from 4 to 11 mm. in length, were after 11 h. between 7 and 16 mm.; 3 which were at first from 6 to 8 mm. after 26 h. were 11.5 to 18 mm. in length; and lastly, 4 radicles which were at first 5 to 8 mm. after 46 h. were 18 to 23 mm. in length. The control or ungreased radicles were not invariably attracted towards the bottom of the sieve. But on one occasion 12 out of 13, which were observed for periods between 22 h. and 36 h., were thus attracted. On two other occasions taken together, 38 out of 40 were similarly attracted. On another occasion only 7 out of 14 behaved in this manner, but after two more days the proportion of the curved increased to 17 out of 23. On a last occasion only 11 out of 20 were thus attracted. If we add up these numbers, we find that 78 out of 96 of the control specimens curved themselves towards the bottom of the sieve. Of the specimens with greased tips, 2 alone out of the 20 (but 7 of these were not observed for a sufficiently long time) thus curved themselves. We can, therefore, hardly doubt that the tip for a length of 2 mm. is the part which is sensitive to a moist atmosphere, and causes the upper part to bend towards its source.

The tips of 15 radicles were cauterised with nitrate of silver, and they grew as well as those above described with greased tips. After an interval of 24 h., 9 of them were not at all curved towards the bottom of the sieve; 2 were curved towards it at angles of 20° and 12° from their former vertical position, and 4 had come into close contact with it. Thus the destruction of the tip for a length of about 1 mm. prevented the curvature of the greater number of these radicles to the adjoining damp surface. Of 24 control specimens, 23 were bent to the sieve, and on a second occasion 15 out of 16 were similarly curved in a greater or less degree. These control trials are included in those given in the foregoing paragraph.

Avena sativa.—The tips of 13 radicles, which projected between 2 and 4 mm. from the bottom of the sieve, many of them not quite perpendicularly downwards, were coated with the black grease for a length of from 1 to 1½ mm. The sieves were inclined at 30° with the horizon. The greater number of these radicles were examined after 22 h., and a few after 25 h., and within these intervals they had grown so quickly as to have nearly doubled their lengths. With the ungreased radicles the chief seat of curvature is at a distance of not less than between 3.5 and 5.5 mm., and not more than between 7 and 10 mm. from the apex. Out of the 13 radicles with greased tips, 4 had not moved at all towards the sieve; 6 were deflected towards it and from the perpendicular by angles varying between 10° and 35°; and 3 had come into close contact with it. It appears, therefore, at first sight that greasing the tips of these radicles had checked but little their bending to the adjoining damp surface. But the inspection of the sieves on two occasions produced a widely different impression on the mind; for it was impossible to behold the radicles with the black greased tips projecting from the bottom, and all those with ungreased tips, at least 40 to 50 in number, clinging closely to it, and feel any doubt that the greasing had produced a great effect. On close examination only a single ungreased radicle could be found which had not become curved towards the sieve. It is probable that if the tips had been protected by grease for a length of 2 mm. instead of from 1 to 1½ mm., they would not have been affected by the moist air and none would have become curved.

Triticum vulgare.—Analogous trials were made on 8 radicles of the common wheat; and greasing their tips produced much less effect than in the case of the oats. After 22 h., 5 of them had come into contact with the bottom of the sieve; 2 had moved towards it 10° and 15°, and one alone remained perpendicular. Not one of the very numerous ungreased radicles failed to come into close contact with the sieve. These trials were made on Nov. 28th, when the temperature was only 4.8° C. at 10 A.M. We should hardly have thought this case worth notice, had it not been for the following circumstance. In the beginning of October, when the temperature was considerably higher, viz., 12° to 13° C., we found that only a few of the ungreased radicles became bent towards the sieve; and this indicates that sensitiveness to moisture in the air is increased by a low temperature, as we have seen with the radicles of Vicia faba relatively to objects attached to their tips. But in the present instance it is possible that a difference in the dryness of the air may have caused the difference in the results at the two periods.

