Neutron scattering in photosynthesis research: recent advances and perspectives for testing crop plants
Language English Country Netherlands Media print-electronic
Document type Journal Article
PubMed
32488447
PubMed Central
PMC8556207
DOI
10.1007/s11120-020-00763-6
PII: 10.1007/s11120-020-00763-6
Knihovny.cz E-resources
- Keywords
- Macro-organization, Neutron scattering, Regulatory mechanisms, Structural flexibility, Thylakoid membrane,
- MeSH
- Photosynthesis * MeSH
- Scattering, Small Angle MeSH
- Neutrons MeSH
- Thylakoids * metabolism MeSH
- Publication type
- Journal Article MeSH
The photosynthetic performance of crop plants under a variety of environmental factors and stress conditions, at the fundamental level, depends largely on the organization and structural flexibility of thylakoid membranes. These highly organized membranes accommodate virtually all protein complexes and additional compounds carrying out the light reactions of photosynthesis. Most regulatory mechanisms fine-tuning the photosynthetic functions affect the organization of thylakoid membranes at different levels of the structural complexity. In order to monitor these reorganizations, non-invasive techniques are of special value. On the mesoscopic scale, small-angle neutron scattering (SANS) has been shown to deliver statistically and spatially averaged information on the periodic organization of the thylakoid membranes in vivo and/or, in isolated thylakoids, under physiologically relevant conditions, without fixation or staining. More importantly, SANS investigations have revealed rapid reversible reorganizations on the timescale of several seconds and minutes. In this paper, we give a short introduction into the basics of SANS technique, advantages and limitations, and briefly overview recent advances and potential applications of this technique in the physiology and biotechnology of crop plants. We also discuss future perspectives of neutron crystallography and different neutron scattering techniques, which are anticipated to become more accessible and of more use in photosynthesis research at new facilities with higher fluxes and innovative instrumentation.
Institute of Plant Biology Biological Research Centre POB 521 6701 Szeged Hungary
Neutron Scattering Division Oak Ridge National Laboratory Oak Ridge TN 37830 USA
See more in PubMed
Andersen KH, et al. The instrument suite of the European spallation source. Nucl Instrum Methods Phys Res Sect A. 2020;957:163402.
Bar Eyal L, et al. Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria. Proc Natl Acad Sci. 2017;114(35):9481–9486. PubMed PMC
Berthold DA, Babcock GT, Yocum CF. A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett. 1981;134(3):321.
Cardoso MB, Smolensky D, Heller WT, O'Neill H. Insight into the structure of light-harvesting complex II and its stabilization in detergent solution. J Phys Chem B. 2009;113(51):16377–16383. PubMed
Chen JC-H, Hanson BL, Fisher SZ, Langan P, Kovalevsky AY. Direct observation of hydrogen atom dynamics and interactions by ultrahigh resolution neutron protein crystallography. Proc Natl Acad Sci. 2012;109(38):15301–15306. PubMed PMC
Coates L, Robertson L. Ewald: an extended wide-angle Laue diffractometer for the second target station of the spallation neutron source. J Appl Crystallogr. 2017;50(Pt 4):1174–1178. PubMed PMC
Dekker JP, Boekema EJ. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta Bioenergy. 2005;1706(1–2):12–39. PubMed
Demé B, Cataye C, Block MA, Maréchal E, Jouhet J. Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J. 2014;28(8):3373–3383. PubMed
Doster W, Cusack S, Petry W. Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature. 1989;337(6209):754–756. PubMed
Engelman DM, Moore PB. A new method for the determination of biological quarternary structure by neutron scattering. Proc Natl Acad Sci. 1972;69(8):1997–1999. PubMed PMC
Fitter J, Gutberlet T, Katsaras J. Neutron scattering in biology. Berlin, Heidelberg: Springer-Verlag; 2006.
Garab G. Linear and circular dichroism. In: Amesz J, Hoff AJ, editors. Biophysical techniques in photosynthesis. Dordrecht: Kluwer Academic Publishers; 1996. pp. 11–40.
Golub M, Irrgang K-D, Rusevich L, Pieper J. Vibrational dynamics of plant light-harvesting complex LHC II investigated by quasi- and inelastic neutron scattering. EPJ Web Conf. 2015;83:02004.
