Construction and maintenance mechanisms of efficient photosynthetic systems at three different scaling …

• Abstract
• Introduction
• The nitrogen optimization theory
• Meaning of leaf thickness
• Mechanisms responsible for optimum nitrogen allocation within herbaceous plants
• Analyses of the tree photosynthetic system
• Concluding remarks
• Literature cited
• Figures

Biology Articles » Anatomy & Physiology » Physiology, Plant » Construction and Maintenance of the Optimal Photosynthetic Systems of the Leaf, Herbaceous Plant and Tree: an Eco-developmental Treatise » Meaning of leaf thickness

Meaning of leaf thickness

- Construction and Maintenance of the Optimal Photosynthetic Systems of the Leaf, Herbaceous Plant and Tree: an Eco-developmental Treatise

 

 
CO₂ diffusion from the air to the chloroplast stroma
Because the problem of leaf thickness is closely related to CO₂ diffusion, CO₂ diffusion within a leaf will be considered first (Fig. 3). In photosynthesizing C₃ leaves, CO₂ concentration in the substomatal cavity, C_s, is lower than that in the ambient air, C_a, and CO₂ diffuses into the leaf along the gradient of CO₂ concentration. C_s can be estimated by the gas exchange technique. In a vigorously photosynthesizing leaf, the bulk CO₂ concentration in the intercellular spaces, C_i, is lower than C_s due to the resistance to CO₂ diffusion in the intercellular spaces (Parkhurst, 1994). CO₂ concentration in the chloroplast stroma, C_c, in C₃ plants is even lower than C_i. Recent technological innovations, including pulse-modulated fluorometry and concurrent measurement of carbon isotope discrimination and gas exchange, have enabled us to estimate C_c. For some species, C_c as low as half of C_a was reported (for a review, see Evans and Loreto, 2000). This indicates that resistance to CO₂ diffusion from the ambient air to the chloroplast stroma is substantial.

Conductance for CO₂ diffusion through stomata (g_s) has been well studied and the drawdown of CO₂ concentration, C_a – C_i, is about 60–120 µmol mol^–1 when C_a is 360 µmol mol^–1 (Evans and Loreto, 2000). Stomatal conductance can be approximated as:

gs = naD / (π r /4 + l)

(3)

where n is stomatal density (m^–2), a is stomatal pore area in m², D is binary diffusion coefficient of CO₂ in the air. In this approximation, a stoma is assumed to be a tube having radius r (m) and length l (m), respectively (Meidner and Mansfield, 1968). When stomata are open, na would be 0·005–0·02. Let us assume r is 5 µm and l is 10 µm. At 25°C, D is 1·55 x 10^–5 m² s^–1. Then, g_s ranges from 5·6 to 23 mm s^–1 or 0·22 to 0·86 mol CO₂ m^–2 s^–1. These are comparable to the reported stomatal conductance.

Similarly, the conductance in the intercellular spaces is approximated as g_ias = Dp/d, where p is porosity, is tortuosity of the mesophyll intercellular spaces, and d is distance for CO₂ diffusion. p usually ranges from 0·2 to 0·5. Let us assume = 1·5, for instance. Given that d is 100 µm (the average value for the leaf having a 200-µm-thick mesophyll), g_ias would range from 10 to 50 mm s^–1 or, from 0·8 to 2·0 mol CO₂ m^–2 s^–1. For the amphistomatous leaves, g_ias further increases by three- to four-fold (Parkhurst et al., 1988; Terashima et al., 2001). These values are much larger than the maximum stomatal conductance. Thus, it is unlikely that g_ias is a major limiting factor of leaf photosynthesis, in particular, in amphistomatous leaves.

