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First published online September 28, 2007; 10.1104/pp.107.107318 Plant Physiology 145:680-690 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities1,[W],[OA]Department of Biological Sciences, University of Essex, Colchester, United Kingdom (J.I.L.M., T.L.); and Laboratoire d'Ecologie Systématique et Evolution, Département d'écophysiologie végétale, Faculté des sciences d'Orsay, Université Paris XI, 91405 Orsay, France (G.C.)
Substantial lateral CO2 diffusion rates into leaf areas where stomata were blocked by grease patches were quantified by gas exchange and chlorophyll a fluorescence imaging in different species across the full range of photosynthetic photon flux densities (PPFD). The lateral CO2 flux rate over short distances was substantial and very similar in five dicotyledonous species with different vascular anatomies (two species with bundle sheath extensions, sunflower [Helianthus annuus] and dwarf bean [Phaseolus vulgaris]; and three species without bundle sheath extensions, faba bean [Vicia faba], petunia [Petunia hybrida], and tobacco [Nicotiana tabacum]). Only in the monocot maize (Zea mays) was there little or no evident lateral CO2 flux. Lateral diffusion rates were low when PPFD <300 µmol m–2 s–1 but approached saturation in moderate PPFD (300 µmol m–2 s–1) when lateral CO2 diffusion represented 15% to 24% of the normal CO2 assimilation rate. Smaller patches and higher ambient CO2 concentration increased lateral CO2 diffusion rates. Calculations with a two-dimensional diffusion model supported these observations that lateral CO2 diffusion over short distances inside dicotyledonous leaves can be important to photosynthesis. The results emphasize that supply of CO2 from nearby stomata usually dominates assimilation, but that lateral supply over distances up to approximately 1 mm can be important if stomata are blocked, particularly when assimilation rate is low.
Photosynthesis in leaves depends on the diffusion of CO2 from the ambient air through stomata and leaf air spaces into the chloroplasts in the mesophyll cells. This CO2 diffusion poses an important limitation on photosynthesis, and much research is focused on understanding the various components, such as the factors that control stomatal aperture (Nilson and Assmann, 2007  ), the value of the so-called internal or mesophyll conductance (Yamori et al., 2006), and the role of aquaporins and carbonic anhydrase in CO2 assimilation (Flexas et al., 2006). Stomata are discrete points of CO2 entry that can be widely spaced (e.g. interpore distances 24–340 µm are cited in Willmer and Fricker, 1996). Therefore, CO2 diffusion inside leaves is partly in a lateral (paradermal) direction (Parkhurst, 1994), although if stomata are open, diffusion in the vertical, transverse direction probably dominates due to the arrangement of cells and the connectivity of air spaces (Morison and Lawson, 2007). Stomatal apertures across leaves are often not uniform (e.g. Weyers and Lawson, 1997; Mott and Peak, 2007) and differences in aperture might lead to substantial lateral diffusion with stomata in one region potentially supplying CO2 to an adjacent region of the leaf, depending on the permeability of leaf tissue (Parkhurst, 1994). The permeability depends on leaf anatomy, particularly mesophyll cell size and shape, packing density, and the vascular anatomy (Pieruschka et al., 2005; Morison and Lawson, 2007). Many species have bundle sheath extensions (BSE) consisting of achlorophyllous parenchyma cells (Wylie, 1952; McClendon, 1992) that appear to provide a better supply of water to the epidermis (Kenzo et al., 2007) and may also allow local penetration of light into leaves (Vogelmann, 1989; Karabourniotis et al., 2000). In some species, these BSE can divide the mesophyll into discrete compartments or areoles leading to heterogeneous photosynthesis (Terashima, 1992; Morison and Lawson, 2007). It is usually concluded that no lateral diffusion will occur in heterobaric species with BSE but it will in homobaric leaf anatomies without BSE (Terashima, 1992; Evans and von Caemmerer, 1996; Jahnke and Krewitt, 2002). However, the importance of lateral CO2 diffusion to photosynthesis in leaves has been debated recently (Morison et al., 2005; Pieruschka et al., 2005, 2006).
