JXB Advance Access originally published online on October 22, 2004
Journal of Experimental Botany 2005 56(411):461-468; doi:10.1093/jxb/eri012
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RESEARCH PAPER |
Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may ‘lock-in’ lutein-based photoprotection during acclimation to strong light
1Photobioenergetics Group, Research School of Biological Sciences, Australian National University, Box 475 Canberra, ACT 2601, Australia
2Biosphere 2 Center, Columbia University, Oracle, AZ 85623, USA
3Dipartimento Scientifico e Tecnologico, Università di Verona, Strada Le Grazie 15, 37234 Verona, Italy
¶ Present address and to whom corresponence should be sent: School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia. Fax: +61 2 6125 0313. E-mail: barry.osmond{at}anu.edu.au
Received 21 April 2004; Accepted 16 August 2004
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Abstract |
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The kinetics of response to strong light have been examined in deeply shaded leaves of the tropical tree legume (Inga sp.) which have extraordinarily high levels of the
-xanthophyll lutein-epoxide that are co-located in pigment–protein complexes of the photosynthetic apparatus with the ß-xanthophyll violaxanthin. As in other species, rapidly reversible photoprotection (measured as non-photochemical chlorophyll fluorescence quenching) is initiated within the time frame of sun-flecks (minutes), before detectable conversion of violaxanthin to antheraxanthin or zeaxanthin. Photoprotection is stabilized within hours of exposure to strong light by simultaneously engaging the reversible violaxanthin cycle and a slowly reversible conversion of lutein-epoxide to lutein. It is proposed that this lutein ‘locks in’ a primary mechanism of photoprotection during photoacclimation in this species, converting efficient light-harvesting antennae of the shade plant into potential excitation dissipating centres. It is hypothesized that lutein occupies sites L2 and V1 in light-harvesting chlorophyll protein complexes of photosystem II, facilitating enhanced photoprotection through the superior singlet and/or triplet chlorophyll quenching capacity of lutein. Key words: Inga sp., lutein-epoxide, photoacclimation, photoprotection, photosynthesis, xanthophyll cycles
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Plant leaves are exposed to light intensities from darkness to full sunlight on a daily basis and adjust photosynthetic activity over four orders of magnitude in photon flux. The photosynthetic apparatus maintains high efficiencies of light use in shade, while engaging rapidly reversible mechanisms for tolerating excess light (photoprotection; Demmig Adams and Adams III, 1992
; Horton et al., 1996; Niyogi, 1999), for repair of damage (photoinactivation; Aro et al., 1993; Chow et al., 2002) that inevitably occurs in the highly energetic, primary photochemical processes in the reaction centres, and for photoacclimation in response to sustained changes in light environment (Osmond et al., 1999). There is now an extensive literature based on in vivo (Hurry et al., 1997; Verhoeven et al., 1999) and in vitro studies (Ruban et al., 1993, 1999; Bassi et al., 1993; Ruban and Horton, 1995) that deal with mechanistic aspects of xanthophyll pigment-dependent photoprotection (Bassi and Caffarri, 2000; Horton et al., 2000). Recent research, ranging from ecology (Gilmore and Ball, 2000; Matsubara et al., 2002) to molecular genetics (Niyogi, 1999; Li et al., 2000, 2002a) to photobiophysics (Gilmore, 2001; Li et al., 2002b) has established the central importance of a light-driven cycle of ß-xanthophylls (V-cycle) in photoprotection.
In the earliest reports of the V-cycle (Demmig et al., 1987) the identity of the antheraxanthin peak on HPLC was uncertain, and it was listed as possibly lutein-epoxide (Lx), an -xanthophyll first noted in the tissues of green tomato fruit (Rabinowitch et al., 1975). Small amounts of Lx are frequently found in leaf tissues of different species (Young, 1993) and it is commonly reported in TLC surveys of lichen pigments (Czeczuga et al., 1996). Subsequent research has confirmed that an additional cycle of -xanthophylls (Lx-cycle; interconversion of Lx-lutein; Lx
L) is present in the photosynthetic tissues of the parasite dodder (Cuscuta reflexa Roxb.; Bungard et al., 1999; Snyder et al., 2004), in leaves of mistletoes in the Loranthaceae (Amyema miquelii (Lehm. Ex Miq.) Tiegh.; Matsubara et al., 2001, 2002, 2003), and in leaves of Quercus spp. (García-Plazaola et al., 2002, 2003). Structural analogies between AZ and LxL interconversions by violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZE) suggest that the Lx-cycle could serve as an additional, more slowly relaxing mechanism for ‘sustained energy dissipation in understorey leaves after the occurrence of the first sun-fleck or the formation of gaps within the forest canopy’ (García-Plazaola et al., 2003).
