Hanno Richter, University of Agricultural Sciences, Vienna, and Pierre Cruiziat, PIAF-INRA-UBP, France

August, 2002

The history of physiology shows many examples of the same debate on how biological systems function, some saying that this functioning is mainly the result of specific properties of the living systems, others affirming that physical laws still play a major role, at least in some aspects. In fact, as we now see more clearly, properties of living cells and physical laws which apply to all living and non living systems continuously interact and cannot be separated. The history of our understanding of sap ascent in plants, and especially in trees, is a beautiful example for this classical debate.

Period of Preparation (Before 1889)

Attempts to explain water transport in plants started with a search for analogies with blood circulation in vertebrates, a physiological process previously elucidated by William Harvey (1628) and Marcello Malpighi (1661). Malpighi, who was also a pioneer in plant anatomy, studied the construction of stem wood and became convinced that vessels (tracheae) served for air transport, while the fibres should transport water. Stephen Hales in 1727 was most likely, the first scientist to show that water in plants is transported unidirectionally from the soil to the transpiring leaves; he could only speculate on the tissues conducting water in the stem. In 1798, the Imperial Academy of Scientists in Erlangen (Germany) organized a prize competition to clear up two questions not yet fully understood at that time:

1) Which one of the known main parts of a plant (cortex, sapwood, heartwood and pith) is conducting the ascending sap? 2) Is sap descending in the cortex towards the root and into it? And if so, which is the pathway from the interior parts into the cortex?

Heinrich Cotta, who won the competition, gave the correct answer (sapwood) to the first question and, while not denying the descent of sap in the “cortex” (i.e., the phloem), emphasized the fact that this descending sap contains solutes in high concentration and is therefore different from the sap in the sapwood, so that plant saps do not truly circulate.

Although the transporting tissue became thus finally identified in the 18th and early 19th centuries, the pathway problem lingered on at the microscopic level well into the second half of the 19th century. There were lively disputes on whether the lumen of a conducting xylem element (a tracheid or a trachea) is filled with water, with air or with a sequence of air bubbles interspersed with water (a so-called “Jamin chain”). According to their opinion on this problem, various authors suggested different routes for water ascent. Water was thus assumed to move in the lignified cell walls of air-filled conduits by Unger, Sachs and Pfeffer, or to be transported in the lumen by Boehm, Strasburger and Schwendener, among others. De Candolle and and some followers even credited intercellular spaces with a role in transport.

The anatomical arguments gradually became inseparable from the task of identifying a suitable driving force for water movement. In a way, the idea that living cells should play a major role in lifting and moving the water seemed natural enough; the “vitalists” were however neither able to identify living cells prominently involved in water transport nor to suggest plausible mechanisms for their action. Nevertheless they kept fighting against the “physicists” and their cohesion-tension theory (CTT) well into the 20th century. Great names in plant physiology among the vitalists, such as S. Schwendener and W. Pfeffer, were later followed by A. Ursprung and others as champions in the fight for an essential role of the protoplasm in water ascent. Indeed, even J. Joly and H. H. Dixon, two of the earliest protagonists of the CTT, preserved some “vitalist” convictions for a long time.

A Decisive Step: 1889–1924

The crucial period for our current views on the mechanism of water transport in plants were the years between 1889 and 1896. As a cornerstone we have a monumental book, Eduard Strasburger’s Über den Bau und die Verrichtungen der Leitungsbahnen in den Pflanzen (On construction and function of the conduits in plants) written in 1891. Strasburger, who is mostly remembered for his outstanding contributions to plant cytology, gave an encyclopedic compilation of old and recent work done on pathways and mechanisms of water transport in the plant body. As Sir Francis Darwin stated in 1896: “It is difficult to praise too highly this great effort of Strasburger’s.”

Strasburger himself was an adherent of the school of physics and provided some strikingly efficient demonstrations of water being lifted to considerable heights without any involvement of living cells (Figure 1). He showed that woody stems with their lower end immersed in concentrated solutions of copper sulfate or picric acid and severed by a cut made below the surface of the liquid, will readily suck the solution up. Immediately upon contact, the poisonous fluid kills all living cells in its way, but the copper or the acid arrive in the transpiring leaves and kill them as well. The uptake of the solution and the loss of water from the dead leaves may continue for several weeks, and new solutions of a different color may be lifted in a dead stem.