The internal conductance (g_i), the conductance for CO₂ diffusion from the surface of mesophyll cell walls to the chloroplast stroma, via plasma membrane, cytoplasm and chloroplast envelope, is not very large, although it had been frequently assumed to be infinite. Evans and Loreto (2000) summarized the data on g_i which ranges from 0·03 to 0·6 mol CO₂ m^–2 s^–1 bar^–1. At the atmospheric pressure of 1 bar (101 kPa), these g_i values correspond to 0·03–0·6 mol CO₂ m^–2 s^–1 of mature leaves and appear to differ depending on plant functional types (Fig. 4). g_i values for annual herbs such as crop species are greatest and range from 0·2 to 0·6 mol CO₂ s^–1 bar^–1 (Evans and Loreto, 2000). On the other hand, the values of evergreen broad-leaved trees are much lower, ranging from 0·03 to 0·2 mol CO₂ m^–2 s^–1 bar^–1 (Hanba et al., 1999; Evans and Loreto, 2000). In mesic deciduous trees, g_i values are intermediate between those of annual herbs and evergreen trees. Among them, g_i values for the tree species that develop leaves successively appear to be greater than those for flush type species (Hanba et al., 2001). Castanea sativa, a Mediterranean deciduous chestnut, had g_i of 0·1 mol CO₂ m^–2 s^–1 bar^–1 (Lauteri et al., 1997). This is the lowest record for deciduous trees and is comparable to those of evergreen trees.

 
g_i in a pioneer clonal plant Polygonum cuspidatum (= Reynoutria japonica; Kogami et al., 2001; Sakata et al., 2002) decreased with increasing altitude: g_i for the plants at the altitude of 10 m was 0·2 mol CO₂ m^–2 s^–1 bar^–1, while that for the plants at 2500 m was 0·076 mol CO₂ m^–2 s^–1 bar^–1 (Kogami et al., 2001). If this effect of altitude on g_i is general, the trend of changes in carbon isotope composition with altitude (Körner et al., 1988) can be explained.

It has been shown that internal conductance increases with the increase in cumulated surface area of chloroplasts that face the intercellular spaces (S_c; Evans and Loreto, 2000). This indicates that increasing the effective area for CO₂ dissolution increases internal conductance. In this respect, it is noteworthy that thick sun leaves have larger S_c than thin shade leaves. Although the surface area of mesophyll facing the intercellular spaces (S_mes) is not as good a parameter as S_c, g_i for the species of the same functional type appears to be roughly proportional to S_mes. The decrease in distance from the mesophyll surface to the plasma membrane by having thin cell walls should be effective in increasing internal conductance because diffusion of CO₂ in water is lower than that in air by 10^–4. On the other hand, low g_i values in evergreen tree leaves (Hanba et al., 1999; Miyazawa and Terashima, 2001) and alpine plants can be attributed to thick mesophyll cell walls.

Interestingly, g_i can change drastically without marked changes in S_c and/or cell wall thickness. For example, the decrease in g_i was reported for the plants under water stress (Flexas et al., 2002) or salt stress (Delfine et al., 1998, 1999) conditions. These studies indicate that CO₂ permeability of membranes would change. Aquaporins, the most abundant proteins in plant plasma membranes, mainly transfer water molecules according to the gradient of the water potential. However, it was shown that animal aquaporin 1 transports CO₂ as well as water (Cooper and Boron, 1998; Nakhoul et al., 1998; Yang et al., 2000). In these studies, Xenopus oocytes and/or liposomes were used and the CO₂ permeability was monitored as changes in pH.

g_i were estimated based on concurrent measurements of gas exchange and fluorescence in the leaves of Vicia faba and Phaseolus vulgaris, in the presence or absence of HgCl₂, a potential inhibitor of most of the aquaporins. Because g_i and hydraulic conductivity of the mesophyll cells decreased at the same concentration range of HgCl₂, it is proposed that aquaporins are involved in diffusion of CO₂ across the plasma membrane (Terashima and Ono, 2002). Temperature dependence of g_i also indicated involvement of protein(s) in CO₂ diffusion from the intercellular spaces to chloroplast stroma (Bernacchi et al., 2002). Very recently, it was shown that the aquaporin 1 from Nicotiana tabacum transfers CO₂ using Xenopus oocytes (Uehlein et al., 2003). The study of Hanba et al. (2004) on transgenic rice plants, in which barley aquaporin was overexpressed, also confirmed their proposal; with the increase in aquaporin abundance, g_i clearly increased. Besides abundance of aquaporin, conductance for CO₂ through aquaporin could also be regulated by pH (Tourmaire-Roux, 2003), and by phosphorylation (Maurel et al., 1997; Kjellbom et al., 1999). In summary, g_i is determined by S_c, wall thickness, and by abundance and the state or conductivity of aquaporins.

