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First published online September 7, 2007; 10.1104/pp.107.106872 Plant Physiology 145:997-1005 (2007) © 2007 American Society of Plant Biologists Photoprotection in the Lichen Parmelia sulcata: The Origins of Desiccation-Induced Fluorescence Quenching1Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1
Lichens, a symbiotic relationship between a fungus (mycobiont) and a photosynthetic green algae or cyanobacteria (photobiont), belong to an elite group of survivalist organisms termed resurrection species. When lichens are desiccated, they are photosynthetically inactive, but upon rehydration they can perform photosynthesis within seconds. Desiccation is correlated with both a loss of variable chlorophyll a fluorescence and a decrease in overall fluorescence yield. The fluorescence quenching likely reflects photoprotection mechanisms that may be based on desiccation-induced changes in lichen structure that limit light exposure to the photobiont (sunshade effect) and/or active quenching of excitation energy absorbed by the photosynthetic apparatus. To separate and quantify these possible mechanisms, we have investigated the origins of fluorescence quenching in desiccated lichens with steady-state, low temperature, and time-resolved chlorophyll fluorescence spectroscopy. We found the most dramatic target of quenching to be photosystem II (PSII), which produces negligible levels of fluorescence in desiccated lichens. We show that fluorescence decay in desiccated lichens was dominated by a short lifetime, long-wavelength component energetically coupled to PSII. Remaining fluorescence was primarily from PSI and although diminished in amplitude, PSI decay kinetics were unaffected by desiccation. The long-wavelength-quenching species was responsible for most (about 80%) of the fluorescence quenching observed in desiccated lichens; the rest of the quenching was attributed to the sunshade effect induced by structural changes in the lichen thallus.
Lichens are made up of two main components: the mycobiont, or fungal portion, and the photobiont, which may be algae or cyanobacteria. The mycobiont affords protection for the photobiont that supplies energy to the mycobiont in the form of reduced carbons. Lichens can contain several different photobionts, these may be different types of green algae, cyanobacteria, or a mixture of the two (Green et al., 2002  ). It has, however, been observed that the green algae Trebouxia is the most abundant photobiont, and it is found in approximately 75% of lichenized relationships (Green et al., 2002). Trebouxia species have been found living outside a mycobiont; however, this is rarely seen.
Lichens are poikilohydric and can survive severe bouts of desiccation, which has profound effects on most physiological factors. This is manifested by a reduction in growth rates and reduced photosynthesis (Scheidegger et al., 1995
With water as its electron donor, PSII is an obvious target of desiccation-induced damage. PSII often suffers from light-induced damage (Aro et al., 1993 PSII activity is often assessed in vivo by the measurement of variable chlorophyll (Chl) a fluorescence, which originates from active PSII reaction centers. The minimal level of fluorescence (FO) is associated with open reaction centers that have an oxidized primary quinone electron acceptor (QA). Closed reaction centers, where QA is reduced, exhibit a maximal yield of fluorescence (FM). Exposure of PSII to saturating light induces an increase in fluorescence from FO to the FM level that is often used as a measure of PSII activity. The difference between FM and FO (FM – FO) is called variable fluorescence (FV).
In lichens, the desiccated state is characterized by a shutdown of PSII, manifested by the lack of FV. Desiccated lichens emit a level of fluorescence much lower than FO of hydrated lichens. Upon exposure to water, an immediate increase in fluorescence, back to FO, is observed, followed by a resumption of normal PSII activity as indicated by a return of FV upon exposure to saturating light flashes (Heber et al., 2000
The decrease in fluorescence emission observed in desiccated lichens is likely associated with their phototolerance and could be caused by multiple mechanisms. One mechanism occurs primarily in the fungal thallus and involves structural changes that induce changes in light-scattering and shading properties. During desiccation, the algae aggregate and change shape to limit exposure to light, while at the same time the lichen thallus curls to minimize the available surface area and reduce light absorbance (Scheidegger et al., 1995
Protection from photodamage also exists within the photobiont. Many photobionts contain the carotenoid zeaxanthin that is involved in nonphotochemical quenching (Demmig-Adams and Adams, 1990 Previous studies have characterized the desiccated state of lichens using steady-state spectroscopy and pulse amplitude-modulated (PAM) Chl a fluorescence measurements. While these methods provide information about the relative decrease in measured fluorescence and the spectral properties of the quenched and unquenched states, they are not able to separate decreases in emission induced by changes in the structural organization and/or light-scattering properties of the thallus from mechanisms of fluorescence quenching within the photosynthetic apparatus.
