Darwin's Backyard

by James T. Costa

  A role for gravity in downward root growth was established in the early nineteenth century by the celebrated English experimental plant breeder Thomas Knight, whom we learned about in Chapter 6. In a paper presented to the Royal Society in 1806, Knight noted that if gravitation were the cause of the downward growth of the radicle, it must act either on the growing tissue during its formation, or on the motion of the sap and other liquids within the cells. Thus, Knight reasoned, “as gravitation could produce these effects only whilst the seed remained at rest, and in the same position relative to the attraction of the earth, I imagined that its operation would become suspended by constant and rapid change of the position of the germinating seed, and that it might become counteracted by the agency of centrifugal force.”17 On a small waterwheel along a stream in his garden, like that used to mill grain, Knight affixed a number of soaked beans to the wheel’s circumference with their radicles pointing in all directions. He set the wheel spinning, and noted that no matter what direction the growing radicles initially pointed, they soon extended outwards away from the center of the wheel. Knight concluded that the radicles were influenced by centrifugal force, therefore suggesting that they must be similarly influenced by gravity when growing in their normal situation. Darwin did not comment on Knight’s experiment, but agreed with his conclusion about the importance of gravity. Geotropism was real, but the important question for him was, did gravity act directly upon the radicle, as Knight seemed to suggest, or was this another case of a stimulus-response reaction like with canary grass? The title of the chapter on the subject in Power of Movement signals his answer: “Sensitiveness to gravitation, and its transmitted effects.”

  The key word is “transmitted.” The definitive demonstration is straightforward: a controlled experiment testing for geotropic response with root tips intact versus root tips in some way removed or destroyed. It turned out that the Darwins did not think of this experiment first: just a few years earlier in 1872 a young plant physiologist in Poland, Theophil Ciesielski, published his doctoral dissertation on the downward curvature of roots. Ciesielski noted the difference between the region of cell growth and extension in the radicle and the zone of sensitivity at the tip influencing downward movement, and showed that removing the tip resulted in a loss of downward growth, or gravity sensitivity. The Darwins agreed, and in Power of Movement credited Ciesielski with this discovery. For the sake of completeness they replicated Ciesielski’s tip-excision experiments in various ways, including amputation and killing the tip with chemical treatment. These measures effectively knocked out the geotropic response, but it could be restored if the tips were allowed to grow back. They concluded that although most authors thought radicles bent in response to gravity, in fact “we now know that it is the tip alone which is acted on, and that this part transmits some influence to the adjoining parts, causing them to curve downwards. Gravity does not appear to act in a more direct manner on a radicle, than it does on any lowly organised animal, which moves away when it feels some weight or pressure.”18

  Common bean (Vicia faba) radicles grown horizontally for nearly 24h. (A, B, C) Radicle tips cauterized with silver nitrate, preventing a geotropic response. (D, E, F) Radicle tips left intact, showing normal geotropism. From Darwin (1880), p. 531.

  This conclusion put the Darwins on a collision course with one Julius von Sachs, distinguished professor of physiology at the University of Würzburg in Germany. At that time Germany was at the cutting edge of physiological research, and Sachs’s laboratory was one of the finest. Sachs made his name with acclaimed work on transpiration, seed germination, and flowering. Frank, who was fluent in German, made two visits to Sachs’s lab in Würzburg in the late 1870s to learn the latest techniques, and he also learned a great deal by reading German scientific papers and Sachs’s own well-known 1868 text, the Lehrbuch der Botanik. His personal acquaintance with Sachs did not seem to help reduce friction between the German botanist and his father, however. In fact, Sachs eventually broke off his relationship with Frank after the perceived affront of the Darwins’ suggesting that he was incorrect in his experimental conclusions over geotropism.

  Sachs knew of Ciesielski’s experiments and had one of his research assistants replicate them. Curiously, he failed to get the same result as Ciesielski and concluded that the Pole was incorrect: the radicle tips were not sensitive to gravity, he declared, and there were no so-called transmitted effects. Charles and Frank were puzzled by this, since their experiments clearly confirmed Ciesielski and they said so in print. Apparently their sin was not to simply disagree with Sachs, however, but to suggest there was a problem with his experimental technique. Adding insult to injury, in The Power of Movement Charles asserted that Ciesielski “[spoke] confidently of the obliteration of all geotropic action” with good reason, and that “it seems probable that Sachs unintentionally amputated the radicles on which he experimented, not strictly in a transverse direction.”19 In other words, if the tips were sliced off at a bit of an angle, some tiny piece of tip tissue might have remained, enough to show some geotropic response and lead Sachs astray. The German savant took this as a grave personal affront, priding himself as having exemplary experimental technique, with his laboratory the very embodiment of cutting-edge science.

