103
Views
0
CrossRef citations to date
0
Altmetric
Original Articles

How does ionizing radiation affect amyloidogenesis in plants?

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 922-933 | Received 27 Oct 2023, Accepted 07 Mar 2024, Published online: 26 Mar 2024

References

  • Antonets KS, Belousov MV, Sulatskaya AI, Belousova ME, Kosolapova AO, Sulatsky MI, Andreeva EA, Zykin PA, Malovichko YV, Shtark OY, et al. 2020. Accumulation of storage proteins in plant seeds is mediated by amyloid formation. PLoS Biol. 18(7):e3000564. doi:10.1371/journal.pbio.3000564
  • Bentolila S, Oh J, Hanson MR, Bukowski R. 2013. Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet. 9(6):e1003584. doi:10.1371/journal.pgen.1003584
  • Berthomieu C, Hienerwadel R. 2009. Fourier transform infrared (FTIR) spectroscopy. Photosynth Res. 101(2-3):157–170. doi:10.1007/s11120-009-9439-x
  • Beyaz R, MacAdam JW. 2023. X-radiation of Lotus corniculatus L. seeds improves germination and initial seedling growth. Int J Radiat Biol. 99(11):1794–1799. doi:10.1080/09553002.2023.2204961
  • Beyaz R. 2020. Impact of gamma irradiation pretreatment on the growth of common vetch (Vicia sativa L.) seedlings grown under salt and drought stress. Int J Radiat Biol. 96(2):257–266. doi:10.1080/09553002.2020.1688885
  • Bieler S, Estrada L, Lagos R, Baeza M, Castilla J, Soto C. 2005. Amyloid formation modulates the biological activity of a bacterial protein. J Biol Chem. 280(29):26880–26885. doi:10.1074/jbc.M502031200
  • Bourgeois M, Jacquin F, Savois V, Sommerer N, Labas V, Henry C, Burstin J. 2009. Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics. 9(2):254–271. doi:10.1002/pmic.200700903
  • Bremer J, Baumann F, Tiberi C, Wessig C, Fischer H, Schwarz P, Steele AD, Toyka KV, Nave K-A, Weis J, et al. 2010. Axonal prion protein is required for peripheral myelin maintenance. Nat Neurosci. 13(3):310–318. doi:10.1038/nn.2483
  • Castillejo M-Á, Iglesias-García R, Wienkoop S, Rubiales D. 2016. Label-free quantitative proteomic analysis of tolerance to drought in Pisum sativum. Proteomics. 16(21):2776–2787. doi:10.1002/pmic.201600156
  • Castle AR, Gill AC. 2017. Physiological functions of the cellular prion protein. Front Mol Biosci. 4:19. doi:10.3389/fmolb.2017.00019
  • Chakrabortee S, Kayatekin C, Newby GA, Mendillo ML, Lancaster A, Lindquist S. 2016. Luminidependens (LD) is an Arabidopsis protein with prion behavior. Proc Natl Acad Sci U S A. 113(21):6065–6070. doi:10.1073/pnas.1604478113
  • Coustou V, Deleu C, Saupe S, Begueret J. 1997. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci U S A. 94(18):9773–9778. doi:10.1073/pnas.94.18.9773
  • de Dios Alché J, M'rani-Alaoui M, Castro AJ, Rodríguez-García MI. 2004. Ole e 1, the major allergen from Olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination. Plant Cell Physiol. 45(9):1149–1157. doi:10.1093/pcp/pch127
  • Dorone Y, Boeynaems S, Flores E, Jin B, Hateley S, Bossi F, Lazarus E, Pennington JG, Michiels E, De Decker M, et al. 2021. A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation. Cell. 184(16):4284–4298.e27. doi:10.1016/j.cell.2021.06.009
