Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development

[EN] The NOOT-BOP-COCH-LIKE (NBCL) genes are orthologs of Arabidopsis thaliana BLADE-ON-PETIOLE1/2. The NBCLs are developmental regulators essential for plant shaping, mainly through the regulation of organ boundaries, the promotion of lateral organ differentiation and the acquisition of organ identity. In addition to their roles in leaf, stipule and flower development, NBCLs are required for maintaining the identity of indeterminate nitrogen-fixing nodules with persistent meristems in legumes. In legumes forming determinate nodules, without persistent meristem, the roles of NBCL genes are not known. We thus investigated the role of Lotus japonicus NOOT-BOP-COCH-LIKE1 (LjNBCL1) in determinate nodule identity and studied its functions in aerial organ development using LORE1 insertional mutants and RNA interference-mediated silencing approaches. In Lotus, LjNBCL1 is involved in leaf patterning and participates in the regulation of axillary outgrowth. Wild-type Lotus leaves are composed of five leaflets and possess a pair of nectaries at the leaf axil. Legumes such as pea and Medicago have a pair of stipules, rather than nectaries, at the base of their leaves. In Ljnbcl1, nectary development is abolished, demonstrating that nectaries and stipules share a common evolutionary origin. In addition, ectopic roots arising from nodule vascular meristems and reorganization of the nodule vascular bundle vessels were observed on Ljnbcl1 nodules. This demonstrates that NBCL functions are conserved in both indeterminate and determinate nodules through the maintenance of nodule vascular bundle identity. In contrast to its role in floral patterning described in other plants, LjNBCL1 appears essential for the development of both secondary inflorescence meristem and floral meristem.This work was supported by the CNRS and by the grants ANR-14-CE19-0003 (NOOT) from the Agence National de la Recherche (ANR) to PR. This work has benefited from the facilities and expertise of the Servicio de Microscopia Electronica Universitat Politecnica de Valencia (Spain, http://www.upv.es/entidades/SME/) and of the IMAGIF Cell Biology Unit of the Gif campus (France, www.imagif.cnrs.fr) which is supported by the Conseil General de l'Essonne. The authors thank Dr Mathias Brault from the Institute of Plant Sciences Paris-Saclay (France) for providing the pFRN: RNAi plasmid, A. rhizogenes ARqua1 strain and control GUS:RNAi construction, and Dr Simona Radutoiu from the University of Aarhus (Denmark), for providing the Na-Borate/TRIZOL RNA extraction protocol. We are grateful to Dr Cristina Ferrandiz from the Instituto de Biologia Molecular y Celular de Plantas (Spain) for help in interpreting the identity of the meristems in the SEM pictures and Professor Frederique Guinel from the University of Wilfrid Laurier (Canada) for help in interpreting the identity of L. japonicus nodule vascular tissues. We thank Dr Julie Hofer from the University of Auckland (New Zealand), for manuscript revision and English language polishing.Magne, K.; George, J.; Berbel Tornero, A.; Broquet, B.; Madueño Albi, F.; Andersen, S.; Ratet, P. (2018). Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development. The Plant Journal. 94(5):880-894. https://doi.org/10.1111/tpj.13905S880894945Aida, M., & Tasaka, M. (2006). Genetic control of shoot organ boundaries. Current Opinion in Plant Biology, 9(1), 72-77. doi:10.1016/j.pbi.2005.11.011Aida, M., & Tasaka, M. (2006). Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex. Plant Molecular Biology, 60(6), 915-928. doi:10.1007/s11103-005-2760-7Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell, 9(6), 841-857. doi:10.1105/tpc.9.6.841AKASAKA, Y. (1998). Morphological Alterations and Root Nodule Formation inAgrobacterium rhizogenes-mediated Transgenic Hairy Roots of Peanut (Arachis hypogaeaL.). Annals of Botany, 81(2), 355-362. doi:10.1006/anbo.1997.0566Benlloch, R., Berbel, A., Ali, L., Gohari, G., Millán, T., & Madueño, F. (2015). Genetic control of inflorescence architecture in legumes. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.00543Berbel, A., Ferrándiz, C., Hecht, V., Dalmais, M., Lund, O. S., Sussmilch, F. C., … Madueño, F. (2012). VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nature Communications, 3(1). doi:10.1038/ncomms1801Blázquez, M. A., Ferrándiz, C., Madueño, F., & Parcy, F. (2006). How Floral Meristems are Built. Plant Molecular Biology, 60(6), 855-870. doi:10.1007/s11103-006-0013-zBrown, S. M., Oparka, K. J., Sprent, J. I., & Walsh, K. B. (1995). Symplastic transport in soybean root nodules. Soil Biology and Biochemistry, 27(4-5), 387-399. doi:10.1016/0038-0717(95)98609-rChen, Y., Chen, W., Li, X., Jiang, H., Wu, P., Xia, K., … Wu, G. (2013). Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant and Cell Physiology, 55(1), 183-193. doi:10.1093/pcp/pct171Cho, E., & Zambryski, P. C. (2011). ORGAN BOUNDARY1defines a gene expressed at the junction between the shoot apical meristem and lateral organs. Proceedings of the National Academy of Sciences, 108(5), 2154-2159. doi:10.1073/pnas.1018542108Couzigou, J.-M., & Ratet, P. (2015). NOOT-Dependent Control of Nodule Identity: Nodule Homeosis and Merirostem Perturbation. Biological Nitrogen Fixation, 487-498. doi:10.1002/9781119053095.ch49Couzigou, J.-M., Zhukov, V., Mondy, S., Abu el Heba, G., Cosson, V., Ellis, T. H. N., … Ratet, P. (2012). NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes. The Plant Cell, 24(11), 4498-4510. doi:10.1105/tpc.112.103747Couzigou, J.-M., Magne, K., Mondy, S., Cosson, V., Clements, J., & Ratet, P. (2015). The legume NOOT-BOP-COCH-LIKE genes are conserved regulators of abscission, a major agronomical trait in cultivated crops. New Phytologist, 209(1), 228-240. doi:10.1111/nph.13634Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., & Scheible, W.-R. (2005). Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis. Plant Physiology, 139(1), 5-17. doi:10.1104/pp.105.063743Dong, Z., Zhao, Z., Liu, C., Luo, J., Yang, J., Huang, W., … Luo, D. (2005). Floral Patterning in Lotus japonicus. Plant Physiology, 137(4), 1272-1282. doi:10.1104/pp.104.054288Ehrhardt, D., Atkinson, E., & Long. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science, 256(5059), 998-1000. doi:10.1126/science.10744524Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Cai, Z., … Luo, D. (2006). Control of petal shape and floral zygomorphy in Lotus japonicus. Proceedings of the National Academy of Sciences, 103(13), 4970-4975. doi:10.1073/pnas.0600681103Ferguson, B. J., & Reid, J. B. (2005). Cochleata: Getting to the Root of Legume Nodules. Plant and Cell Physiology, 46(9), 1583-1589. doi:10.1093/pcp/pci171Ferraioli, S., Tatè, R., Rogato, A., Chiurazzi, M., & Patriarca, E. J. (2004). Development of Ectopic Roots from Abortive Nodule Primordia. Molecular Plant-Microbe Interactions®, 17(10), 1043-1050. doi:10.1094/mpmi.2004.17.10.1043Franssen, H. J., Xiao, T. T., Kulikova, O., Wan, X., Bisseling, T., Scheres, B., & Heidstra, R. (2015). Root developmental programs shape the Medicago truncatula nodule meristem. Development, 142(17), 2941-2950. doi:10.1242/dev.120774Gonzalez-Rizzo, S., Crespi, M., & Frugier, F. (2006). The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti. The Plant Cell, 18(10), 2680-2693. doi:10.1105/tpc.106.043778Gourion, B., Sulser, S., Frunzke, J., Francez-Charlot, A., Stiefel, P., Pessi, G., … Fischer, H.-M. (2009). The PhyR-σEcfGsignalling cascade is involved in stress response and symbiotic efficiency inBradyrhizobium japonicum. Molecular Microbiology, 73(2), 291-305. doi:10.1111/j.1365-2958.2009.06769.xGourlay, C. W., Hofer, J. M. I., & Ellis, T. H. N. (2000). Pea Compound Leaf Architecture Is Regulated by Interactions among the Genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS. The Plant Cell, 12(8), 1279-1294. doi:10.1105/tpc.12.8.1279Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M. K., & Bonfante, P. (2009). Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist, 182(1), 200-212. doi:10.1111/j.1469-8137.2008.02725.xGuinel, F. C. (2009). Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types. Botany, 87(12), 1117-1138. doi:10.1139/b09-074Ha, C. M. (2003). The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development, 130(1), 161-172. doi:10.1242/dev.00196Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2004). BLADE-ON-PETIOLE1 Encodes a BTB/POZ Domain Protein Required for Leaf Morphogenesis in Arabidopsis thaliana. Plant and Cell Physiology, 45(10), 1361-1370. doi:10.1093/pcp/pch201Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2007). BLADE-ON-PETIOLE1 and 2 Control Arabidopsis Lateral Organ Fate through Regulation of LOB Domain and Adaxial-Abaxial Polarity Genes. The Plant Cell, 19(6), 1809-1825. doi:10.1105/tpc.107.051938Handberg, K., & Stougaard, J. (1992). Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal, 2(4), 487-496. doi:10.1111/j.1365-313x.1992.00487.xHepworth, S. R., & Pautot, V. A. (2015). Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01052Hepworth, S. R., Zhang, Y., McKim, S., Li, X., & Haughn, G. W. (2005). BLADE-ON-PETIOLE–Dependent Signaling Controls Leaf and Floral Patterning in Arabidopsis. The Plant Cell, 17(5), 1434-1448. doi:10.1105/tpc.104.030536Hepworth, S. R., Klenz, J. E., & Haughn, G. W. (2005). UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta, 223(4), 769-778. doi:10.1007/s00425-005-0138-3Hibara, K., Karim, M. R., Takada, S., Taoka, K., Furutani, M., Aida, M., & Tasaka, M. (2006). Arabidopsis CUP-SHAPED COTYLEDON3 Regulates Postembryonic Shoot Meristem and Organ Boundary Formation. The Plant Cell, 18(11), 2946-2957. doi:10.1105/tpc.106.045716Høgslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M. A., Goffard, N., … Stougaard, J. (2009). Dissection of Symbiosis and Organ Development by Integrated Transcriptome Analysis of Lotus japonicus Mutant and Wild-Type Plants. PLoS ONE, 4(8), e6556. doi:10.1371/journal.pone.0006556JARVIS, B. D. W., PANKHURST, C. E., & PATEL, J. J. (1982). Rhizobium loti, a New Species of Legume Root Nodule Bacteria. International Journal of Systematic Bacteriology, 32(3), 378-380. doi:10.1099/00207713-32-3-378Karim, M. R., Hirota, A., Kwiatkowska, D., Tasaka, M., & Aida, M. (2009). A Role for Arabidopsis PUCHI in Floral Meristem Identity and Bract Suppression. The Plant Cell, 21(5), 1360-1372. doi:10.1105/tpc.109.067025Khan, M., Xu, M., Murmu, J., Tabb, P., Liu, Y., Storey, K., … Hepworth, S. R. (2011). Antagonistic Interaction of BLADE-ON-PETIOLE1 and 2 with BREVIPEDICELLUS and PENNYWISE Regulates Arabidopsis Inflorescence Architecture. Plant Physiology, 158(2), 946-960. doi:10.1104/pp.111.188573Koch, B., & Evans, H. J. (1966). Reduction of Acetylene to Ethylene by Soybean Root Nodules. Plant Physiology, 41(10), 1748-1750. doi:10.1104/pp.41.10.1748Krall, L., Wiedemann, U., Unsin, G., Weiss, S., Domke, N., & Baron, C. (2002). Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, 99(17), 11405-11410. doi:10.1073/pnas.172390699Kumagai, H., & Kouchi, H. (2003). Gene Silencing by Expression of Hairpin RNA in Lotus japonicus Roots and Root Nodules. Molecular Plant-Microbe Interactions®, 16(8), 663-668. doi:10.1094/mpmi.2003.16.8.663Levin, J. Z., & Meyerowitz, E. M. (1995). UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. The Plant Cell, 7(5), 529-548. doi:10.1105/tpc.7.5.529Long, J., & Barton, M. K. (2000). Initiation of Axillary and Floral Meristems in Arabidopsis. Developmental Biology, 218(2), 341-353. doi:10.1006/dbio.1999.9572Małolepszy, A., Mun, T., Sandal, N., Gupta, V., Dubin, M., Urbański, D., … Andersen, S. U. (2016). The LORE 1 insertion mutant resource. The Plant Journal, 88(2), 306-317. doi:10.1111/tpj.13243McKim, S. M., Stenvik, G.-E., Butenko, M. A., Kristiansen, W., Cho, S. K., Hepworth, S. R., … Haughn, G. W. (2008). The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development, 135(8), 1537-1546. doi:10.1242/dev.012807Mun, T., Bachmann, A., Gupta, V., Stougaard, J., & Andersen, S. U. (2016). Lotus Base: An integrated information portal for the model legume Lotus japonicus. Scientific Reports, 6(1). doi:10.1038/srep39447Norberg, M. (2005). The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development, 132(9), 2203-2213. doi:10.1242/dev.01815Okamoto, S., Yoro, E., Suzaki, T., & Kawaguchi, M. (2013). Hairy Root Transformation in Lotus japonicus. BIO-PROTOCOL, 3(12). doi:10.21769/bioprotoc.795Oldroyd, G. E. D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology, 11(4), 252-263. doi:10.1038/nrmicro2990Oldroyd, G. E. D., & Downie, J. A. (2008). Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes. Annual Review of Plant Biology, 59(1), 519-546. doi:10.1146/annurev.arplant.59.032607.092839Pate, J. S., Gunning, B. E. S., & Briarty, L. G. (1969). Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta, 85(1), 11-34. doi:10.1007/bf00387658Ping, J., Liu, Y., Sun, L., Zhao, M., Li, Y., She, M., … Ma, J. (2014). Dt2 Is a Gain-of-Function MADS-Domain Factor Gene That Specifies Semideterminacy in Soybean. The Plant Cell, 26(7), 2831-2842. doi:10.1105/tpc.114.126938Quandt, H.-J. (1993). Transgenic Root Nodules ofVicia hirsuta:A Fast and Efficient System for the Study of Gene Expression in Indeterminate-Type Nodules. Molecular Plant-Microbe Interactions, 6(6), 699. doi:10.1094/mpmi-6-699Roux, B., Rodde, N., Jardinaud, M.