Ubiquitin-like and ubiquitinylated proteins associated with the maternal cell walls of Scenedesmus obliquus 633 as identified by immunochemistry and LC-MS/MS proteomics.
Scenedesmus
Cell walls
Extramembranous compartment
Proteome
Ubiquitin
Journal
Protoplasma
ISSN: 1615-6102
Titre abrégé: Protoplasma
Pays: Austria
ID NLM: 9806853
Informations de publication
Date de publication:
04 Oct 2024
04 Oct 2024
Historique:
received:
14
11
2023
accepted:
23
09
2024
medline:
4
10
2024
pubmed:
4
10
2024
entrez:
4
10
2024
Statut:
aheadofprint
Résumé
The cell walls of green algae Scenedesmus obliquus are complex, polymeric structures including an inner cellulose layer surrounded by an algaenan-containing trilaminar sheath. The process of autosporulation leads to the formation of sporangial (maternal) cell walls, which are released into the medium after sporangial autolysis. In this study, a fraction of maternal cell wall material (CWM) was isolated from the stationary phase cultures of Scenedesmus obliquus 633 and subjected to immunofluorescence microscopy using polyclonal anti-ubiquitin antibodies. The water-extracted polypeptide fraction from the maternal cell walls was then analyzed using immunoblotting and LC-MS/MS. An immunoanalysis showed the presence of several peptides reactive with polyclonal anti-ubiquitin serum, with apparent molecular masses of c. 12, 70, 120, 200, and > 250 kDa. Cell wall-associated peptides were identified on the basis of LC-MS/MS spectra across NCBI databases, including the Scenedesmaceae family (58 records), the Chlorophyceae class (37 records), and Chlamydomonas reinhardtii (18 records) corresponding to the signatures of 95 identified proteins. In particular, three signatures identified ubiquitin and ubiquitin-related proteins. In the maternal cell walls, immunoblotting analysis, immunofluorescence microscopy, and LC-MS/MS proteomics collectively demonstrated the presence of ubiquitin-like epitopes, ubiquitin-specific peptide signatures, and several putative ubiquitin conjugates of a higher molecular mass. These results support the presence of ubiquitin-like proteins in the extramembranous compartment of Scenedesmus obliquus 633 and suggest that protein ubiquitination plays a significant role in the formation and functional integrity of the maternal cell walls in green algae.
Identifiants
pubmed: 39365352
doi: 10.1007/s00709-024-01994-3
pii: 10.1007/s00709-024-01994-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Aarthy A, Kumari S, Turkar P, Subramanian S (2018) An insight on algal cell disruption for biodiesel production. Asian J Pharm Clin Res 11(2):21–26. https://doi.org/10.22159/ajpcr.2018.v11i2.22481
doi: 10.22159/ajpcr.2018.v11i2.22481
Albenne C, Canut H, Jamet E (2013) Plant cell wall proteomics: the leadership of Arabidopsis thaliana. Front Plant Sci 4:1664–2462. https://doi.org/10.3389/FPLS.2013.00111
doi: 10.3389/FPLS.2013.00111
Albenne C, Canut H, Hoffmann L, Jamet E (2014) Plant cell wall proteins: a large body of data, but what about runaways? Proteomes 2(2):224–242. https://doi.org/10.3390/PROTEOMES2020224
doi: 10.3390/PROTEOMES2020224
pubmed: 28250379
pmcid: 5302738
Armenteros JJA, Salvatore M, Emanuelsson O, Winther O, Von Heijne G, Elofsson A, Nielsen H (2019) Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance 2(5):e201900429. https://doi.org/10.26508/LSA.201900429
doi: 10.26508/LSA.201900429
Badarudeen B, Anand U, Mukhopadhyay S, Manna TK (2021) Ubiquitin signaling in the control of centriole duplication. FEBS J 289(16):4830–4849. https://doi.org/10.1111/FEBS.16069
doi: 10.1111/FEBS.16069
pubmed: 34115927
Baudelet PH, Ricochon G, Linder M, Muniglia L (2017) A new insight into cell walls of Chlorophyta. Algal Res 25:333–371. https://doi.org/10.1016/J.ALGAL.2017.04.008