Operation of the Lx-cycle also raises the enigmatic role of lutein in photoprotection (Pogson and Rissler, 2000; Gilmore, 2001). It is shown here that shade leaves of another exotic plant, the tropical tree legume (Inga sp.) contain extraordinarily high levels of Lx that are co-located in photosynthetic membranes with V. Kinetic experiments with these tissues show that the quantitative conversion of Lx to L is only slowly reversible, and suggest that a re-evaluation of current concepts of xanthophyll functions in photoprotection and photoacclimation may be necessary for these plants.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Leaves were used from 12-year-old, 10–15 m high trees of Inga sp. (tentatively identified as Inga sapindoides Willd., native in central and western South America; T Pennington, personal communication) that were grown in the demonstration laboratories (DL) and the enclosed controlled environment tropical forest mesocosm (TFM; Leigh et al., 1999
) of the Biosphere 2 Laboratory (B2L; Osmond et al., 2004). Leaves in different parts of the canopy were accessed with ladders, climbing ropes, and a hydraulic lift, to facilitate photosynthetic measurements with hand-held instruments. Leaf photosynthetic CO2-exchange was measured with a portable gas exchange system (model 6400 Li-Cor Inc., Lincoln, Nebraska) and fluorescence measurements in situ and in the laboratory were made with a mini-PAM (H Walz, Effeltrich, Germany).
Leaf discs (0.64 cm2) were prepared for laboratory measurements from leaves collected predawn and kept in the dark on moist tissue at 25 °C. They were illuminated at 630 µmol photons m–2 s–1 (from a quartz iodide projector lamp) and at each data point, Non-photochemical chlorophyll fluorescence quenching (NPQ) was measured on one disc from each leaf using a mini-PAM, before being frozen in liquid nitrogen for pigment analysis. The efficiency of PSII 
was calculated as 
where 
is the yield of chlorophyll fluorescence in a saturating flash in the light and Fs is the steady-state level of yield in the light (Genty et al., 1989). NPQ was calculated as 
where Fm is the yield of chlorophyll fluorescence in a saturating flash in dark-adapted leaves (Bilger and Björkman, 1990). Photosynthetic electron transport rate (ETR) was calculated as 
using measurements of incident PPFD on leaves at the time of fluorescence analysis and allowing for equal distributions of PPFD between both photosystems and a leaf reflectance of 16%.
During experiments in the canopy, discs were taken from the same areas of the leaf as used for fluorescence measurements in situ, were frozen in liquid nitrogen, and kept at –80 °C until analysis. Pigments were exhaustively extracted by grinding in a cooled mortar and pestle with 1 ml of 80% acetone/water followed by 2–4 ml of 100% acetone, centrifuged at 10 000 rpm for 5 min, and syringe filtered before separation by HPLC (Allsphere ODS-1 5 µ column; Jasco model PU 1580, AS 1555, HG 980–31, and MN 1510 multi-wavelength detector) using the solvents and protocols modified from Gilmore and Yamamoto (1991). Pigments were identified by retention times and absorption spectra, and quantified as described by Matsubara et al. (2001). Thylakoids were prepared from shade leaves of Inga sp. and isolated pigment–protein complexes were fractionated by sucrose density ultracentrifugation as described previously (Caffarri et al., 2001: Matsubara et al., 2003). The xanthophyll composition of different fractions was measured by HPLC.
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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The predawn pigment compositions of Inga leaves sampled from shade and sun parts of the DL canopy showed that Lx was more abundant in shade leaves in which its concentration exceed that of V by up to 3.5-fold (Table 1). Shade leaves always had higher levels of
-carotene than ß-carotene (Thayer and Björkman, 1990), and the -xanthophyll synthesis pathway, in which L is converted to Lx presumably by ZE, predominated in shade leaves. Similar data (shade 43, sun 15–30 mmol Lx mol–1 Chl; shade 33, sun 38–43 mmol V+A+Z mol–1 Chl) were observed early in the day in leaves sampled in situ over a 15 month period (n=11–22) in the TFM. De-epoxidation of the V-cycle pigments was measurable in the sun leaves ((A+Z)/(V+A+Z)=0.12–0.15), but not in shade leaves. Because the total Lx+L was similar in shade and sun leaves of the same plant, it seems plausible that Lx was converted to L by VDE in Inga leaves during shade–sun acclimation, analogous to the light-induced V
A+Z conversions of the V-cycle.
