by Ivan SUDNITSYN, Dr. Sc. (Biol.), leading research fellow of the Soil Science Department, Lomonosov Moscow State University; Yevgeny SHEIN, Dr. Sc. (Biol.), Head of the Chair of Soil Physics and Reclamation, Soil Science Department, Lomonosov Moscow State University

As living organisms came out of the ocean to the land surface 500 mln years ago, their major concern was to get water and retain it in their own body since water made up more than half of it. Terrestrial plants succeeded best of all because they learned to absorb moisture from soil and cut the rate of its evaporation. The mechanisms thus developed have been the subject-matter of plant anatomy and physiology for several centuries. However, specialists failed to reveal certain important details till in the early 1970s our scientists laid the foundation of a new science, the ecological hydrophysics of soils.

Passing by train or car the deserts of Central Asia (Kara Kum, Kyzyl Kum, Repetek) stretching over thousands of kilometers, you will see that bushes and even trees grow everywhere in a real scorcher. The famous saxauls also grow there. These "drought-resistant champions" manage to pierce more than a tenmeter soil column by their roots and reach the waterbearing layer. But the desired liquid turns out to be as much mineralized as seawater (or even more salty)--to drink it just try! Like it is in the sea, H₂O molecules are

tightly bound by ions and molecules of dissolved substances and are inaccessible to organisms devoid of special devices for their absorption. It is not accidental that shipwreck victims die of thirst most often. But desert plants, the xerophytes, make do even with soil brines! There is another way of survival when cactuses--having no long roots-extract from almost dry soil tiny droplets of moisture (retained with great force there!) and keep them from evaporation in overly dry hot air for a long time. These are succulent plants.

But how do living organisms cope? The most sophisticated and elaborate anatomic and physiological mechanisms developed by them for hundreds of millions of years are the subject-matter of plant anatomy and physiology. This science has discovered a good deal of interesting things in several centuries it has been in existence. The British scientists Alden Craft, Herbert Currie and Clifford-Ralph Stocking, who published in 1949 the monograph "Water in Plant Physiology" (translated into Russian by Dmitry Sabinin, Professor of Moscow State University, who came to a tragic end in 1951 with the crackdown on national genetics*), established that plant cells possessed "a suction power" enabling them to imbibe water from solutions of different substances via the finest (semipermeable) pores of root cell membranes. This suction power results from the action of osmotic pressure** of cytoplasm (P_os) and the suction capacity of the finest capillaries permeating cell walls (P_c); it has a pressure dimension and is called therefore a "moisture pressure in plants" (P_p).

ORIGIN OF A NEW SCIENCE

Physiologists studied water absorption by plants usually from comparatively large volumes of salt solutions in their laboratory vessels. Determining P_os in these

* See: S. Popov, "Life Devoted to Science", Science in Russia, No. 6, 2010.--Ed.

** Osmotic pressure, excessive hydrostatic pressure on a solution separated from a pure solvent by a semipermeable membrane, which tends to equalize their concentrations owing to the molecular cross diffusion of dissolved substance and solvent.--Ed.

conditions presents no problem. But with soil the situation is different: the osmotic pressure of moisture present there in the form of microscopic droplets depends heavily on its concentration, and the surface of soil particles, too, attracts this "elixir of life". Therefore, plant physiologists and soil scientists failed to measure the total pressure of water (let us denote it as P_s) for a long time, and that blocked further scientific inquiry.

In the middle of the last century members of the Institute of Forestry of the USSR Academy of Sciences, plant physiologist Judith Tselniker and one of the authors of this paper, soil scientist Ivan Sudnitsyn, developed a simultaneous measurement procedure for the above-mentioned values P_p and P_s in plants and in soils where they grew. In 1958, in the national journal Soil Science Sudnitsyn published new important results. One found a relationship among the moisture pressure in oak tissue, the total water pressure in soil and water absorption by plants directly in the natural environment, namely, in the oak forest laid out in the early 20th century on a stretch of the southern black earth zone to the design of the great Russian scientist and originator of the genetic soil science Vasily Dokuchaev. Thereupon a new science, the ecological hydrophysics of soils, was born. It looked into the regularities of moisture movement in the soil-plant-atmosphere system.