Previously, using combined chlorophyll a fluorescence imaging and gas exchange measurements, we showed that in moderate light there was strong CO2 depletion in leaf areas where stomata were blocked with grease in one homobaric species (Commelina communis) and one heterobaric species (dwarf bean [Phaseolus vulgaris]; Morison et al., 2005
Part of the disagreement in these recent articles may reside in the different techniques used and the different species examined and part in the importance of lateral CO2 transfer varying with net CO2 assimilation rate (A; Lawson and Morison, 2006
Imaging Photosynthesis in Regions with Blocked Stomata Applying a 4-mm diameter grease patch to mature leaves of tobacco in moderate photosynthetic photon flux density (PPFD; 400 µmol m–2 s–1) inhibited photosynthesis underneath the patch, as measured by the quantum efficiency of PSII (Fq'/Fm'; Fig. 1 ). The chlorophyll a fluorescence images show a substantial reduction of Fq'/Fm' under the patch in the wild-type plants at an ambient CO2 mole fraction (Ca) of 300 µmol mol–1, and at the patch center, Fq'/Fm' dropped to <0.05 (Fig. 1A). The decrease of Fq'/Fm' was less severe and the area affected smaller when Ca was increased to 850 µmol mol–1 (Fig. 1B). With Ca = 1,580 µmol mol–1, the Fq'/Fm' decline was much smaller, although in the middle of the patch, Fq'/Fm' was only 0.25 compared to 0.4 outside the patch (Fig. 1C). When patches were applied to transgenic plants with reduced Rubisco (small subunit, SSu) and, consequently, reduced A, the Fq'/Fm' was substantially lower outside the patch but was still reduced to <0.05 in the patch center in normal Ca (Fig. 1D). In these transgenic plants, the grease patch effect became more noticeable in higher Ca (850 µmol mol–1), because Fq'/Fm' outside the patch increased (Fig. 1E). Even in the highest Ca, there was still a noticeable small patch with a drop of Fq'/Fm' from approximately 0.3 to 0.17 (Fig. 1F).
In the 1% O2 concentrations used, Fq'/Fm' was linearly related to A (Morison et al., 2005 ). Thus, each pixel's Fq'/Fm' value can be transformed to an A value using a calibration derived from A and Fq'/Fm' for the whole leaf area in the chamber prior to patch application. Transects of the derived A averaged from three leaves (Fig. 2
) show that A in the wild-type plants dropped to only approximately 1 µmol m–2 s–1 in the patch center in low Ca but was slightly higher in the SSu plants. The effect of the patch on A extended slightly beyond the area greased (approximately 0.3 mm), presumably because the additional CO2 sink in the patch reduces Ci in the surrounding area. However, there is some uncertainty in the precise placement and the spread of grease at the patch margins on application, which makes it difficult to determine the exact zone of effect. Transects calculated when Ca = 850 µmol mol–1 show an increase in A across the whole transect, and they are similar for wild-type and SSu plants because the increased Ca compensated for the lower Rubisco content in the transgenic plants. In even higher Ca, the reduction in Fq'/Fm' in the patch was slight, and the effect of the patch on photosynthesis in the two plant types was identical.
Assuming that the grease blocks stomata completely (see below), A should have declined to close to zero in these low O2 conditions if there were no lateral CO2 flux. Therefore, the A values in the patched area on these transects are lateral CO2 flux rates (Alateral) to a particular point. When Ca = 300 µmol mol–1, the mean Alateral was 5.6 and 4.7 µmol m–2 s–1 in wild-type and transgenic plants, respectively, compared to 14.1 and 8.2 µmol m–2 s–1 in ungreased areas (potential assimilation rate [Ap]). Therefore, the transgenic plants had higher values of Alateral/Ap (0.58) compared to 0.40 in wild type. In the highest Ca, the patterns of the A transects were very similar in transgenic and wild-type plants and values of Alateral/Ap were the same, approximately 0.82.