-F., Timmers, T., Sauviac, L., Cottret, L., … Gamas, P. (2014). An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. The Plant Journal, 77(6), 817-837. doi:10.1111/tpj.12442Schultz, E. A., & Haughn, G. W. (1991). LEAFY, a Homeotic Gene That Regulates Inflorescence Development in Arabidopsis. The Plant Cell, 771-781. doi:10.1105/tpc.3.8.771Sinharoy, S., & DasGupta, M. (2009). RNA Interference Highlights the Role of CCaMK in Dissemination of Endosymbionts in the Aeschynomeneae Legume Arachis. Molecular Plant-Microbe Interactions®, 22(11), 1466-1475. doi:10.1094/mpmi-22-11-1466Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., & Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, 92(7), 2647-2651. doi:10.1073/pnas.92.7.2647Soyano, T., Kouchi, H., Hirota, A., & Hayashi, M. (2013). NODULE INCEPTION Directly Targets NF-Y Subunit Genes to Regulate Essential Processes of Root Nodule Development in Lotus japonicus. PLoS Genetics, 9(3), e1003352. doi:10.1371/journal.pgen.1003352Suzaki, T., Yoro, E., & Kawaguchi, M. (2015). Leguminous Plants: Inventors of Root Nodules to Accommodate Symbiotic Bacteria. International Review of Cell and Molecular Biology, 111-158. doi:10.1016/bs.ircmb.2015.01.004Takeda, S., Hanano, K., Kariya, A., Shimizu, S., Zhao, L., Matsui, M., … Aida, M. (2011). CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. The Plant Journal, 66(6), 1066-1077. doi:10.1111/j.1365-313x.2011.04571.xTavakol, E., Okagaki, R., Verderio, G., Shariati J., V., Hussien, A., Bilgic, H., … Rossini, L. (2015). The Barley Uniculme4 Gene Encodes a BLADE-ON-PETIOLE-Like Protein That Controls Tillering and Leaf Patterning. Plant Physiology, 168(1), 164-174. doi:10.1104/pp.114.252882Udvardi, M., & Poole, P. S. (2013). Transport and Metabolism in Legume-Rhizobia Symbioses. Annual Review of Plant Biology, 64(1), 781-805. doi:10.1146/annurev-arplant-050312-120235Van de Velde, W., Guerra, J. C. P., Keyser, A. D., De Rycke, R., Rombauts, S., Maunoury, N., … Goormachtig, S. (2006). Aging in Legume Symbiosis. A Molecular View on Nodule Senescence in Medicago truncatula. Plant Physiology, 141(2), 711-720. doi:10.1104/pp.106.078691Verdier, J., Torres-Jerez, I., Wang, M., Andriankaja, A., Allen, S. N., He, J., … Udvardi, M. K. (2013). Establishment of theLotus japonicusGene Expression Atlas (LjGEA) and its use to explore legume seed maturation. The Plant Journal, 74(2), 351-362. doi:10.1111/tpj.12119WALSH, K. B., McCULLY, M. E., & CANNY, M. J. (1989). Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway. Plant, Cell and Environment, 12(4), 395-405. doi:10.1111/j.1365-3040.1989.tb01955.xWang, Q., Hasson, A., Rossmann, S., & Theres, K. (2015). Divide et impera : boundaries shape the plant body and initiate new meristems. New Phytologist, 209(2), 485-498. doi:10.1111/nph.13641Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., … Yang, J. (2011). Petal Development in Lotus japonicus. Journal of Integrative Plant Biology, 53(10), 770-782. doi:10.1111/j.1744-7909.2011.01072.xWerner, G. D. A., Cornwell, W. K., Sprent, J. I., Kattge, J., & Kiers, E. T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Communications, 5(1). doi:10.1038/ncomms5087Wopereis, J., Pajuelo, E., Dazzo, F. B., Jiang, Q., Gresshoff, P. M., de Bruijn, F. J., … Szczyglowski, K. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal, 23(1), 97-114. doi:10.1046/j.1365-313x.2000.00799.xWu, X.-M., Yu, Y., Han, L.-B., Li, C.-L., Wang, H.-Y., Zhong, N.-Q., … Xia, G.-X. (2012). The Tobacco BLADE-ON-PETIOLE2 Gene Mediates Differentiation of the Corolla Abscission Zone by Controlling Longitudinal Cell Expansion. Plant Physiology, 159(2), 835-850. doi:10.1104/pp.112.193482Xu, M., Hu, T., McKim, S. M., Murmu, J., Haughn, G. W., & Hepworth, S. R. (2010). Arabidopsis BLADE-ON-PETIOLE1 and 2 promote floral meristem fate and determinacy in a previously undefined pathway targeting APETALA1 and AGAMOUS-LIKE24. The Plant Journal, 63(6), 974-989. doi:10.1111/j.1365-313x.2010.04299.xXu, C., Park, S. J., Van Eck, J., & Lippman, Z. B. (2016). Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes & Development, 30(18), 2048-2061. doi:10.1101/gad.288415.116Yaxley, J. (2001). Leaf and Flower Development in Pea (Pisum sativum L.): Mutants cochleata andunifoliata. Annals of Botany, 88(2), 225-234. doi:10.1006/anbo.2001.1448Žádníková, P., & Simon, R. (2014). How boundaries control plant development. Current Opinion in Plant Biology, 17, 116-125. doi:10.1016/j.pbi.2013.11.013Zhang, S., Sandal, N., Polowick, P. L., Stiller, J., Stougaard, J., & Fobert, P. R. (2003). Proliferating Floral Organs (Pfo ), a Lotus japonicus gene required for specifying floral meristem determinacy and organ identity, encodes an F-box protein. The Plant Journal, 33(4), 607-619. doi:10.1046/j.1365-313x.2003.01660.

