Transpiration: how many functions?
Article first published online: 6 AUG 2008
© The Author (2008). Journal compilation © New Phytologist (2008)
Volume 179, Issue 4, pages 905–907, September 2008
How to Cite
Raven, J. A. (2008), Transpiration: how many functions?. New Phytologist, 179: 905–907. doi: 10.1111/j.1469-8137.2008.02595.x
- Issue published online: 6 AUG 2008
- Article first published online: 6 AUG 2008
- mass flow;
- nutrient supply;
- water-use efficiency
Water vapour loss is often regarded as a necessary evil for organisms exchanging O2 and CO2 with the atmosphere. As the gases are metabolized in solution inside cells, there has to be a wet cell-surface across which the gases exchange, and water vapour is lost to the almost invariably unsaturated atmosphere. In plants the latent heat of evaporation of water comes in part from the light energy unavoidably dissipated in photosynthesis. As an unavoidable process, there have been suggestions of additional functions of transpiration, especially in view of the very large range of transpiratory water losses per unit growth among C3 vascular plants and the occurrence of transpiration in the dark in C3 and C4 plants that do not have net CO2 fixation. In this issue of New Phytologist, Cramer et al. (pp. 000–000) have built on knowledge that transpiratory mass flow of water through soil is important in moving some nutrients to the root surface and present results consistent with the stimulation of nutrient supply to plant roots by mass flow through the soil as a component of the regulation of the rate of transpiration.
‘... can it be concluded that the increased water loss is a result of natural selection in evolution increasing mass flow of nutrients to the root surface?’
The simplistic view of how embryophytes living on land deal with the unavoidable loss of water vapour in photosynthesis and the frequently irregular supply of water in precipitation divides them into two categories: poikilohydric (i.e. with little or no capacity to limit transpiratory water loss) and homoiohydric (i.e. with significant capacity to limit transpiratory water loss). Unless the poikilohydric organisms live in permanently wet habitats they are subject to periodic drying out, and persistence in drier habitats requires desiccation tolerance. Homoiohydric organisms are generally not desiccation tolerant except in reproductive and dispersal stages, such as dispersed spores (including pollen grains) and seeds and fruits. Homoiohydric plants comprise most terrestrial vegetation today: Continence Conquers Continents. This neat pigeonholing of plants on land into the categories poikilohydric or homoiohydric, or into the partly similar categories desiccation-tolerant or desiccation-intolerant, has been criticized by Proctor & Tuba (2002), who rightly point out that strict poikilohydry and strict homoiohydry are the extremes of a continuum, as are complete tolerance or total intolerance of desiccation.
Nevertheless, it is convenient to consider sporophytes of terrestrial vascular plants as predominantly homoiohydric and desiccation intolerant, obtaining photosynthetically active radiation (PAR) and essentially all of their carbon as CO2 from the atmosphere, and water and the great majority of nutrient elements (other than carbon) from the soil. The energy balance of terrestrial plant canopies is described by the Penman–Monteith equation, with energy storage in net primary productivity accounting for a minor component of the absorbed short-wavelength radiation (mainly PAR), and the rest contributing the latent heat of evaporation in transpiration and the loss of sensible heat (Jones, 1992).
Stomata are major determinants of the fate of absorbed short-wave radiation as energy storage in net photosynthesis and energy dissipation by transpiration (although these two fates are not in direct proportion as a function of stomatal aperture), on the one hand, and increased canopy temperature and energy dissipation other than through transpiration, on the other hand. The stomata respond to the atmospheric and internal leaf environment, the latter crucially including chemical signals that have been generated by below-ground parts of the plant in response to the soil environment and permitting the pre-emptive function of stomata in restricting gas exchange before the plant becomes significantly desiccated (Hetherington & Woodward, 2003). The Cowan–Farquhar (Cowan, 1977; Cowan & Farquhar, 1977) approach to modelling stomatal behaviour, in terms of optimizing carbon gain per unit water lost in transpiration, has been very successful.
However, Cramer et al. point out that the optimization modelling is based on stomatal behaviour during periods on net CO2 assimilation, so does not take into account nocturnal transpiration in C3 and C4 plants (Caird et al., 2007). The same applies to the use of δ13C as a surrogate for stomatal conductance relative to the biochemical capacity for photosynthesis. There is also (Cramer et al.) evidence that transpiratory mass flow of water through soils is important in moving some nutrients to the root surface (Barber & Cushman, 1981). Cramer et al. (2008) point out that the water transpired per unit dry matter accumulated by plants increases when growth is limited by nutrient supply (Raven et al., 2004), which is consistent with a role for increased water flow through soil compensating in part for decreased availability of nutrients in the soil. The fact that such transpiratory responses also occur in hydroponic cultures where, under well-stirred conditions, there would be no increase in nutrient flux to the root surface, does not rule out a role of increasing nutrient fluxes through the soil (Cramer et al.) if the signal for increased water flux is related to nutrient availability at the root surface. In this connection, Cramer et al. point out that nitrate delivered to the leaf in the xylem is among the determinants of stomatal behaviour (Wilkinson et al., 2007). Finally, Cramer et al. comment on the very wide variation in the measured transpiratory water loss per unit dry matter accumulation among C3 plants (Wright et al., 2004).
