A plant science manifesto

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John Passioura

CSIRO, Division of Plant Industry, Canberra

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Figure 1 Structures and processes in plant biology span dimensions from micrometres to kilometres, and time intervals from microseconds to millennia. Genotype × environment interactions apply to all these levels and are implicit in our analysis of short-term function in particular genotypes, as well as in our understanding of long-term adaptive change and hence evolution of new genotypes. (Based on Osmond and Chow 1988)

Soil–plant–atmosphere

Plants are wet inside, and with rare exceptions will die if they do not remain so. But this is not to say that their outside surfaces are necessarily wet. On the contrary, they are usually dry to your touch. If a drop of water is placed on a leaf it will usually sit there, precariously, roughly in the form of a hemisphere, because the external leaf surface is hydrophobic. It is essential that the surface be hydrophobic and poorly permeable to water, for a free water surface can lose water at rates approaching 1 mm per hour on a hot day. An unprotected leaf would lose its entire water content within a few minutes at these rates of evaporation unless it had a prodigious ability to replace the lost water.

Plants originated in the sea and there faced little risk of drying out. They could not grow on land until they had evolved facilities both to control and to make good the evaporative losses from their leaves. Control is achieved partly by means of a cuticle, a poorly permeable layer that covers photosynthetic surfaces of plants, and partly by means of the stomata, variable pores in these surfaces, which largely prevent evaporation when shut and allow CO2 assimilation to proceed rapidly when open. Evaporative losses from leaves are made good by roots, which can extract water from the soil, sometimes, if necessary, from very great depths, and by the vascular system, which contains conduits that carry the water from roots to transpiring leaves.

This book, Plants in Action, has much to say about leaves and their stomata, roots and vascular system, but it is worthwhile trying to imagine what other paths evolution might have taken in enabling plants to grow on land. Development of roots and a vascular system seems unavoidable, at least in higher plants, whose internal milieu must be much more strongly buffered against environmental changes than that of, say, lichens, or resurrection plants, those oddities that can dehydrate completely without losing the integrity of their cells and which can respond to rewatering so rapidly that they can be photosynthesising again within hours. But what of stomata? Why have them at all? Do plants really need to transpire? This question has several aspects to it, some of which have vexed plant physiologists for a long time. One aspect is this: plants grow by assimilating CO2 from the air and fixing it in organic form with the help of sunlight, that is, they photosynthesise. Evolution has not (yet?) provided them with a membrane that is permeable to CO2 but impermeable to water vapour; there-fore the outer covering of the leaves, which must be largely impermeable to water vapour, must have valves to let CO2 in. Transpiration is an unavoidable accompaniment of the uptake of CO2. Unavoidable if plants are to photosynthesise rapidly and thus keep up with their neighbours during evolution. However, there is one species, Stylites andicola, that has taken an alternative route. This plant has no stomata. CO2 is taken up by its roots and is transported to leaves through continuous air passages in its roots and stems. This species grows in the Peruvian desert on an average annual rainfall of 30 mm with an interval between rains that often lasts for years. As might be expected, it grows very slowly, even when conditions are good (Keeley, Osmond and Raven 1984).

The point of this preamble is that active cells must be well hydrated and that evolution has produced various structures that enable higher plants to keep their cells wet enough to function — to divide, to grow, to photosynthesise, to transport, to respire, to excrete, to defend, to communicate — even though most of these cells are in the shoots of plants and so are not only remote from their supply of water, but are also exposed to a very drying environment.

Concepts in plant science: an example from physics

This book uses many different conceptual frameworks for discussing how plants work. The reason for using many frame-works derives from the way that our minds comprehend the complex world around us by dividing it into a hierarchy of conceptual layers, each one nested within the one above like Matruschka dolls (consider, for example: subatomic particles, atoms, molecules, grains, bricks, walls, buildings, cities). Each of these conceptual layers has its own terms, ideas and principles, and much of what we call ‘understanding’ involves translating the terms and ideas of one layer into those of the adjacent layers. We can pour some concrete into this rather abstract mould by taking as an example the relationship between the ideal gas laws and the kinetic theory of gases.

The pressure, P, volume, V, absolute temperature, T, and number of moles, n, of an enclosed ideal gas are related thus: PV = nRT, where R is the universal gas constant. This relationship is useful in that it helps explain many everyday phenomena such as the behaviour of a bicycle pump and the leavening of baked bread. Moreover, this law can itself be explained, and the simplest vehicle for doing so is the kinetic theory of gases: we imagine that the gas consists of myriad molecules (n × Avogadro’s Number), each of given mass but of negligible volume, moving randomly in an enclosed space, each with its own velocity which is changed only by perfectly elastic collisions with other molecules or with the enclosing wall.