Based on the observation of an enhanced 720-nm fluorescence emission feature in desiccated lichens, it was previously suggested that a red-shifted form of Chl acts as a putative long-wavelength quencher (Heber and Shuvalov, 2005 In this study, we investigate the mechanism of fluorescence quenching in desiccated lichens using a combination of time-resolved and steady-state fluorescence spectroscopy at room and low temperatures. This approach allowed us to separate and quantify the contributions of mechanisms that serve to minimize the absorption of light by the photobiont (sunshades) from mechanisms involving the dissipation of absorbed energy by the photosynthetic apparatus of the photobiont (quenchers).
PAM Measurements
A representative PAM trace of hydration is shown in Figure 1
. As observed previously for other species of lichens (Bukhov, 2004
Steady-State Room Temperature Fluorescence Spectroscopy
Room temperature fluorescence emission spectra of P. sulcata are shown in Figure 2
. Fluorescence spectra of desiccated samples showed an apparent PSII peak at 685 nm and a broad (720–750 nm) long-wavelength emission peaking at 740 nm. Interestingly, the relative contribution of the 685-nm peak increases dramatically from its start as a relatively low amplitude shoulder in the desiccated sample to becoming the dominant peak in fully hydrated lichens. In addition, overall emission from both regions increases greatly in the sample during hydration. Similar results were reported by Heber and Shuvalov (2005)
Steady-State 77 K Emission Spectra Low temperature fluorescence emission spectra allow for the observation of Chl forms associated with PSII and PSI and were determined for desiccated and hydrated samples (Fig. 3 ). The 77 K emission spectrum of the hydrated lichen sample was similar to spectra of most green algae and shows characteristic contributions from two shoulders at 685 and 695 nm (PSII associated) and a peak at 720 nm (PSI associated). In desiccated lichens, the overall fluorescence yield at 77 K was approximately 10 times lower than in hydrated lichens and the spectra in Figure 3 have been normalized to facilitate comparison. In desiccated lichens, the contributions from PSII at 685 and 695 nm were barely discernable, and the spectrum is dominated by the PSI emission at 720 nm. The longer wavelength band, peaking at 740 nm, observed at room temperature appeared largely absent from the 77 K spectra of both hydrated and desiccated samples. However, the PSI emission peak in the desiccated sample appears slightly red shifted, which may indicate increased fluorescence under desiccated conditions from longer wavelength (>720 nm) forms, as was observed for the room temperature fluorescence data. The apparently minor contribution of the long-wavelength pigments to the low temperature emission spectra would be consistent with a quenching role.
Room Temperature Time-Resolved Fluorescence Decay Kinetics
To obtain a better understanding of the origin of fluorescence bands observed in the steady-state spectra of the lichens, we measured the picosecond fluorescence decay kinetics of desiccated and hydrated P. sulcata (Fig. 4
). Hydrated lichens show decay kinetics that are typical of green algae and higher plants at both the FO and FM states (Wendler and Holzwarth, 1987
To determine the origin of components contributing to the fluorescence decay, kinetic measurements were taken at 11 emission wavelengths covering the range from 660 to 760 nm. The data collected at all detection wavelengths were analyzed with a model of parallel decaying compartments to determine the spectra of decay components and further explore the origins of desiccation-induced quenching. The resulting decay-associated spectra (DAS) are shown in Figure 5 . Four decay components were required to describe the fluorescence decay kinetics at FD and FM and five at FO (Fig. 5). Of the five components contributing to decay at FO, the spectral shape (peaks at 720 and 700 nm) and lifetimes of the two fast decay components (  1 = 40 ps and 2 = 90 ps) were indicative of PSI emission. We assigned the next two slower components (1 = 300 ps and 2 = 640 ps), which had emission peaks in the 685 to 690 nm region, to PSII. The last slow decay component, 5 = 2.1 ns with very low amplitude and peak in the 685- to 690-nm region, was assigned to a small fraction of closed PSII reaction centers and/or uncoupled antenna.