The chlorophyll fluorescence imaging was performed with moderate PPFD to give high measurement sensitivity and under low O2 to inhibit photorespiration and produce a linear relationship between A and Fq'/Fm'. To examine the magnitude of lateral CO2 diffusion across a range of PPFD during normal CO2 assimilation, we used a gas exchange approach. The response of CO2 assimilation rate to PPFD was measured in areas of attached leaves before and after grease patches were applied to both leaf surfaces (Fig. 3A
). The patches were evenly spaced and covered approximately one-half of the leaf, and five species were examined: petunia (Petunia hybrida), faba bean, sunflower (Helianthus annuus), dwarf bean, and maize (Zea mays). Normal ambient CO2 and O2 concentrations were used. In petunia, the transpiration rate (Tr) when greased (Trc) was reduced to 0.47 of that of the leaves prior to covering (Fig. 3B), exactly matching the proportion of leaf area not covered by grease, indicating that the grease blocked the stomata completely. However, the assimilation rate when greased (Ac) was only reduced to 0.60 of that prior to covering at PPFD
In faba bean (a homobaric species) and in sunflower and dwarf bean (heterobaric species) there were similar results (Supplemental Figs. S1–S3) to those with petunia. The values of Ac/A were significantly larger than Trc/Tr in all PPFD and increased to >0.8 at the lowest PPFD. Thus, the ratio of the change in CO2 assimilation to the change in transpiration ([Ac/A]/[Trc/Tr], equivalent to Ac x Tr/A x Trc; Fig. 4 ) was significantly larger than unity in all these four dicotyledonous species. This is strong evidence that lateral CO2 diffusion into the greased areas with blocked stomata was substantial. In contrast, in leaves of the heterobaric, monocot species maize, Ac/A was very similar to Trc/Tr (both approximately 0.55; Supplemental Fig. S4). Therefore, Ac x Tr/A x Trc was close to 1.0 (Fig. 4), indicating very little lateral CO2 flux.
The lateral diffusion rate was calculated as the CO2 assimilation in excess of that expected from the remaining uncovered portion of the leaf (which was assumed to photosynthesize at the rate prior to patch application, i.e. A) as:
As the light-saturated CO2 assimilation rates differed between species (Fig. 3; Supplemental Figs. S1–S4), we estimated the contribution that lateral flux made to A in the covered areas by expressing Alateral as a proportion of Ap, i.e. the assumed rate of assimilation of the covered area if it had not been covered (Ap = A x fc; Fig. 5B). In sunflower, petunia, dwarf bean, and faba bean, the lateral CO2 flux represented approximately 20%, 24%, 20%, and 15%, respectively, of the assimilation rates possible in moderate to high light intensities (PPFD  600 µmol m–2 s–1). When PPFD was  200 µmol m–2 s–1, the lateral CO2 flux was a much larger proportion (up to 64%, 83%, 95%, and 87%, respectively). In maize, the lateral flux represented a significant proportion of Ap (maximum of 18%) only in low PPFD. However, it should be noted that with the low fluxes in these PPFD, the potential measurement errors increased and the errors in calculating the greased area and repositioning the leaf chamber exactly became relatively more important. The calculated lateral CO2 fluxes shown in Figure 5 are substantial and are the integrated fluxes into all the individual patches, each of which presumably shows spatial gradients similar to those measured in tobacco (Fig. 1). Figure 1 also shows that in normal Ca, the central area of the 4-mm patches used on the tobacco was contributing little to leaf photosynthesis. Given the 12- x 5.8-mm diameter patches used for the light response experiments, it can be calculated that the Alateral values represent an outer area of approximately 0.5 to 0.9 mm of each patch photosynthesizing at the potential rates. Therefore, smaller patches should produce higher lateral CO2 fluxes, which we confirmed by comparing 4.5- and 5.8-mm diameter patches in faba bean leaves (Fig. 6A ; Supplemental Fig. S5). With the smaller patches, the lateral CO2 flux doubled to 3.4 µmol m–2 s–1, but the shape of the Alateral response to PPFD was very similar, showing saturation in approximately 300 µmol m–2 s–1. At higher PPFD, Alateral represented some 24% of Ap in these leaves compared to 15% with larger patches (Fig. 6B). As the perimeter length of the 24 smaller patches was 56% longer than the perimeter of the 12 larger patches, the lateral flux per unit perimeter length was similar and in both cases is equivalent to a zone of approximately 0.5 mm in each patch photosynthesizing at the potential rate (or 1 mm at one-half the potential rate, etc.). Figure 6A also demonstrates the sensitivity of the calculated Alateral to the exact determination of patch size. Although 5.8-mm diameter is the best estimate of the real grease patch size on the leaf, if the patch was just 0.2 mm larger or smaller, the calculated Alateral would be up to 45% higher or lower in moderate to high PPFD.