Figure 1   Strasburger’s great work (ca. 1890).

Joseph Boehm provided an equally impressive demonstration in 1892. He showed that water could be lifted to considerable heights even by dead twigs (killed in boiling water). Such twigs keep transpiring, and, if connected via a water-filled capillary to a reservoir of mercury, they can raise this fluid to over 760 mm. This would equal the weight of a water column more than 10 m high. Boehm repeatedly stated “capillarity” (another term for surface tension) was involved in lifting the water column, but he never identified the site of action of this force. One can deduce from his writings that he probably located the necessary menisci directly in the xylem walls.

It was thus well established by experiments that the force lifting water had to be a purely physical one, and this was what Strasburger emphasized in his book. However, he was reluctant to speculate on the exact nature of forces or mechanisms, thinking that the time was not ripe for such a bold move forward. Strasburger ruled out a number of physical forces that were credited with a role in water transport, such as fluctuations in barometric pressure acting on the air in the Jamin chains. This is the moment when Boehm came forth with a significant statement; in 1893, in his last paper published in the year of his death, he directed his readers to the idea that cohesion in the water column must play a decisive role for the whole question. He wrote:

“The cause of the seemingly paradoxical fact that mercury in the air-free manometer is drawn up above the height in the dry barometer is simple enough, and it has been known, as I have only recently become aware of, already for some time (Helmholtz 1873, p. 492). If the mercury is to fall, the cohesion of water must be overcome. By the amount of the force necessary for this, the weight of the mercury column, which so to say is suspended from the twig and the glass- and rubber- walls, is reduced.”

Unlike gases, solids and liquids can be subjected to high tensions until they fail. This is understandable for solids, such as a bar of steel, but less so for liquids. Failure by cavitation (emergence of a vapor phase) is unique to liquids. If no cavitation occurs, liquids should be able to withstand very high tensions. Such tensions have been measured as early as 1850 by Berthelot and later by Jäger in 1892. The resulting values were extremely variable (tens to thousands of bars) and depended on the experimental conditions and the nature of the liquid (polar liquids such as water or nonpolar ones, e.g., helium). It was therefore hazardous to use these values for xylem sap. Many authors reported the presence of bubbles in the xylem sap, but a clear account of their effects on the tensile strength of sap was missing. The state of affairs and the impossibility to change it by experiments provided convincing evidence that CTT would last a very long time, even after the remarkable step in this direction made by Dixon.

The next important event was a scientific journey by two newcomers to the field of water transport, Messrs. J. Joly and H. H. Dixon from Trinity College, Dublin. The first was a professor of Geology and the second a professor of Botany. In the summer of 1893 they visited Eduard Strasburger in Bonn where he showed them some of his experiments and discussed the most recent literature on the ascent of sap in plants. Among them was Boehm’s paper from the same year (which they cited later). Joly and Dixon said, “and since then we have occupied ourselves with some considerations as to the cause of the ascent of liquid in trees. It was not, however, till late spring (1894) that we had leisure to enter definitely on the research.” The first published notice of their ideas and experiments was an abstract in the Proceedings of the Royal Society of London in November 1894. The full account was given in the Philosophical Transactions of the Royal Society of London (B.), Vol. 186, 1895.

Obviously the sight of only the abstract prompted Eugen Askenasy (Professor of Botany in Heidelberg) to reveal his ideas which he had nurtured for a long time. Askenasy had not yet published anything on the water relations of plants till then as his main interest being the taxonomy of marine algae. However, in December 1894 and February 1895 he published in the Verhandlungen des Naturhistorisch-Medicinischen Vereins zu Heidelberg, Neue Folge 5, a paper showing a remarkable grasp of the whole topic and theoretical ideas very similar to those in Dixon and Joly’s full paper. What were these new ideas? The most important common feature to both papers was the identification of the cell walls of parenchyma cells, whether living or dead, as the sites where surface tensions develop due to the transpiration of water. Both papers emphasized that a moist cell wall is impermeable to air, so that even at negative pressures air cannot be sucked into conducting elements. A somewhat “vitalist” idea in Askenasy’s paper was the (rather complicated and unnecessary) assumption that the increased surface tension created by transpiration should be first used for removing water from the protoplast, and only the “osmotic force” created should exert a pulling action on the water threads in the conducting elements held together by cohesion. This idea was taken up a short time later in a paper by Dixon.