doi: 10.1016/J.ALGAL.2017.04.008
Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8(2):93–99. https://doi.org/10.1002/ELPS.1150080203
doi: 10.1002/ELPS.1150080203
Boevink PC (2017) Exchanging missives and missiles: the roles of extracellular vesicles in plant-pathogen interactions. J Exp Bot 68(20):5411–5414. https://doi.org/10.1093/JXB/ERX369
doi: 10.1093/JXB/ERX369
pubmed: 29190393
pmcid: 5853247
Burczyk J (1973) The chemical composition and ultrastructure of the cell wall of Scenedesmus obliquus. II. Amino acids, proteins and antigens. Folia Histochemica et Cytochemica 11(2):135–154
pubmed: 4206341
Burczyk J (1979) Carotenoids localised in the cell wall of Chlorella and Scenedesmus. Bullet Serie Des Sci Biol 27:13–19
Burczyk J (1987) Biogenetic relationship between ketocarotenoids and sporopollenins in green algae. Phytochemistry 26(1):113–119. https://doi.org/10.1016/S0031-9422(00)81493-4
doi: 10.1016/S0031-9422(00)81493-4
Burczyk J, Hesse M (1981) The ultrastructure of the outer cell wall layer of Chlorella mutants with and without sporopollenin. Plant Syst Evol 138:121–137. https://doi.org/10.1007/BF00984613
doi: 10.1007/BF00984613
Burczyk J, Loos E (1995) Cell wall-bound enzymatic activities in Chlorella and Scenedesmus. J Plant Physiol 146(5–6):748–750. https://doi.org/10.1016/S0176-1617(11)81943-7
doi: 10.1016/S0176-1617(11)81943-7
Burczyk J, Grzybek H, Banaś J, Banaś E (1970) Presence of cellulase in the algae Scenedesmus. Exp Cell Res 63(2–3):451–453. https://doi.org/10.1016/0014-4827(70)90236-3
doi: 10.1016/0014-4827(70)90236-3
pubmed: 5490343
Burczyk J, Grzybek H, Banaś J, Banaś E (1971) Studies on the ultrastructure of cell walls of Scenedesmus. Acta Med Pol 12:143–146
pubmed: 5562646
Burczyk J, Szkawran H, Zontek I, Czygan F-C (1981) Carotenoids in the outer cell-wall layer of Scenedesmus (Chlorophyceae). Planta 151:247–250. https://doi.org/10.1007/BF00395176
doi: 10.1007/BF00395176
pubmed: 24301850
Burczyk J, Termińska-Pabis K, Śmietana B (1995) Cell wall neutral sugar composition of chlorococcalean algae forming and not forming acetolysis resistant biopolymer. Phytochemistry 38(4):837–841. https://doi.org/10.1016/0031-9422(94)00694-O
doi: 10.1016/0031-9422(94)00694-O
Burczyk J, Śmietana B, Termińska-Pabis K, Zych M, Kowalowski P (1999) Comparison of nitrogen content amino acid composition and glucosamine content of cell walls of various chlorococcalean algae. Phytochemistry 51(4):491–497. https://doi.org/10.1016/S0031-9422(99)00063-1
doi: 10.1016/S0031-9422(99)00063-1
Burczyk J, Zych M, Ioannidis NE, Kotzabasis K (2014) Polyamines in cell walls of chlorococcalean microalgae. Zeitschrift Fur Naturforschung - Section C J Biosci 69(1–2):75–80. https://doi.org/10.5560/znc.2012-0215
doi: 10.5560/znc.2012-0215
Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49(1):281–309. https://doi.org/10.1146/annurev.arplant.49.1.281
doi: 10.1146/annurev.arplant.49.1.281
pubmed: 15012236
Chung, K. P., & Zeng, Y. (2017). An overview of protein secretion in plant cells. In: Jiang, L. (eds) Plant Protein Secretion: Methods and Protocols, Methods in Molecular Biology, 1662, 19–32. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7262-3_2
Clague MJ, Urbé S (2017) Integration of cellular ubiquitin and membrane traffic systems: focus on deubiquitylases. FEBS J 284(12):1753–1766. https://doi.org/10.1111/FEBS.14007
doi: 10.1111/FEBS.14007
pubmed: 28064438
pmcid: 5484354
Clemente HS, Kolkas H, Canut H, Jamet E (2022) Plant cell wall proteomes: the core of conserved protein families and the case of non-canonical proteins. Int J Mol Sci 23(8):4273. https://doi.org/10.3390/IJMS23084273
doi: 10.3390/IJMS23084273
