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Curling During Desiccation Protects the Foliose Lichen Lobaria Pulmonaria Against Photoinhibition

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Curling During Desiccation Protects the Foliose Lichen Lobaria Pulmonaria Against Photoinhibition Oecologia (2006) 149:553–560 DOI 10.1007/s00442-006-0476-2 ECOPHYSIOLOGY Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition Milon Barták · Knut Asbjørn Solhaug · Hana Vráblíková · Yngvar Gauslaa Received: 14 October 2005 / Accepted: 26 May 2006 / Published online: 28 June 2006 © Springer-Verlag 2006 Abstract This study aims to assess the photoprotec- photoinhibition in desiccated L. pulmonaria thalli dur- tive potential of desiccation-induced curling in the ing high light exposures. light-susceptible old forest lichen Lobaria pulmonaria by using chlorophyll Xuorescence imaging. Naturally Keywords Chlorophyll Xuorescence imaging · curled thalli showed less photoinhibition-induced limi- Lobaria pulmonaria · Photoprotection · Poikilohydric tations in primary processes of photosynthesis than organisms artiWcially Xattened specimens during exposures to 450 mol m¡2 s¡1 in the laboratory after both 12- Abbreviations (medium dose treatment) and 62-h duration (high Chl Chlorophyll dose treatment). Thallus areas shaded by curled lobes HD High light dose during light exposure showed unchanged values of MD Medium light dose X measured chlorophyll uorescence parameters (FV/ PS II Photosystem II FM, PS II), whereas non-shaded parts of curled thalli, PS II Quantum yield of photochemical as well as the mean for the entire Xattened thalli, reactions in photosystem II showed photoinhibitory limitation after light treat- ments. Furthermore, the chlorophyll Xuorescence imaging showed that the typical small-scale reticulated Introduction ridges on the upper side of L. pulmonaria caused a spatial, small-scale reduction in damage due to minor Light is a vital ecological factor for a lichen-forming shading. Severe dry-state photoinhibition readily fungus being dependent on a close symbiotic associa- occurred in Xattened and light-treated L. pulmonaria, tion with its autotrophic photobiont partner. The although the mechanisms for such damage in a desic- amount of light received by the photobiont during peri- cated and inactive stage are not well known. Natural ods of thallus hydration may determine lichen growth curling is one strategy to reduce the chance for serious (Dahlman and Palmqvist 2003), and thereby also the success of the lichen in forest ecosystems. At the same W Communicated by Otto Lange time, light represents a signi cant stress factor, not only because direct solar radiation promotes rapid des- M. Barták · H. Vráblíková iccation in poikilohydric organisms, but also because Department of Plant Physiology and Anatomy, excess light may cause severe and long-lasting photoin- Masaryk University, Kotlarska 2, 61137 Brno, Czech Republic hibition in lichens (Gauslaa and Solhaug 1996, 2000). In this paper, we deWne photoinhibition to be a sus- K. A. Solhaug · Y. Gauslaa (&) tained depression of maximal photochemical quantum Department of Ecology and Natural Resource Management yield of PS II. Desiccated lichens are assumed to be (Urbygningen), Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway resistant to high light, because desiccation reduces the e-mail: [email protected] transmittance of solar radiation through a protecting 123 554 Oecologia (2006) 149:553–560 upper cortex (Ertl 1951; Gauslaa and Solhaug 2001), eVects of curling by studying the spatial variation of and stabilizes the photosynthetic apparatus by causing photoinhibition with chlorophyll Xuorescence imaging. a functional disconnection of its components (Sigfrids- Since little is known about the nature of photoinhibi- son 1980; Bilger et al. 1989). However, in nature, tion in desiccated lichens, we also aim at using the lichens experience considerably longer periods of high results to discuss mechanisms for photoinhibition in dry solar radiation in the desiccated compared to the lichens. hydrated state (Lange et al. 1999), since they dry rap- idly in the sun. Furthermore, repair mechanisms are switched oV during desiccation. Extended excess light Materials and methods has been shown to cause more damage in the air-dry compared to the hydrated state in some old forest Ten branched thalli were collected in October 2003 lichens (Gauslaa and Solhaug 1999, 2004), although the from a rich L. pulmonaria population on stems of Salix site of the damage is not well known. In such a perspec- caprea in old, open and mixed boreal forests with Picea tive, various processes taking place during desiccation abies in Østmarka (59°50ЈN 10°59ЈE), SE Norway. Col- should be carefully examined to search for co-acting lected lichens were air dried at room temperature at photoprotective strategies. low light and stored at 4°C for 1 week before experi- Lichen communities appear more dominant and ments started. Each thallus was then cut in two pieces impressive to a human eye when hydrated, because at a major branching point, resulting in two similar loss of water during clear weather decreases thallus lobes; mean dry weight, 100 