Fig. 4.6A, B Correlation between photosynthetic capacity and nitrogen levels in leaves of: A Pisum hispidum (closed symbols) and Pisum auritum (open symbols); B Diplacus aurantiacus (closed symbols) and Solidago altissima (open symbols). r correlation coefficients. (After: A Field 1988; B Evans 1988)
Reich et al. (1994) have presented a detailed investigation of these relations performed in two open and disturbed sites and three late successional forest types in the Amazon basin, which differed in light climate and nutritional status (Fig. 4.7). Photosynthesis-N relations are steepest and intercepts on the x-axis (N-levels) are highest in the disturbed open habitats with high resource acquisition and rapid plant growth (lines a and b in Fig. 4.7A,B), which also have the highest rates of photosynthesis (sun plants). Among the other sites, under N-limitation curves were steeper (lines d and e in Fig. 4.7A) than when P plus Ca were more deficient (line c in Fig. 4.7A). This was somewhat less clearly seen, when leaf N was expressed on a leaf area basis (Fig. 4.7B) as compared to the leaf mass basis (Fig. 4.7A), so that besides species and site characteristics a certain effect of the basis of data expression, i.e. mass or leaf area is also noted.
Leaf nitrogen (mmol m"2)
Leaf nitrogen (mmol m"2)
Fig. 4.7A, B Photosynthesis/leaf-nitrogen relationships in five different forest types near San Carlos de Rio Negro, Venezuela (1°56r N, 67°03r W) at ~ 100 m a.s.l. in the north central Amazon basin. Disturbed sites, high resource regeneration sites: a cultivated, and b early secondary suc-cessional Tierra Firme plots. Late successional forest types: c Tierra Firme, P- and Ca-limited; d Caatinga, N-limited; e Bana, P- and N-limited. Curves were drawn from the y-intercepts and slopes of linear regressions given by Reich et al. (1994) for the various samples of a total of 23 species, which they studied at the five sites. The lengths of the lines in each case indicate the range in which points were obtained. Results are expressed on a mass basis (A) as well as on an area basis (B)
4.1.3 The Origin of High-Irradiance Stress and General Plant Responses
The biological stress concept has shown us that stress can result from low or high dosage of any particular environmental factor (Box 3.1). In sun plants increased chlorophyll a/b ratios and a comparatively small size of chlorophyll a and b binding antennae (Sect. 4.1.2) contribute to protection from too high irradiance (Krause et al. 2001). Conversely shade plants, or phenotypes considered in Sects. 4.1.1 and 4.1.2, are adapted to low irradiance stress typical of the interior of dense forests. Stress by high irradiance might generally appear to be more characteristic of open habitats like savannas. However, it is also found in deciduous and semi-deciduous dry forests and in the upper canopy of wet forests. Moreover, in view of the very high light intensities of some light flecks (Sect. 4.2.1), it may even be a particular problem for the shade-adapted plants in the understory of moist forests. Finally, shade plants of the forest floor may be suddenly exposed to high irradiance when gaps are created by falling trees. Hence, it is necessary to address of how plants avoid damage from excess irradiation. Strategies of avoidance include vertical leaf angles and small lamina areas (He et al. 1996) and chloroplast movements (Augustynowicz and Gabrys 1999; Gorton et al. 1999).
With respect to excess absorbed irradiance first it is necessary to recall the various states of excitation and relaxation of chlorophyll in the photosystems (Box 4.3). Excitation to the 2nd singlet level follows absorption of photons of blue light, while red light causes excitation to the 1st singlet level. Relaxation from the 2nd singlet state occurs by emission of heat, while there are several ways of relaxation from the 1st singlet state to the ground level. The normal means of energy dissipation in photosynthesis is photochemical work (Box 4.3), i.e. the eventual reduction of CO2 fixed via RuBISCO. This, however, under certain circumstances may become a limiting process, e.g. due to:
• low intercellular CO2-concentrations in leaves due to high CO2-fixation rates following over saturation of the photosynthetic apparatus by PPFD,
• closure of stomata to reduce transpirational loss of water in response to high irradiance and heat with the concomitant consequence of low intercellular CO2-concentrations,
• general over excitation of the photosynthetic apparatus and over reduction of the redox-elements of the photosynthetic electron-transport chain (see Box 4.2).