The tobacco chlorophyll a fluorescence images and assimilation rate transects (Fig. 1) also showed that the lateral flux of CO2 increased as the ambient CO2 concentration increased. We confirmed this effect using the patches with gas exchange measurements, as Alateral increased in sunflower almost in proportion to a 4-fold increase in Ca from 370 to 1,450 µmol mol–1 (Fig. 7A ). Importantly, Alateral increased substantially across the range of PPFD in the higher Ca, indicating that the saturation response of Alateral to PPFD in lower Ca is due to the limited supply of CO2. However, Alateral/Ap showed saturation at the same PPFD as at lower Ca (Fig. 7B). In these experiments in high Ca, the reduction in transpiration rate when covered was more than fc (Supplemental Fig. S6). While there is no obvious explanation, it suggested an alternative estimate of Alateral using the Trc/Tr measured at each PPFD rather than the fixed fc (see Eq. 1). However, this modification produced estimates of Alateral similar to those from Equation 1 (shown as "recalculated" in Fig. 7A).
Modeling Lateral Diffusion into Patched Areas
The difference in lateral CO2 diffusion observed between the four dicot species and the monocot maize (Fig. 5A) was probably due largely to anatomical differences. However, it may also be affected by the different response of A to Ci between plants with C3 and C4 photosynthesis, because mesophyll cells along the diffusion pathway can reduce Ci to much lower values in a C4 species. The effect of such different A/Ci relationships was explored using the 2-D model previously developed to understand lateral CO2 diffusion into leaf patches with blocked stomata at this scale (Gallouët and Herbin, 2005
The modeled transects were used to calculate the lateral fluxes into the greased mesophyll area (in the same proportion to the ungreased area as in the gas exchange experiments), assuming different Dc' (Fig. 9A ). This demonstrates that for any feasible Dc' value ( 40%), the modeled lateral CO2 diffusion in petunia is largely unaffected by PPFD over the range used here (200–1,500 µmol m–2 s–1), agreeing with the measurements in Figure 5. Furthermore, using the Alateral rates in Figure 5 to interpolate in Figure 9A suggests that an appropriate Dc' value for petunia is approximately 20% of the free air value. The model was also used to examine the sensitivity of Alateral to the patch size, assuming a Dc' of 20% (Fig. 9B). The modeled values of Alateral/Ap match well those measured for petunia with 5.8-mm diameter patches at the three PPFD used (see Fig. 5). The values of Alateral/Ap also matched the figures calculated for the wild-type tobacco with 4-mm patches (0.4) and the relative lateral CO2 flux increased sharply with smaller patches, as the measurements with faba bean showed (compare Figs. 9B and 6B). The relative lateral diffusion was slightly reduced with larger patches when the preindustrial atmospheric CO2 concentration was used (Fig. 9B), although the calculation did not take into account any alterations of the A/Ci response parameters with growth in a different CO2 concentration.
The experiments here using both chlorophyll a fluorescence imaging and gas exchange measurements with grease patches on leaves allowed the quantification of a substantial lateral CO2 diffusion rate across a range of light intensities in five dicotyledonous species, two of them previously classified as homobaric and two heterobaric (Fig. 5). Only in the monocot maize was there very little lateral CO2 diffusion. In all the dicot species, the lateral diffusion rate saturated at moderate PPFD in present day CO2 concentrations. The results emphasize that local stomata usually supply CO2 to the adjacent mesophyll, but when stomata are blocked, significant lateral CO2 diffusion can occur over short distances up to approximately 1 mm. While in our recent fluorescence imaging work (Morison and Lawson, 2007 ) we showed qualitatively that there were differing amounts of lateral diffusion in different species, we could not quantify the rates, as the images were not calibrated with simultaneous measurements of A. Furthermore, in our previous work with fluorescence imaging on two species, dwarf bean and C. communis (Morison et al., 2005), we emphasized the decline in Ci to low concentrations within approximately 0.3 to 0.5 mm of the grease patch periphery and thus did not assess the overall contribution of lateral CO2 diffusion to photosynthesis in the whole patch directly. The results here modify our earlier interpretation of the quantitative significance of lateral CO2 diffusion to photosynthesis.