  There was more going on here than a bruised ego. In short, Sachs was contemptuous of the Darwins’ work in large part because of the rough-and-ready style and home environment of their approach, for their failing to use the sophisticated instruments and controlled conditions of the German labs. The run-in with Sachs was thus symptomatic of a deeper issue, a sea change in the conduct of science in the late nineteenth century; historian Soraya de Chadarevian has aptly characterized their disagreement as a disconnect between old-fashioned “country-house” science and the emerging new laboratory-based science of the time. This was bound up with the increasing professionalization of science in the same period; Charles Darwin was of course very much in the tradition of the gentleman-naturalist, while Sachs was a brash, talented professional who had risen from humble beginnings to assume the botany chair at a fine university. He had won acclaim putting the latest high-tech equipment to good use, and had no use for Darwin’s brand of drawing-room puttering with potted plants.

  But ego surely played a role too. Sachs had a deserved reputation as a skilled experimentalist, which meant the suggestion of not only incorrect conclusions but sloppy technique was like pouring lemon juice on a cut. As excellent a scientist as Sachs may have been, unfortunately he was not as well known for his generosity of spirit. Already touchy about the term “circumnutation,” which Charles and Frank coined to replace Sachs’s own term “revolving nutation,” things came to a head over geotropism. In his 1882 book on plant physiology Sachs was publicly dismissive of what he called the Darwins’ “unskillfully made and improperly explained” experiments, and a more personal animus is evident in his private notebook: “Personal acquaintances often have their good side. I first became aware of the whole wre[t]chedness of Darwin’s activities when Francis Darwin studied here in 1878 and 79; I had the opportunity to look behind the scenes and when the miserable book ‘On Movements’ appeared, I realized that here we are dealing with literary rascals.”20 Strong words from the esteemed professor! The Darwins thought there must be some mistake, as they in fact had high regard for Sachs and cited his excellent work in many places in The Power of Movement. But it never occurred to them to be deferential to authority on any scientific point, let alone one with which their experiments disagreed. Frank traveled to Würzburg to see if he could make amends, but was curtly dismissed by Sachs and never saw him again.

  As de Chadarevian concluded, if time has vindicated the Darwins’ conclusions about root radicles and climbers, it has also vindicated the philosophy of Sachs: in the ensuing century, the science of country-house laboratories and gentleman-naturalists was replaced nearly wholesale by professional science conducted in specialized laboratories and with precision equipment. In
the years following the death of his father in 1882, Frank himself was in the vanguard of this movement in Britain, becoming first Lecturer and then Reader in Botany at Cambridge, and was among an influential cohort of young scientists bringing to Britain the cutting-edge experimental techniques they learned in Germany. Geotropism remained a research interest, and when, around the turn of the century, the “statolith theory” of gravity-sensing was proposed, Frank tested and supported the theory in an ingenious manner.

  Plant statoliths are starch granules (technically called amyloplasts) found in specialized oblong cells (statocytes) near the root tip. They function in the same way as otoliths, the tiny calcium carbonate granules of the inner ear that play a role in our sense of balance. (In fact, the term statolith was coined to correspond to otolith, as the mechanism of balance and orientation in animals was discovered earlier.) In both cases the granules can free-fall within their cells in response to gravity and pile up on whatever side of the cell is “down,” where they trigger a signal. In the case of the otoliths in our ears the signal is triggered by touching and bending tiny hairs that line the inner walls of the cell; the nerve impulse is carried to our brain, which together with other input (from our eyes, for example) uses the information from these cells to gauge our body’s position and keep us upright. In the case of the plants there are molecular chemical sensors in the cells rather than hairs. The plants lack nerves, despite Darwin’s notion of his “sagacious” and “crafty” plants as animal-like, but the effect is the same: the signal is carried from the statocytes to the zone of active cell growth further up the radicle, and between the growth rate of different cells in that zone and changes in cell turgor pressure the root tip can be turned and guided in the right direction. Like us, the plants can tell which way is up and which is down.

  Frank became fascinated by the statolith theory of geotropism, and pointed out that the experimental evidence for the theory was persuasive but incomplete. For example, he felt that experimental support for the theory based on destruction of the starch granules was suggestive but not definitive, since the demonstrated loss of geotropism in those cases could have been incidental to the loss of some other function simply as a result of eliminating the granules. Working with sorghum seedlings, he carried out experiments based on the destruction of the starch granules by heating. Finding that both sensitivity to gravity and to light seemed to be affected, and not suspecting that statoliths could also play a role in upward—“heliotropic”—shoot growth, he concluded that “these and other similar experiments showed us that we had no right to conclude that the loss of geotropic capacity depended on the absence of the special mechanism (statoliths), but rather that the loss of the starch may perhaps be no more than a symptom of exhaustion which shows itself both geo- and heliotropically.”