Box 4.3 Light absorption, chlorophyll excitation and relaxation
Absorption spectra of the reaction-centre pigment chlorophyll a and the antenna pigments chlorophyll b and caro-tenoids (see Box 4.2).
Box 4.3 (Continued)
B. Ground state and excitation states with substates (horizontal lines) and relaxation of chlorophyll:
Absorption of the more energy-rich blue-light quanta (shorter wave-lengths)
leads to the second and third excited singlet state (half-life 10-14 -10-15 s). Absorption of the less energy-rich red-light quanta (longer wavelengths) leads to the first excited singlet state (half-life 10-9 -10-11 s). Relaxation can occur by transition between systems, and energy is dissipated as heat. Transition from the first singlet state to the triplet state (half-life 10-410-2 s) is only probable when the whole system is overexcited. Relaxation from the first singlet state to the ground state in addition to energy dissipation as heat can occur by emission of light as fluorescence. Relaxation from the triplet state to the ground state is possible by the emission of light as phosphorescence. Energy transfer from the first singlet state and the triplet state can lead to photochemical work, i.e. CO2-assimilation or photorespiration in the case of the first singlet state and formation of oxygen radicals and photodamage in the case of the triplet state.
Overall there is a set of several means of dissipating excitation of chlorophyll a in photosystem II (see Boxes 4.3 and 4.4):
• PS II photochemistry, due to CO2 or O2 binding,
• relaxation by emission as fluorescence (Sect. 4.1.7),
• relaxation by energy transfer to photosystem I,
• transfer of excitation from the 1st singlet state to the triplet state, which is correlated with a change of electron spin from antiparallel to parallel.
One valve for dissipation of surplus energy is photochemical work. Increased contents of electron-transfer-chain components and RuBISCO are, of course, protec tive (Ramalho et al. 1999). A photochemical work different from CO2 assimilation is photorespiration. This is possible, since RuBISCO (ribulosebisphosphate carboxylase/oxygenase) not only reacts with CO2 but also with O2 and can oxygenate ribulosebisphosphate to form phosphoglycolate, which is metabolized in the pho-torespiratory reaction cycle. However, this still may be of limited capacity to avoid adverse effects of overenergization, which leads to photoinhibition. The primary site of photoinhibition is photosystem II. It can be protected by energy dissipation as heat which is correlated with chlorophyll fluorescence. These are important functions which need to be treated in separate sections (Sects. 4.1.4 and 4.1.7, respectively).
Energy transfer to photosystem I is also called spill over. Intact photosystem II in higher plants is located in the appressed thylakoid regions of chloroplast grana (Box 4.2) but for spill over the peripheral light harvesting complexes of photosystem II get phosphorylated by a specific kinase and are transferred to the stroma region of the thylakoids. This is a reversible process highly regulated by irradiance and the redox state of plastoquinone, PQH2 (see Box 4.2).
The triplet state is much more stable, i.e. it has a much longer half-life, than the two singlet states. Therefore, it may lead to the formation of reactive oxygen species and oxygen radicals with the subsequent destruction of pigments, lipids and membranes. Radical scavengers or antioxidants are a number of redox substances, such as dihydroascorbate, reduced glutathione and for the chloroplast especially tocopherol (Krieger-Liszkay and Trebst 2006) and the enzymatic reactions of superoxide dismutases. The xanthophyll cycles of chloroplasts also are mechanisms for the scavenging of highly reactive singlet oxygen (Sect. 4.1.4).