Collins GA, Goldberg AL (2020) Proteins containing ubiquitin-like (Ubl) domains not only bind to 26S proteasomes but also induce their activation. Proc Natl Acad Sci USA 117(9):4664–4674. https://doi.org/10.1073/PNAS.1915534117
doi: 10.1073/PNAS.1915534117
pubmed: 32071216
pmcid: 7060731
Daino H, Matsumura I, Takada K, Odajima J, Tanaka H, Ueda S, Shibayama H, Ikeda H, Hibi M, Machii T, Hirano T, Kanakura Y (2000) Induction of apoptosis by extracellular ubiquitin in human hematopoietic cells: possible involvement of STAT3 degradation by proteasome pathway in interleukin 6-dependent hematopoietic cells. Blood 95(8):2577–2585. https://doi.org/10.1182/BLOOD.V95.8.2577
doi: 10.1182/BLOOD.V95.8.2577
pubmed: 10753837
de Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34(suppl_2):W362–W365. https://doi.org/10.1093/NAR/GKL124
doi: 10.1093/NAR/GKL124
pubmed: 16845026
pmcid: 1538847
Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WGT (2012) The cell walls of green algae: a journey through evolution and diversity. Frontiers in Plant Science 3:82. https://doi.org/10.3389/fpls.2012.00082
doi: 10.3389/fpls.2012.00082
pubmed: 22639667
pmcid: 3355577
Domozych DS (2016) Biosynthesis of the cell walls of the algae. In: M. A. Borowitzka, J. Beardall, & J. A. Raven (Eds.), The Physiology of Microalgae. Developments in Applied Phycology, vol 6 (pp. 47–63). Springer International Publishing. https://doi.org/10.1007/978-3-319-24945-2_2
Domozych DS (2019) Algal cell walls. In: eLS (pp. 1–11). John Wiley & Sons, Ltd (Ed.). https://doi.org/10.1002/9780470015902.a0000315.pub4
Doroodian P, Hua Z (2021) The ubiquitin switch in plant stress response. Plants 10(2):246. https://doi.org/10.3390/PLANTS10020246
doi: 10.3390/PLANTS10020246
pubmed: 33514032
pmcid: 7911189
Dunker S, Wilhelm C (2018) Cell wall structure of coccoid green algae as an important trade-offbetween biotic interference mechanisms and multidimensional cell growth. Front Microbiol 9:719. https://doi.org/10.3389/fmicb.2018.00719
doi: 10.3389/fmicb.2018.00719
pubmed: 29706940
pmcid: 5908957
Foot N, Henshall T, Kumar S (2017) Ubiquitination and the regulation of membrane proteins. Physiol Rev 97(1):253–281. https://doi.org/10.1152/physrev.00012.2016
doi: 10.1152/physrev.00012.2016
pubmed: 27932395
Gong M, Wang H, Chen M, Bao D, Zhu Q, Tan Q (2016) A newly discovered ubiquitin-conjugating enzyme E2 correlated with the cryogenic autolysis of Volvariella volvacea. Gene 583(1):58–63. https://doi.org/10.1016/j.gene.2016.02.038
doi: 10.1016/j.gene.2016.02.038
pubmed: 26927519
Herrmann J, Lerman LO, Lerman A (2007) Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res 100(9):1276–1291. https://doi.org/10.1161/01.RES.0000264500.11888.F0
doi: 10.1161/01.RES.0000264500.11888.F0
pubmed: 17495234
Hicke L (2001) A new ticket for entry into budding vesicles—ubiquitin. Cell 106(5):527–530. https://doi.org/10.1016/S0092-8674(01)00485-8
doi: 10.1016/S0092-8674(01)00485-8
pubmed: 11551499
Imam SH, Buchanan MJ, Shin HC, Snell WJ (1985) The Chlamydomonas cell wall: characterization of the wall framework. J Cell Biol 101(4):1599–1607. https://doi.org/10.1083/JCB.101.4.1599
doi: 10.1083/JCB.101.4.1599
pubmed: 2413047
Ishaq AG, Matias-Peralta HM, Basri H (2016) Bioactive compounds from green microalga Scenedesmus and its potential applications: a brief review. Pertanika J Trop Agric Sci 39(1):1–16
Jackson EK, Mi E, Ritov VB, Gillespie DG (2018) Extracellular ubiquitin(1–76) and ubiquitin(1–74) regulate cardiac fibroblast proliferation. Hypertension 72(4):909–917. https://doi.org/10.1161/HYPERTENSIONAHA.118.11666
doi: 10.1161/HYPERTENSIONAHA.118.11666
pubmed: 30354710
Jankowski A (1964) Research on the selection of algae for mass cultures. Doctoral dissertation (in Polish). National Research Institute of Animal Production, Kraków, Poland.
