Leaf Form and Photosynthesis (PDF)

Leaf Form and Photosynthesis Author(s): William K. Smith, Thomas C. Vogelmann, Evan H. DeLucia, David T. Bell and Kelly A. Shepherd Source: BioScience , Dec., 1997, Vol. 47, No. 11 (Dec., 1997), pp. 785-793 Published by: Oxford University Press on behalf of the American Institute of Biological Scien...

Leaf Form and Photosynthesis Author(s): William K. Smith, Thomas C. Vogelmann, Evan H. DeLucia, David T. Bell and Kelly A. Shepherd Source: BioScience , Dec., 1997, Vol. 47, No. 11 (Dec., 1997), pp. 785-793 Published by: Oxford University Press on behalf of the American Institute of Biological Sciences Stable URL: https://www.jstor.org/stable/1313100 REFERENCES Linked references are available on JSTOR for this article: https://www.jstor.org/stable/1313100?seq=1&cid=pdf- reference#references_tab_contents You may need to log in to JSTOR to access the linked references. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at https://about.jstor.org/terms American Institute of Biological Sciences and Oxford University Press are collaborating with JSTOR to digitize, preserve and extend access to BioScience This content downloaded from 64.189.4.202 on Wed, 09 Oct 2024 03:00:10 UTC All use subject to https://about.jstor.org/terms  Leaf Form and Photosynthesis Do leaf structure and orientation interact to regulate internal light and carbon dioxide? William K. Smith, Thomas C. Vogelmann, Evan H. DeLucia, David T. Bell, and Kelly A. Shepherd M orphological and anatomi- tosynthetic performance. This rela- cal features of plant leaves tionship includes a strong coupling are commonly associated Terrestrial plants between leaf structure and orienta- with metabolic type (e.g., Kranz tion that is not documented in the responded to the literature and that has not been at- anatomy of C4 species), amount of sun exposure (e.g., sun and shade amount of sunlight tributed to photosynthetic function. leaves), or water stress (e.g., xero- We describe field observations of morphism). However, although the and stress in a given correlations among leaf structural primary function of the leaf is to symmetry, leaf orientation, and the absorb and process sunlight and car- habitat by evolving resulting amount of incident sun- bon dioxide for photosynthesis, few light on both leaf surfaces. We also structural features of leaves have been leaf structural summarize physiological and bio- related mechanistically to these tasks. physical evidence of the impact of For example, it has been known for properties in concert this structural symmetry on the cap- over a century that the internal with leaf orientational ture and processing of sunlight and anatomy of leaves is characterized carbon dioxide for photosynthesis. by different cell layers (e.g., the pali- capabilities We propose that the evolution of sade and spongy mesophyll) and that leaf structural symmetry is based on stomatal pores can be located on one leaf orientation and the regulation or both sides of a leaf. Yet, only re- Koike 1988, Reich et al. 1991, Walter of incident sunlight and is driven by cently has any functional relationship 1973), but mechanistic evidence a common functional theme-maxi- between leaf form and photosynthetic pointing to a complex influence of mizing photosynthesis per unit leaf performance been suggested. leaf structure on photosynthesis has biomass by regulating light and car- A variety of ecological studies havebeen obtained only recently (Tera- bon dioxide gradients inside the leaf. correlated numerous leaf structural shima and Hikosaka 1995, Vogel- Although differences in chloroplast parameters with photosynthetic per- mann et al. 1996a). A comprehen- abundance, physiology, and behav- formance (e.g., Abrams and Kubiske sive synthesis of the functional ior at different locations across the 1990, 1994, Hinckley et al. 1989, significance of leaf structure, as re-mesophyll are also important to this lated to photosynthesis, has yet to becentral theme (e.g., Evans 1996, William K. Smith (e-mail: wksmith@uwyo. proposed. In addition, no studies Terashima 1992, Terashima and have associated leaf structural char- Hikosaka 1995), these topics are not edu) and Thomas C. Vogelmann (e-mail: [email protected]) are professors in the acteristics with differences in leaf emphasized. Department of Botany, University of Wyo-orientation relative to the Sun, de- For a typical plant leaf, sunlight is ming, Laramie, WY 82071-3165. Evan H. spite the recognition that both incident on the upward-facing DeLucia (e-mail: [email protected]) is an structure and orientation can have (adaxial) side, whereas carbon diox- associate professor in the Department of dominant influences on whole-leaf ide uptake occurs predominately at Plant Biology, University of Illinois, Ur- photosynthesis. the lower (abaxial) side, where most, bana, IL 61801. David T. Bell (e-mail: In this article, we present a syn- if not all, of the leaf stomatal pores [email protected]) is an associate professor and Kelly A. Shepherd is a re- thesis of current findings in ecology,are found (Figure 1; Meidner and search assistant in the Department of physiology, and biochemistry that Mansfield 1986). Thus, whereas Botany, The University of Western Austra- points to a fundamental relationship chloroplasts just beneath the upper lia, Nedlands, WA 6907 Australia. ? 