In our work with tobacco, we used the linear relationship of A and Fq'/Fm' to calculate A directly from the fluorescence images. Although the decline in A was sharp in the 0.3- to 0.8-mm periphery of patches (Figs. 1 and 2), the overall assimilation supported by lateral CO2 flux within the patch was substantial, and in wild-type plants in normal Ca it was 40% of the assimilation rate outside the patch. Furthermore, the comparison of the wild-type and transgenic tobacco (Figs. 1 and 2) emphasizes that lateral CO2 diffusion depends on both the CO2 gradient (and hence on Ca) and the rate of CO2 uptake by the mesophyll cells along the pathway. Previous work with these transgenic Rubisco antisense plants has shown that the leaf anatomy was similar to that of the wild type but their A was only 25% of wild type in normal Ca (von Caemmerer et al., 1994
In the four dicotyledonous species measured with gas exchange, the Alateral values were quite similar despite the very different leaf anatomies and the presence and absence of BSE. In high PPFD, Alateral represented some 15% to 24% of the Ap (Fig. 5). These values are specific to the particular patch size and conditions used, as Alateral and Alateral/Ap both increased when smaller patches or higher Ca were used (Figs. 6 and 7). In higher Ca, the lateral Ci gradient was increased, enabling more lateral diffusion deeper into the patched area, and the slope of the A/Ci relationship for the cells along the pathway was reduced, with consequent higher A in the patch, as is also evident in the tobacco chlorophyll fluorescence images (Fig. 1). The lateral CO2 diffusion rates approached saturation in relatively low PPFD despite some differences in photosynthetic rates and in growing conditions (glasshouse or growth cabinet). The saturation was caused by the balance between the integrated assimilation rate of cells at different distances from the patch edge and the higher photosynthetic demand for CO2 at higher PPFD, as is illustrated in the modeled A transects (Fig. 8). The diffusion model calculations (Fig. 9A) showed that with large patches there is a small increase in Alateral at the highest PPFD (also evident in some of the data sets in Fig. 5). However, when expressed relative to A when not patched, Alateral was constant across PPFD >600 µmol m–2 s–1 (Fig. 9B).
Interestingly, light response curves of leaves usually show a light saturation of calculated Ci (e.g. Morison and Jarvis, 1983
The good agreement between the measured and modeled Alateral values and their responses to PPFD and patch diameter gives confidence in the observations presented here (compare Figs. 5 and 9, and 2 and 8). However, the model is only a 2-D approximation and does not represent the vertical gradients in Ci and A that must exist in leaves because of the light and photosynthetic characteristics profiles and the differences between cell types such as found in C4 species. The model calculations used only gas exchange measurements and A/Ci data obtained on unpatched leaves for parameterization and a range of assumed effective Dc' values. Previous evaluation of the model showed that when fitted to measured Ci patterns in patched leaves, it estimated feasible Dc' values (Gallouët and Herbin, 2005
The large Alateral values determined here might be surprising, as two of the species (sunflower and dwarf bean) are normally described as heterobaric and have BSE on some veins. However, determining the distribution of such extensions on different vein orders and their continuity and, hence, their effectiveness as diffusion barriers is difficult (Weyers and Lawson, 1997
These results both agree and contrast with those of Pieruschka et al. (2006)
The monocot maize was markedly different from the four dicots and showed almost no lateral CO2 diffusion. This difference agrees with the contrasting effect of Ca on Fq'/Fm' in patched areas of these species (Morison and Lawson, 2007
It may be suggested that the lateral CO2 fluxes found here are particular to the experimental system used with the artificial grease patches. Certainly, if patchy stomatal behavior occurs in particular areoles bounded by veins with continuous BSE, then lateral CO2 transfer may not be appreciable. This is evident in many chlorophyll fluorescence images of patchy stomatal behavior (e.g. Eckstein et al., 1996
Pieruschka et al. (2006)
Plant Material