Finally, the facts just given with respect to Phaseolus multiflorus, Vicia faba, and Avena sativa show, as it seems to us, that a layer of grease spread for a length of 1½ to 2 mm. over the tip of the radicle, or the destruction of the tip by caustic, greatly lessens or quite annuls in the upper and exposed part the power of bending towards a neighbouring source of moisture. We should bear in mind that the part which bends most, lies at some little distance above the greased or cauterised tip; and that the rapid growth of this part, proves that it has not been injured by the tips having been thus treated. In those cases in which the radicles with greased tips became curved, it is possible that the layer of grease was not sufficiently thick wholly to exclude moisture, or that a sufficient length was not thus protected, or, in the case of the caustic, not destroyed. When radicles with greased tips are left to grow for several days in damp air, the grease is drawn out into the finest reticulated threads and dots, with narrow portions of the surface left clean. Such portions would, it is probable, be able to absorb moisture, and thus we can account for several of the radicles with greased tips having become curved towards the sieve after an interval of one or two days. On the whole, we may infer that sensitiveness to a difference in the amount of moisture in the air on the two sides of a radicle resides in the tip, which transmits some influence to the upper part, causing it to bend towards the source of moisture. Consequently, the movement is the reverse of that caused by objects attached to one side of the tip, or by a thin slice being cut off, or by being slightly cauterised. In a future chapter it will be shown that sensitiveness to the attraction of gravity likewise resides in the tip; so that it is the tip which excites the adjoining parts of a horizontally extended radicle to bend towards the centre of the earth.

SECONDARY RADICLES BECOMING VERTICALLY GEOTROPIC BY THE DESTRUCTION OR INJURY OF THE TERMINAL PART OF THE PRIMARY RADICLE.

Sachs has shown that the lateral or secondary radicles of the bean, and probably of other plants, are acted on by geotropism in so peculiar a manner, that they grow out horizontally or a little inclined downwards; and he has further shown[^[10]] the interesting fact, that if the end of the primary radicle be cut off, one of the nearest secondary radicles changes its nature and grows perpendicularly downwards, thus replacing the primary radicle. We repeated this experiment, and planted beans with amputated radicles in friable peat, and saw the result described by Sachs; but generally two or three of the secondary radicles grew perpendicularly downwards. We also modified the experiment, by pinching young radicles a little way above their tips, between the arms of a U-shaped piece of thick leaden wire. The part pinched was thus flattened, and was afterwards prevented from growing thicker. Five radicles had their ends cut off, and served as controls or standards. Eight were pinched; of these 2 were pinched too severely and their ends died and dropped off; 2 were not pinched enough and were not sensibly affected; the remaining 4 were pinched sufficiently to check the growth of the terminal part, but did not appear otherwise injured. When the U-shaped wires were removed, after an interval of 15 days, the part beneath the wire was found to be very thin and easily broken, whilst the part above was thickened. Now in these four cases, one or more of the secondary radicles, arising from the thickened part just above the wire, had grown perpendicularly downwards. In the best case the primary radicle (the part below the wire being 1½ inch in length) was somewhat distorted, and was not half as long as three adjoining secondary radicles, which had grown vertically, or almost vertically, downwards. Some of these secondary radicles adhered together or had become confluent. We learn from these four cases that it is not necessary, in order that a secondary radicle should assume the nature of a primary one, that the latter should be actually amputated; it is sufficient that the flow of sap into it should be checked, and consequently should be directed into the adjoining secondary radicles; for this seems to be the most obvious result of the primary radicle being pinched between the arms of a U-shaped wire.

[10] ‘Arbeiten Bot. Institut., Würzburg,’ Heft iv. 1874, p. 622.

This change in the nature of secondary radicles is clearly analogous, as Sachs has remarked, to that which occurs with the shoots of trees, when the leading one is destroyed and is afterwards replaced by one or more of the lateral shoots; for these now grow upright instead of sub-horizontally. But in this latter case the lateral shoots are rendered apogeotropic, whereas with radicles the lateral ones are rendered geotropic. We are naturally led to suspect that the same cause acts with shoots as with roots, namely, an increased flow of sap into the lateral ones. We made some trials with Abies communis and pectinata, by pinching with wire the leading and all the lateral shoots excepting one. But we believe that they were too old when experimented on; and some were pinched too severely, and some not enough. Only one case succeeded, namely, with the spruce-fir. The leading shoot was not killed, but its growth was checked; at its base there were three lateral shoots in a whorl, two of which were pinched, one being thus killed; the third was left untouched. These lateral shoots, when operated on (July 14th) stood at an angle of 8° above the horizon; by Sept. 8th the unpinched one had risen 35°; by Oct. 4th it had risen 46°, and by Jan. 26th 48°, and it had now become a little curved inwards. Part of this rise of 48° may be attributed to ordinary growth, for the pinched shoot rose 12° within the same period. It thus follows that the unpinched shoot stood, on Jan. 26th, 56° above the horizon, or 34° from the vertical; and it was thus obviously almost ready to replace the slowly growing, pinched, leading shoot. Nevertheless, we feel some doubt about this experiment, for we have since observed with spruce-firs growing rather unhealthily, that the lateral shoots near the summit sometimes become highly inclined, whilst the leading shoot remains apparently sound.