The interesting thing about these two descriptions of a gas, one phenomenological and the other particulate, is that they appear, at first sight, to have little connection with each other. The ideas of volume and number are common to both descriptions, but not those of pressure, temperature and velocity. A molecule does not have a pressure or a temperature, and PV = nRT does not embrace velocity. The two descriptions are examples of different conceptual layers, and each has terms and ideas that are peculiar to it. Yet the two layers are connected and the apparently disparate terms are related. The connection comes by considering the average properties of a large number of molecules because P is proportional to T and both are in turn proportional to the mean square velocity of the molecules.

This example of a connection between conceptual layers comes from classical physics, but note that the phenomeno-logical discovery (gas laws) was made long before the par-ticulate explanation (kinetic theory) was available. Indeed, this sequence is universal in any scientific exploration of natural hierarchically organised systems and the subsystems that comprise them. In effect, we need to know collective behaviour (e.g. PV = nRT) before we can ask pertinent questions about the parts (e.g. how can we best summarise the behaviour of a legion of elastically colliding molecules). The reason that we first need to appreciate integral behaviour of the whole system is that the problem of summarising the behaviour of the parts is underspecified. We need to specify at least two constraints when considering the general kinetic behaviour of gas molecules before we can derive the gas laws, namely, (1) there is a fixed number of molecules, and (2) they are enclosed within a bounding wall. The kinetic theory applies as well to the earth’s atmosphere as it does to an enclosed gas, but then we need to consider different constraints. We replace the constraint of an enclosed space with that of an infinite space bounded internally by the earth’s surface, and subject to a gravitational field. History has shown that in practice we do not become aware of the extra information we need, that is, constraints on the behaviour of a subsystem (e.g. a molecule or a cell), until we have considered the behaviour of the system as a whole (e.g. a gas or a tissue). This is a crucial principle that highlights the importance of exploring plant behaviour at all levels of organisation. Only by articulating connections be-tween all the layers can we hope to have a comprehensive understanding of how plants work.

Functional analysis of plants

What then are the conceptual layers into which we divide plant science? To some extent these are arbitrary, but are commonly as follows: community, whole plant, organ, tissue, cell, organelle, membrane, molecule (polymer, monomer, gene) (some of which are shown in Figure 1). These layers are essentially structural, but implied in them are processes occurring at a range of time scales, from geological, for evolutionary processes such as those that led to the facilities that are essential for plants to grow on land, through hours for cell division, to microseconds for conversion of radiant energy to chemical energy within chloroplasts.

In discussing how plants work it is useful to invoke the concept of function. This concept most clearly distinguishes biology from physics and chemistry, although ‘function’ is held to be indecorous by many biologists, for they see it as imbuing evolution with a sense of purpose that they deny exists. Whether or not evolution has a purpose is a philosophical question that is beyond the concern of this book, but there is no great difficulty with the concept of function in normal biological usage. It is simply a way of recognising that unlike simple physico-chemical systems that can be adequately studied using a linear train of thought, biological systems, when viewed at a long enough time scale, are recursive, as illustrated by the loop in Figure 2. If the loop was not complete, the structures that comprise it would not exist. Clockwise flow around the loop represents analysis at progressively finer levels in the manner of physics and chemistry, but the loop is open for clockwise flow, and stops at ‘Gene (frequency)’. Anticlockwise flow represents a process-based explanation of integral functions, and in terms of biological events is essential for closing this loop by producing the next generation. Functional explanations are ideas about the influence of given structures or processes on the ability of a plant to transmit its genes into the next generation.

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Figure 2 A reductionist approach in plant science generates new knowledge at progressively finer levels of organisation. This sequence is shown here by progress in a clockwise direction from community via component parts to molecule and eventually gene. In principle, a knowledge of genotype × environment interactions at these various levels of organisation enables integration of process-based concepts. That sequence is shown here as progress in an anti-clockwise direction from gene to community, and thence to the next generation; for without this loop being closed none of the structures within it would exist. (Original diagram courtesy J.B. Passioura)

Debates often occur between proponents of process and integrative explanations, and are generally specious. To under-stand biological phenomena thoroughly, and apply basic principles to commonplace situations, we need to analyse in the reductionist sense (clockwise in Figure 2), as well as extrapolate from component processes in an integrative sense (anticlockwise in Figure 2).

Accordingly, Plants in Action has adopted genotype x environment interactions as a fundamental theme for processes and adaptation in higher plants which leads to integrative explanations: processes in the sense that physiologists attempt to define the genetically determined workings of plants that have fitted them to a given niche in nature; adaptation in the sense that ever-changing environmental conditions impose an unrelenting selection pressure for genotypes with traits better suited to new conditions. A thorough knowledge of such processes can then underpin explanations of adaptation in nature and performance in cultivation.

Further reading

Passioura, J.B. (1979). ‘Accountability, philosophy and plant physiology’, Search, 10, 347–350.

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