Molecular Dynamics of Chloroplast Membranes Isolated from Wild-Type Barley and a Brassinosteroid-Deficient Mutant Acclimated to Low and High Temperatures

. 2020 Dec 29 ; 11 (1) : . [epub] 20201229

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33383794

Grantová podpora
2018/31/N/NZ9/02430 National Science Centre (Poland) - International
No. CZ.02.1.01/0.0/0.0/16_019/0000827 European Regional Development Fund - International

Plants have developed various acclimation strategies in order to counteract the negative effects of abiotic stresses (including temperature stress), and biological membranes are important elements in these strategies. Brassinosteroids (BR) are plant steroid hormones that regulate plant growth and development and modulate their reaction against many environmental stresses including temperature stress, but their role in modifying the properties of the biological membrane is poorly known. In this paper, we characterise the molecular dynamics of chloroplast membranes that had been isolated from wild-type and a BR-deficient barley mutant that had been acclimated to low and high temperatures in order to enrich the knowledge about the role of BR as regulators of the dynamics of the photosynthetic membranes. The molecular dynamics of the membranes was investigated using electron paramagnetic resonance (EPR) spectroscopy in both a hydrophilic and hydrophobic area of the membranes. The content of BR was determined, and other important membrane components that affect their molecular dynamics such as chlorophylls, carotenoids and fatty acids in these membranes were also determined. The chloroplast membranes of the BR-mutant had a higher degree of rigidification than the membranes of the wild type. In the hydrophilic area, the most visible differences were observed in plants that had been grown at 20 °C, whereas in the hydrophobic core, they were visible at both 20 and 5 °C. There were no differences in the molecular dynamics of the studied membranes in the chloroplast membranes that had been isolated from plants that had been grown at 27 °C. The role of BR in regulating the molecular dynamics of the photosynthetic membranes will be discussed against the background of an analysis of the photosynthetic pigments and fatty acid composition in the chloroplasts.

Zobrazit více v PubMed

Koyro H.-W., Ahmad P., Geissler N. Abiotic stress responses in plants: An overview. In: Ahmad P., Prasad M., editors. Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer; New York, NY, USA: 2012. pp. 1–28.

Hasanuzzaman M., Hossain M.A., da Silva J.A.T., Fujita M. Plant response and tolerance to abiotic oxidative stress: Antioxidant defense is a key factor. In: Venkateswarlu B., Shanker A., Shanker C., Maheswari M., editors. Crop Stress and Its Management: Perspectives and Strategies. Springer; Dordrecht, The Netherlands: 2012. pp. 261–315.

Prasad M.N.V., Rengel Z. Plant acclimation and adaptation to natural and anthropogenic stress. Ann. N. Y. Acad. Sci. 1998;851:216–223. doi: 10.1111/j.1749-6632.1998.tb08996.x. DOI

Horváth I., Glatz A., Nakamoto H., Mishkind M.L., Munnik T., Saidi Y., Goloubinoff P., Harwood J.L., Vigh L. Heat shock response in photosynthetic organisms: Membrane and lipid connections. Prog. Lipid Res. 2012;51:208–220. doi: 10.1016/j.plipres.2012.02.002. PubMed DOI

Gzyl-Malcher B., Zembala M., Filek M. Effect of tocopherol on surface properties of plastid lipids originating from wheat calli cultivated in cadmium presence. Chem. Phys. Lipids. 2010;163:74–81. doi: 10.1016/j.chemphyslip.2009.11.001. PubMed DOI

Strzałka K., Kostecka-Gugała A., Latowski D. Carotenoids and environmental stress in plants: Significance of carotenoid-mediated modulation of membrane physical properties. Russ. J. Plant Physiol. 2003;50:168–173. doi: 10.1023/A:1022960828050. DOI

Mitchell J.W., Mandava N., Worley J.F., Plimmer J.R., Smith M.V. Brassins—A new family of plant hormones from rape pollen. Nat. Cell Biol. 1970;225:1065–1066. doi: 10.1038/2251065a0. PubMed DOI

Grove M.D., Spencer G.F., Rohwedder W.K., Mandava N., Worley J.F., Warthen J.D., Steffens G.L., Flippen-Anderson J.L., Cook J.C. Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nat. Cell Biol. 1979;281:216–217. doi: 10.1038/281216a0. DOI

Bajguz A., Hayat S. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 2009;47:1–8. doi: 10.1016/j.plaphy.2008.10.002. PubMed DOI

Sadura I., Janeczko A. Physiological and molecular mechanisms of brassinosteroid-induced tolerance to high and low temperature in plants. Biol. Plant. 2018;62:601–616. doi: 10.1007/s10535-018-0805-4. DOI

