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Keywords:

  • leaf curling;
  • photosynthetic asymmetry;
  • stomata;
  • sunlight incidence

Patterns in leaf structural asymmetry among vascular plants have prompted a long-standing and continuing interest in the effects on photosynthetic performance (DeLucia et al., 1991). Leaf curling, most often interpreted as a response to water stress (e.g. Heckathorn & DeLucia, 1991), represents a dynamic behavioral response in plants whereby the normal sunlight orientation of the two leaf surfaces may be reversed. The large majority of plant species (those with the C3 metabolic pathway) have leaves that are oriented approximately horizontally and have an accompanying asymmetry (dorso-ventral) in both external morphology (e.g. stomatal distribution) and internal anatomy (e.g. differentiated mesophyll cells) (Fig. 1a). This leaf asymmetry generates the well-known sun vs shade leaf structure that can function to increase the overlap of absorbed sunlight and CO2 inside the leaf, and thus photosynthetic efficiency (Smith et al., 1997). In contrast, there are also numerous plant species that have a more inclined leaf orientation and do not have sun/shade differences in leaf structure, but have more equal numbers of stomata on the two leaf surfaces. In particular, species with C4 metabolism often have a distinct ‘Kranz’ internal anatomy (chlorophyll-containing cells concentrated around vascular bundles) that is perceived as not having the structural capability to regulate the distribution of absorbed sunlight inside the leaf (Fig. 1b). Rather, CO2-concentrating mechanisms and increased phloem loading are known to contribute to high photosynthesis in C4 species, particularly in high-sunlight environments. In this issue of New Phytologist, Soares et al. (pp. 186–198) report on an imaginative and thorough set of experiments showing that a C4 grass species, during natural leaf curling that reversed the orientation of the upper and lower leaf surfaces, had accompanying stomatal and biochemical changes inside the leaf that enhanced its photosynthetic capability. Remarkably, stomata closed on the opposite, newly shaded side of the leaf, while adjacent cells appeared completely inactivated photosynthetically. This dramatic asymmetry in stomatal and photosynthetic function occurred only when the lower leaf surface became illuminated via curling. Thus, the photosynthetic response to sunlight incidence on a particular leaf side was not based on leaf structural differences determined during leaf development, as commonly reported in C3 species. Instead, a more dynamic, biochemical response occurred that linked sunlight incidence to the behavior of stomata and photosynthetic cells throughout the full thickness of the leaf. This rapid response capability during leaf curling suggests an alternative adaptive venue in C4 plants, one that is much more temporally dynamic than the developmentally determined changes in leaf structure found in C3 plants (i.e. sun/shade leaves). Photosynthetic enzymes (e.g. Rubisco and phosphoenolpyruvate carboxylase (PEPC)) were also activated in photosynthetic cells near the sunlit surface with open stomata, where both light intensity and CO2 concentration were high. Although not reported in Soares et al., a major enhancement in leaf water use efficiency (during leaf curling) would be expected.

image

Figure 1. Typical C3 and C4 leaf structure. (a) The well-documented differentiation of mesophyll cells (e.g. palisade and spongy) in the thicker sun leaves of C3 species enhances propagation and dispersal of absorbed sunlight (shown schematically), while an increasingly equal distribution of stomata on the two leaf sides significantly enhances CO2 supply. The hatched curve represents no structural effects on internal gradients; solid lines show the increased overlap of absorbed light and CO2 resulting from structural effects. (b) The typical leaf structure of C4 species (e.g. grasses and other monocots) includes a more equal distribution of stomata on the two leaf sides, but no strong differentiation of cells (concentrated around the vascular tissue bundles, i.e. ‘Kranz’ anatomy) that might enhance light and CO2 overlap inside the leaf.

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‘This dramatic asymmetry in stomatal and photosynthetic function occurred only when the lower leaf surface became illuminated via curling’

Photosynthetic asymmetry in plant leaves

  1. Top of page
  2. Photosynthetic asymmetry in plant leaves
  3. Experimental approach
  4. Supporting data
  5. Concluding perspectives and future research
  6. References