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Operation of the V-cycle and the possible operation of the Lx-cycle were investigated in situ in sun and shade leaves of Inga sp. throughout the day (Figs 1, 2). Sun leaves of plants in the DL that were exposed to high irradiances in the early afternoon achieved maximum assimilation rates of 8.5 µmol CO2 m–2 s–1 at a light intensity of 850 µmol photons m–2 s–1. They showed the expected decline in PSII efficiency (measured as
) and an increased capacity for the thermal dissipation of excess light in the afternoon (measured as NPQ) concurrently with the de-epoxidation of V (Fig. 1). Unexpectedly, however, the 4-fold lower Lx pool in sun leaves did not change significantly throughout the day and, in marked contrast to the recovery of the V pool, there was no evidence of epoxidation of L to Lx in the subsequent 5 h dark period. Shade leaves of Inga sp. growing in the DL had assimilation rates of only 0.6 µmol CO2 m–2 s–1 at a light intensity of 20 µmol photons m–2 s–1. They maintained high PSII photochemical efficiency, did not engage in thermal dissipation, and retained high Lx and V pools throughout the day (Fig. 1). Similar results were obtained with sun leaves of plants growing in the TFM (Fig. 2). These surprising results suggest that ZE has a very low affinity for, or access to, L in sun leaves (Matsubara et al., 2003) and that, compared with other species (Bungard et al., 1999; Matsubara et al., 2001; García-Plazaola et al., 2003), epoxidation reactions in the Lx-cycle may not be as responsive to rapid changes in light as in the V-cycle. Given the low levels of Lx in sun leaves, and the very slow epoxidation of L to Lx, it is questionable whether LxL functions as a cycle in Inga sp.
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The light-dependent activity of the V- and Lx-cycles and relationships to NPQ were examined further in deep shade leaves of Inga sp. by treating discs with simulated sun-flecks (white light at 600 µmol photons m–2 s–1). In short-term (6 min) experiments, NPQ increased rapidly, then quickly relaxed during the subsequent dark period (Fig. 3A) without detectable conversion of pigments in the V- or Lx-cycle (Fig. 3B). It is well known from experiments with mutants and inhibitors that quenching can be triggered by a mechanism activated within a 10–20 s exposure to excess light without significant de-epoxidation of xanthophylls (Pogson et al., 1998
; Niyogi, 1999; Horton et al., 2000). The rapid development of NPQ in the absence of pigment conversion (the qE component of qN; Horton and Hague, 1988) presumably reflects primary 
pH-dependent protein conformational changes in light-harvesting pigment–protein complexes (Ruban and Horton, 1995; Horton et al., 2000; Bassi and Caffarri, 2000), perhaps sensed by the psbS gene product (Li et al., 2000, 2002a, b), that convert them to exciton dissipating centres; the so-called Quenching 1 mechanism (Morisinotto et al., 2003). However, Finazzi et al. (2004) recently confirmed that, as proposed by Weis and Berry (1987), the initially rapid, zeaxanthin independent NPQ is a pH based mechanism in PSII core complexes rather than in the antenna. Intense illumination of shade leaves with low photosynthetic capacity would be expected to generate strong transthylakoid pH gradients quickly. This exciton dissipating function may be subsequently stabilized by conversion of Lx to L and fine-tuned by the reversible de-epoxidation of V to A+Z; the so-called Quenching 2 mechanism (Morisinotto et al., 2003). These kinetic experiments suggest it is most unlikely that either the V- or Lx-cycle has primary roles in photoprotection against sun-flecks of short duration in shaded leaves of this species.
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Stabilization of NPQ in Inga sp. by de-epoxidation of xanthophylls is indicated by acceleration of the kinetics, without increasing the amplitude, of NPQ in both shade and sun leaves following a 15 min induction period that facilitated some de-epoxidation. When comparing sun and shade leaves, NPQ increased slightly more rapidly, but to the same extent, in shade leaves (Fig. 3C), in spite of the faster conversion of V to A+Z in sun leaves after 6 min (shade 0.6–2.5; sun 1.5–12.5 mmol A+Z mol–1 Chl), and in spite of the higher, but unchanged, pool of L in sun leaves (shade 107; sun 140 mmol L mol–1 Chl). In both sun and shade leaves, the kinetics, but not the amplitude, of NPQ were accelerated by inducing photosynthesis for 15 min in 600 µmol photons m–2 s–1 and allowing dark relaxation for 30 min before repeating the dark-to-light transition. Again, NPQ developed faster in shade than in sun leaves (Fig. 3D), in spite of lower pool sizes of de-epoxidized xanthophylls (shade 6.6–7.6; sun 25.3–28.5 mmol A+Z mol–1 Chl), and higher, but unchanged, pools of L in sun leaves (shade 114; sun 156 mmol L mol–1 Chl). The relationships of these processes in Inga sp. to the qE and qI components of qN (Horton and Hague, 1988
; Horton et al., 1996) are not clear.