Sadura I., Libik-Konieczny M., Jurczyk B., Gruszka D., Janeczko A. Plasma membrane ATPase and the aquaporin HvPIP1 in barley brassinosteroid mutants acclimated to high and low temperature. J. Plant Physiol. 2020;244:153090. doi: 10.1016/j.jplph.2019.153090. PubMed DOI

Sadura I., Libik-Konieczny M., Jurczyk B., Gruszka D., Janeczko A. HSP transcript and protein accumulation in brassinosteroid barley mutants acclimated to low and high temperatures. Int. J. Mol. Sci. 2020;21:1889. doi: 10.3390/ijms21051889. PubMed DOI PMC

Rudolphi-Szydło E., Sadura I., Filek M., Gruszka D., Janeczko A. The impact of mutations in the HvCPD and HvBRI1 genes on the physicochemical properties of the membranes from barley acclimated to low/high temperatures. Cells. 2020;9:1125. doi: 10.3390/cells9051125. PubMed DOI PMC

Bojko M., Olchawa-Pajor M., Goss R., Schaller-Laudel S., Strzałka K., Latowski D. Diadinoxanthin de-epoxidation as important factor in the short-term stabilization of diatom photosynthetic membranes exposed to different temperatures. Plant Cell Environ. 2018;42:1270–1286. doi: 10.1111/pce.13469. PubMed DOI

Strzałka K., Hara-Nishimura I., Nishimura M. Changes in physical properties of vacuolar membrane during transformation of protein bodies into vacuoles in germinating pumpkin seeds. Biochim. Biophys. Acta (BBA) Biomembr. 1995;1239:103–110. doi: 10.1016/0005-2736(95)00141-O. PubMed DOI

Jajić I., Wisniewska-Becker A., Sarna T., Jemioła-Rzemińska M., Strzałka K. EPR spin labeling measurements of thylakoid membrane fluidity during barley leaf senescence. J. Plant Physiol. 2014;171:1046–1053. doi: 10.1016/j.jplph.2014.03.017. PubMed DOI

Pottosin I., Shabala S. Transport across chloroplast membranes: Optimizing photosynthesis for adverse environmental conditions. Mol. Plant. 2016;9:356–370. doi: 10.1016/j.molp.2015.10.006. PubMed DOI

Gruszka D., Szarejko I., Maluszynski M. Identification of barley DWARF gene involved in brassinosteroid synthesis. Plant Growth Regul. 2011;65:343–358. doi: 10.1007/s10725-011-9607-9. DOI

Gruszka D., Gorniak M., Glodowska E., Wierus E., Oklestkova J., Janeczko A., Maluszynski M., Szarejko I. A reverse-genetics mutational analysis of the barley HvDWARF gene results in identification of a series of alleles and mutants with short stature of various degree and disturbance in BR biosynthesis allowing a new insight into the process. Int. J. Mol. Sci. 2016;17:600. doi: 10.3390/ijms17040600. PubMed DOI PMC

Sadura I., Pociecha E., Dziurka M., Oklestkova J., Novak O., Gruszka D., Janeczko A. Mutations in the HvDWARF, HvCPD and HvBRI1 genes-involved in brassinosteroid biosynthesis/signalling: Altered photosynthetic efficiency, hormonal homeostasis and tolerance to high/low temperatures in barley. J. Plant Growth Regul. 2019;38:1062–1081. doi: 10.1007/s00344-019-09914-z. DOI

Pociecha E., Dziurka M., Oklestkova J., Janeczko A. Brassinosteroids increase winter survival of winter rye (Secale cereale L.) by affecting photosynthetic capacity and carbohydrate metabolism during the cold acclimation process. Plant Growth Regul. 2016;80:127–135. doi: 10.1007/s10725-016-0149-z. DOI

Janeczko A., Pociecha E., Dziurka M., Jurczyk B., Libik-Konieczny M., Oklestkova J., Novak O., Pilarska M., Filek M., Rudolphi-Skórska E., et al. Changes in content of steroid regulators during cold hardening of winter wheat—Steroid physiological/biochemical activity and impact on frost resistance. Plant Physiol. Biochem. 2019;139:215–228. doi: 10.1016/j.plaphy.2019.03.020. PubMed DOI

Fowler D.B., Limin A.E., Wang S.-Y., Ward R. Relationship between low-temperature tolerance and vernalization response in wheat and rye. Can. J. Plant Sci. 1996;76:37–42. doi: 10.4141/cjps96-007. DOI

Wu X., Yao X., Chen J., Zhu Z., Zhang H., Zha D.S. Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol. Plant. 2014;36:251–261. doi: 10.1007/s11738-013-1406-7. DOI

Thussagunpanit J., Jutamanee K., Kaveeta L., Chai-Arree W., Pankean P., Homvisasevongsa S., Suksamrarn A. Comparative effects of brassinosteroid and brassinosteroid mimic on improving photosynthesis, lipid peroxidation, and rice seed set under heat stress. J. Plant Growth Regul. 2015;34:320–331. doi: 10.1007/s00344-014-9467-4. DOI