1997 between the evolution of leaf form epidermis of this leaf should experi- American Institute of Biological Sciences. (structure and orientation) and pho- ence the highest light regimes, the December 1997 785 This content downloaded from 64.189.4.202 on Wed, 09 Oct 2024 03:00:10 UTC All use subject to https://about.jstor.org/terms Figure 1. A cross-sec- Incident sunlight Smith 1994, 1997, Smith and tion of a typical leaf McClean 1989). However, this same showing the opposing U er water repulsion may also create a gradients of internal epidermis ? O? monolayer of small water droplets over the entire leaf surface. Because light ide andsunlight when carbon is diox- uepidermisal in- ' CO?i of the lensing effects of these water cident on the upper leaf droplets, a highly variable sunlight surface and stomata are o pattern develops over the leaf sur- present predominantly i 5 ) % on the lower surface. face, ranging from full shade to over Two pairs of hypotheti- pongy 20 times full sun at focal points be- cal curves are drawn: Lower c. neath individual droplets (Brewer et one pair (dashed lines) epidermis Stomata al. 1991). In most species tested, a shows strong gradients Photosynthetic layer of leaf trichomes holds the dew that generate a narrow droplets above the leaf surface, well zone of overlap (indi- beyond their focal distances, greatly cated by small bracket) between high light and carbon dioxide, reducing and another the potential damage ofpair this (sol lines) shows smaller gradients that generate a broader zone focused of overlap sunlight (large bracke to the photosyn- between high light and carbon dioxide. A broader zone of overlap would generate thetic system. greater photosynthesis per unit leaf biomass, which may be a fundamental driving for Another common feature of the in the evolution of leaf form (i.e., structure and orientation). leaf epidermis is their lens-like cells, which were originally thought to be carbon dioxide concentration is high-asymmetric leaves, when structurally involved in orienting the leaf toward est on the opposite sidewhich of the leaf, naturally the sun (Haberlandt 1914). More intercept direct sun- next to the lower epidermis. light only Steep, on one surface, are illumi- recently, however, it has become clear opposing gradients in light nated onand in the opposite side instead that these lens-like epidermal cells carbon dioxide would not seem to be (e.g., Evans et al. 1993, Kirschbaum both collect and focus incident light optimal for maximizing photosyn- 1987, Poulson and DeLucia 1993, into the leaf interior, possibly to en- thetic efficiency across the entire Terashima 1989). hance photosynthesis (Bone et al. 1985, thickness of the leaf (Figure 1). It Increasing evidence implicates the Lee 1986, Poulson and DeLucia 1993, seems logical that leaf form would leaf surface and all of the major cell Poulson and Vogelmann 1990). These have evolved so as to maximize photo- types within a leaf (i.e., epidermis, findings also show that the geometry synthesis per unit leaf biomass in the palisade, and spongy mesophyll)of asindividual epidermal cells may face of these opposing internal gradi- influencing the capture and internal vary according to sunlight exposure. ents of light and carbon dioxide. processing of absorbed sunlight Spherical epidermal cells may be (Vogelmann et al. 1996a). Moreover,more beneficial in shaded environ- Does leaf structure regulate orientational and corresponding ments, adding a much greater ab- internal light? structural effects may have strong sorbing area, not only for the pre- influences on photosynthetic prop-dominant levels of less intense diffuse Considerable evidence indicates that erties. Chloroplast acclimation to light, but also for the direct sunlight the structural properties of leaves altered light regimes appears unable(sunflecks) that penetrate the canopy (apart from changes in chloroplasts) to compensate entirely for alterations at low angles of incidence (Smith et may influence photosynthetic per-in natural light regimes or normal al. 1989). In addition, spherical epi- formance. Most of this evidence leaf optical properties. dermal cells would focus light to the comes from observations (Terashima shallow depths that are necessary for and Hikosaka 1995) that the shape Upper epidermis. Leaf surface struc-these typically thinner shade leaves. of the light-response curve of photo- tures, such as epicuticular waxes andIn sunnier habitats, more elliptical synthesis (i.e., the amount of carbon epidermal hairs, have been reportedepidermal cells would generate fixed per amount of light) can to be affect whole-leaf photosynthesisdeeper focal points for a more even due to alterations in absorbed sun- altered by changing the angle of inci- distribution of internal light through- out thicker leaves (Vogelmann