Seeds of sunflower (Helianthus annuus) ‘Rigasol’ and maize (Zea mays) ‘Adonis’ were sown in a peat- and loam-based compost and grown in controlled environment cabinets in Orsay at 23°C/18°C day/night, 250 to 300 µmol m–2 s–1 PPFD for 16 h/d. Seedlings of petunia (Petunia hybrida) mixed hybrids were planted into a bed of loam soil in a heated glasshouse in Orsay in late March. Tobacco (Nicotiana tabacum) ‘W38’ plants were either wild type or from selfed T2 progeny of a tobacco transformant with an antisense gene directed against the Rubisco SSu driven by the cauliflower mosaic virus 35S promoter (Hudson et al., 1992 All plants were well watered throughout, and young but fully expanded leaves were used for all measurements. Measurements were made on attached fourth or fifth leaves of 3- to 5-week-old faba bean plants and the fully expanded primary leaves of dwarf bean, although very similar results were obtained with the terminal leaflet of the first trifoliate. Petunia shoots were excised from the 12- to 16-week-old plants in the glasshouse and recut under water before measurement. For maize, the third leaves of 6-week-old plants were used, still attached, and the chamber was placed on the first third of the leaf from the tip. For sunflower, excised second or third leaves of 4- to 6-week-old plants were used.
Images of chlorophyll a fluorescence were obtained on attached tobacco leaves essentially as described previously by Morison et al. (2005) Using the CF imager software, parts of the Fq'/Fm' images with the patch and some surrounding leaf areas were isolated, smoothed using a loss-less, low pass spatial filter, and the data transferred to MATLAB (v. 7.0, The MathWorks). For comparison between conditions, average transects of Fq'/Fm' were calculated from three rows of pixels along the horizontal axis passing through the center of the patch image. Transects were averages of three wild-type and three transgenic plants.
Responses of A to PPFD (A/Q curves) were measured using identical portable gas exchange systems at Colchester and Orsay. They were the Li-6400 (LiCor) with standard leaf chamber, using white chamber seals and red and blue LED light source. Air humidity was supplied and controlled using a dew-point generator (Li-610, LiCor). Initially, leaves were allowed to stabilize for approximately 30 to 45 min to the leaf chamber conditions, where CO2 was maintained at 360 µmol mol–1, 21% O2, leaf temperature of 25°C, a PPFD of 300 µmol m–2 s–1, and a controlled water vapor pressure difference of approximately 0.8 kPa. After stabilization, an A/Q curve was constructed by first decreasing, then increasing the PPFD in steps lasting approximately 5 to 10 min. The final measurement was a repeat at 300 µmol m–2 s–1 PPFD. Then, approximately one-half the leaf area was covered with grease in 12- x 5.8-mm diameter patches and applied to both leaf surfaces using neoprene foam discs as before. The grease used depended on the experiment, as the silicone grease (Rhodosil) damaged faba bean leaves, so nonsilicone grease was used (Glisseal, Borer Chemie). The leaf was placed back in the chamber in an identical position and allowed to stabilize for approximately 30 min. After stabilization, a second A/Q curve was constructed, identical to that described above. With faba bean, an additional set of experiments was done with 24- x 4.4-mm diameter patches. Grease patches had no noticeable effect on leaf appearance for several days after plants were returned to the glasshouse or cabinet. For petunia and maize, A/Ci response curves were also measured at three different PPFD: 200, 600, and 1,500 µmol m–2 s–1.
The 2-D mathematical model implemented in MATLAB developed and described by Gallouët and Herbin (2005)
The following materials are available in the online version of this article.
J.I.L.M. is grateful to the Université Paris XI (Faculté des Sciences d'Orsay) for the support of the visiting professorship and we thank Neil Baker (University of Essex) for suggesting the collaboration and sharing his expertise in chlorophyll a fluorescence. Received August 15, 2007; accepted September 10, 2007; published September 28, 2007.
1 This work was supported by the Université Paris XI (visiting professorship to J.I.L.M.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: James I.L. Morison (morisj{at}essex.ac.uk).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.107318 * Corresponding author; e-mail morisj{at}essex.ac.uk.
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ABSTRACT
RESULTS