mg; area, 9.7 cm2 (Fig. 1). area by shrinking and/or curling. Such a simple visual The ten pairs were randomly divided to two sets, Wve observation shows that most lichens undergo hygro- pairs in each. All lobes were slowly sprayed with deion- scopic movements. These movements are particularly ized water and left on moist Wlter papers in darkness at distinct in foliose vagrant desert lichens that roll up in a room temperature for 24 h before pre-measurements ball and expose their lower surface during desiccation of chlorophyll Xuorescence parameters. Afterwards, (Rogers 1971; Lumbsch and Kothe 1988), which the lobes desiccated at room temperature in darkness. assumingly protects the algal layer against excessive The curled lobes desiccated without any hindrance, light (Rogers 1977). However, sessile foliose lichens Xattened samples desiccated between sheets of Wlter also shrink and curl (Ertl 1951), although their move- papers with a light pressure on top preventing curling. ments are less spectacular and rarely mentioned in lit- Both sets were exposed to light (450 mol m¡2 s¡1) erature. Lobe tips and margins often roll up or bend to in a ventilated growth cabinet at 13°C. This light is a more vertical position during drying, enhancing the approximately 25% of maximal natural levels encoun- topography of the lichen surface. Such movements tered in open habitats during clear summer days (Gau- have the potential to shade the photobiont layer, but slaa and Solhaug 2000). Light was supplied by one also to place the young photobiont layer more parallel mercury metal halide lamp (Osram Powerstar HQI-BT to sunrays when the sun is high. Curling during desicca- 400 W daylight; Osram, Norway). This lamp does not tion reduces light-induced damage in poikilohydric produce UV-B or UV-C (unpublished data). An alu- vascular plants (Muslin and Homann 1992; Lebkue- minium foil with a hole was placed between the lamp cher and Eickmeier 1992; Farrant et al. 2003; Lebkue- and the samples, screening a substantial part of the cher and Eickmeier 1993), and was recently reviewed diVuse, reXected light. This set up produced a fairly as one of various photoprotective mechanisms in desic- unidirectional and uniform light level at an area suY- cation tolerant plants (Alpert and Oliver 2002). ciently large for mounting the lichens. Desiccated An increasing number of physiological studies in curled and Xattened lichens were fastened by double- lichens have been devoted to photoprotection by pig- sided Scotch tape to a white styrofoam plate. A fan ments of xanthophyll cycle pool, photoprotective pig- installed at 1 m distance avoided excessive heating by ments, and antioxidative substances (e.g., Demmig- convectional cooling. The wind did not cause move- Adams et al. 1990a; Solhaug and Gauslaa 1996; Barták ments in the thalli. During the exposure, thallus tem- et al. 2004; Vráblíková et al. 2006). However, not much perature was recorded by six thermocouples placed in is known about the photoprotective potential of lichen three curled and three Xattened lobes. The exposure curling. In this study, Lobaria pulmonaria (L.) HoVm., a experiment was run twice, one set was exposed for 62 h high-light susceptible foliose old forest lichen (Gauslaa of continuous exposure (high dose, HD), one for 12 h and Solhaug 1999), was exposed to high light in the dry only (medium dose, MD). During the light exposures, state in a naturally curled position and in a Xattened the thallus temperature was 26.5°C. There were no sig- position. We aim to quantify possible photoprotective niWcant temperature diVerences between the curled 123 Oecologia (2006) 149:553–560 555 Fig. 1 False colour images of chlorophyll Xuorescence im- age data of curled (a–d) and Xattened (e–h) L. pulmonaria thalli. a, e Photos of thalli; b, f FV/FM before light treatment; c, g FV/FM immediately after light treatment; d, h contour of thalli with marked places of analysis for Tables 1 and 2 a e b f c g Shaded Basal Tip Unshaded d Subtip h and Xattened lobes, or between the two dose experi- used because previous experiments have shown that L. ments (two-way ANOVA; data not shown), meaning pulmonaria can be kept desiccated for longer periods V V that the level of desiccation could not di er between in the dark without adverse e ects on FV/FM values the curled and Xattened pair. No dark controls were (Gauslaa and Solhaug 1999). 123 556 Oecologia (2006) 149:553–560 After exposure, photos were taken of all lobe pairs three sample areas were chosen for a single lobe. One to document the location and degree of curling. Then, area was located close to the tip where curling would lobes were hydrated with sprayings of deionized water, occur under unrestricted drying, the other two areas in and chlorophyll Xuorescence parameters were mea- subtip and basal part, respectively. This second sured after 3, 5, 24, 48 and 72 h in the hydrated state in approach assessed the eVect of shading on photochem- darkness at room temperature for those receiving the ical processes of photosynthesis at a lobe level by cal- HD, and after 3, 5 and 24 h for those exposed to the culating means of chlorophyll Xuorescence parameters MD.
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