The components contributing to the decay of fluorescence at FO (Fig. 5) had DAS in the short-wavelength range (660–700 nm), which were similar to those previously studied in the free growing green algae, Trebouxia, which also included decay components with lifetimes of 80 ps, 300 ps, 600 ps, and 2 ns (Wendler and Holzwarth, 1987 ). We resolved an additional short component (5 = 40 ps) in this study and assigned it to PSI. Fast decay components with similar lifetimes have been reported in recent studies of various PSI preparations from higher plants (Croce et al., 2000; Ihalainen et al., 2002; Melkozernov et al., 2004) and PSI-rich thylakoid membrane compartments (Veerman et al., 2007). Two distinct PSI decay components are thought to originate from the peripheral and inner PSI antenna (Croce et al., 2000; Melkozernov et al., 2004). It is noteworthy that in all of these previous studies, the amplitude of the 40-ps component was larger than the 80-ps component, indicating a larger size of the inner PSI antenna; while in P. sulcata it is the another way round. This observation may indicate a different organization of the peripheral PSI antenna in this organism. There are also significant differences in the spectral shapes of the 40- and 90-ps components, which may be indicative of a mixture of PSII and PSI contributions in the 90-ps component. Interestingly, although the DAS of the PSII components were similar to previously reported DAS in the range of 660 to 700 nm, they appeared to have unusual long-wavelength contributions. It is well established that PSII emission in many organisms, including higher plants and cyanobacteria, has only one peak at 685 nm at room temperature. In this study, we observed a pronounced long-wavelength emission peaking at 740 nm that had the same decay kinetics as fluorescence at 685 nm in both of the PSII decay components. This observation suggests that a novel long-wavelength pigment species is energetically coupled to PSII pigments. If this is the case, then DAS components with the same spectral signatures are expected to also be observed in hydrated samples in the FM state and in the desiccated samples (FD) as well.
Four components were required to fit the fluorescence decay kinetics of P. sulcata at FM. Only one PSI-associated component was observed with a lifetime of 50 ps and an emission peak at 700 nm. This component is likely a mixture of the two decay components we observed at FO. As expected, the closure of PSII reaction centers resulted in a pronounced slow down of PSII-associated decay components. We observed two decay components with lifetimes of 1.48 ns and 2.1 ns that had DAS, which appeared to be the same as the 300- and 600-ps components observed in the FO state. The appearance of peaks in both the characteristic PSII region of about 685 nm and in the long-wavelength region from 720 to 740 nm strongly supports the idea that a long-wavelength emitter is energetically coupled to PSII. We found that an additional 410-ps component was required to fit the data. The origin of this component is not quite clear. It resembles DAS of PSII components, but its long-wavelength emission peak is shifted to 710 nm. It is known that PSII has complex decay kinetics at FM. For example, in a previous study of the algae Scenedesmus obliquus, PSII decay kinetics were described by three components: 380, 1,300, and 2,100 ps (Roelofs and Holzwarth, 1990 The DAS of desiccated P. sulcata are dominated by two short lifetime components at 40 and 80 ps. Both components exhibited shapes reminiscent of PSII components observed at both FO and FM. However, the spectra were broadened as compared to PSII components, most likely due to convolution with PSI components that would have similar lifetimes. The consistent spectral shape of the PSII DAS components observed at all three measured states indicates that the long-wavelength pigment pool is energetically coupled to PSII regardless of the physiological state of the reaction centers. A 240-ps component of low amplitude was also observed in the desiccated sample with peaks at 685 and 720 nm. This component is somewhat similar to the 300-ps PSII component observed in the FO DAS and may reflect a small fraction of relatively unquenched PSII. The relatively large contribution of the 720-nm peak to this component suggests some contribution from PSI; however, the 240-ps lifetime is longer than expected. There was also a very low amount of a long-lived component (1.1-ns lifetime) with significant short- and long-wavelength contributions that may arise from uncoupled antennae.