Kessler E, Czygan F-C (1970) Physiologische und biochemische Beiträge zur Taxonomie der Gattung Chlorella. Arch Mikrobiol 70(3):211–216. https://doi.org/10.1007/BF00407711
doi: 10.1007/BF00407711
pubmed: 4245108
Kramer RM, Shende VR, Motl N, Pace CN, Scholtz JM (2012) Toward a molecular understanding of protein solubility: increased negative surface charge correlates with increased solubility. Biophys J 102(8):1907–1915. https://doi.org/10.1016/J.BPJ.2012.01.060
doi: 10.1016/J.BPJ.2012.01.060
pubmed: 22768947
pmcid: 3328702
Krogh A, Larsson B, Von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. https://doi.org/10.1006/jmbi.2000.4315
doi: 10.1006/jmbi.2000.4315
pubmed: 11152613
Kuo EYH, Lee TM (2021) Molecular mechanisms underlying the acclimation of Chlamydomonasreinhardtii against nitric oxide stress. Front Plant Sci 12:690763. https://doi.org/10.3389/fpls.2021.690763
doi: 10.3389/fpls.2021.690763
pubmed: 34421944
pmcid: 8374494
Kwon YT, Ciechanover A (2017) The ubiquitin code in the ubiquitin-proteasome system and autophagy. Trends Biochem Sci 42(11):873–886. https://doi.org/10.1016/j.tibs.2017.09.002
doi: 10.1016/j.tibs.2017.09.002
pubmed: 28947091
Lamport DTA, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary cell wall architecture. Plant Physiol 156(1):11–19. https://doi.org/10.1104/PP.110.169011
doi: 10.1104/PP.110.169011
pubmed: 21415277
pmcid: 3091064
Lipman NS, Jackson LR, Trudel LJ, Weis-Garcia F (2005) Monoclonal versus polyclonal antibodies: distinguishing characteristics, applications, and information resources. ILAR J 46(3):258–268. https://doi.org/10.1093/ILAR.46.3.258
doi: 10.1093/ILAR.46.3.258
pubmed: 15953833
Liu X, Wolfe R, Welch LR, Domozych DS, Popper ZA, Showalter AM (2016) Bioinformatic identification and analysis of extensins in the plant kingdom. PLoS ONE 11(2):e0150177. https://doi.org/10.1371/JOURNAL.PONE.0150177
doi: 10.1371/JOURNAL.PONE.0150177
pubmed: 26918442
pmcid: 4769139
Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann Limnol Int J Limnol 39(2):85–101. https://doi.org/10.1051/LIMN/2003014
doi: 10.1051/LIMN/2003014
Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84(2):281–291. https://doi.org/10.1007/S00253-009-1935-6
doi: 10.1007/S00253-009-1935-6
pubmed: 19330327
Martín-Villanueva S, Gutiérrez G, Kressler D, de la Cruz J (2021) Ubiquitin and ubiquitin-like proteins and domains in ribosome production and function: chance or necessity? Int J Mol Sci 22(9):4359. https://doi.org/10.3390/ijms22094359
doi: 10.3390/ijms22094359
pubmed: 33921964
pmcid: 8122580
Mcqueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91(14):6574–6578. https://doi.org/10.1073/PNAS.91.14.6574
doi: 10.1073/PNAS.91.14.6574
pubmed: 11607483
pmcid: 44245
Møller SR, Yi X, Velásquez SM, Gille S, Hansen PLM, Poulsen CP, Olsen CE, Rejzek M, Parsons H, Zhang Y, Wandall HH, Clausen H, Field RA, Pauly M, Estevez JM, Harholt J, Ulvskov P, Petersen BL (2017) Identification and evolution of a plant cell wall specific glycoprotein glycosyl transferase. ExAD Scientific Reports 7:45341. https://doi.org/10.1038/srep45341
doi: 10.1038/srep45341
pubmed: 28358137
Noda S, Yamaguchi M, Tsurumaki Y, Takahashi Y, Nishikubo N, Hattori T, Demura T, Suzuki S, Umezawa T (2013) ATL54, a ubiquitin ligase gene related to secondary cell wall formation, is transcriptionally regulated by MYB46. Plant Biotechnol 30(5):503–509. https://doi.org/10.5511/plantbiotechnology.13.0905b