et al. light. For example, high solar reflec- dence of direct-beam light, the direc- tional composition of the incident 1996a). Moreoever, any bending of tance from pubescent leaves of desert light (i.e., whether the beam is broad-leaf dif- species results in optimal incident, direct-beam sunlight by epi- fuse or direct), and the type ofleaf leaftemperatures, reduced transpi-dermal cells is important for length- structure (i.e., whether it is asym- ration, and enhanced photosynthe-ening photon path lengths inside the metric or symmetric). Experimen- sis (Ehleringer and Werk 1986, leaf and, thus, increasing the prob- tally disrupting the parallel rays of Johnson 1975, Smith 1978). Also, ability for absorption by chloroplasts direct-beam light by using a light the hydrophobic nature of leaf pu- (Vogelmann et al. 1996b). diffuser caused substantial alter- bescence found in numerous species ations in the light response of photo-may prevent a water film from form- Mesophyll. The optical properties of synthesis (DeLucia et al. 1991, cell layers inside leaves (i.e., the pali- ing during dew and rainfall, a poten- Terashima 1989). Similar alterations sade and spongy mesophyll) also tially large barrier to photosynthetic in photosynthesis have been observed carbon dioxide exchange (Brewer and appear to regulate the internal distri- 786 BioScience Vol. 47 No. 11 This content downloaded from 64.189.4.202 on Wed, 09 Oct 2024 03:00:10 UTC All use subject to https://about.jstor.org/terms bution of sunlight for enhanced pho- stantial gradients in light do appearalthough this study did not measure tosynthesis (Vogelmann 1993, Vogel- to form across the leaf mesophyll internal light and carbon dioxide. mann et al. 1996a). For example, the (Vogelmann et al. 1996a), with cor- Logically, photosynthesis could be more columnar palisade cells typical responding effects on whole-leaf pho- maximized if chloroplasts were situ- of thick sun leaves act as light con- tosynthesis, carbon dioxide levels ated at locations within the meso- duits that propagate light deeper into inside leaves have not been mea- phyll at which both light levels and the mesophyll (Figure 1), thus dis- sured directly, and much less is carbon dioxide availability were op- tributing light more evenly through- known about their characteristics timized by the appropriate combina- out the leaf (Terashima 1989, Vogel- (Parkhurst 1994). However, rela- tion of leaf orientation and struc- mann and Martin 1993). In addition, tively large gradients of carbon di- ture. The observation that mesophyll the cell walls of the spherical spongy oxide across the mesophyll thickness cell surface area, chlorophyll con- mesophyll cells and the large frac- have been estimated (Parkhurst 1978) centration, and photosynthetic ac- tion of air space in the leaf interior using indirect methods that measure tivity per unit leaf thickness are not generate large quantities of scattered carbon dioxide exchange in whole uniform across the leaf thickness in- light, increasing light absorption by leaves that are exposed to carrier dicates that certain strata of the leaf chloroplasts within the mesophyll gases infused from different sides ofmay experience an optimum overlap (DeLucia et al. 1996). Overall, inter- the leaf (Parkhurst and Mott 1990). of the opposing light (from above) nal light scattering within leaves gen- Estimates of up to a 16 Pa pressure and carbon dioxide (from below) erates photon fluence levels three to difference in internal carbon dioxide gradients (Terashima and Hikosaka four times greater than sunlight inci- between opposite leaf sides have been 1995). Evaluation of the relation- dent on the leaf surface, enhancing reported for leaves with large, ex- ship among leaf thickness, stomatal the absorption of weakly absorbed perimental differences in ambient distribution, and whole-leaf photo- wavelengths in particular (Vogel- carbon dioxide concentrations be- synthesis could provide ecophysiologi- mann 1993). tween the two leaf surfaces and nearly cal evidence for the importance of the equal numbers of stomata on both overlap of light and carbon dioxide Lower epidermis. Another funda- sides of the leaf (Parkhurst et al. gradients inside the leaf. mental influence of epidermal struc-1988). Actual gradients of carbon ture on photosynthesis may result dioxide inside natural leaves may beThe interaction of leaf from leaf bicoloration, in which the less, although the common occur- orientation and structure leaf side that faces away from the rence of stomata on only one side of sun is lighter in color than the leaf the leaf would enhance steeper gradi- If leaf orientation and structure do surface facing toward the sun. ents that would be in opposition to the interact to regulate sunlight absorp- Bicoloration is especially common in light gradient (Figure 1). Parkhurst tion and distribution inside the leaf, species that occupy more shaded (1994) concluded that intercellular then the structural asymmetry iden- habitats (Smith 1981). Bicoloration gaseous diffusion is a substantial limi-tified above (e.g., epidermal lens cells could enhance "light-trapping" in tation to photosynthetic carbon di-and palisade cells beneath the upper the spongy mesophyll by providing a oxide assimilation in the large num- leaf surface of horizontal leaves) reflective surface on the internal side ber of species that have thick leaves should correspond to the quantity of the lower epidermis (Lin and and stomata on the lower leaf sur- and type of sunlight incident on each Ehleringer 1983, Smith 1981, face only. To date, measurements of leaf surface. The focusing capabili- Woolley 1971). In these studies, both re- light and carbon dioxide gradi- ties of epidermal lens cells require moval of the lower epidermis of ents a within the same leaf are not direct-beam sunlight (diffuse light is bicolored leaf resulted in large in- available for any plant species. poorly focused by any lens), whereas creases in light transmittance. The Although carbon dioxide gradi- palisade cells, if they function to reflective properties of the spongy ents have not been measured directly propagate light deeper into the leaf, mesophyll and of the inside of inside the leaves, experiments using pulse should occur beneath the leaf sur- lower epidermis are also important dosages of labeled carbon dioxide, face with greatest incident light. If for increased light retention and ab-subsequent paradermal section- carbon dioxide is to be supplied ad- with sorption in bicolored leaves (DeLucia ing and autoradiography, have equately to the increased mesophyll and Nelson 1993, DeLucia et al. shown variation in the location of cell area in sun leaves, then the cor- 1996). carboxylation activity inside leaves responding increase in leaf thickness (Nishio et al. 1993). Initial studies should be accompanied by a more Light and carbon dioxide indicated that the internal light gra- equal distribution of stomata on both dients of sun and shade leaves of leaf sides. However, few ecological gradients in leaves spinach did not correspond to the studies have related the occurrence It is reasonable to expect leaf orien- carbon fixation gradient (Nishio et of these structural differences in leaf tation and structure to interact so al. 1993). However, a subsequent study symmetry, thickness, and stomatal that high light areas inside a leafreported are that light absorption profiles distribution with differences in inci- matched with high carbon dioxide predicted from chlorophyll concen- dent light between the two leaf sur- concentrations. Otherwise, full pho- tration gradients did match carbon faces under natural field conditions. tosynthetic potential will not be dioxide fixation profiles measured One might also expect to find achieved (Figure 1). Although sub-within spinach leaves (Evans 1996), changes in leaf structure that would December 1997 787 This content downloaded from 64.189.4.202 on Wed, 09 Oct 2024 03:00:10 UTC All use subject to https://about.jstor.org/terms diminish light absorption when a the frequent appearance of species sampling, the five communities were plant is experiencing other sources with leaf and stem succulence (e.g., composed of a high diversity of ever- of stress-that is, when light is not green species only, whose leaves must cacti and euphorbs) are further ex- limiting but temperature, water, or endure seasonal drought (Beard amples of the occurrence of cylindri- nutrients may be. Numerous studies 1990, Pate and McComb 1982). Such cal geometry in highly stressful habi- have documented the detrimental tats. (We address the functional stress "tolerators" may be particu- impact of high light on photosyn- significance of a cylindrical leaf formlarly indicative of adaptive relation- thetic performance, especially when in terms of light and carbon dioxide ships between leaf form and func- a plant is under stress from other processing for photosynthesis in the tion (Fahn and Cutler 1992, Levitt environmental factors (Baker and next section.) 1980). Bowyer 1994). For example, one Most terrestrial plant species with For the five Australian communi- rarely observes leaves of any species thin, laminar leaves have many more ties, strong positive correlations oc- oriented perpendicular to full sun-stomata on the lower side of the leaf curred between total daily sunlight light, unless leaf temperatures are than on the upper side (i.e., they areand the proportion of species in a low and transpirational water is hypostomatous), although a signifi-given community with thicker leaves, abundant (Smith 1978). High inci- cant fraction (including most grasses)more cylindrical leaves, an inclined dent sunlight will result in leaf wilt have almost equal numbers of sto- leaf orientation, palisade cell layers (midday wilt) even for plants whose mata on both leaf surfaces (i.e., they on both leaf sides, and stomata on roots are in water-saturated soil are amphistomatous; Meidner and both leaf sides (Smith et al. in press). (Young and Smith 1980). Mansfield 1986). Only a few species Also, the presence of palisade cell One of the best-documented ob- with thin, laminar leaves have sto- layers on both