Despite the major differences in structural leaf symmetry found within the plant kingdom, relatively little information exists on specific photosynthetic impacts of sunlight incidence on different surfaces of the same leaf. In fact, few measurements exist that quantify differences in sunlight incidence on each leaf side under natural field conditions. During typical photosynthesis measurements in the field or laboratory, only the amount of downward, hemispherical irradiance is typically measured, without concern for the amount of sunlight striking both leaf surfaces. Yet, a host of leaf structural parameters with documented photosynthetic impacts have been strongly associated with both the amount of incident sunlight on each leaf surface and the ratio of these amounts (Smith et al., 1998). Also, the stomata of several understory species, found predominately on the lower leaf surface that received low and slowly changing sunlight incidence, responded linearly to sunlight incidence on the upper-facing leaf surface during morning stomatal opening (Smith, 1981). The mechanistic process by which plant leaves sense and respond photosynthetically to asymmetric sunlight incidence is unknown; in particular, the coordination of the stomatal uptake (CO2 supply) and the CO2 demand of the sunlit photosynthetic cells within the leaf remains to be elucidated.

Ideally, for plant leaves, there should exist a CO2 supply and demand control system that is coupled tightly to sunlight incidence. In C3 species, characteristic changes in leaf structure as a result of changes in irradiance intensity occur only during developmental cellular differentiation (e.g. Smith et al., 1997). Even the unusual leaf structure of the needle-like leaves of conifer species appears to utilize another, purely structural adaptive strategy (more cylindrical leaf morphology and radial anatomy) that replaces the functional benefits of typical C3 cell differentiation to photosynthetic performance (Johnson et al., 2005).

Experimental approach

  1. Top of page
  2. Photosynthetic asymmetry in plant leaves
  3. Experimental approach
  4. Supporting data
  5. Concluding perspectives and future research
  6. References

A clever and insightful aspect of the approach of Soares et al. was the selection of a C4 species with nearly equal numbers of stomata on the two leaf sides, and a characteristic leaf structure that is, typically, highly symmetric compared with C3 plants. The choice of a C4 species eliminated the possibility of an effect of leaf structure on sunlight distribution and CO2 diffusion inside the leaf, an effect that is already known to exist for C3 species. Also, the fact that this class of plants can assimilate internally generated CO2 (from respiration and photorespiration) for photosynthesis in the absence of light, and with closed stomata, was an important part of this experimental design. Thus, differences in the response of stomata to incident sunlight (adaxial or abaxial) were measured experimentally, and additional, supporting measurements were made that would add credibility to their conclusions about mechanisms (see ‘Supporting data’ below). The investigators’ design of a CO2 gas exchange system that enables accurate measurement of photosynthetic CO2 exchange from the whole leaf, as well as from each of the two leaf surfaces separately, is also a significant contribution to the field.

Supporting data

  1. Top of page
  2. Photosynthetic asymmetry in plant leaves
  3. Experimental approach
  4. Supporting data
  5. Concluding perspectives and future research
  6. References

Soares et al. also provide data showing the effects of elevated ambient CO2 (during growth) and the more instantaneous interactions with the calculated concentration of CO2 in the intercellular air spaces (Ci) between the stomata and the photosynthetic cells. This Ci term is easily calculated from standard gas exchange measurements and is often employed to help understand the dynamics involved in the coordination of stomatal supply of CO2 vs the demand by the photosynthetic cells inside the leaf. For example, a high Ci may indicate either a low cellular demand (often stress related), or a degree of stomatal opening that is unnecessarily high and, thus, expensive in terms of transpirational water loss. A low Ci value might reflect a strong stomatal limitation where CO2 supply is not keeping up with CO2 demand.

In summary, the following supportive data presented by Soares et al. eliminated other possible mechanisms that might provide alternative explanations for their conclusions.

  • • 
    Photosynthesis was equal on the two leaf sides when illumination was on the adaxial side, but was asymmetric and substantially greater overall when the abaxial side was illuminated, with zero photosynthesis and complete stomatal closure occurring adaxially.
  • • 
    When light was directed to the adaxial surface, stomata closed on both leaf surfaces, even under decreasing Ci conditions when stomatal opening should typically increase.
  • • 
    Illumination of the abaxial surface (simulating leaf curling effects) led to complete stomatal closure on the adaxial surface and complete cessation of leaf photosynthesis, indicating no internal transport of CO2 from the leaf side with open stomata (i.e. abaxial) or photosynthetic assimilation of metabolically generated CO2 on the side with closed stomata and low illumination.
  • • 
    No differences in whole-leaf optical properties (absorptance, reflectance, and transmittance) occurred for one leaf side vs the other.
  • • 
    Photosynthetic enzyme proteins were distributed uniformly across the leaf thickness in plants grown under unenriched CO2.