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This consensus article reviews the various aspects of the non-pharmacological management of osteoporosis, including the effects of nutriments, physical exercise, lifestyle, fall prevention, and hip protectors. Vertebroplasty is also briefly reviewed. Non-pharmacological management of osteoporosis is a broad concept. It must be viewed as an essential part of the prevention of fractures from childhood through adulthood and the old age. The topic also includes surgical procedures for the treatment of peripheral and vertebral fractures and the post-fracture rehabilitation. The present document is the result of a consensus, based on a systematic review and a critical appraisal of the literature. Diets deficient in calcium, proteins or vitamin D impair skeletal integrity. The effect of other nutriments is less clear, although an excessive consumption of sodium, caffeine, or fibres exerts negative effects on calcium balance. The deleterious effects of tobacco, excessive alcohol consumption and a low BMI are well accepted. Physical activity is of primary importance to reach optimal peak bone mass but, if numerous studies have shown the beneficial effects of various types of exercise on bone mass, fracture data as an endpoint are scanty. Fall prevention strategies are especially efficient in the community setting, but less evidence is available about their effectiveness in preventing fall-related injuries and fractures. The efficacy of hip protectors remains controversial. This is also true for vertebroplasty and kyphoplasty. Several randomized controlled studies had reported a short-term advantage of vertebroplasty over medical treatment for pain relief, but these findings have been questioned by recent sham-controlled randomized clinical studies

The Beta-adrenergic agonist, Ractopamine, increases skeletal muscle expression of Asparagine Synthetase as part of an integrated stress response gene program

Abstract Synthetic beta-adrenergic agonists (BA) have broad biomedical and agricultural application for increasing lean body mass, yet a poor understanding of the biology underpinning these agents is limiting further drug discovery potential. Growing female pigs (77 ± 7 kg) were administered the BA, Ractopamine (20 ppm in feed), or the recombinant growth hormone (GH), Reporcin (10 mg/48 hrs injected) for 1, 3, 7, 13 (n = 10 per treatment, per time point) or 27 days (n = 15 per treatment). Using RNA-sequencing and inferred pathway analysis, we examined temporal changes to the Longissimus Dorsi skeletal muscle transcriptome (n = 3 per treatment, per time point) relative to a feed-only control cohort. Gene expression changes were affirmed by quantitative-PCR on all samples (n = 164). RNA-sequencing analysis revealed that BA treatment had greater effects than GH, and that asparagine synthetase (Asns) was the 5th most significantly increased gene by BA at day 3. ASNS protein expression was dramatically increased by BA treatment at day 7 (p < 0.05). The most significantly increased gene at day 3 was activating transcription factor 5 (Atf5), a transcription factor known to regulate ASNS gene expression. Gene and protein expression of Atf4, another known regulator of Asns expression, was not changed by BA treatment. Expression of more than 20 known Atf4 target genes were increased by BA treatment, suggesting that BA treatment induces an integrated stress response (ISR) in skeletal muscle of pigs. In support of this, mRNA expression of sestrin-2 (Sesn2) and cyclin-dependant kinase 1 alpha (Cdkn1a), two key stress-responsive genes and negative regulators of cellular growth, were also strongly increased from day 3 of BA treatment. Finally, tRNA charging was the most significantly enriched pathway induced by BA treatment, suggesting alterations to the translational capacity/efficiency of the muscle. BA-mediated changes to the skeletal muscle transcriptome are highly indicative of an integrated stress response (ISR), particularly genes relating to amino acid biosynthesis and protein translational capacity

Frequently asked questions about chlorophyll fluorescence, the sequel

[EN] Using chlorophyll (Chl) a fluorescence many aspects of the photosynthetic apparatus can be studied, both in vitro and, noninvasively, in vivo. Complementary techniques can help to interpret changes in the Chl a fluorescence kinetics. Kalaji et al. (Photosynth Res 122: 121-158, 2014a) addressed several questions about instruments, methods and applications based on Chl a fluorescence. Here, additionalChl a fluorescence-related topics are discussed again in a question and answer format. Examples are the effect of connectivity on photochemical quenching, the correction of F-V/F-M values for PSI fluorescence, the energy partitioning concept, the interpretation of the complementary area, probing the donor side of PSII, the assignment of bands of 77 K fluorescence emission spectra to fluorescence emitters, the relationship between prompt and delayed fluorescence, potential problems when sampling tree canopies, the use of fluorescence parameters in QTL studies, the use of Chl a fluorescence in biosensor applications and the application of neural network approaches for the analysis of fluorescence measurements. The answers draw on knowledge fromdifferent Chl a fluorescence analysis domains, yielding in several cases new insights.Kalaji, H.; Schansker, G.; Brestic, M.; Bussotti, F.; Calatayud, A.; Ferroni, L.; Goltsev, V.... (2017). Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Research. 132(1):13-66. https://doi.org/10.1007/s11120-016-0318-yS13661321Adams WW III, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Plant 186:390–398Adams WW III, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration series chlorophyll fluorescence: a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 583–604Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990a) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180:166–174Adams WW III, Winter K, Schreiber U, Schramel P (1990b) Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal senescence. Plant Physiol 93:1184–1190Alfonso M, Montoya G, Cases R, Rodriguez R, Picorel R (1994) Core antenna complexes, CP43 and CP47, of higher plant photosystem II. Spectral properties, pigment stoichiometry, and amino acid composition. Biochemistry 33:10494–10500Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B Biol 104:1–8Allakhverdiev SI, Klimov VV, Carpentier R (1994) Variable thermal emission and chlorophyll fluorescence in photosystem II particles. Proc Natl Acad Sci USA 491:281–285Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples platoquinone redox state to distribution of excitation energy between photosystems. Nature 291:21–25Amesz J, van Gorkom HJ (1978) Delayed fluorescence in photosynthesis. Annu Rev Plant Physiol 29:47–66Ananyev GM, Dismukes GC (1996) Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation: Mn stoichiometry and detection of a new intermediate. Biochemistry 35:4102–4109Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15:11–26Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180Anithakumari AM, Nataraja KN, Visser RGF, van der Linden G (2012) Genetic dissection of drought tolerance and recovery potential by quantitative trait locus mapping of a diploid potato population. Mol Breed 30:1413–1429Antal TK, Krendeleva TE, Rubin AB (2007) Study of photosystem 2 heterogeneity in the sulfur-deficient green alga Chlamydomonas reinhardtii. Photosynth Res 94:13–22Antal TK, Matorin DN, Ilyash LV, Volgusheva AA, Osipov A, Konyuhow IV, Krendeleva TE, Rubin AB (2009) Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer. Photosynth Res 102:67–76Araus JL, Amaro T, Voltas J, Nakkoul H, Nachit MM (1998) Chlorophyll fluorescence as a selection criterion for grain yield in durum wheat under Mediterranean conditions. Field Crops Res 55:209–223Argyroudi-Akoyunoglou J (1984) The 77 K fluorescence spectrum of the Photosystem I pigment-protein complex CPIa. FEBS Lett 171:47–53Arnold WA (1991) Experiments. Photosynth Res 27:73–82Arnold WA, Thompson J (1956) Delayed light production by blue-green algae, red algae and purple bacteria. J Gen Physiol 39:311–318Aro EM, Hundal T, Carlberg I, Andersson B (1990) In vitro studies on light-induced inhibition of PSII and D1-protein degradation at low temperatures. Biochim Biophys Acta 1019:269–275Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation protein damage and turnover. Biochim Biophys Acta 1143:113–134Arsalane W, Parésys G, Duval JC, Wilhelm C, Conrad R, Büchel C (1993) A new fluorometric device to measure the in vivo chlorophyll a fluorescence yield in microalgae and its use as a herbicide monitor. Eur J Phycol 28:247–252Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16Bailey 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 213:794–801Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:659–668Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621Ballottari 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 282:8947–8958Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132:485–493Barber J, Malkin S, Telfer A (1989) The origin of chlorophyll fluorescence in vivo and its quenching by the photosystem II reaction centre. Philos Trans R Soc Lond B 323:227–239Barra M, Haumann M, Loja P, Krivanek R, Grundmeier A, Dau H (2006) Intermediates in assembly by photoactivation after thermally accelerated disassembly of the manganese complex of photosynthetic water oxidation. Biochemistry 45:14523–14532Baumann HA, Morrison L, Stengel DB (2009) Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol Environ Safe 72:1063–1075Bauwe H, Hagemann M, Fernie A (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336Beck WF, Brudvig GW (1987) Reactions of hydroxylamine with the electron-donor side of photosystem II. Biochemistry 26:8285–8295Belgio E, Kapitonova E, Chmeliov J, Duffy CDP, Ungerer P, Valkunas L, Ruban AV (2014) Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nat Commun 5:4433. doi: 10.1038/ncomms5433Bell DH, Hipkins MF (1985) Analysis of fluorescence induction curves from pea chloroplasts: photosystem II reaction centre heterogeneity. Biochim Biophys Acta 807:255–262Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB (2015) Modeling of the redox state dynamics in photosystem II of Chlorella pyrenoidosa Chick cells and leaves of spinach and Arabidopsis thaliana from single