Mesophyll conductance: constraint on carbon acquisition by C3 plants

Carbon metabolism of photosynthesis is remarkably similar across most of the biosphere. The well-accepted Calvin-Benson cycle is the dominant biochemical with remarkable few organisms carrying out alternative carbon fixation biochemistry. On the other hand, many different mechanisms exist to enhance carbon dioxide acquisition, especially C4 metabolism and crassulacean acid metabolism (CAM) among land plants. However, most land plants rely on diffusion of carbon dioxide from their environment to ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco). There are two primary resistances to this diffusion, the stomatal pore and the path through the mesophyll, from the cell wall inside the leaf to the Rubisco molecule. Because the flux of carbon dioxide is inversely related to resistance, the inverse of resistance, the conductance to diffusion has been nearly universally used in place of resistance since the 1980s. The effects of mesophyll conductance (gm) on photosynthesis have been studied for many years but there have been two large increases in the number of papers published, one in the early 1990s and one about 2007 (see Fig. 1). Papers on mesophyll conductance as a function of year of publication. Thompson Reuters Web of Science was searched for papers with the topic ‘mesophyll conductance’ or ‘mesophyll resistance’. The resulting list was trimmed to remove papers not relevant to CO2 transfer resistance in plant leaves and the resulting number of papers per year is plotted. Stomatal conductance can regulate water loss, setting up a tradeoff between hunger and thirst. Unlike stomatal conductance, reducing gm does not conserve water and presumably should be minimized to maximize plant fitness. The effect of stomatal conductance on photosynthesis was estimated by calculating the concentration (or partial pressure) of carbon dioxide in the intercellular spaces of the leaf. The origins of this calculation and experimental evidence to support it were reviewed in 1982 (Farquhar & Sharkey 1982). However, it was shown that abscisic acid and other stresses can cause the leaf to behave as though it is made up of small patches, each operating differently and that it was not possible to average these patches. Fortunately, patchiness has proven to be limited in how much it invalidates the concept of intercellular CO2 concentration. Mesophyll conductance has been more difficult to assess. Again, early concepts were reviewed in 1982 (Farquhar & Sharkey 1982). The original Farquhar model of photosynthesis used an infinite mesophyll conductance because estimates of gm were lacking. The experimental material used to test the biochemical details of the Farquhar model (Phaseolus vulgaris) had a very high gm and this allowed great progress in understanding the biochemistry underlying photosynthetic responses to the environment even in the absence of estimates of gm. In 1982, Joe Berry visited the Australian National University where I was a postdoc with Graham Farquhar. We began studies, later joined by John Evans, to use stable isotopes to measure gm (Evans et al. 1986). Techniques to estimate gm using just gas exchange, or gas exchange plus chlorophyll fluorescence, were developed in the early 1990s. In my opinion, these are less precise than the stable isotope method but are much more readily available and they sparked the first of two major increases in the number of gm papers (Fig. 1). The second major increase in the yearly rate of publication of gm papers occurred in 2007 and corresponded to the availability of tunable diode lasers (TDL) for making online measurements of isotope fractionation and an international conference on gm held on Mallorca. Plant, Cell & Environment featured a picture of a tunable diode laser system on the front cover in 2007 (Barbour et al. 2007) and the Journal of Experimental Botany published a special issue resulting from the conference on Mallorca (Flexas et al. 2009). The hypothesis that CO2 transfer occurs through aquaporins (Flexas et al. 2006) has also stimulated significant interest in the process of CO2 diffusion through C3 leaves. There are a number of important people in the field, and publications continue (40 for 2012 as of August 9). Papers published in 2011 and 2012 have been collected into a Plant, Cell & Environment Virtual Issue available at http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-3040/homepage/virtual_special_issue_-_mesophyll_conductance.htm [Correction added on 14 November 2012, after the first online publication: the link to the VSI has been updated]. Important new insights into stable isotope effects, distribution of sinks and sources within the mesophyll, the temperature response and CO2 responses, are described. The insights into the inner workings of gas distribution in the C3 leaf have been impressive. However, I think it is important to keep in mind that each Rubisco molecule will have a unique position relative to sources of CO2 and there will be a limit to the scale over which a single number, the value of the leaf gm, will be a useful descriptor. The value we use for stomatal conductance and gm assumes that the leaf is homogeneous. I continue to find it surprising how often this assumption gives reasonable results. For now, for many purposes, the bulk parameter known as gm remains useful. The recent work on gm is varied, bringing to light more and more information about what controls photosynthetic capacity. The gas exchange equations that have been in use for three decades were reported to have an inconsistency that may have caused errors in the estimates of gm for isotopes (Farquhar & Cernusak 2012). The effects of water vapour outward flux on inward flux of CO2 is taken into account in estimating stomatal conductance but it usually is not considered for each isotopolog. Isotopes were used to show that water and CO2 can share diffusion pathways inside of leaves, not just during diffusion through stomata (Ferrio et al. 2012). Leaf anatomy is expected to be important as shown by Tosens et al. (2012) within a species and even within a single leaf (Kodama et al. 2011). Peguero-Pina et al. (2012) show that leaf anatomical properties can explain differences in gm between two species of Aibes while Scafaro et al. (2011) show that wild rice relatives have a lower gm than cultivated rice and this can be explained by leaf anatomy. A concept that has been around for some time is that in C3 plants, reassimilation of photorespired CO2 could be favoured over diffusion back to the intercellular airspace (Loreto, Delfine & Di Marco 1999). Two papers address this directly and show that (1) it occurs, and (2) it affects the estimate of gm (Busch et al. 2012; Tholen et al. 2012). This could be particularly important in understanding the effect of temperature on gm, and the interaction of gm and photorespiration on carbon discrimination was investigated (Tazoe et al. 2011; Evans & von Caemmerer 2012) using the TDL system. Mesophyll conductance is usually considered at the level of the individual leaf. Two recent papers estimate the role of gm at the canopy scale: Schäufele, Santrucek & Schnyder (2011), Ubierna & Marshall (2011). Perhaps the most interesting effect reported in the past 2 years is that temperature changes can cause an electrical signal to travel that can reduce photosynthetic capacity by reducing gm (Galléet al. 2012). The signal that travels through plants is fascinating. It may be related to the reactive oxygen species (ROS) wave described by Mittler et al. (2011). How the signal reduces gm will be an interesting story and so it would appear that there will be many more papers on the fascinating topic of CO2 diffusion into leaves during photosynthesis.