Block M.A., Dorne A.J., Joyard J., Douce R. Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J. Biol. Chem. 1983;258:13281–13286. PubMed

Filek M., Sieprawska A., Kościelniak J., Oklestkova J., Jurczyk B., Telk A., Biesaga-Kościelniak J., Janeczko A. The role of chloroplasts in the oxidative stress that is induced by zearalenone in wheat plants—The functions of 24-epibrassinolide and selenium in the protective mechanisms. Plant Physiol. Biochem. 2019;137:84–92. doi: 10.1016/j.plaphy.2019.01.030. PubMed DOI

Sedmak J., Grossberg S.E. A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250. Anal. Biochem. 1977;79:544–552. doi: 10.1016/0003-2697(77)90428-6. PubMed DOI

Trela A., Silska G., Chyc M., Latowski D., Kruk J., Szymańska R. Tocochromanols and fatty acid composition in flax (Linum usitatissimum L.) accessions. Acta Soc. Bot. Pol. 2019;88:1–12. doi: 10.5586/asbp.3636. DOI

Lichtenthaler H.K. Methods in Enzymology. Volume 148. Academic Press; Orlando, FL, USA: 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes; pp. 350–382.

Oklestkova J., Tarkowská D., Eyer L., Elbert T., Marek A., Smržová Z., Novák O., Fránek M., Zhabinskii V.N., Strnad M. Immunoaffinity chromatography combined with tandem mass spectrometry: A new tool for the selective capture and analysis of brassinosteroid plant hormones. Talanta. 2017;170:432–440. doi: 10.1016/j.talanta.2017.04.044. PubMed DOI

Tarkowská D., Novák O., Oklestkova J., Strnad M. The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS. Anal. Bioanal. Chem. 2016;408:6799–6812. doi: 10.1007/s00216-016-9807-2. PubMed DOI

Marsch D. Electron spin resonance: Spin labels. In: Grell E., editor. Membrane Spectroscopy. Volume 31. Springer; Berlin/Heidelberg, Germany: 1981. pp. 51–137.

Berliner L.J. Spin labeling in enzymology: Spin-labeled enzymes and proteins. Methods Enzymol. 1978;49:418–480. doi: 10.1016/s0076-6879(78)49020-2. PubMed DOI

Mikami K., Murata N. Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog. Lipid Res. 2003;42:527–543. doi: 10.1016/S0163-7827(03)00036-5. PubMed DOI

Los D.A., Murata N. Membrane fluidity and its roles in the perception of environmental signals. Biochim. Biophys. Acta (BBA) Biomembr. 2004;1666:142–157. doi: 10.1016/j.bbamem.2004.08.002. PubMed DOI

Hölzl G., Dörmann P. Chloroplast lipids and their biosynthesis. Annu. Rev. Plant Biol. 2019;70:51–81. doi: 10.1146/annurev-arplant-050718-100202. PubMed DOI

Schwertner H.A., Biale J.B. Lipid composition of plant mitochondria and of chloroplasts. J. Lipid Res. 1973;14:235–242. PubMed

Janeczko A., Hura K., Skoczowski A., Idzik I., Biesaga-Kościelniak J., Niemczyk E. Temperature-dependent impact of 24-epibrassinolide on the fatty acid composition and sugar content in winter oilseed rape callus. Acta Physiol. Plant. 2009;31:71–79. doi: 10.1007/s11738-008-0202-2. DOI

Fedina E., Yarin A., Mukhitova F., Blufard A., Chechetkin I. Brassinosteroid-induced changes of lipid composition in leaves of Pisum sativum L. during senescence. Steroids. 2017;117:25–28. doi: 10.1016/j.steroids.2016.10.009. PubMed DOI

Filek M., Rudolphi-Skórska E., Sieprawska A., Kvasnica M., Janeczko A. Regulation of the membrane structure by brassinosteroids and progesterone in winter wheat seedlings exposed to low temperature. Steroids. 2017;128:37–45. doi: 10.1016/j.steroids.2017.10.002. PubMed DOI

Janeczko A., Gruszka D., Pociecha E., Dziurka M., Filek M., Jurczyk B., Kalaji H.M., Kocurek M., Waligórski P. Physiological and biochemical characterisation of watered and drought-stressed barley mutants in the HvDWARF gene encoding C6-oxidase involved in brassinosteroid biosynthesis. Plant Physiol. Biochem. 2016;99:126–141. doi: 10.1016/j.plaphy.2015.12.003. PubMed DOI

Havaux M. Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci. 1998;3:147–151. doi: 10.1016/S1360-1385(98)01200-X. DOI