  He then devised a means of testing for the importance of statoliths by intensifying rather than removing their effects. His “tuning fork” method involved subjecting the seedlings to constant vibration, reasoning that if the response to gravity stems from “contact-irritability” by the statoliths within the cells, then the effect ought to be magnified if the statoliths could be made to continually jiggle and bounce on the cell wall they were resting on. He hypothesized that this would increase the stimulus, rather like increasing the stimulus to your ear by repeatedly ringing a door bell, pressing and removing your finger over and over in rapid succession. He rigged up a tuning fork to continually vibrate, and connected the tines of the fork to metal boxes in which he placed up to a half-dozen seedlings with their radicles growing horizontally. A similar number was set up in adjacent control boxes with no direct contact with the tuning fork. After vibrating the treatments for a time he placed both treatments and controls into an instrument called a klinostat—a device invented by Sachs to negate the effects of gravity by rotation, based on the waterwheel principle that Knight had used in his garden. A few hours later, Frank measured the curvature of the radicles, and lo and behold, those subjected to vibration showed considerably greater curvature than the controls. He repeated the process with several species and under various conditions; besides the geotropism of the radicle Frank also measured the upward curvature of the shoot (looking at effects on what he called “heliotropism”—shoot growth toward light, and so generally away from the direction of gravity’s pull). Reporting his results to the Royal Society, Frank concluded that vibration did not affect the shoot response but clearly affected the radicles; he therefore supported the statolith theory of geotropism with his device. His father would have been proud of his son’s experimental ingenuity.

  Coming Full Circle

  The experimental work on shoot, tendril, and root movement I discuss in this chapter is just a fraction of the many research questions explored in The Power of Movement in Plants; another research agenda of the Darwins focused on “sleep” in plants—both the diurnal movement of leaves and other organs and the touch sensitivity seen in the leaves of some species like mimosa or sensitive plant. We haven’t space enough to delve into these ingenious experiments, too, but the underlying point was the same: to better understand plant sense perception and its myriad adaptations, qualities that at once underscore their common origin with animals and illustrate the evolutionary principles of diversification and co-optation. In his characteristically self-deprecating way, Darwin referred to The Power of Movement in Plants as “dry as dust” in a letter to his publisher. Fair enough, it’s not exactly a page-turner. Okay, it’s far from a page-turner—but of course it was not meant to be. But The Movements and Habits of Climbing Plants—which grew to over 200 pages by the second edition—and The Power of Movement in Plants—running to 573 pages—together constituted a botanical tour-de-force, helping open up new research avenues in plant sense perception that remain vital today, and also helping to solidify Darwin’s evolutionary vision of a truly universal Tree of Life.

  That unitary vision was never far beneath the surface for Darwin. Consider his concluding remarks in both of these botanical works. In the last paragraphs of Climbing Plants he remarked that “The most interesting point in the natural history of climbing plants is their diverse powers of movement,” and that “the most different organs—the stem, flower-peduncle, petiole, mid-ribs of the leaf or leaflets, and apparently aërial roots—all possess this power.”21 His deeper interest is evident in the last paragraph: “It has often been vaguely asserted,” he says, “that plants are distinguished from animals by not having the power of movement. It should rather be said that plants acquire and display this power only when it is of some advantage to them.” He points to the tendril-bearers, which provide a lesson in “how high in the scale of organization a plant may rise.” It is worth looking closely at the language he uses in the final sentences:

  It first places its tendrils ready for action, as a polypus places its tentacula. If the tendril be displaced, it is acted on by the force of gravity and rights itself. It is acted on by the light, and bends towards or from it, or disregards it, whichever may be most advantageous. During several days the tendril or internodes, or both, spontaneously revolve with a steady motion. The tendril strikes some object, and quickly curls round and firmly grasps it. In the course of some hours it contracts into a spire, dragging up the stem, and forming an excellent spring. All movements now cease. By growth the tissues soon become wonderfully strong and durable.22

  Note his carefully chosen words, expressing what can only be read as deliberate actions of the plant: it places its tendrils, just as a marine invertebrate polyp places its tentacles, and can right itself. It bends toward or from light, or disregards it. A tendril spontaneously revolves, and one striking an object quickly curls around and firmly grasps it. Over time it contracts, dragging up the stem of the climber.

  Yes, tendrils are superb adaptations for seeking, grasping, and helping the plant climb—they move with intentionality relevant to their mode of life. Tendril-bearers certainly have ascended “high in the scale of organization,” as Dar
win put it—in a manner of speaking one might say they used those tendrils to climb the Tree of Life. He concludes, finally, that “the tendril has done its work, and done it in an admirable manner.” Indeed, and the intentionality, the behavior of the climbers, is really of a piece with that found in the probing shoot or radicle. Hence the very last sentence in The Power of Movement echoes that of Climbing Plants: “It is hardly an exaggeration to say that the tip of the radicle thus endowed, and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements.”23 An animal in plant’s clothing.

  Experimentising: Seek and Ye Shall Find

  Climbing plants were nearly as “sagacious” to Darwin as his beloved Drosera, illustrating for him several evolutionary principles. Seemingly animal-like in their powers of movement and sense perception, they too point to the fundamental underlying unity of plants and animals. Shoots that incessantly rotate, tendrils that probe and grasp, roots that can tell down from up . . . these responses to touch, light, and gravity may take place in slow motion, but they are “behaviors” nonetheless.