Low temperature fluorescence decay kinetics were measured to facilitate the identification of the quenching species. At room temperature, the broad absorption and emission spectra of antenna chromophores make it possible for a quencher of relatively high energy to still efficiently quench emission from a broad range of emitters. However, at low temperatures, only a long-wavelength quencher would be able to decrease the fluorescence lifetime of low energy pigments.
Assignment of DAS components at low temperature is complicated due to pronounced decay components arising from unidirectional energy transfer from higher energy to lower energy pigments that are mostly irreversible at 77 K. This is clearly observed in the short-wavelength spectral region (680–730 nm) of the measured DAS in P. sulcata (Fig. 6
). The general trend in this spectral region is that shorter wavelength components have shorter lifetimes and the fastest lifetime component (20 ps) exhibits the shortest wavelength peak at 680 nm. Such behavior is expected for systems where several long-wavelength forms are coupled to the bulk short-wavelength pool. Similar features have been observed in PSII, PSI, and light-harvesting complex II (LHCII) of many other photosynthetic organisms where long-wavelength pigment pools are not quenched and have long lifetimes at low temperature (Mullineaux et al., 1993
Photoprotection in Desiccated Lichens: Sunscreen or Excited State Decay? The ability of lichens to survive severe desiccation while exposed to solar radiation is correlated with a large decrease in the yield of steady-state Chl a fluorescence emission. Photoprotection associated with a decreased yield of fluorescence could arise from the action of a sunscreen-type mechanism that decreases the amount of light absorbed by the photobiont and/or an excitation energy-quenching mechanism that safely dissipates energy absorbed by the photosynthetic apparatus as heat.
There are changes in the morphology of the thallus of lichens upon desiccation that increase light scattering and decrease the transmission of light to the photobiont. This sunscreen mechanism must contribute, at least in part, to the decrease in fluorescence characteristic of desiccated lichens. Increased scattering could both decrease the amount of light reaching the photobiont and increase the reabsorption of emitted fluorescence. But by how much, and is there another quenching mechanism? Based on the observation of a relative increase in the contribution of long-wavelength emission in fluorescence spectra of desiccated lichens, it was previously suggested that low energy Chl forms may act as a quencher of PSII (Heber and Shuvalov, 2005
Our steady-state emission spectroscopy confirmed a relative increase in long-wavelength Chl a fluorescence in desiccated lichens. However, we observed a somewhat broader emission than previously reported with a peak at 740 nm, and the long-wavelength emission was also clearly present in hydrated lichens. Increased self-absorption of fluorescence resulting from increased light scattering within the thallus could result in a red shift of fluorescence emission. The largest distortion of the emission spectra would arise at the red edge of absorption, around 670 to 680 nm, and would be expected to red shift the maximum of the short-wavelength emission peak at 685 nm. Upon normalizing the spectra of Figure 2 to the short-wavelength emission peak (data not shown), we found no significant distortion of the blue edge or shift of the 685-nm peak. In addition, our room temperature fluorescence decay kinetics revealed the presence of novel short lifetime components in desiccated lichens that were associated with both PSII emission and long-wavelength emission. This is clear evidence for excited state energy quenching. Our data showed that long-wavelength emission was also present in hydrated lichens at both FO and FM where its fluorescence lifetimes were identical to those of PSII. This important result indicates a tight energetic coupling between the long-wavelength emitters and PSII antenna. In desiccated lichens, we observe deexcitation of the bulk PSII pool with a rate constant of 25 ns–1. This rate is almost 8 times faster than the rate constant for exciton trapping in active PSII species at FO (3 ns–1; Roelofs et al., 1992
To summarize our results and put them in the context of excitation energy transfer and electron transport, we show a simplified kinetic model of PSII in lichens, which includes a desiccation-induced quencher (Fig. 7
). The model, based on previous PSII models (Roelofs and Holzwarth, 1990
How much do the two mechanisms, sunscreen and excitation energy quenching, contribute to the measured decrease in fluorescence yield in desiccated lichens? Fluorescence yield changes measured by the analysis of steady-state fluorescence emission spectra or with a PAM Chl a fluorometer will be affected by contributions from both of these mechanisms. In contrast, yield changes determined from an analysis of changes in the excited state decay lifetimes will only be influenced by excitation energy quenching. Comparing these two techniques allowed us to determine that most of the decrease in fluorescence emission was a result of excitation energy quenching within the photobiont. In all of our samples, less than 25% of the observed fluorescence decrease in desiccated lifetimes arose from the sunscreen effect of desiccated thallus.