In 1970-1975 this challenging problem was handled by postgraduates of the Chair of Soil Physics and Reclamation in the Soil Science Department of Moscow State University Nikolai Muromtsev (today Dr. Sc. (Biol.), Head of the Soil Hydrology Laboratory, Dokuchaev Soil Science Institute), Chiang Kong-Tau (today Dr. Sc. (Biol.), Deputy Head of the Department of Ecology, Hanoi University, Vietnam), one of the authors of this paper Yevgeny Shein and many other young researchers. As a result, in 1979 Sudnitsyn generalized the new data in his monograph "Movement of Soil Moisture and Water Consumption by Plants" (Moscow University Publishers, Moscow, 1979). Similar studies were carried out abroad: in 1970 the in-depth work dealing with the plant water conditions (Ralph Slacher) was published.

It is on record that plant cell protoplasm contains on the average as much as 85 percent of water, but if this value drops below 33 percent, proteins lose their vital activity. Specialists looked into how the physiological and biochemical processes in plants change with moisture variation. These data are summed up in the monographs of the famous botanist and member of the USSR

Academy of Sciences Nikolai Maksimov (1952), and the outstanding plant physiologist Alexei Alexeev, Dr. Sc. (Biol.) (1948), and also in the works of other researchers. They proved that cutting water supply results in a substantial impairment of photosynthesis and, as a consequence, in a decrease in plant biomass buildup and productivity.

The point is that the amount of moisture in cells of land plants depends on the relationship between the rate of its suction from soil, its inside movement and its evaporation to the atmosphere due to gas exchange essential for photosynthesis. But since photosynthesis is a precondition for plant existence, plants have to absorb water. This fact as well as the lower rate of water evaporation (transpiration) is part and parcel of the vital strategy of these wonderful organisms. Success can be ensured by a deep and multiple root system and by xerophytic properties, i.e. the small evaporating surface of leaves, their thick outer coating (downy and waxcoated), their widely spaced and small stomas (whose lumen can be decreased with the reduction of tissue moisture), and other factors. Some groups of plants (ephemers) are notable for an extremely short period of active growth timed for the high content of moisture in soil.

Since transpiration (Tr) is the prime cause of dehydration of plants, this phenomenon was studied most carefully. The theoretical works of Anatoly Budagovsky, Dr. Sc. (Geogr.), of the Institute of Geography of the USSR Academy of Sciences (1964) and the experiments of meteorologist Anatoly Alpatyev (1954) have shown that given a sufficient amount of moisture in soil and if the vegetation cover is close and homogeneous (in height and other parameters) in a rather large territory, the actual Tr is equal to the potential one (Tr_o). In other words, transpiration under these conditions is maximal, and its value is determined mainly by the intensity of heat energy inflow to the evaporating surface. However, the peculiarities of plants as living self-regulating objects are manifest but weakly in an optimal situation like that.

Naturally, in the conditions of an open vegetation cover and especially if it is not leveled in height (separate groups of trees in a field), the specifics of its geometry affects heavily the rate of Tr (per unit of soil surface). However, in a drought period, when the availability of moisture drops so that the rate of its absorption by plants decreases, their physiology and soil properties come into play.

PRESSURE DIFFERENTIALS IN PLANTS

Up to the mid-20th century specialists used the following four levels of soil moisture to describe the water supply of land plants: optimal (field water capacity); one corresponding to growth retardation of plants (on interruption of the contact between the root layer and the water-bearing bed by means of minute vessels); one conditioning a stable wilting; and a situation when moisture is not available. Meanwhile, transition from one of above levels to another is rather smooth, and we have seen at the present stage of research that a continuous functional relationship exists between soil moisture and the condition of plants. The phenomena taking place in a situation of mutual changes are complex but can be understood and described if the thermodynamic approach is used.

Now, let us consider our objects to be a totality of elementary thermodynamic systems*. A living cell can

* Thermodynamic system, a physical system consisting of a large number of particles and capable of energy and substance exchange with the environment.--Ed.

serve as such "elementary unit"; if it is assumed that a thermodynamic equilibrium* or a state close to it is attained between its separate parts. In that case the external (mechanical) pressure (P_m) on a cell is formed by several components: pressure of the surrounding cells and its own walls on the protoplasm (turgor); weight of a plant, to which our "elementary unit" belongs; pressing of wind and precipitations on the upper part of the plant and that of soil on a plant roots, etc. Osmotic pressure (P_os) is conditioned by substances present in the cell in the form of solutions and hydrated (containing molecules of H₂O) colloids. Capillary pressure (P_c) manifests itself in pores of its membranes, if the gaseous phase is present in the intercellular space and, consequently, an air-water interface occurs. (Note that the gravitational field is conditioned by the constant gradient P_c in the vertical direction, downward and sometimes it is compensated by the opposite total vector of

* Thermodynamic equilibrium, the state of a system when its macroscopic values (temperature, pressure, volume, entropy) remain constant.--Ed.

other kinds of pressure, which is a rather rare case of equilibrium.)