When long-term (180 min) sun-flecks were applied to shade leaves, NPQ increased to and maintained the same value as observed above, but was now accompanied by extensive de-epoxidation of both V and Lx (Fig. 3E, F). It was also noted that formation of L in parallel with de-epoxidation of Lx, which has always been assumed for plants with the Lx cycle (Rabinowitch et al., 1975; Bungard et al., 1999; Matsubara et al., 2001), but has thus far been demonstrated only in Quercus robur (García-Plazaola et al., 2002, 2003), was undoubtedly seen in shade leaves of Inga sp. in this experiment. Although V, A and Lx are substrates for VDE in vitro (Yamamoto and Higashi, 1978; Matsubara et al., 2003), the affinities for V and A (and probably for Lx) differ, and enzymes from different plants also seem to have different affinities for these substrates. Furthermore, it is difficult to compare the increase in L with the increase in A+Z as L and A can be synthesized by one-step conversion by VDE, while Z requires two steps. The nearly stoichiometric de-epoxidation of Lx into L that occurred concomitantly with the VA+Z conversion in shade leaves over the period of long-term sun-flecks simulation (Fig. 3E, F) contrasts with the very different responses of the Lx and V cycles observed in sun leaves in the in situ diurnal time-courses (Figs 1, 2). Thus, these results further support the notion that the distinct diurnal patterns of the two cycles in sun leaves of Inga sp. may primarily reflect different epoxidase activities.
In terms of the pigment conversion kinetics, the slowly reversible de-epoxidation of Lx to L is analogous to the slowly reversible de-epoxidation of V to Z in the sustained high levels of Z, which was mainly reported for plants exposed to bright light at low temperatures (Verhoeven et al., 1999; Gilmore and Ball, 2000; Matsubara et al., 2002). However, unlike the sustained high levels of Z, the ‘locked-in’ portion of L in sun leaves of Inga sp. does not result in pH-independent sustained fluorescence quenching, as can be inferred from the high Fv/Fm measured before dawn (Fig. 1A). Hence, in terms of the fluorescence kinetics and the requirement of pH formation, the slowly reversible Lx-L conversion seems to be more relevant to qE rather than qI. Interestingly, the nocturnally retained Z+A in two Yucca species growing in the Mojave Desert was engaged in the sustained energy dissipation only on a cold winter night, but not on a warm summer night (Barker et al., 2002). The situation of Yucca in summer may bear some analogy with the Lx-L in Inga sp.
Xanthophyll pigments are specifically distributed in pigment–protein complexes of photosynthetic membranes, and these distributions are related to structural and photobiophysical functions of the pigments (Caffarri et al., 2001; Snyder et al., 2004; Liu et al., 2004). Different photosynthetic membrane fractions from shade leaves of Inga were separated by sucrose density ultracentrifugation and it was found that the distributions of V and Lx were remarkably similar (Table 2). About 50% was found in the fraction containing trimeric light-harvesting antenna complexes of photosystem II (LHCII) with nearly 30% in the fraction containing photosystem I (LHCI). The result is consistent with previous reports on the localization of VAZ in Vinca major (Verhoeven et al., 1999) and of Lx in other plants containing this pigment (Matsubara et al., 2003; Snyder et al., 2004) and suggests that, potentially, Lx may be structurally and functionally equivalent to V. Notably, fluorescence excitation spectroscopic analysis showed that Lx bound to LHCII cannot transfer energy to Chl a (data not shown), a behaviour that has previously been described for V bound to the peripheral site V1 of LHCII (Ruban et al., 1999; Caffarri et al., 2001).