Golub M, Rusevich L, Irrgang K-D, Pieper J. Rigid versus flexible protein matrix: light-harvesting complex II exhibits a temperature-dependent phonon spectral density. J Phys Chem B. 2018;122(28):7111–7121. PubMed
Golub M, Moldenhauer M, Schmitt F-J, Feoktystov A, Mändar H, Maksimov E, Friedrich T, Pieper J. Solution structure and conformational flexibility in the active state of the orange carotenoid protein: part I. Small-angle scattering. J Phys Chem B. 2019;123(45):9525–9535. PubMed
Golub M, Moldenhauer M, Schmitt F-J, Lohstroh W, Maksimov EG, Friedrich T, Pieper J. Solution structure and conformational flexibility in the active state of the orange carotenoid protein. Part II: quasielastic neutron scattering. J Phys Chem B. 2019;123(45):9536–9545. PubMed
Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON, Ünnep R, Nagy G, Zsiros O, Dana S, Solymosi K, Garab G, Szabó I, Spetea C, Lundin B. A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun. 2016;7:11654. PubMed PMC
Holm JK (2004) Structure and structural flexibility of chloroplast thylakoid membranes. Ph.D., Roskilde University
Hussein R, Ibrahim M, Chatterjee R, Coates L, Müh F, Yachandra VK, Yano J, Kern J, Dobbek H, Zouni A. Optimizing crystal size of photosystem II by macroseeding: toward neutron protein crystallography. Cryst Growth Des. 2018;18(1):85–94. PubMed PMC
Jakubauskas D, Kowalewska Ł, Sokolova AV, Garvey CJ, Mortensen K, Jensen PE, Kirkensgaard JJK. Ultrastructural modeling of small angle scattering from photosynthetic membranes. Sci Rep. 2019;9(1):19405. PubMed PMC
Karlsson PM, Herdean A, Adolfsson L, Beebo A, Nziengui H, Irigoyen S, Ünnep R, Zsiros O, Nagy G, Garab G, Aronsson H, Versaw WK, Spetea C. The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. Plant J. 2015;84:99–110. PubMed
Knox RS, Davidovich MA. Theory of fluorescence polarization in magnetically oriented photosynthetic systems. Biophys J. 1978;24(3):689–712. PubMed PMC
Liberton M, Collins AM, Page LE, O'Dell WB, O'Neill H, Urban VS, Timlin JA, Pakrasi HB. Probing the consequences of antenna modification in cyanobacteria. Photosynth Res. 2013;118(1–2):17–24. PubMed
Liberton M, Page LE, O'Dell WB, O'Neill H, Mamontov E, Urban VS, Pakrasi HB. Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. J Biol Chem. 2013;288(5):3632–3640. PubMed PMC
Lu X, Selvaraj B, Ghimire-Rijal S, Orf GS, Meilleur F, Blankenship RE, Cuneo MJ, Myles DAA. Neutron and X-ray analysis of the Fenna–Matthews–Olson photosynthetic antenna complex from Prosthecochloris aestuarii. Acta Crystallogr Sect F. 2019;75(3):171–175. PubMed PMC
Markó M, Nagy G, Aprigliano G, Oksanen E. Chapter seven—neutron macromolecular crystallography at the European spallation source. In: Moody PCE, editor. Methods in enzymology. Cambridge: Academic Press; 2020. pp. 125–151. PubMed
Meilleur F, Coates L, Cuneo MJ, Kovalevsky A, Myles DAA. The neutron macromolecular crystallography instruments at Oak Ridge national laboratory: advances, challenges, and opportunities. Crystals. 2018;8:388.
Nagy G. Structure and dynamics of photosynthetic membranes as revealed by neutron scattering. Grenoble: Université de Grenoble; 2011.