A sum of the abovementioned forces is called "a total pressure of moisture" (P). Besides, all the above components are manifest also in soil.

Let us now turn from the theory to actual figures. In ecological hydrophysics it is common practice to consider P_c on the groundwater surface to be equal to zero. Accordingly, in partially moisture-saturated plants and soils the equilibrium capillary pressure has a negative value. The above-said field (minimum) water capacity is often associated with P_c = -0.33 atm, the moisture of stable wilting with P_c = -15 atm and the maximum hygroscopic moisture corresponds to P_c = -30 atm.

As noted above, equilibrium is a rare case for the soil-plant-atmosphere system, as the ambient air is saturated but partially with moisture. For example, if its relative moisture is equal to 90 percent, P = -140 atm, but in a dry summer period the pressure drops to -1,000 atm and lower. In a normally wet plant the pressure reaches only several atmospheres below zero, and since, due to the laws of nonequilibrium thermodynamics, water can move only in the direction of pressure relief, it begins to evaporate if the stomas of leaves are open. First, transpiration of moisture takes place from cell walls of the mesophile* exterior layer of leaves having the capillary structure. As a consequence, water menisci are drawn inside capillaries, their curvature increases, and P_c decreases respectively.

Evaporation proceeds also from high-polymer organic substances of the capillary walls, which involves a drop of P_os. Under the action of this pressure differential the moisture flows to cell walls from the cell protoplasm, where both P_os and P_c decrease eventually. In turn, the change of P_os and P_c causes the water to rise from the deeper layers of the mesophile to its outer layers. The pressure drop goes gradually to deeper levels, down to the vessels supplying water to the leaf; but if in remote cells P = -15 atm, in close proximity it is yet higher (P = -5--10 atm).

ACTIVE AND PASSIVE ABSORPTION OF "LIFE ELIXIR"

The next stage of the moisture route inside plants is represented by xylem vessels** connecting the system of roots and leaves. It has been known that water in this water-conducting tissue forms continuous fibers transferring hydrostatic tension (P_c). Their ability to avoid breakup even at

* Mesophile (leaf pulp), the tissue of a green plant, in which essential synthetic processes take place.--Ed.

** Xylem, the main water-conducting tissue of vascular plants.--Ed.

high gradients of the capillary pressure is determined by mutual attraction forces of H₂O molecules exceeding 10,000 atm, unless impeded by dissolved gases (because bubbles of volatile substances break up the solid water body). But plant vessels have few, if any, of them; therefore even drop of P_c to -100 atm is not fatal, as thin "ducts" remain filled with moisture also during drought, and capillary pressure gradients in them can reach 20 atm/m.

Let us look into the world hidden inside plant roots. Here xylem vessels make contact with central vascular cylinder tissues (assemblage of conducting elements in a plant), and they, in their turn, adjoin the endoderm (internal one-row layer of tight cells of the primary cortex) and absorbing cells. A P_c drop in vessels is transferred via water-saturated cell membranes and protoplasm to the outer layer of the cortex. Then pressure in plant root cells becomes less than in soil, and they begin to suck in moisture.

Besides, the conducting system of roots can be connected with their outer surface also via capillaries within the intercellular space (they are wide enough). If soil moisture is high, water can come also by such route and at a much higher rate than through protoplasmatic membranes having low water permeability.

In a severe soil drought some groups of root meristem* cells are isolated through suberification of their walls and thus retain moisture sufficient for their vital capacity. As soon as the tight situation is over, they grow again and form new roots.

We have traced the passive absorption of moisture by plants. As a matter of fact, it is "a transpiration pump" set to work as moisture evaporates from leaves. But our green neighbors on the planet have mastered "active" mecha-

* Meristem, a generalized name for plant tissues. They consist of actively dividing cells, retaining their physiological activity all through their life and providing a continuous buildup of plant mass.--Ed.

nisms as well. People got ised to the fact that "tears" (actually xylem exudate or liquid containing organic and amino acids) seemingly come up on leaves of some plants and from their cut-off stems. Specialists designate the process of water ejection onto the surface under the action of the root pressure as guttation (from the Latin gutta, or drop), the effect described by physiologist Dmitry Sabinin in 1949. But this process cannot be explained only by the superiority of P_os of soil solution over P_os of xylem exudate. Plant exudate is also due to some peculiarities of liquid in the vacuoles of plant cells (cellular fluid) and the rate of cytoplasm hydratability. Besides, water can be also put in motion by an electrical potential difference occurring along the way of its movement. But this calls for a substantial expenditure of energy, with respiration being its source in living organisms. There is a direct connection between its intensity and the rate of moisture absorption, as noted in 1948 by Dr. Alexeev.