flash-induced fluorescence quantum yield changes on the 100 ns–10 s time scale. Photosynth Res 125:123–140Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269:344–346Bennett J (1983) Regulation of photosynthesis by reversible phosphorylation of the light-harvesting chlorophyll a/b protein. Biochem J 212:1–13Bennett J, Shaw EK, Michel H (1988) Cytochrome b6f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes. Eur J Biochem 171:95–100Bennoun P (2002) The present model for chlororespiration. Photosynth Res 73:273–277Bennoun P, Li Y-S (1973) New results on the mode of action of 3,-(3,4-dichlorophenyl)-1,1-dimethylurea in spinach chloroplasts. Biochim Biophys Acta 292:162–168Berden-Zrimec M, Drinovec L, Zrimec A (2011) Delayed fluorescence. In: Suggett DJ, Borowitzka M, Prášil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications, developments in applied phycology, vol 4. Springer, The Netherlands, pp 293–309Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026Bernacchi CJ, Leakey ADB, Heady LE, Morgan PB, Dohleman FG, McGrath JM, Gillespie GM, Wittig VE, Rogers A, Long SP, Ort DR (2006) Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO2 and ozone concentrations for 3 years under fully open-air field conditions. Plant Cell Environ 29:2077–2090Betterle N, Ballotari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall’Osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284:15255–15266Bielczynski LW, Schansker G, Croce R (2016) Effect of light acclimation on the organization of photosystem II super and sub-complexes in Arabidopsis thaliana. Front Plant Sci. doi: 10.3389/fpls.2016.00105Björkman O, Demmig-Adams B (1995) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 17–47Blubaugh DJ, Cheniae GM (1990) Kinetics of photoinhibition in hydroxylamine-extracted photosystem II membranes: relevance to photoactivation and site of electron donation. Biochemistry 29:5109–5118Bock A, Krieger-Liszkay A, Ortiz de Zarate IB, Schönknecht G (2001) Cl—channel inhibitors of the arylaminobenzoate type act as photosystem II herbicides: a functional and structural study. Biochemistry 40:3273–3281Bode S, Quentmeier CC, Liao P-N, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106:12311–12316Boekema EJ, Van Roon H, Van Breemen JFL, Dekker JP (1999) Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur J Biochem 266:444–452Bolhar-Nordenkampf HR, Long SP, Baker NR, Öquist G, Schreiber U, Lechner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current Instrumentation. Funct Ecol 3:497–514Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12Bouges-Bocquet B (1980) Kinetic models for the electron donors of photosystem II of photosynthesis. Biochim Biophys Acta 594:85–103Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve; changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystem I and II. Biochim Biophys Acta 635:542–551Brestič M, Živčák M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Das AB, Rout GR (eds) Molecular stress physiology of plants. Springer, New Dehli, pp 87–131Brestič M, Cornic G, Fryer MJ, Baker NR (1995) Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196:450–457Brestič M, Živčák M, Kalaji HM, Allakhverdiev SI, Carpentier R (2012) Photosystem II thermo-stability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105Brody SS, Rabinowitch E (1957) Excitation lifetime of photosynthetic pigments in vitro and in vivo. Science 125:555–563Brudvig GW, Casey JL, Sauer K (1983) The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution. Biochim Biophys Acta 723:366–371Bukhov NG, Boucher N, Carpentier R (1997) The correlation between the induction kinetics of the photoacoustic signal and chlorophyll fluorescence in barley leaves is governed by changes in the redox state of the photosystem II acceptor side; a study under atmospheric and high CO2 concentrations. Can J Bot 75:1399–1406Bukhov N, Egorova E, Krendeleva T, Rubin A, Wiese C, Heber U (2001) Relaxation of variable chlorophyll fluorescence after illumination of dark-adapted barley leaves as influenced by the redox states of electron carriers. Photosynth Res 70:155–166Buschmann C, Koscányi L (1989) Light-induced heat production correlated with chlorophyll fluorescence and its quenching. Photosynth Res 21:129–136Bussotti F (2004) Assessment of stress conditions in Quercus ilex L. leaves by O-J-I-P chlorophyll a fluorescence analysis. Plant Biosystems 13:101–109Bussotti F, Agati G, Desotgiu R, Matteini P, Tani C (2005) Ozone foliar symptoms in woody plants assessed with ultrastructural and fluorescence analysis. New Phytol 166:941–955Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Salvatori E, Manes F, Schaub M, Strasser RJ (2011a) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19–30Bussotti F, Pollastrini M, Cascio C, Desotgiu R, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Pellegrini E, Carucci MG, Salvatori E, Fusaro L, Piccotto M, Malaspina P, Manfredi A, Roccotello E, Toscano S, Gottardini E, Cristofori A, Fini A, Weber D, Baldassarre V, Barbanti L, Monti A, Strasser RJ (2011b) Conclusive remarks. Reliability and comparability of chlorophyll fluorescence data from several field teams. Environ Exp Bot 73:116–119Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378Byrdin