These possibilities led Cramer et al. to carry out experiments designed to examine the effects of varying the dependence of nutrient delivery to the root surface by mass flow through the soil on the ratio of transpiration to photosynthetic carbon assimilation. They used the South African winter rainfall grass Enhartia calycina J.E. Sim from nine sites along a rainfall gradient growing in sand. One treatment was ‘interception’ because the roots and the fertilizer pellets were in the same volume of sand, and nutrients could reach the root surface by interception (root growth) as well as by diffusion and mass flow. The other treatment was ‘mass flow’, in which the fertilizer pellets were supplied in sand in a compartment at the centre of the growth vessel that was separated from the sand containing the roots by a mesh-screened polyvinyl chloride (PVC) pipe that roots could not penetrate but which allowed diffusion and, especially, mass flow of nutrients to the roots.
The ‘mass flow’ plants had statistically significantly lower (mean of 35%) relative growth rates than the ‘interception’ plants. The ‘mass flow’ plants also had statistically significantly higher stomatal conductance, transpiration rate and intercellular space CO2 concentration than the ‘interception’ plants, and also a statistically significantly higher net photosynthetic rate, although the difference between the ‘mass flow’ and the ‘interception’ plants was not as great as for the other three parameters. The higher stomatal conductance and intercellular CO2 concentration resulted, as expected, in a more negative δ13C value of leaves of ‘mass flow’ than of ‘interception’ plants. There was no difference between treatments in the fraction of the plants contributed by roots.
Cramer et al. suggested that the higher leaf area-based rate of net photosynthesis, despite the lower relative growth rate, of the ‘mass flow’ plants than of the ‘interception’ plants could be attributed to a greater respiratory carbon loss by the roots of the ‘mass flow’ plants as a result of the (assumed) lower concentration of nutrients at the root surface, and hence a greater energy cost per unit nutrient taken up by the roots. However, in the absence of measurements of the leaf area per plant dry matter (leaf area ratio or LAR) it is not possible to be certain that the higher photosynthetic rate of ‘mass flow’ plants on a leaf area basis means a greater rate of carbon fixation in net photosynthesis per unit plant dry matter than would be needed to support the measured lower relative growth, assuming the same fractional respiratory loss for the two treatments. However, this possibility would require a so much lower LAR in the ‘mass flow’ than in the ‘interception’ plants that it would have been noticed when examining the plants. The same point applies to the measured transpiration rate on leaf area basis in relation to the rate of water loss from the whole plant; there is no estimate of water loss per unit dry matter, or per unit dry matter gain, by the plants in the two treatments.
The content of nitrogen (N) and potassium (K) on a leaf dry matter basis was not significantly different between ‘interception’ and ‘mass flow’ plants. The leaf dry matter of ‘mass flow’ plants had significantly more sodium (Na), calcium (Ca), zinc (Zn), manganese (Mn), phosphorus (P) and copper (Cu), and significantly less iron (Fe) and magnesium (Mg), than did the leaf dry matter of ‘interception’ plants. The finding that the leaf content on a dry matter basis of eight of the ten elements examined was either the same (two) or higher (six) in the ‘mass flow’ plants than for the ‘interception’ plants is taken by Cramer et al. to indicate that increased mass flow of most nutrient elements compensates, or more than compensates, for the absence of the interception component of nutrient acquisition in the ‘mass flow’ plants. This conclusion is reasonable, although there are implicit assumptions about the relevance of the transpiration rate measured in the LICOR gas-exchange apparatus on a leaf area basis to the water loss by the growing plant, and that leaf dry matter (for the elemental analysis) has the same relation to leaf area (for the gas exchange) in the ‘interception’ plants as in the ‘mass flow’ plants.
Accepting that there is indeed increased water loss per unit dry matter gain in the nutrient-limited ‘mass flow’ plants, can it be concluded that the increased water loss is a result of natural selection in evolution increasing the mass flow of nutrients to the root surface? While this is a possibility, it is also possible that it is an emergent property of the operation of mechanisms that have evolved in relation to other functions. This is, of course, a comment which could be made about many traits that are suggested to have significance in natural selection, so it is helpful to bring in data from plants whose growth is limited by a factor other than nutrient uptake from soil. Such a factor is PAR; using δ13C as a surrogate for water loss per unit dry matter gain (see Raven & Farquhar, 1990), there is a greater potential for water loss per unit dry matter gain during slower growth at low PAR than during faster growth at higher PAR in the C3 aroid Dieffenbachia longispatha Engler and Krause (Skillman et al., 2005), although the phenotypic effect of PAR for growth on water-use efficiency in nature is complex (Bacon, 2004). Here it is difficult to see a role for increased mass flow through soil per unit plant growth when there would be expected to be relatively no less nutrient acquisition by interception or diffusion for the small, low-PAR plants than for the larger, high-PAR plants. There are also data showing a lower water-use efficiency and growth rate of C3 plants grown at the lower CO2 levels found at the last glacial maximum than of similar plants grown in present-day CO2 (Polley et al., 1993); work on a red alga (which, of course, lacks stomata) that relies on diffusive CO2 entry for photosynthesis (Kübler et al., 1999) confirms that the increased diffusive conductance relative to photosynthetic capacity in vascular plants grown at low CO2 is a stomatal response. These two examples show that decreased growth rate as a result of lower PAR or lower CO2, like nutrient limitation, increase transpiration per unit dry matter gain.
The work reported by Cramer et al. (2008) is certainly interesting, and should be followed up by, for example, considering soil rather than sand where elements such as P and Fe are expected to be less mobile, and also by investigating mycorrhizal plants.
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