Remarkably, by decreasing the pressure in leaves, plants can regulate transpiration within certain limits so as not to wither away. But at some critical level of pressure (P_cr) in roots the leaf stomas close automatically, moisture evaporation from them slows down dramatically, and a green organism saves itself from dehydration and death of photosynthetic cells. However, at that time the flow of carbon dioxide to the leaf stops as well, and, consequently, photosynthesis also comes to a stop. For a time plants can live without this vital process (by subsisting on the organic matter pool); yet an overly long pause will be fatal.

HOW TO OVERCOME DROUGHT?

Soil dehydration is a major cause of reduction of water inflow to leaves (and hence also transpiration). It must be understood that its granulometric composition (ratio of the quantity of sand, silt and mud particles) affects the coefficient of hydraulic conductivity and the life of plants. Moisture inflow to roots in a loamy soil, will be higher than in a sandy-loam soil, with all other conditions being equal.

Of no less importance are also the natural properties of plants, both genotypical and those revealed in a particular vital cycle (phenotypical). For example, drought-

resistant plants (xerophytes) are notable for the lowest values of P_cr (on the average below - 15 atm), while water-resistant plants (hygrophytes)--for the highest values (on the average above -5 atm); mesophytes* hold an intermediate position. Concentration of roots, also affects heavily P_cr: in plants with a more branched system of roots, the interval of soil optimal moisture is wider, with other things being equal.

The ability of plants to absorb soil moisture depends also on their growth phases. For example, when during tillering sprouts shoot forth from underground stem nodes at the beginning of oats vegetation, P_cr = -7 atm, but at the time of the growth of the main stem ("shooting"), this parameter decreases to -15 atm, and, finally, as the spike is formed, the situation changes again, and P_cr =-5 atm.

In one and the same plant in the same growth phase the value P_cr may essentially vary depending on meteorological conditions associated with the growth of a green organism at previous stages. For example, even

* Mesophytes, land plants adapted to habitat with more or less sufficient but not excessive moistering of soil.--Ed.

such a mesophyte as oat can adapt to periodic soil droughts becoming more resistant to them, which helps it survive, whereas the unadapted species die. Of course, the plant biomass decreases in bad years: after one soil drought by 8 percent, two droughts by 26 percent and three droughts by 44 percent. The point is that despite the acquired resistance, in dry weather many physiological processes are suppressed, those responsible for photosynthesis intensity and accumulation of organic substance.

By the way, meteorological factors can be taken account of by means of a potential transpiration value, Tr_o: the higher the speed of the wind and the lower atmospheric moisture, the higher this parameter. As a result, plants will wither in arid winds even if there is much water in soil, when an atmospheric drought sets in.

Thus, to ensure a maximum crop it is inadmissible to decrease the moisture pressure in soil to the critical value. In special experiments specialists try to determine the P_cr value for each combination of plant-soil-meteorological conditions to sustain optimal conditions--or those close to them--during vegetation.

It should be noted that almost all kinds of agricultural plants (except for sugar cane and rice at the first stages of growth) are not able to cope with oxygen shortage in soil. Both living organisms inhabiting the soil and roots have to breathe; but if all pores are filled with water, they fail to quickly deliver oxygen from the atmosphere. But when the largest capillaries are filled with air, diffusion of the laif-giving gas is accelerated.

Today research in ecological hydrophysics of soils in Russia is done mainly at our department and in the Dokuchaev Soil Institute (Moscow). In recent years specialists of Moscow State University carried out a research program of soil moisture effects on microorganisms inhabiting the soil. Our findings have revealed that some species of actinomycetes (Actinomyces)*, namely streptomycetes (Streptomyces), inhabiting the desert soils are capable of growing and propagating even in extremely arid soils (at P_s below -900 atm). Such information helps better understand life strategy in a critical period as living organisms came out of the ocean to dry land. Possibly those were the drought-resistant species of streptomycetes, which pioneered in settling on heretofore dead territories of the Earth.

* Actinomycetes, bacteria capable of forming at some stages of their growth, a branching mycelium (fungaceous bacteria) living mainly in the soil.--Ed.