doi: 10.5511/plantbiotechnology.13.0905b
Pan S, Jeevanandam J, Danquah MK (2019) Benefits of algal extracts in sustainable agriculture. In: Hallmann A. and Rampelotto P.H (Eds.) Grand Challenges in Algae Biotechnology. Grand Challenges in Biology and Biotechnology, Springer Nature Switzerland AG, 501–534. https://doi.org/10.1007/978-3-030-25233-5_14
Pappas P (1971) The use of a chrome alum-gelatin (subbing) solution as a general adhesive for paraffin sections. Stain Technol 46(3):121–124. https://doi.org/10.3109/10520297109067835
doi: 10.3109/10520297109067835
pubmed: 4105404
Picciotto S, Santonicola P, Paterna A, Rao E, Raccosta S, Romancino DP, Noto R, Touzet N, Manno M, di Schiavi E, Bongiovanni A, Adamo G (2022) Extracellular vesicles from microalgae: uptake studies in human cells and Caenorhabditis elegans. Front Bioeng Biotechnol 10:1–11. https://doi.org/10.3389/fbioe.2022.830189
doi: 10.3389/fbioe.2022.830189
Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochimica Et Biophysica Acta - Mol Cell Res 1695(1–3):55–72. https://doi.org/10.1016/J.BBAMCR.2004.09.019
doi: 10.1016/J.BBAMCR.2004.09.019
Pickett-Heaps JD, Staehelin LA (1975) The ultrastructure of Scenedesmus (Chlorophyceae). II. Cell division and colony formation. J Phycol 11:186–202. https://doi.org/10.1111/j.1529-8817.1975.tb02766.x
doi: 10.1111/j.1529-8817.1975.tb02766.x
Pinski A, Betekhtin A, Skupien-rabian B, Jankowska U, Jamet E, Hasterok R (2021) Changes in the cell wall proteome of leaves in response to high temperature stress in brachypodium distachyon. Int J Mol Sci 22(13):6750. https://doi.org/10.3390/ijms22136750
doi: 10.3390/ijms22136750
pubmed: 34201710
pmcid: 8267952
Rashidi B, Trindade LM (2018) Detailed biochemical and morphologic characteristics of the green microalga Neochloris oleoabundans cell wall. Algal Res 35:152–159. https://doi.org/10.1016/J.ALGAL.2018.08.033
doi: 10.1016/J.ALGAL.2018.08.033
Regente M, Pinedo M, Clemente HS, Balliau T, Jamet E, de La Canal L (2017) Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. J Exp Bot 68(20):5485–5495. https://doi.org/10.1093/JXB/ERX355
doi: 10.1093/JXB/ERX355
pubmed: 29145622
Rippka E, Deruelles J, Waterbury NB (1979) Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. Microbiology 111(1):1–61. https://doi.org/10.1099/00221287-111-1-1
doi: 10.1099/00221287-111-1-1
Roberts K, Grief C, Hills GJ, Shaw PJ (1985) Cell wall glycoproteins: structure and function. J Cell Sci Suppl 2:105–127. https://doi.org/10.1242/JCS.1985.SUPPLEMENT_2.6
doi: 10.1242/JCS.1985.SUPPLEMENT_2.6
pubmed: 3867667
Rutter BD, Innes RW (2017) Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiol 173(1):728–741. https://doi.org/10.1104/PP.16.01253
doi: 10.1104/PP.16.01253
pubmed: 27837092
Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6(12):242. https://doi.org/10.1186/GB-2005-6-12-242
doi: 10.1186/GB-2005-6-12-242
pubmed: 16356276
pmcid: 1414085
Schnell JD, Hicke L (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278(38):35857–35860. https://doi.org/10.1074/JBC.R300018200
doi: 10.1074/JBC.R300018200
pubmed: 12860974