  • Espargaró A, Llabrés S, Saupe SJ, Curutchet C, Luque FJ, Sabaté R. 2020. On the binding of congo red to amyloid fibrils. Angew Chem Int Ed Engl. 59(21):8104–8107. doi:10.1002/anie.201916630
  • Faris R, Moore RA, Ward A, Race B, Dorward DW, Hollister JR, Fischer ER, Priola SA. 2017. Cellular prion protein is present in mitochondria of healthy mice. Sci Rep. 7(1):41556. doi:10.1038/srep41556
  • Gábrišová D, Klubicová K, Danchenko M, Gömöry D, Berezhna VV, Skultety L, Miernyk JA, Rashydov N, Hajduch M. 2015. Do cupins have a function beyond being seed storage proteins? Front Plant Sci. 6:1215. doi:10.3389/fpls.2015.01215
  • Garai, Sampurna, Singla-Pareek, Sneh L, Sopory, Sudhir K, Kaur, Charanpreet, Yadav, Gitanjali, Citu,. 2021. Complex networks of prion-like proteins reveal cross talk between stress and memory pathways in plants. Front Plant Sci. 12:707286. doi:10.3389/fpls.2021.707286
  • Gibbings D, Leblanc P, Jay F, Pontier D, Michel F, Schwab Y, Alais S, Lagrange T, Voinnet O. 2012. Human prion protein binds Argonaute and promotes accumulation of microRNA effector complexes. Nat Struct Mol Biol. 19(5):517–524, S1. doi:10.1038/nsmb.2273
  • Gómez-Pérez D, Chaudhry V, Kemen A, Kemen E. 2021. Amyloid proteins in plant-associated microbial communities. Microb Physiol. 31(2):88–98. doi:10.1159/000516014
  • Greenwald J, Riek R. 2010. Biology of amyloid: structure, function, and regulation. Structure. 18(10):1244–1260. doi:10.1016/j.str.2010.08.009
  • Hazenberg BPC, Limburg PC, Bijzet J, Van Rijswijk MH. 1999. A quantitative method for detecting deposits of amyloid A protein in aspirated fat tissue of patients with arthritis. Ann Rheum Dis. 58(2):96–102. doi:10.1136/ard.58.2.96
  • Jung J-H, Barbosa AD, Hutin S, Kumita JR, Gao M, Derwort D, Silva CS, Lai X, Pierre E, Geng F, et al. 2020. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature. 585(7824):256–260. doi:10.1038/s41586-020-2644-7
  • Kamiie J, Aihara N, Uchida Y, Kobayashi D, Yoshida Y, Kuroda T, Sakaue M, Sugihara Y, Rezeli M, Marko-Varga G. 2020. Amyloid-specific extraction using organic solvents. MethodsX. 7:100770. doi:10.1016/j.mex.2019.100770
  • Kan A, Birnbaum DP, Praveschotinunt P, Joshi NS. 2019. Congo red fluorescence for rapid in situ characterization of synthetic curli systems. Appl Environ Microbiol. 85(13):e00434-19. doi:10.1128/AEM.00434-19
  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 10(6):845–858. doi:10.1038/nprot.2015.053
  • Kiani D, Borzouei A, Ramezanpour S, Soltanloo H, Saadati S. 2022. Application of gamma irradiation on morphological, biochemical, and molecular aspects of wheat (Triticum aestivum L.) under different seed moisture contents. Sci Rep. 12(1):11082. doi:10.1038/s41598-022-14949-6
  • Kim SJ, Rahbar R, Hegde RS. 2001. Combinatorial control of prion protein biogenesis by the signal sequence and transmembrane domain. J Biol Chem. 276(28):26132–26140. doi:10.1074/jbc.M101638200
  • Kovač V, Čurin Šerbec V. 2022. Prion protein: the molecule of many forms and faces. IJMS. 23(3):1232. doi:10.3390/ijms23031232
  • Kriegler T, Lang S, Notari L, Hessa T. 2020. Prion protein translocation mechanism revealed by pulling force studies. J Mol Biol. 432(16):4447–4465. doi:10.1016/j.jmb.2020.05.022