leaf sides was corre- servations of ecological patterns inmata exclusively on the upper leaflated more strongly with a lower leaf structure, already mentioned side (e.g., lily pads; Brewer and Smithratio (top-to-bottom) of incident sun- above, is the ability of most species 1995). Increased leaf thickness has light than with the total amount of to develop sun leaves under high been associated with a more equal sunlight incident on the upper leaf sunlight exposure (e.g., Boardman number of stomata on both leaf sur- surface only. By contrast, the num- 1977, Hansen 1917). In general, sun faces for numerous species and taxaber of species with distinctly bicol- leaves are smaller in dimension (at (Parkhurst 1978). Mott and Michael-ored leaves (with the top side darker least width, if not also length) but son (1991) reported that increasedthan the bottom side) was greater in greater in thickness (e.g., De Soyza incident light generated an increasethe more mesic, shaded communi- and Kinkaid 1991, Johnson 1978, in both leaf thickness and the num- ties. Because these understory spe- Nobel 1991, Smith 1978). This re- ber of stomata on the upper leaf cies also had typical shade leaf struc- duced leaf dimension in sun leaves surface in Ambrosia cordifolia. Hav-ture, leaf bicoloration was strongly generates a significant increase in ing stomata on both sides of a thicker correlated with the thin, laminar leaf convective heat dissipation, an im- sun leaf may increase the supply of structure and horizontal leaf display. portant factor for plant survival in carbon dioxide to the mesophyll cellsSimilarly, leaf bicoloration was drier, high-sun habitats, where over- (Mott et al. 1982, Parkhurst 1994, nearly ubiquitous in understory heating and high transpiration rates Parkhurst and Mott 1990). These plants of the subalpine zone of the are detrimental (Gates 1980). studies provide evidence that the Rocky Mountains (Smith 1981). The greater leaf thickness charac- presence of stomata on both leaf Corresponding changes in leaf teristic of sun leaves results in a sub- surfaces greatly enhances carbon di- orientation and structure in response stantial increase in mesophyll cell oxide supply to the greater meso- to seasonal changes in stress is an- surface area for carbon dioxide ab- phyll cell area found in thicker sun other example of the strong interac- sorption, providing a structural leaves, both of which may be neces- tion between leaf structure and ori- mechanism for the observed increases sary to support the greater photo- entation. For example, the numerous in photosynthesis per unit leaf area, synthetic rates per unit leaf surface drought-deciduous species in the even though photosynthesis per unit area. Thus, both stomatal distribu- deserts of the southwestern United leaf biomass may remain unchanged tion and mesophyll cell area contrib- States develop large, ephemeral (Nobel 1980). A greater mesophyll ute to the higher rates of photosyn- leaves with horizontal orientation cell area also generates greater wa- thesis in sun leaves. soon after rainfall (Beatley 1974). ter-use efficiency because of the sub- In a recent study, leaf structuralAs the soil dries, these initial leaves stantially greater impact on carbon and orientational data were collected are replaced by smaller, more in- dioxide uptake than transpirational for numerous evergreen species fromclined leaves. With increasing soil water loss. For species native to the five communities in Western Austra- dryness, numerous species shed these most sun exposed, stressful habitats lia to evaluate possible associations leaves and only green stems remain, (e.g., desert shrubs, subalpine and between leaf structure and orienta- generating a more inclined arrange- boreal conifer trees), smaller, thicker tion (Smith et al. in press). These ment of curved photosynthetic sur- leaves become almost cylindrical, communities occur along opposing faces within the crown. Smith and with a more inclined leaf orienta- gradients in annual rainfall and daily Nobel (1977, 1978) also reported tion. Similarly, photosynthetic stems incident sunlight due to an increase that high incident light had the great- commonly replace true leaves in ev- in understory species in the more est effect on leaf morphology (e.g., ergreen shrubs of hot deserts, and mesic communities. At the time of size, thickness, pubescence) and 788 BioScience Vol. 47 No. 11 This content downloaded from 64.189.4.202 on Wed, 09 Oct 2024 03:00:10 UTC All use subject to https://about.jstor.org/terms Table 1. Influence of incident sunlight and stress level of the habitat on leaf orientational and structural characteristics and on photosynthetic potential in 234 species (86 families) of native plants (sampled predominantly from five Western Australia communities). Modified slightly from Smith et al. 1997. Environmental conditions High sun,a High sun, Low sun,a Low sun, Leaf form low stressb high stressb low stress high stress Orientation Horizontal; tracks the sun Vertical or cylindrical; Horizontal Horizontal avoids the sun Top-to-bottom ratio of >3.5c