4.1.4 Dissipation of Excitation Energy in the Form of Heat: The Role of Xanthophylls
Dissipation of surplus excitation energy in the form of heat is mediated by cycles of xanthophylls. The zeaxanthin cycle is one of the most important photoprotec-tional mechanisms in photosynthesis (Demmig-Adams et al. 1996; Gilmore 1997; Gilmoreand Govindjee 1999). It binds harmful singlet activated oxygen (xOj) andis a futile cycle in terms of energy turnover. The basic metabolic reactions are shown in Box 4.4. The xanthophylls of the zeaxanthin cycle are peripherally associated with the light harvesting complex of photosystem II, LHCII (Horton and Ruban 2005). Singlet activated oxygen is bound in the formation of the epoxides antheraxanthin and violaxanthin from zeaxanthin, which also requires redox energy in the form of NADPH + H+. The zeaxanthin cycle only functions when a trans-thylakoid proton gradient, ApH, is built up by photosynthetic electron transport. The ApH otherwise used to power photophosphorylation is the primary controlling factor of the zeax-anthin cycle. ApH and the electrons are used for deepoxidation and the return of the cycle to zeaxanthin when the originally harmful oxygen is eventually reduced to water and the energy of redox equivalents, electrons and ApH across the thylakoid
The zeaxanthin-cycle scheme was originally proposed by Hager (1980) and later forcefully propagated by Demmig-Adams (1990), Demmig-Adams and Adams (1992) and Pfündel and Bilger (1994). The turnover in the cycle involves detoxification of singlet activated oxygen ^O;) and energy dissipation, namely binding of activated oxygen by oxidation of zeaxanthin to violaxanthin (epoxidation) and dissipation of the energy of photosynthetic electron transport by rereduction (deepoxidation) to zeaxanthin. The epoxidase is located on the stroma side and the de-epoxidase on the thylakoid-lumen side of the thylakoid membrane, and the pH optima of the epoxidase (pH 7.5) and the deepoxidase (pH 5.2) correspond to the prevailing conditions in the chloroplast stroma and the thylakoid interior, respectively. The deepoxidase is mobile within the thy-lakoid lumen at neutral pH but becomes membrane-bound when the pH drops and a pH gradient is established across the thylakoid membrane by photosyn-thetic electron flow (Hager and Holocher 1994); it has a narrow pH optimum at pH 5.2 and is presumed to be activated by the photosynthetic electron transport via acidification of the lumenal pH (Büch et al. 1994). Ascorbate is a cofactor in the deepoxidation reaction (not drawn in the cycle itself).
An additional xanthophyll-cycle is the lutein/lutein-epoxide cycle. While zeaxanthin has two ß-ionon rings and can form two epoxides, lutein has one a-ionon ring and only one ß-ionon ring, and therefore, can form only one epoxide. The deepoxidase is the same as in the zeaxanthin-cycle (violaxanthin deepox-idase), while the epoxidase either is the same as the zeaxanthin epoxidase or a homologous enzyme (Matsubara et al. 2001, 2003).
membranes is effectively dissipated as heat. The zeaxanthin cycle directly protects PSII rather than PSI but may indirectly protect also PSI by restricting electron flow (Barth et al. 2001).
As an alternative, or in addition, to their function in the futile zeaxanthin cycle, xanthophylls may be involved in directly affecting the structure of the light-harvesting complex itself (Horton et al. 1994) and thus diverting excitation by absorbed photons from the reaction centre of photosystem II (PSII). Zeaxanthin can bind to the internal binding site of the xanthophyll lutein in LHCII (Horton and Ruban 2005). Zeaxanthin binds in dependence of ApH at the thylakoid membrane (Gilmore 1997; Gilmore and Yamasaki 1998; Gilmore et al. 1998; Gilmore and Govindjee 1999) causing conformational changes of the system, possibly involving aggregation of the light-harvesting complex of PSII, which may be facilitated by an absence of violaxanthin and/or a presence of zeaxanthin and converting the reaction centre of PSII into a centre dissipating heat (Bilger and Björkman 1994; Horton et al. 1994; Gilmore et al. 1996; Horton and Ruban 2005) through charge separation of a chlorophyll-zeaxanthin heterodimer (Holt et al. 2005). This mechanism operates under prolonged and very extreme excessive light, while the zeaxanthin cycle responds to much lower and variable levels of excess light (Gilmore et al. 1996).
Box 4.4 (Continued)
Box 4.4 (Continued)
Independent of the zeaxanthin-cycle, zeaxanthin can also directly function as an antioxidant and prevent lipid oxidation removing epoxy groups from fatty acids, where violaxanthin formation provides protection against lipid peroxidation (Schindler and Lichtenthaler 1996; Baroli et al. 2003).
Thus, three possible xanthophyll mechanisms are listed by Schindler and Lichtenthaler (1996), namely:
• reaction of zeaxanthin with highly reactive oxygen species and the futile energy dissipating zeaxanthin cycle,
• aggregation/dissociation of the light-harvesting complex,
• reaction of zeaxanthin with reactive oxygen species.