  • Lancaster AK, Nutter-Upham A, Lindquist S, King OD. 2014. PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition. Bioinformatics. 30(17):2501–2502. doi:10.1093/bioinformatics/btu310
  • Li B, Zeng Y, Cao W, Zhang W, Cheng L, Yin H, Wu Q, Wang X, Huang Y, Lau WCY, et al. 2021. A distinct giant coat protein complex II vesicle population in Arabidopsis thaliana. Nat Plants. 7(10):1335–1346.,. doi:10.1038/s41477-021-00997-9
  • Li J, Zhang F. 2021. Amyloids as building blocks for macroscopic functional materials: designs, applications and challenges. IJMS. 22(19):10698. doi:10.3390/ijms221910698
  • Liao L, Cheng D, Wang J, Duong DM, Losik TG, Gearing M, Rees HD, Lah JJ, Levey AI, Peng J. 2004. Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J Biol Chem. 279(35):37061–37068. doi:10.1074/jbc.M403672200
  • Linke RP. 2006. Congo red staining of amyloid: improvements and practical guide for a more precise diagnosis of amyloid and the different amyloidoses. In: Uversky VN, Fink AL, editors. Protein misfolding, aggregation, and conformational diseases. Vol. 4. Boston, MA: Springer US; p. 239–276. doi:10.1007/0-387-25919-8_12
  • Maji SK, Schubert D, Rivier C, Lee S, Rivier JE, Riek R. 2008. Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol. 6(2):e17. doi:10.1371/journal.pbio.0060017
  • Martin M-J, Orchard S, Magrane M, Ahmad S, Alpi E, Bowler-Barnett EH, Britto R, Bye-A-Jee H, The UniProt Consortium, Bateman A., et al. 2023. UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 51(D1):D523–D531. doi:10.1093/nar/gkac1052
  • Milošević J, Petrić J, Jovčić B, Janković B, Polović N. 2020. Exploring the potential of infrared spectroscopy in qualitative and quantitative monitoring of ovalbumin amyloid fibrillation. Spectrochim Acta A Mol Biomol Spectrosc. 229:117882. doi:10.1016/j.saa.2019.117882
  • Monge-Morera M, Lambrecht MA, Deleu LJ, Louros NN, Rousseau F, Schymkowitz J, Delcour JA. 2021. Heating wheat gluten promotes the formation of amyloid-like fibrils. ACS Omega. 6(3):1823–1833. doi:10.1021/acsomega.0c03670
  • Movasaghi Z, Rehman S, Rehman IU. 2007. Raman spectroscopy of biological tissues. Appl Spectrosc Rev. 42(5):493–541. doi:10.1080/05704920701551530
  • Narita H, Shima T, Iizuka R, Uemura S. 2023. N-terminal region of Drosophila melanogaster Argonaute2 forms amyloid-like aggregates. BMC Biol. 21(1):78. doi:10.1186/s12915-023-01569-3
  • Nasi GI, Aktypi FD, Spatharas PM, Louros NN, Tsiolaki PL, Magafa V, Trougakos IP, Iconomidou VA. 2021. Arabidopsis thaliana plant natriuretic peptide active domain forms amyloid-like fibrils in a pH-dependent manner. Plants (Basel). 11(1):9. doi:10.3390/plants11010009
  • Nizhnikov AA, Ryzhova TA, Volkov KV, Zadorsky SP, Sopova JV, Inge-Vechtomov SG, Galkin AP. 2016. Interaction of prions causes heritable traits in Saccharomyces cerevisiae. PLoS Genet. 12(12):e1006504. doi:10.1371/journal.pgen.1006504
  • Nováková S, Šubr Z, Kováč A, Fialová I, Beke G, Danchenko M. 2020. Cucumber mosaic virus resistance: comparative proteomics of contrasting Cucumis sativus cultivars after long-term infection. J Proteomics. 222:103674. doi:10.1016/j.jprot.2019.103626
