Abstract
Photosynthetic organisms have evolved photoprotective mechanisms to acclimate to light intensity fluctuations in their natural growth environments. Photosystem (PS) II subunit S (PsbS) and light-harvesting complex (LHC) stress-related proteins (LhcSR) are essential for triggering photoprotection in vascular plants and green algae, respectively. The activity of both proteins is strongly enhanced in the moss Physcomitrella patens under high-light conditions. However, their role in regulating photosynthesis acclimation in P. patens under fluctuating light (FL) conditions is still unknown. Here, we compare the responses of wild-type (WT) P. patens and mutants lacking PsbS (psbs KO) or LhcSR1 and 2 (lhcsr KO) to FL conditions in which the low-light phases were periodically interrupted with high-light pulses. lhcsr KO mutant showed a strong reduction in growth with respect to WT and psbs KO under FL conditions. The lack of LhcSR not only decreased the level of non-photochemical quenching, resulting in an over-reduced plastoquinone pool, but also significantly increased the PSI acceptor limitation values with respect to WT and psbs KO under FL conditions. Moreover, in lhcsr KO mutant, the abundance of PSI core and PSI–LHCI complex decreased greatly under FL conditions compared with the WT and psbs KO. We proposed that LhcSR in P. patens play a crucial role in moss acclimation to dynamic light changes.
Similar content being viewed by others
References
Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107:11128–11133
Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci USA 110:4111–4116
Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro EM (2015) Photoprotection of photosystems in fluctuating light intensities. J Exp Bot 66:2427–2436
Ashton NW, Grimsiey NH, Cove DJ (1979) Analysis of gametophytic development in the moss, Physcomittrella patens, using auxin and cytokinin resistent mutants. Planta 144:427–435
Bonente G, Pippa S, Castellano S, Bassi R, Ballottari M (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J Biol Chem 287:5833–5847
Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2010) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577
Chaux F, Burlacot A, Mekhalfi M, Auroy P, Blangy S, Richaud P, Peltier G (2017) Flavodiiron proteins promote fast and transient O2 photoreduction in Chlamydomonas. Plant Physiol 174:1825–1836
Dall’Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R (2017) Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat Plants 3:17033
Ganeteg U, Külheim C, Andersson J, Jansson S (2004) Is each light-harvesting complex protein important for plant fitness? Plant Physiol 134:502–509
Gao S, Gu WH, Xiong Q, Ge F, Xie XJ, Li J, Chen WZ, Pan GH, Wang GC (2015) Desiccation enhances phosphorylation of PSII and affects the distribution of protein complexes in the thylakoid membrane. Physiol Plant 153:492–502
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytol 196:763–773
Gerotto C, Alboresi A, Meneghesso A, Jokel M, Suorsa M, Aro E-M, Morosinotto T (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc Natl Acad Sci USA 113:12322–12327
Girolomoni L, Cazzaniga S, Pinnola A, Perozeni F, Ballottari M, Bassi R (2019) LHCSR3 is a nonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 116:4212–4217
Jokel M, Johnson X, Peltier G, Aro E-M, Allahverdiyeva Y (2018) Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light. Plant J 94:822–835
Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q A redox state and excitation energy fluxes. Photosynth Res 79:209–218
Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–860
Külheim C, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93
Li XP, 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
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol 50:333–359
Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:1–8
Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521
Peng LW, Shimizu H, Shikanai T (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J Biol Chem 283:34873–34879
Pinnola A, Dall’Osto L, Gerotto C, Morosinotto T, Bassi R, Alboresi A (2013) Zeaxanthin binds to light-harvesting complex stress-related protein to enhance nonphotochemical quenching in Physcomitrella patens. Plant Cell 25:3519–3534
Pinnola A, Cazzaniga S, Alboresi A, Nevo R, Levin-Zaidman S, Reich Z, Bassi R (2015) Light-harvesting complex stress-related proteins catalyze excess energy dissipation in both photosystems of Physcomitrella patens. Plant Cell 27:3213–3227
Pinnola A, Alboresi A, Nosek L, Semchonok D, Rameez A, Trotta A, Barozzi F, Kouřil R, Dall’Osto L, Aro EM (2018) A LHCB9-dependent photosystem I megacomplex induced under low light in Physcomitrella patens. Nat Plants 4:910–919
Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal AA, Van AH, Robert B, Horton P, Van GR (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578
Schreiber U, Klughammer C (2008) Saturation pulse method for assessment of energy conversion in PSI. Pam Appl Notes 1:1–14
Shimakawa G, Ishizaki K, Tsukamoto S, Tanaka M, Sejima T, Miyake C (2017) The Liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647
Storti M, Alboresi A, Gerotto C, Aro E-M, Finazzi G, Morosinotto T (2019) Role of cyclic and pseudo-cyclic electron transport in response to dynamic light changes in Physcomitrella patens. Plant Cell Environ 42:1590–1602
Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S (2012) Proton gradient regulation5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948
Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735
Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021
Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:1066
Xie X, Gao S, Gu W, Pan G, Wang G (2013) Desiccation induces accumulations of antheraxanthin and zeaxanthin in intertidal macro-alga Ulva pertusa (Chlorophyta). PLoS ONE 8:e72929
Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012
Acknowledgements
The authors have no conflict of interest. This study was supported by National Natural Science Foundation of China (No. 41976097), the National Key R&D Program of China (2018YFD0901500), the Key Deployment Project of the Centre for Ocean Mega-Research of Science, the Chinese Academy of Sciences (COMS2019Q02), the Major Scientific and Technological Innovation Projects in Shandong Province (2019JZZY010815), China Agriculture Research System of MOF and MARA (CARS-50), the North Jiangsu Science and Technology Special Project (LYG-SZ201916), and the Science and technology Project of Dongtou District (N2016Y18A).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gao, S., Pinnola, A., Zhou, L. et al. Light-harvesting complex stress-related proteins play crucial roles in the acclimation of Physcomitrella patens under fluctuating light conditions. Photosynth Res 151, 1–10 (2022). https://doi.org/10.1007/s11120-021-00874-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-021-00874-8