Nagy G, Posselt D, Kovács L, Holm JK, Szabó M, Ughy B, Rosta L, Peters J, Timmins P, Garab G. Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering. Biochem J. 2011;436(2):225–230. PubMed
Nagy G, Szabó M, Ünnep R, Káli G, Miloslavina Y, Lambrev PH, Zsiros O, Porcar L, Timmins P, Rosta L, Garab G. Modulation of the multilamellar membrane organization and of the chiral macrodomains in the diatom Phaeodactylum tricornutum revealed by small-angle neutron scattering and circular dichroism spectroscopy. Photosynth Res. 2012;111(1–2):71–79. PubMed
Nagy G, Kovács L, Ünnep R, Zsiros O, Almásy L, Rosta L, Timmins P, Peters J, Posselt D, Garab G. Kinetics of structural reorganizations in multilamellar photosynthetic membranes monitored by small angle neutron scattering. Eur Phys J E. 2013;36(7):69. PubMed
Nagy G, Garab G, Pieper J (2014a). Neutron scattering in photosynthesis research contemporary problems of photosynthesis. In: Allakhverdiev SI, Rubin AB, Shuvalov VA (eds) Moscow, Izhevsk Institute of Computer Science, pp 69–121
Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G, Minagawa J. Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proc Natl Acad Sci USA. 2014;111(13):5042–5047. PubMed PMC
Neylon C. Small angle neutron and X-ray scattering in structural biology: recent examples from the literature. Eur Biophys J. 2008;37(5):531–541. PubMed
Pieper J, Renger G. Flash-induced structural dynamics in photosystem II membrane fragments of green plants. Biochemistry. 2009;48(26):6111–6115. PubMed
Pieper J, Irrgang KD, Renger G, Lechner RE. Density of vibrational states of the light-harvesting complex II of green plants studied by inelastic neutron scattering. J Phys Chem B. 2004;108(29):10556–10565.
Pieper J, Hauß T, Buchsteiner A, Baczynski K, Adamiak K, Lechner RE, Renger G. Temperature- and hydration-dependent protein dynamics in photosystem II of green plants studied by quasielastic neutron scattering. Biochemistry. 2007;46(40):11398–11409. PubMed
Pieper J, Trapp M, Skomorokhov A, Natkaniec I, Peters J, Renger G. Temperature-dependent vibrational and conformational dynamics of photosystem II membrane fragments from spinach investigated by elastic and inelastic neutron scattering. Biochim Biophys Acta Bioenergy. 2012;1817(8):1213–1219. PubMed
Posselt D, Nagy G, Kirkensgaard JJ, Holm JK, Aagaard TH, Timmins P, Rétfalvi E, Rosta L, Kovács L. Garab G (2012) Small-angle neutron scattering study of the ultrastructure of chloroplast thylakoid membranes—periodicity and structural flexibility of the stroma lamellae. Biochim Biophys Acta. 1817;8:1220–1228. PubMed
Russo D, Lambreva MD, Simionesco CA, Sebban P, Rea G. Dynamics properties of photosynthetic microorganisms probed by incoherent neutron scattering. Biophys J. 2019;116(9):1759–1768. PubMed PMC
Sadler DM, Worcester DL. Neutron diffraction studies of oriented photosynthetic membranes. J Mol Biol. 1982;159(3):467–482. PubMed
Sokolov AP, Sakai VG. Experimental Techniques for studies of dynamics in soft materials. In: Sakai VG, Alba-Simionesco C, Chen SH, editors. Dynamics of soft matter. Neutron scattering applications and techniques. Boston: Springer; 2012.
Stingaciu LR, O'Neill H, Liberton M, Urban VS, Pakrasi HB, Ohl M. Revealing the dynamics of thylakoid membranes in living cyanobacterial cells. Sci Rep. 2016;6:19627. PubMed PMC
Stingaciu L-R, O'Neill HM, Liberton M, Pakrasi HB, Urban VS. Influence of chemically disrupted photosynthesis on cyanobacterial thylakoid dynamics in Synechocystis sp. PCC 6803. Sci Rep. 2019;9(1):5711–5711. PubMed PMC
Stuhrmann HB. Neutron small-angle scattering of biological macromolecules in solution. J Appl Cryst. 1974;7(2):173–178.
Svergun D, Koch MHJ. Small-angle scattering studies of biological macromolecules in solution. Rep Prog Phys. 2003;66(10):1735–1782.