  • Olrichs NK, Mahalka AK, Kaloyanova D, Kinnunen PK, Bernd Helms J. 2014. Golgi-associated plant pathogenesis related protein 1 (GAPR-1) forms amyloid-like fibrils by interaction with acidic phospholipids and inhibits Aβ aggregation. Amyloid. 21(2):88–96. doi:10.3109/13506129.2014.882304
  • Perez-Riverol Y, Bai J, Bandla C, García-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M, et al. 2022. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50(D1):D543–D552. doi:10.1093/nar/gkab1038
  • Pernis M, Skultety L, Shevchenko V, Klubicova K, Rashydov N, Danchenko M. 2020. Soybean recovery from stress imposed by multigenerational growth in contaminated Chernobyl environment. J Plant Physiol. 251:153219. doi:10.1016/j.jplph.2020.153219
  • Pham CLL, Kwan AH, Sunde M. 2014. Functional amyloid: widespread in nature, diverse in purpose. In Perrett S, editor. Essays in biochemistry. Vol. 56. London (UK): Portland Press; p. 207–219. doi:10.1042/bse0560207
  • Rahman MM, Pires RS, Herneke A, Gowda V, Langton M, Biverstål H, Lendel C. 2023. Food protein-derived amyloids do not accelerate amyloid β aggregation. Sci Rep. 13(1):985. doi:10.1038/s41598-023-28147-5
  • Richardson RB. 2009. Ionizing radiation and aging: rejuvenating an old idea. Aging (Albany NY). 1(11):887–902. doi:10.18632/aging.100081
  • Robinson PJ, Pinheiro TJT. 2010. Phospholipid composition of membranes directs prions down alternative aggregation pathways. Biophys J. 98(8):1520–1528. doi:10.1016/j.bpj.2009.12.4304
  • Santos J, Ventura S. 2021. Functional amyloids germinate in plants. Trends Plant Sci. 26(1):7–10. doi:10.1016/j.tplants.2020.10.001
  • Sawaya MR, Hughes MP, Rodriguez JA, Riek R, Eisenberg DS. 2021. The expanding amyloid family: Structure, stability, function, and pathogenesis. Cell. 184(19):4857–4873. doi:10.1016/j.cell.2021.08.013
  • Schonberger SJ, Edgar PF, Kydd R, Faull RLM, Cooper GJS. 2001. Proteomic analysis of the brain in Alzheimer’s disease: molecular phenotype of a complex disease process. Proteomics. 1(12):1519. ­doi:10.1002/1615-9861(200111)1:12<1519::aid-prot1519>3.0.co;2-l
  • Schulz H, Baranska M. 2007. Identification and quantification of valuable plant substances by IR and Raman spectroscopy. Vib Spectrosc. 43(1):13–25. doi:10.1016/j.vibspec.2006.06.001
  • Schwacke R, Ponce-Soto GY, Krause K, Bolger AM, Arsova B, Hallab A, Gruden K, Stitt M, Bolger ME, Usadel B. 2019. MapMan4: a refined protein classification and annotation framework applicable to multi-omics data analysis. Mol Plant. 12(6):879–892. doi:10.1016/j.molp.2019.01.003
  • Shen Y, Posavec L, Bolisetty S, Hilty FM, Nyström G, Kohlbrecher J, Hilbe M, Rossi A, Baumgartner J, Zimmermann MB, et al. 2017. Amyloid fibril systems reduce, stabilize and deliver bioavailable nanosized iron. Nat Nanotechnol. 12(7):642–647. doi:10.1038/nnano.2017.58
  • Sinha N, Zahra T, Gahane AY, Rout B, Bhattacharya A, Basu S, Chakrabarti A, Thakur AK. 2023. Protein reservoirs of seeds are amyloid composites employed differentially for germination and seedling emergence. Plant J. 116(2):329–346. doi:10.1111/tpj.16429
  • Škodová-Sveráková I, Záhonová K, Juricová V, Danchenko M, Moos M, Baráth P, Prokopchuk G, Butenko A, Lukáčová V, Kohútová L, et al. 2021. Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum. BMC Biol. 19(1):251. doi:10.1186/s12915-021-01186-y