M, Rimke I, Schlodder E, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: Are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–1007Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476Calatayud A, Ramirez JW, Iglesias DJ, Barreno E (2002) Effects of ozone on photosynthetic CO2 exchange, chlorophyll a fluorescence and antioxidant systems in lettuce leaves. Physiol Plant 116:308–316Cascio C, Schaub M, Novak K, Desotgiu R, Bussotti F, Strasser RJ (2010) Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions. Environ Exp Bot 68:188–197Cazzaniga S, Dall’Osto L, Kong S-G, Wada M, Bassi R (2013) Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. Plant J 76:568–579Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288Chaudhary N, Singh S, Agrawal SB, Agrawal M (2013) Assessment of six Indian cultivars of mung bean against ozone by using foliar injury index and changes in carbon assimilation, gas exchange, chlorophyll fluorescence and photosynthetic pigments. Environ Monit Assess 185:7793–7807Chen J, Kell A, Acharya K, Kupitz C, Fromme P, Jankowiak R (2015) Critical assessment of the emission spectra of various photosystem II core complexes. Photosynth Res 124:253–265Cheng L, Fuchigami LH, Breen PJ (2000) Light absorption and partitioning in relation to nitrogen content ‘Fuji’ apple leaves. J Am Soc Hortic Sci 125:581–587Choi CJ, Berges JA, Young EB (2012) Rapid effects of diverse toxic water pollutants on chlorophyll a fluorescence: variable responses among freshwater microalgae. Water Res 46:2615–2626Chow WS, Aro EM (2005) Photoinactivation and mechanisms of recovery. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase, advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 627–648Chow WS, Fan DY, Oguchi R, Jia H, Losciale P, Youn-Il P, He J, Öquist G, Shen YG, Anderson JM (2012) Quantifying and monitoring functional photosystem II and the stoichiometry of the two photosystems in leaf segments: approaches and approximations. Photosynth Res 113:63–74Christensen MG, Teicher HB, Streibig JC (2003) Linking fluorescence induction curve and biomass in herbicide screening. Pest Manag Sci 59:1303–1310Codrea CM, Aittokallio T, Keränen M, Tyystjärvi E, Nevalainen OS (2003) Feature learning with a genetic algorithm for fluorescence fingerprinting of plant species. Pattern Recognit Lett 24:2663–2673Conjeaud H, Mathis P (1980) The effect of pH on the reduction kinetics of P-680 in tris-treated chloroplasts. Biochim Biophys Acta 590:353–359Conrad R, Büchel C, Wilhelm C, Arsalane W, Berkaloff C, Duval JC (1993) Changes in yield of in-vivo fluorescence of chlorophyll a as a tool for selective herbicide monitoring. J Appl Phycol 5:505–516Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publisher, Dordrecht, pp 347–366Cornic G, Fresneau C (2002) Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystems II during a mild drought. Ann Bot 89:887–894Correia MJ, Chaves MMC, Pereira JS (1990) Afternoon depression in photosynthesis in grapevine leaves—evidence for a high light stress effect. J Exp Bot 41:417–426Cotrozzi L, Remorini D, Pellegrini E, Landi M, Massai R, Nali C, Guidi L, Lorenzini G (2016) Variations in physiological and biochemical traits of oak seedlings grown under drought and ozone stress. Physiol Plant 157:69–84Croce R, Zucchelli G, Garlaschi FM, Bassi R, Jennings RC (1997) Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35:8572–8579Cser K, Vass I (2007) Radiative and non-radiative charge recombination pathways in photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6308. Biochim Biophys Acta 1767:233–243Czyczyło-Mysza I, Tyrka M, Marcińska Skrzypek E, Karbarz M, Dziurka M, Hura T, Dziurka K, Quarrie SA (2013) Quantitative trait loci for leaf chlorophyll fluorescence parameters, chlorophyll and carotenoid contents in relation to biomass and yield in bread wheat and their chromosome deletion bin assignments. Mol Breed 32:189–210D’Haene SE, Sobotka R, Bučinská L, Dekker JP, Komenda J (2015) Interaction of the PsbH subunit with a chlorophyll bound to histidine 114 of CP47 is responsible for the red 77 K fluorescence of Photosystem II. Biochim Biophys Acta 1847:1327–1334Dang NC, Zazubovich V, Reppert M, Neupane B, Picorel R, Seibert M, Jankowiak R (2008) The CP43 proximal antenna complex of higher plant photosystem II revisited: modeling and hole burning study. J Phys Chem B 112:9921–9933Dau H (1994) Molecular mechanisms and quantitative models of variable Photosystem II fluorescence. Photochem Photobiol 60:1–23Dau H, Sauer K (1992) Electric field effect on the picosecond fluorescence of photosystem II and its relation to the energetics and kinetics of primary charge separation. Biochim Biophys Acta 1102:91–106Dau H, Zaharieva I, Haumann M (2012) Recent developments in research on water oxidation by photosystem II. Curr Opin Chem Biol 16:3–10de Wijn R, van Gorkom HJ (2001) Kinetics of electron transfer from QA to QB in photosystem II. Biochemistry 40:11912–11922de Wijn R, van Gorkom HJ (2002) The rate of charge recombination in photosystem II. Biochim Biophys Acta 1553:302–308Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102:269–352Degl’Innocenti E, Guidi L, Soldatini GF (2002) Characteriz