An additional xanthophyll-cycle is the lutein/lutein epoxide cycle (Box 4.4). Lutein is an intrinsic component of the light harvesting complex of PSII. It facilitates enhanced photoprotection through its superior singlet and/or triplet chlorophyll quenching (Matsubara et al. 2005). The lutein cycle operates in parallel to the zeaxanthin-cycle in some plants, e.g. in mistletoes (Sect. 6.5) and the tropical Fabaceae Inga (Matsubara et al. 2001,2003, 2005).
Over energization of the photosynthetic light harvesting apparatus is always a potential danger and ecophysiologically the xanthophylls provide an important protective machinery for many circumstances. Plants permanently exposed to full sunlight have effective protective mechanisms (Krause et al. 2006) and young leaves develop them to a higher degree than mature leaves (Krause et al. 1995). Zeaxanthin-cycle dependent energy dissipation is an extremely flexible process and can kinetically respond within seconds to minutes. Via adaptive changes of pool sizes of the xan-thophylls time-scales of days up to seasons can be covered (Demmig-Adams et al. 1996). Ecophysiologically the zeaxanthin-cycle, for example, is operative in the light-exposed phenotypes of bromeliads in the tropics, zeaxanthin was only detected in the yellow high-light plants of Bromelia humilis (see Fig. 4.3) and not in the shade plants (Fetene et al. 1990) and also plays a significant role in Guzmania monostachia (Maxwell et al. 1994, 1995). A survey of several other sun and shade plants including tropical rainforest species also showed that sun plants possessed larger xantho-phyll pools and greater maximal zeaxanthin and antheraxanthin contents than shade plants. Sun plants displayed a greater maximal capacity for photoprotective energy dissipation via the pigments than plants acclimated to very low irradiance, and in sun leaves the reduction state of PSII at full sun light remained at a much lower level than in shade leaves (Demmig-Adams and Adams 1994; Gilmore 1997). In the vertical light gradients in tropical forests levels of zeaxanthin-cycle pigments increase from the forest floor to the canopy (Logan et al. 1996). Xanthophyll pool size and zeaxanthin-cycle activity are also enhanced when photosynthesis is under nitrogen limitation (see Figs. 4.6 and 4.7) (Toth et al. 2002; Cheng 2003).
4.1.5 Damage and Repair of Reaction Centres of Photosystem II: The D\-Protein
Turnover in the xanthophyll-cycle can be very rapid. Alternatively to energy dissipation as heat and especially in the absence of xanthophyll-cycle associated photoprotection (Thiele et al. 1997) a slower process develops, which is irreversible when protein biosynthesis is inhibited. It is due to a functional dissociation between the reaction centres and antennae of photosystem II (see Box 4.2; Demmig-Adams and Adams 1993). The reaction centres of photosystem II are built up of one copy each of a Di- and a D2-protein. The destruction of these proteins prevents coupling of excitation and electron transport via the light trap reaction centres because in the light harvesting complex of PSII (LHCII) excitation is passed to plastoquinone (Q) via the D1-protein. Repair needs protein synthesis (Box 4.5). The D1-protein is al ways destroyed by light even at rather low intensities. Repair is most effective at low irradiance (30|molm-2s-1). The D1-protein is always under turnover, but at high irradiance and without photoprotection repair mechanisms are too slow resulting in damage of D1 in the LHCII (Tyystjärvi and Aro 1996; He and Chow 2003), where light stress is amplified by high temperature stress (Königer et al. 1998). However, this damage which is slowly reversible in the turnover of D1-protein destruction and resynthesis (Box 4.5) is also a mechanism of photoprotection as it inhibits over reduction of the photosynthetic electron transport chain.
Box 4.5 Damage and repair of the reaction centres of photosystem II in light-stress and recovery cycles
Under high light intensities (HL) the Di-protein is first modified reversibly and recovery needs low light intensities (LL); (1). Under further stress the D1-protein is damaged irreversibly (2) and repair needs protein synthesis (3). The turnover of the D2-protein is slower although it also can be damaged irreversibly by light stress (Schäfer and Schmid 1993; Critchley and Russel 1994).
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