Tang K, Blankenship RE. Neutron and light scattering studies of light-harvesting photosynthetic antenna complexes. Photosynth Res. 2012;111(1–2):205–2017. PubMed
Tang K, Urban VS, Wen J, Xin Y, Blankenship RE. SANS investigation of the photosynthetic machinery of Chloroflexus aurantiacus. Biophys J. 2010;99(8):2398–2407. PubMed PMC
Tang K, Zhu L, Urban VS, Collins AM, Biswas P, Blankenship RE. Temperature and ionic strength effects on the chlorosome light-harvesting antenna complex. Langmuir. 2011;27(8):4816–4828. PubMed
Thiyagarajan P, Tiede DM. Detergent micelle structure and micelle–micelle interactions determined by small-angle neutron scattering under solution conditions used for membrane protein crystallization. J Phys Chem. 1994;98(40):10343–40351.
Tiede DM, Thiyagarajan P. Characterization of photosynthetic supramolecular assemblies using small angle neutron scattering. In: Amesz J, Hoff AJ, editors. Biophysical techniquest in photosynthesis. Dordrecht: Kluwer Academic Publishers; 1996. pp. 375–390.
Tiede DM, Littrell K, Marone PA, Zhang R, Thiyagarajan P. Solution structure of a biological bimolecular electron transfer complex: characterization of the photosynthetic reaction center-cytochrome c2 protein complex by small angle neutron scattering. J Appl Cryst. 2000;33(1):560–564.
Ünnep R, Nagy G, Markó M, Garab G. Monitoring thylakoid ultrastructural changes in vivo using small-angle neutron scattering. Plant Physiol Biochem. 2014;S0981–9428(14):00049. PubMed
Ünnep R, Zsiros O, Solymosi K, Kovács L, Lambrev P, Tóth T, Schweins R, Posselt D, Székely NK, Rosta L, Nagy G, Garab G. The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering. Biochim Biophys Acta Bioenergy. 2014;1837(9):1572–1580. PubMed
Ünnep R, Zsiros O, Hörcsik Z, Markó M, Jajoo A, Kohlbrecher J, Garab G. Nagy G (2017) Low-pH induced reversible reorganizations of chloroplast thylakoid membranes—as revealed by small-angle neutron scattering. Biochim Biophys Acta. 1858;5:360–365. PubMed
Vrandecic K, Rätsep M, Wilk L, Rusevich L, Golub M, Reppert M, Irrgang K-D, Kühlbrandt W, Pieper J. Protein dynamics tunes excited state positions in light-harvesting complex II. J Phys Chem B. 2015;119(10):3920–3930. PubMed
Wang Z, Umetsu M, Yoza K, Kobayashi M, Imai M, Matsushita Y, Niimura N, Nozawa T. A small-angle neutron scattering study on the small aggregates of bacteriochlorophylls in solution. Biochim Biophys Acta Bioenergy. 1997;1320(1):73–82.
Wang Z, Muraoka Y, Nagao M, Shibayama M, Kobayashi M, Nozowa T. Determination of the B820 subunit size of a bacterial core light-harvesting complex by small-angle neutron scattering. Biochemistry. 2003;42(39):11555–11560. PubMed
Worcester DL. Neutron beam studies of biological membranes and membrane components. In: Chapman D, Wallach DFH, editors. Biological membranes. London: Academic Press; 1976. pp. 1–44.
Worcester DL, Michalski TJ, Katz JJ. Small-angle neutron scattering studies of chlorophyll micelles: models for bacterial antenna chlorophyll. Proc Natl Acad Sci USA. 1986;83(11):3791–3795. PubMed PMC
Worcester DL, Michalski TJ, Tyson RL, Bowman MK, Katz JJ. Structure, red-shifted absorption and electron transport properties of specific aggregates of chlorophylls. Phys B. 1989;156–157:502.
Zaccai G. How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science. 2000;288:1604–1607. PubMed
Zaccai G, Natali F, Peters J, Řihová M, Zimmerman E, Ollivier J, Combet J, Maurel M-C, Bashan A, Yonath A. The fluctuating ribosome: thermal molecular dynamics characterized by neutron scattering. Sci Rep. 2016;6(1):37138. PubMed PMC