Why are sun leaves thicker than shade leaves?
When expressed on leaf area basis, the light-saturated rate of leaf photosynthesis in C₃ plants strongly depends not only on n_L, contents of the photosynthetic components including Rubisco, cytochrome f, H⁺-ATPase and reaction centres but also on structural parameters such as leaf thickness, leaf mass per area, mesophyll surface area (S_mes) and chloroplast surface area (S_c). The correlation between P_max and S_c is generally stronger than that between P_max and S_mes. Because diffusion of CO₂ in water is 10^–4 of that in the air, the flux via the pathway like b in Fig. 3 should be negligible compared with that of pathway a. Then, it is useless to have mesophyll cell surfaces without chloroplasts (Miyazawa et al., 2003). In fact, when grown with sufficient nutrients, most of the mesophyll cell surfaces facing the intercellular spaces are occupied by chloroplasts, although some unoccupied spaces are indispensable for the plants to re-acclimate to a brighter light environment (Oguchi et al., 2003).

Thickness of chloroplasts is also important. The drawdown of CO₂ concentration from the intercellular spaces to the stroma, C_i – C_c, is proportional to the flux of CO₂ across the liquid phase (including cell wall, plasma membrane, cytosol and chloroplast envelope) per unit chloroplast surface area and to the resistance to CO₂ diffusion from the intercellular spaces to the stroma per unit chloroplast surface area. With the increase in the amount of Rubisco per unit chloroplast surface area, photosynthetic rate per unit chloroplast surface area increases. However, the photosynthetic rate per Rubisco decreases because C_c decreases. From the viewpoint of efficiency of Rubisco use (or nitrogen use), thicker leaves with greater S_c would be advantageous because the amount of Rubisco per unit chloroplast surface area becomes smaller, thereby Rubisco can operate at higher C_c. On the other hand, g_ias increases with leaf thickness, which causes a decrease in the bulk C_i. Moreoever, the construction and maintenance costs of thick leaves are expensive. In these aspects, thick leaves are not advantageous.

The effects of various aspects of mesophyll structure, in particular mesophyll thickness on photosynthesis, were evaluated, using a one-dimensional model of CO₂ diffusion in the leaf (Terashima et al., 2001). First the thickness that gives the maximum photosynthetic rate for leaves with various Rubisco contents per leaf area was calculated. Interestingly, the maximum rate of photosynthesis occurred at an identical mesophyll thickness irrespective of Rubisco content per leaf area. Obviously, this does not explain why sun leaves are thicker than shade leaves. The construction/maintenance cost of the leaf was then taken into account. In this calculation, the mesophyll thickness was regarded as the cost. The mesophyll thickness that realized a given photosynthetic rate per unit mesophyll thickness was compared in model leaves with various Rubisco contents per leaf area. It was found that, with an increase in the Rubisco content per leaf area, the mesophyll thickness that realized a given photosynthetic rate per unit mesophyll thickness increased. This kind of constraint probably explains the strong relationship between the maximum rate of photosynthesis and leaf morphological parameters such as mesophyll thickness. In other words, leaf thickness is determined as a compromise between the increase in chloroplast surface area for CO₂ dissolution and the decrease in the cost of the leaf.

In these simulations, the increase in mesophyll thickness simultaneously means a decrease in g_ias, an increase in S_c and an increase in construction and maintenance carbon costs of the leaf. Alternatively, the leaf can increase S_c and g_ias by decreasing cell size. The leaf with smaller cells is also mechanically tougher. Although xeric or alpine plants show such tendency, leaves do not have very small cells. This could be because leaves exhibiting considerable rates of leaf area expansion, adequate heat capacitance, high efficiency of resource use, etc. have been favoured by natural selection (Terashima et al., 2001).