A widely different agency not rarely causes shoots which naturally would have brown out horizontally to grow up vertically. The lateral branches of the Silver Fir (A. pectinata) are often affected by a fungus, Æcidium elatinum, which causes the branch to enlarge into an oval knob formed of hard wood, in one of which we counted 24 rings of growth. According to De Bary[^[11]], when the mycelium penetrates a bud beginning to elongate, the shoot developed from it grows vertically upwards. Such upright shoots afterwards produce lateral and horizontal branches; and they then present a curious appearance, as if a young fir-tree had grown out of a ball of clay surrounding the branch. These upright shoots have manifestly changed their nature and become apogeotropic; for if they had not been affected by the Æcidium, they would have grown out horizontally like all the other twigs on the same branches. This change can hardly be due to an increased flow of sap into the part; but the presence of the mycelium will have greatly disturbed its natural constitution.

[11] See his valuable article in ‘Bot. Zeitung,’ 1867, p. 257, on these monstrous growths, which are called in German “Hexenbesen,” or “witch-brooms.”

According to Mr. Meehan,[^[12]] the stems of three species of Euphorbia and of Portulaca oleracea are “normally prostrate or procumbent;” but when they are attacked by an Æcidium, they “assume an erect habit.” Dr. Stahl informs us that he knows of several analogous cases; and these seem to be closely related to that of the Abies. The rhizomes of Sparganium ramosum grow out horizontally in the soil to a considerable length, or are diageotropic; but F. Elfving found that when they were cultivated in water their tips turned upwards, and they became apogeotropic. The same result followed when the stem of the plant was bent until it cracked or was merely much bowed.[^[13]]

[12] ‘Proc. Acad. Nat. Sc. Philadelphia,’ June 16th, 1874, and July 23rd, 1875.

[13] See F. Elfving’s interesting paper in ‘Arbeiten Bot. Institut., in Würzburg,’ vol. ii. 1880, p. 489. Carl Kraus (Triesdorf) had previously observed (‘Flora,’ 1878, p. 324) that the underground shoots of Triticum repens bend vertically up when the parts above ground are removed, and when the rhizomes are kept partly immersed in water.

No explanation has hitherto been attempted of such cases as the foregoing,—namely, of secondary radicles growing vertically downwards, and of lateral shoots growing vertically upwards, after the amputation of the primary radicle or of the leading shoot. The following considerations give us, as we believe, the clue. Firstly, any cause which disturbs the constitution[^[14]] is apt to induce reversion; such as the crossing of two distinct races, or a change of conditions, as when domestic animals become feral. But the case which most concerns us, is the frequent appearance of peloric flowers on the summit of a stem, or in the centre of the inflorescence,—parts which, it is believed, receive the most sap; for when an irregular flower becomes perfectly regular or peloric, this may be attributed, at least partly, to reversion to a primitive and normal type. Even the position of a seed at the end of the capsule sometimes gives to the seedling developed from it a tendency to revert. Secondly, reversions often occur by means of buds, independently of reproduction by seed; so that a bud may revert to the character of a former state many bud-generations ago. In the case of animals, reversions may occur in the individual with advancing age. Thirdly and lastly, radicles when they first protrude from the seed are always geotropic, and plumules or shoots almost always apogeotropic. If then any cause, such as an increased flow of sap or the presence of mycelium, disturbs the constitution of a lateral shoot or of a secondary radicle, it is apt to revert to its primordial state; and it becomes either apogeotropic or geotropic, as the case may be, and consequently grows either vertically upwards or downwards. It is indeed possible, or even probable, that this tendency to reversion may have been increased, as it is manifestly of service to the plant.

[14] The facts on which the following conclusions are founded are given in ‘The Variation of Animals and Plants under Domestication,’ 2nd edit. 1875. On the causes leading to reversion see chap. xii. vol. ii. and p. 59, chap. xiv. On peloric flowers, chap. xiii. p. 32; and see p. 337 on their position on the plant. With respect to seeds, p. 340. On reversion by means of buds, p. 438, chap. xi. vol. i.