Acclimatory responses of Arabidopsis to fluctuating light environment: comparison of different sunfleck regimes and accessions

Photosynthesis Research - Tập 113 - Trang 221-237 - 2012
Philipp Alter1,2,3, Anne Dreissen1,2, Fang-Li Luo1,4, Shizue Matsubara1
1IBG-2: Pflanzenwissenschaften, Forschungszentrum Jülich, Jülich, Germany
2Aachen University of Applied Sciences, Aachen, Germany
3Cell Biology and Plant Biochemistry, Universität Regensburg, Regensburg, Germany
4College of Nature Conservation, Beijing Forestry University, Beijing, China

Tóm tắt

Acclimation to fluctuating light environment with short (lasting 20 s, at 650 or 1,250 μmol photons m−2 s−1, every 6 or 12 min) or long (for 40 min at 650 μmol photons m−2 s−1, once a day at midday) sunflecks was studied in Arabidopsis thaliana. The sunfleck treatments were applied in the background daytime light intensity of 50 μmol photons m−2 s−1. In order to distinguish the effects of sunflecks from those of increased daily irradiance, constant light treatments at 85 and 120 μmol photons m−2 s−1, which gave the same photosynthetically active radiation (PAR) per day as the different sunfleck treatments, were also included in the experiments. The increased daily total PAR in the two higher constant light treatments enhanced photosystem II electron transport and starch accumulation in mature leaves and promoted expansion of young leaves in Columbia-0 plants during the 7-day treatments. Compared to the plants remaining under 50 μmol photons m−2 s−1, application of long sunflecks caused upregulation of electron transport without affecting carbon gain in the form of starch accumulation and leaf growth or the capacity of non-photochemical quenching (NPQ). Mature leaves showed marked enhancement of the NPQ capacity under the conditions with short sunflecks, which preceded recovery and upregulation of electron transport, demonstrating the initial priority of photoprotection. The distinct acclimatory responses to constant PAR, long sunflecks, and different combinations of short sunflecks are consistent with acclimatory adjustment of the processes in photoprotection and carbon gain, depending on the duration, frequency, and intensity of light fluctuations. While the responses of leaf expansion to short sunflecks differed among the seven Arabidopsis accessions examined, all plants showed NPQ upregulation, suggesting limited ability of this species to utilize short sunflecks. The increase in the NPQ capacity was accompanied by reduced chlorophyll contents, higher levels of the xanthophyll-cycle pigments, faster light-induced de-epoxidation of violaxanthin to zeaxanthin and antheraxanthin, increased amounts of PsbS protein, as well as enhanced activity of superoxide dismutase. These acclimatory mechanisms, involving reorganization of pigment–protein complexes and upregulation of other photoprotective reactions, are probably essential for Arabidopsis plants to cope with photo-oxidative stress induced by short sunflecks without suffering from severe photoinhibition and lipid peroxidation.

Tài liệu tham khảo

Abarca D, Roldan M, Martin M, Sabater B (2001) Arabidopsis thaliana ecotype Cvi shows an increased tolerance to photo-oxidative stress and contains a new chloroplastic copper/zinc superoxide dismutase isoenzyme. J Exp Bot 52:1417–1425 Adams WWIII, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant Cell Environ 22:125–136 Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639 Athanasiou K, Dyson BC, Webster RE, Johnson GN (2010) Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiol 152:366–373 Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801 Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958 Beligni MV, Lamattina L (2002) Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ 25:737–748 Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566 Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008) The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370 Caffarri S, Croce R, Breton J, Bassi R (2001) The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem 38:35924–35933 Chazdon RL, Pearcy RW (1986a) Photosynthetic responses to light variation in rainforest species. I. Induction under constant and fluctuating light conditions. Oecologia 69:517–523 Chazdon RL, Pearcy RW (1986b) Photosynthetic responses to light variation in rainforest species. II. Caobon gain and photosynthetic efficiency during lightflecks. Oecologia 69:524–531 Czech AS, Strzałka K, Schurr U, Matsubara S (2009) Developmental stages of delayed-greening leaves inferred from measurements of chlorophyll content and leaf growth. Funct Plant Biol 36:654–664 Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24 Demmig-Adams B, Adams WWIII (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15:411–419 Dominici P, Caffarri S, Armenante F, Ceoldo A, Crimi M, Bassi R (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277:22750–22758 Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr A 543:137–145 Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640 Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767 Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520 Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, Fischbach A, Briem S, Dreissen G, Tittmann S, Braun S, De Jaeger I, Metzlaff M, Schurr U, Scharr H, Walter A (2009) Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Funct Plant Biol 36:902–914 Jones MGK, Outlaw WH, Lowry OH (1977) Enzymatic assay of 10–7 to 10–14 moles of sucrose in plant tissues. Plant Physiol 60:379–383 Jung H-S, Niyogi KK (2009) Quantitative genetic analysis of thermal dissipation in Arabidopsis. Plant Physiol 150:977–986 Kalituho L, Rech J, Jahns P (2007) The roles of specific xanthophylls in light utilization. Planta 225:423–439 Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variationin Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172 Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218 Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352 Külheim C, Ågren J, Jansson S (2000) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93 Leakey ADB, Scholes JD, Press MC (2004) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482 Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395 Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874 Logan BA, Baker DH, Adams WWIII, Demmig-Adams B (1997) The response of xanthophyll cycle-dependent energy dissipation in Alocasia brisbanensis to sunflecks in a subtropical rainforest. Aust J Plant Physiol 24:27–33 Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36:20–36 Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant Cell Environ 29:1936–1945 Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134 Ögren E, Sundin U (1996) Photosynthetic responses to variable light: a comparison of species from contrasting habitats. Oecologia 106:18–27 Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362 Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453 Pearcy RW, Calkin H (1983) Carbon dioxide exchange of C3 and C4 tree species in the understory of a Hawaiian forest. Oecologia 58:26–32 Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41 Pons TL, Pearcy RW, Seemann JR (1992) Photosynthesis in flashing light in soybean leaves grown in different conditions. I. Photosynthetic induction state and regulation of ribulose-1,5-bisphosphate carboxylase activity. Plant Cell Environ 15:569–576 Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 279–319 Sims DA, Pearcy RW (1993) Sunfleck frequency and duration affect growth-rate of the understorey plant, Alocasia macrorrhiza. Funct Ecol 7:683–689 Walter A, Scharr H, Gilmer F, Zierer R, Nagel KA, Ernst M, Wiese A, Virnich O, Christ MM, Uhlig B, Jünger S, Schurr U (2007) Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species. New Phytol 174:447–455 Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447 Watling JR, Ball MC, Woodrow IE (1997a) The utilization of lightflecks for growth in four Australian rain-forest species. Funct Ecol 11:231–239 Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997b) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25 Yin ZH, Johnson GN (2000) Photosynthetic acclimation of higher plants to growth in fluctuating light environments. Photosynth Res 63:97–107 Yoshida K, Watanabe CK, Hachiya T, Tholen D, Shibata M, Terashima I, Noguchi K (2011) Distinct responses of the mitochondrial respiratory chain to long- and short-term high light environments in Arabidopsis thaliana. Plant Cell Environ 34:618–628