  • Son Y, Lee CG, Kim JS, Lee H-J. 2023. Low-dose-rate ionizing radiation affects innate immunity protein IFITM3 in a mouse model of Alzheimer’s disease. Int J Radiat Biol. 99(11):1649–1659. doi:10.1080/09553002.2023.2211142
  • Soon WL, Peydayesh M, Mezzenga R, Miserez A. 2022. Plant-based amyloids from food waste for removal of heavy metals from contaminated water. Chem Eng J. 445:136513. doi:10.1016/j.cej.2022.136513
  • Surguchov A, Emamzadeh FN, Surguchev AA. 2019. Amyloidosis and longevity: a lesson from plants. Biology (Basel). 8(2):43. doi:10.3390/biology8020043
  • Szklarczyk D, Kirsch R, Koutrouli M, Nastou K, Mehryary F, Hachilif R, Gable AL, Fang T, Doncheva NT, Pyysalo S, et al. 2023. The STRING database in 2023: protein–protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res. 51(D1):D638–D646. doi:10.1093/nar/gkac1000
  • Takagi J, Renna L, Takahashi H, Koumoto Y, Tamura K, Stefano G, Fukao Y, Kondo M, Nishimura M, Shimada T, et al. 2013. MAIGO5 functions in protein export from Golgi-associated endoplasmic reticulum exit sites in Arabidopsis. Plant Cell. 25(11):4658–4675. doi:10.1105/tpc.113.118158
  • Tong J, Hei TK. 2020. Aging and age-related health effects of ionizing radiation. Rad Med Protect. 1(1):15–23. doi:10.1016/j.radmp.2020.01.005
  • Tyanova S, Temu T, Cox J. 2016. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 11(12):2301–2319. doi:10.1038/nprot.2016.136
  • Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. 2016. The Perseus computational platform for comprehensive analysis of proteomics data. Nat Methods. 13(9):731–740. doi:10.1038/nmeth.3901
  • Vendruscolo M, Fuxreiter M. 2022. Sequence determinants of the aggregation of proteins within condensates generated by liquid-liquid phase separation. J Mol Biol. 434(1):167201. doi:10.1016/j.jmb.2021.167201
  • Villar-Piqué A, Sabaté R, Lopera O, Gibert J, Torne JM, Santos M, Ventura S. 2010. Amyloid-like protein inclusions in tobacco transgenic plants. PLoS One. 5(10):e13625. doi:10.1371/journal.pone.0013625
  • Westergard L, Christensen HM, Harris DA. 2007. The cellular prion protein (PrPC): Its physiological function and role in disease. Biochim Biophys Acta. 1772(6):629–644. doi:10.1016/j.bbadis.2007.02.011
  • Zehrmann A, Härtel B, Glass F, Bayer-Császár E, Obata T, Meyer E, Brennicke A, Takenaka M. 2015. Selective homo- and heteromer interactions between the multiple organellar RNA editing factor (MORF) proteins in Arabidopsis thaliana. J Biol Chem. 290(10):6445–6456. doi:10.1074/jbc.M114.602086
  • Ziska A, Tatzelt J, Dudek J, Paton AW, Paton JC, Zimmermann R, Haßdenteufel S. 2019. The signal peptide plus a cluster of positive charges in prion protein dictate chaperone-mediated Sec61 channel gating. Biol Open. 8(3):bio.040691. doi:10.1242/bio.040691
  • Zou J, Brokx SJ, Taylor DC. 1996. Cloning of a cDNA encoding the 21.2 kDa oleosin isoform from Arabidopsis thaliana and a study of its expression in a mutant defective in diacylglycerol acyltransferase activity. Plant Mol Biol. 31(2):429–433. doi:10.1007/BF00021805

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.