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In vitro studies using recombinant antenna proteins of PSII have shown that L binds to the binding site L1 in Lhcb proteins, whereas another site, L2, has lower specificity and can accommodate L, V, A, and Z depending on availability in protein environment (Caffarri et al., 2001
; Morosinotto et al., 2003). A recent X-ray structure of spinach LHCII indicated two molecules of L in the central part, with ß- and 
-rings oriented towards the lumenal and the stromal surface, respectively (Liu et al., 2004). Interestingly, the amount of L in the free pigment fraction in shade leaves of Inga sp. is 3–5 times lower than that found during the fractionation of thylakoids from maize, barley, and Arabidopsis using the same methods. Thus, it is proposed that, in shade leaves of Inga sp., Lx may eliminate L from the peripheral V1 site, which is located at the monomer–monomer interface and possibly enables efficient singlet excitation energy transfer from chlorophylls to xanthophylls (Liu et al., 2004). Under sustained light exposure L molecules synthesized by the de-epoxidation of high concentrations of Lx in the peripheral site V1 might occupy site L2 as well as V1, displacing V or Lx.
The slow conversion of L to Lx in Inga sp. demands explanation, for clearly the presence of large pools of Lx in shade leaves implies that ZE is active in these tissues. Species and tissues seem to differ markedly in the extent to which L serves as a substrate for ZE (Bouvier et al., 1996; Matsubara et al., 2003), and it is possible that even a low level of activity could lead to high levels of Lx in long-lived leaves in deep shade. Whatever the reason, slowly reversible conversion of Lx to L may provide an effective primary mechanism for sustained photoprotection, since L is a better quencher of singlet and/or triplet chlorophyll than V when bound to the L1 or L2 site of LHCII (Formaggio et al., 2001; Morosinotto et al., 2003). Further, LxL exchange within the peripheral V1 sites may also be involved in modulation of singlet chlorophyll quenching (Liu et al., 2004).
It is suggested that the zero DPS and high Lx condition in shade leaves of Inga sp. may facilitate efficient excitation transfer to reaction centres in weak light, whereas retention of large pools of L and the presence of Z or A might not (Caffarri et al., 2001). In effect, the LHCs might be converted from efficient light-harvesting centres to exciton-dissipating centres by the presence of high levels of L in the peripheral V1 and in the L2 site. Furthermore, the retention of large pools of Lx in deep shade potentially provides a readily available source of L for appropriate placement in LHCs, quickly locking-in sustained photoprotection during photoacclimation within a few h of exposure to strong light. The simultaneous activation of the reversible V-cycle in sun-flecks permits further tuning of exciton dissipation, and over a time frame of days, increases in the size of the V+A+Z pool in sun leaves can be expected (Table 1).
Clearly, additional kinetic experiments and studies of Lx- and V-cycle pigment distribution among antenna complexes are required for proof of these hypotheses, but there are broader implications. Lutein-epoxide seems to be widespread in embryonic leaves in buds of many tree species (Garcia-Plazaola et al., 2004), where its irreversible conversion to L on illumination following bud opening might signal an analogous role in photoprotection of the developing photosynthetic apparatus to that proposed here in shade to sun acclimation of deeply shaded leaves. Lutein-epoxide is also widely reported in other long-lived, light- and stress-tolerant photosynthetic systems such as lichens (Czeczuga et al., 1996) in which its role remains to be elucidated. It seems likely that further studies with a wide spectrum of plant species will advance an understanding of the relationships between the -and ß-xanthophyll pathways and cycles in response to strong light.
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Acknowledgements |
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These experiments were supported by an Australian National University Center for Excellence postgraduate student award and travel grant to SM, a Carnegie Institution postdoctoral fellowship to RM, and a Columbia University postdoctoral fellowship to UR. The research program in the Biosphere 2 Laboratory 2001–2003 was made possible by the vision of Dr Michael Crow, Executive Vice-Provost Columbia University, and the generosity of Mr Edward P Bass. We are grateful to Drs Leif Abrell and John Berger for access to and support of HPLC equipment in the Chemistry Unit at the Biosphere 2 Laboratory, and to Drs Fred Chow, Britta Förster, and Barry Pogson for comments on early drafts of the manuscript.
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Footnotes |
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* Present address: Phytosphäre Institut, Forschungszentrum Jülich, D-52425 Jülich, Germany.
Present address: Institut für Botanik, Technische Universität Darmstadt, Schnittspahnstrasse 3–5, D-64287 Darmstadt, Germany.
Present address: Department of Global Ecology, Carnegie Institution, 290 Panama St, Stanford, CA 94305, USA.
Present address: School of GeoSciences, University of Edinburgh, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, Scotland, UK.
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References |
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