Even though the room temperature decay data showed fast decay components at long wavelengths, it is not clear that the lowest energy emitters are indeed the origin of quenching. Due to the large overlap between the relatively broad absorbance and emission spectra of PSII antenna pigments at room temperature, a quencher of intermediate or relatively high energy could also be responsible for the quenching observed at 685 nm and 740 nm in desiccated lichens. However, our low temperature fluorescence decay measurements showed that the fluorescence lifetime of the longest wavelength emitters remained short at 77 K, clear evidence that the long-wavelength-emitting species is not energetically downhill from the quenching species and is thus actively involved in quenching. This is in contrast to unquenched PSII in higher plants, algae, or cyanobacteria where the longest wavelength emission at 77 K (695 nm) exhibits the longest decay lifetime (3.5 ns; Komura et al., 2006 The decay lifetime of the long-wavelength (740 nm) quenching species at room temperature in desiccated lichens (40 ps) was much faster than the lifetime of the major decay component of PSII with open reaction centers (300 ps), indicating that the quencher can efficiently compete for excitation with open PSII reaction centers. Thus, the long-wavelength quencher closely coupled to PSII identified in this study is clearly capable of providing efficient down-regulation of PSII in desiccated lichens and fast restoration of PSII upon rehydration.
The composition and structure of the long-wavelength quencher is unknown. Tight energetic coupling to PSII reaction centers implies that the red-shifted emission originates from a pigment pool located in the vicinity of PSII. This could be either a group of pigments within the PSII core or a novel antenna pigment-protein complex specific to lichen photobionts. Long-wavelength emission has previously been associated with aggregated LHCII (Ruban and Horton, 1992
Sample Preparation
The lichen Parmelia sulcata was utilized for all measurements. P. sulcata is a relatively small foliose form that is widespread throughout North America and much of Asia. P. sulcata contains the green algae species Trebouxia as photobiont, is believed to be particularly phototolerant, and does not appear to display high irradiance sensitivity in the dry state (Gauslaa et al., 2001
Room temperature fluorescence measurements were all obtained with the use of a standard PAM fluorometer (H. Walz). The pulsed measuring beam had a peak wavelength of 660 nm. Unless stated otherwise, FM was determined by using 500-ms saturation pulses of white actinic light at an intensity of 4,200 µmol m–2 s–1. Rehydration of desiccated samples was achieved by placing the sample on a section of filter paper and adding distilled water to the filter paper. Fluorescence emission spectra were measured at 77 K with Triax-320 imaging spectrograph and back-illuminated, deep-depleted, nitrogen-cooled CCD array (Jobin Yvon). Lichen samples assayed by this method were sandwiched between a glass slide and a purpose-built sample holder. The lichens were hydrated while on the sample holder and then immersed in liquid nitrogen in the case of the 77 K measurements. The excitation wavelength was 435 nm.
A single photon-timing apparatus utilizing a picosecond pulsed diode laser was used to measure the kinetics of Chl fluorescence decays (Vasil'ev et al., 2002 Received August 3, 2007; accepted August 30, 2007; published September 7, 2007.
1 This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (to D.B.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Doug Bruce (dbruce{at}brocku.ca). www.plantphysiol.org/cgi/doi/10.1104/pp.107.106872 * Corresponding author; e-mail dbruce{at}brocku.ca.
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