Nie S., Huang S., Wang S., Cheng D., Liu J., Lv S., Li Q., Wang X. Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front. Plant Sci. 2017;8:1386. doi: 10.3389/fpls.2017.01386. PubMed DOI PMC

Kočová M., Rothová O., Holá D., Kvasnica M., Kohout L. The effects of brassinosteroids on photosynthetic parameters in leaves of two field-grown maize inbred lines and their F1 hybrid. Biol. Plant. 2010;54:785–788. doi: 10.1007/s10535-010-0143-7. DOI

Malaga S., Janeczko A., Janowiak F., Waligórski P., Oklestkova J., Dubas E., Krzewska M., Nowicka A., Surówka E., Rapacz M., et al. Involvement of homocastasterone, salicylic and abscisic acids in the regulation of drought and freezing tolerance in doubled haploid lines of winter barley. Plant Growth Regul. 2020;90:173–188. doi: 10.1007/s10725-019-00544-9. DOI

Jørgensen K., Rasmussen A.V., Morant M., Nielsen A.H., Bjarnholt N., Zagrobelny M., Bak S., Møller B.L. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 2005;8:280–291. doi: 10.1016/j.pbi.2005.03.014. PubMed DOI

Cai Y., Tarin M., Fan L., Xie D., Rong J., He T., Chen L., Zheng Y. Responses of photosynthesis, chloroplast ultrastructure, and antioxidant system of morinda officinalis how to exogenous 2,4-pibrassinolide treatments under high temperature stress. Appl. Ecol. Environ. Res. 2020;18:3981–4004. doi: 10.15666/aeer/1803_39814004. DOI

Zhang F., Lu K., Gu Y., Zhang L., Li W., Tan X. Effects of low-temperature stress and brassinolide application on the photosynthesis and leaf structure of tung tree seedlings. Front. Plant Sci. 2020;10:1767. doi: 10.3389/fpls.2019.01767. PubMed DOI PMC

Krumova S., Zhiponova M., Dankov K., Velikova V., Balashev K., Andreeva T., Russinova E., Taneva S. Brassinosteroids regulate the thylakoid membrane architecture and the photosystem II function. J. Photochem. Photobiol. B Biol. 2013;126:97–104. doi: 10.1016/j.jphotobiol.2013.07.008. PubMed DOI

Bojko M., Olchawa-Pajor M., Chyc M., Goss R., Schaller-Laudel S., Latowski D. Acclimatization of Thalassiosira pseudonana photosynthetic membranes to environmental temperature changes; Proceedings of the 3rd World Congress on New Technologies (NewTech’17); Rome, Italy. 6–8 June 2017; DOI

Dzikovski B., Freed J. Membrane fluidity. In: Roberts G.C.K., editor. Encyclopedia of Biophysics. Springer; Berlin/Heidelberg, Germany: 2013. pp. 1440–1446.

Los D.A., Murata N. Regulation of enzymatic activity and gene expression by membrane fluidity. Sci. Signal. 2000;2000:pe1. doi: 10.1126/stke.2000.62.pe1. PubMed DOI

Staykova M., Stone H.A. The role of the membrane confinement in the surface area regulation of cells. Commun. Integr. Biol. 2011;4:616–618. doi: 10.4161/cib.16854. PubMed DOI PMC

Fujii S., Nagata N., Masuda T., Wada H., Kobayashi K. Galactolipids are essential for internal membrane transformation during Etioplast-to-Chloroplast Differentiation. Plant Cell Physiol. 2019;60:1224–1238. doi: 10.1093/pcp/pcz041. PubMed DOI PMC

Inaba M., Suzuki I., Szalontai B., Kanesaki Y., Los D.A., Hayashi H., Murata N. Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J. Biol. Chem. 2003;278:12191–12198. doi: 10.1074/jbc.M212204200. PubMed DOI

Li B., Zhang C., Cao B., Qin G., Wang W., Tian S. Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. Amino Acids. 2012;43:2469–2480. doi: 10.1007/s00726-012-1327-6. PubMed DOI

Dou X., Li Y., Han J., Zarlenga D., Zhu W., Ren X., Dong N., Li X., Li G. Cholesterol of lipid rafts is a key determinant for entry and post-entry control of porcine rotavirus infection. BMC Veter Res. 2018;14:45. doi: 10.1186/s12917-018-1366-7. PubMed DOI PMC

Beck J.G., Mathieu D., Loudet C., Buchoux S., Dufourc E.J. Plant sterols in “rafts”: A better way to regulate membrane thermal shocks. FASEB J. 2007;21:1714–1723. doi: 10.1096/fj.06-7809com. PubMed DOI

Uemura M., Tominaga Y., Nakagawara C., Shigematsu S., Minami A., Kawamura Y. Responses of the plasma membrane to low temperatures. Physiol. Plant. 2006;126:81–89. doi: 10.1111/j.1399-3054.2005.00594.x. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...