 Growth under enriched CO2 increased twofold, but did not appear to influence substantially the dorso-ventral regulation of photosynthesis based on light incidence on a particular leaf surface. However, enrichment and abaxial illumination did result in a slight decrease in the response of photosynthesis to changes in Ci.

Concluding perspectives and future research

  1. Top of page
  2. Photosynthetic asymmetry in plant leaves
  3. Experimental approach
  4. Supporting data
  5. Concluding perspectives and future research
  6. References

The above findings suggest a regulatory signaling by light-activated stomata that is transmitted across the full thickness of the leaf and causes stomatal closure on the opposite, now low-light leaf surface. This sort of tight coupling between cells experiencing different environmental conditions (sunlight and CO2 concentration) has not been reported before. The rapid transfer of environmental signals to a physiological process over the entire leaf thickness may be similar to the sensing and transfer of environmental signals (e.g. ambient CO2 concentrations) over even greater distances; for example, a signal to alter stomatal size and frequency from a mature leaf to a developing leaf still in the bud stage (e.g. Lake et al., 2001). Such a rapid intercellular communication linking the environment with leaf photosynthesis is an important area for future research (Hanstein & Fell, 2004; Thomas et al., 2004; Yano & Terashima, 2004).

One interesting report involving the interaction of Ci with the possible control system proposed by Soares et al. is the spatial segregation of an intercellular air space that is connected separately to each leaf surface (Long et al., 1989). These results also have functional significance for both the lower (e.g. chloroplast location) and higher (e.g. ecosystem) organizational scales defining the importance of C4 species. These species are photosynthetically distinct in their CO2-concentrating physiology and accompanying high productivity, and are currently targeted for agricultural/commercial development into bio-energy products (e.g. bio-fuel). The authors also point out that the future performance of C4 species under current scenarios of global change (e.g. elevated CO2), compared with the much more abundant C3 species, has not received much attention.

References

  1. Top of page
  2. Photosynthetic asymmetry in plant leaves
  3. Experimental approach
  4. Supporting data
  5. Concluding perspectives and future research
  6. References
  • DeLucia EH, Shenoi HD, Naidu SL, Day TA. 1991. Photosynthetic symmetry of sun and shade leaves of different orientations. Oecologia 87: 5157.
  • Hanstein S, Felle HH. 2004. Nanoinfusion – an integrating tool to study elicitor perception and signal transduction in intact leaves. New Phytologist 161: 591602.
  • Heckathorn SA, DeLucia EH. 1991. Effect of leaf rolling on gas exchange and leaf temperature of Andropogon gerardii and Spartina pectinata. Botanical Gazette 152: 263268.
  • Johnson DM, Smith WK, Vogelmann TC, Brodersen CR. 2005. Leaf architecture and direction of incident light influence mesophyll fluorescence profiles. American Journal of Botany 92: 14251431.
  • Lake JA, Quick WF, Beerling DJ, Woodward FI. 2001. Plant development: signals from mature to new leaves. Nature 411: 154158.
  • Long SP, Forage PK, Bolhar HR. 1989. Separating the contribution of the upper and lower mesophyll to photosynthesis in Zea mays L. leaves. Planta 177: 207216.
  • Smith WK. 1981. Temperature and water relation patterns in subalpine understory plants. Oecologia 48: 353359.
  • Smith WK, Bell DT, Shepherd KA. 1998. Associations between leaf orientation, structure and sunlight exposure in five western Australian communities. American Journal of Botany 84: 16981707.
  • Smith WK, Vogelmann TC, Bell DT, DeLucia EH, Shepherd KA. 1997. Leaf form and photosynthesis. Bioscience 47: 785793.
  • Soares AS, Driscoll SP, Olmos E, Harbinson J, Arrabaça MC, Foyer CH. 2007. Adaxial/abaxial specification in the regulation of photosynthesis and stomatal opening with respect to light orientation and growth with CO2 enrichment in the C4 species Paspalum dilatatum. New Phytologist 177: 186198.
  • Thomas FW, Woodward FI, Quick WP. 2004. Systematic irradiance signaling in tobacco. New Phytologist 161: 193198.
  • Yano S, Terashima I. 2004. Developmental process of sun and shade leaves in Chenopodium album L. Plant, Cell & Environment 27: 781793.