Dixon and Joly further demonstrated the stability of water under tension, even if the water is saturated with air. In addition, they could show that water is lifted even against a gradient in the air pressure (Figure 2). When the water reservoir for a transpiring detached twig was at normal air pressure, while the leaves were enclosed at 3 bars overpressure in a pressure vessel made of glass, the leaves transpired small amounts of water taken up from the reservoir.

Figure 2   With this experiment, Dixon convincingly showed that a leafy branch subjected to a pressure of 3 atmospheres was nevertheless able to draw up water from an external vessel (beneath the pressure chamber) at atmospheric pressure.

There were one or two other papers by the protagonists in Dublin and Heidelberg, and a nice account of the debate (reached at the end of 1896) can be found in the “Report of a discussion on the ascent of water in trees” given at the Liverpool Meeting of the British Association in September of that year (Annals of Botany 10, 1896). By then, quarrels about questions of priority had arisen between Dublin and Heidelberg, provoking the usual nervous references to typewritten manuscripts and their dates of submission, revision, and acceptance. One priority not discussed much was Joseph Boehm’s first statement of the role of cohesion. If mentioned at all, his work was deemed “unclear” or even “confused.” We doubt that this is a correct statement on the paragraph cited above verbatim, because in September of 1896 Boehm had been dead for nearly three years—making it impossible for him to be heard in the heated discussions.

The next truly innovative steps in the history of the cohesion-tension theory came only about 15 years later, when Otto Renner (1911) succeeded in direct measurements of the tensions in conducting elements and H. H. Dixon (1914) wrote his book Transpiration and the Ascent of Sap in Plants. This text became the final acceptation of the cohesion-tension theory. Apparently, Dixon did not continue to work very much on this topic. In 1924, he published a booklet on a closely related subject, The Transpiration Stream, based on three written lectures he had given at the University of London during the same year. He resigned his chair in 1949 and died in Dublin in 1953.

From Dixon To the Present

Curiously, research on the physics of sap ascent stopped more or less completely around the fifties. A determining factor was the lack of suitable methods to prove or disprove convincingly the statements of the CTT on the physical status of the xylem sap. Remember, at the time, neither the concept of water potential nor the experimental methods to measure the physical state of the xylem sap (micropsychrometer and pressure chamber techniques) existed (both concepts were introduced in the early sixties).

Another factor had a very important impact on the direction of future research: Van den Honert’s article “Water transport in plants as a catenary process,” published in 1948. This paper did not discuss the validity of the CTT (it just said that “the cohesion theory will be taken for granted”) but stressed a very simple yet powerful argument: since in well watered plants transpiration and absorption are almost equal, an Ohm’s law analogy can be used to determine the quantitative aspects of water flow from soil to leaves and atmosphere. Here the topic was not the physics of sap ascent; it was to determine which of the different resistances water passes on its way from the soil to the atmosphere is quantitatively most important. Van den Honert’s concluded, “the master-process is always, under any circumstances, the transport in the gaseous part” (i.e., through the stomatal and boundary resistances). During the next thirty years, most studies on water transport dealt with the problem of evaluating gaseous and liquid resistances and their variations with climate and soil conditions. The resurrection of studies concerning the CTT started with the first paper (1966) of a series by John Milburn on the acoustic detection of cavitation in plants. After Milburn, Melvin Tyree, Martin Zimmermann, and their students were the pioneers who completely renewed and further developed the experimental approaches to the CTT. The present state and the most recent fates of this theory may be found in Web Essay 4.3.