Scopes RK (1974) Measurement of protein by spectrophotometry at 205 nm. Anal Biochem 59(1):277–282. https://doi.org/10.1016/0003-2697(74)90034-7
doi: 10.1016/0003-2697(74)90034-7
pubmed: 4407487
Sepulveda P, Lopez-Ribot JL, Gozalbo D, Cervera A, Martinez JP, Chaffin WL (1996) Ubiquitin-like epitopes associated with Candida albicans cell surface receptors. Infect Immun 64(10):4406–4408. https://doi.org/10.1128/IAI.64.10.4406-4408.1996
doi: 10.1128/IAI.64.10.4406-4408.1996
pubmed: 8926122
pmcid: 174390
Shimogawara K, Muto S (1989) Heat shock induced change in protein ubiquitination in Chlamydomonas. Plant Cell Physiol 30(1):9–16. https://doi.org/10.1093/oxfordjournals.pcp.a077722
doi: 10.1093/oxfordjournals.pcp.a077722
Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153(2):485–513. https://doi.org/10.1104/PP.110.156554
doi: 10.1104/PP.110.156554
pubmed: 20395450
pmcid: 2879790
Sibbald SJ, Hopkins JF, Filloramo GV, Archibald JM (2019) Ubiquitin fusion proteins in algae: implications for cell biology and the spread of photosynthesis. BMC Genomics 20:38. https://doi.org/10.1186/s12864-018-5412-4
doi: 10.1186/s12864-018-5412-4
pubmed: 30642248
pmcid: 6332867
Siegelman M, Bond MW, Gallatin WM, John TS, Smith HT, Fried VA, Weissman IL (1986) Cell surface molecule associated with lymphocyte homing is a ubiquitinated branched-chain glycoprotein. Science 231(4740):823–829. https://doi.org/10.1126/science.3003913
doi: 10.1126/science.3003913
pubmed: 3003913
Skjånes K, Rebours C, Lindblad P (2013) Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process. Crit Rev Biotechnol 33(2):172–215. https://doi.org/10.3109/07388551.2012.681625
doi: 10.3109/07388551.2012.681625
pubmed: 22765907
Spain O, Plöhn M, Funk C (2021) The cell wall of green microalgae and its role in heavy metal removal. Physiol Plant 173(2):526–535. https://doi.org/10.1111/PPL.13405
doi: 10.1111/PPL.13405
pubmed: 33764544
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101(2):87–96. https://doi.org/10.1263/JBB.101.87
doi: 10.1263/JBB.101.87
pubmed: 16569602
Sujashvili R (2016) Advantages of extracellular ubiquitin in modulation of immune responses. Mediators Inflamm 2016(1):4190390. https://doi.org/10.1155/2016/4190390
doi: 10.1155/2016/4190390
pubmed: 27642236
pmcid: 5014979
Tordai H, Bányai L, Patthy L (1999) The PAN module: The N-terminal domains of plasminogen and hepatocyte growth factor are homologous with the apple domains of the prekallikrein family and with a novel domain found in numerous nematode proteins. FEBS Lett 461(1–2):63–67. https://doi.org/10.1016/S0014-5793(99)01416-7
doi: 10.1016/S0014-5793(99)01416-7
pubmed: 10561497
Tukaj Z, Bohdanowicz J (1995) Sensitivity to fuel diesel oil and cell wall structure of some Scenedesmus (Chlorococcales) strains. Acta Soc Bot Pol 64(2):139–147. https://doi.org/10.5586/asbp.1995.018
doi: 10.5586/asbp.1995.018
Vallentine P, Hung C-Y, Xie J, van Hoewyk D (2014) The ubiquitin–proteasome pathway protects Chlamydomonasreinhardtii against selenite toxicity, but is impaired as reactive oxygen species accumulate. AoB Plants 6(0):plu062–plu062. https://doi.org/10.1093/AOBPLA/PLU062
doi: 10.1093/AOBPLA/PLU062
pubmed: 25301821
pmcid: 4231294
Ventura SPM, Nobre BP, Ertekin F, Hayes M, Garciá -Vaquero M, Vieira F, Koc M, Gouveia L, Aires-Barros MR, Palavra AMF (2017) Extraction of value-added compounds from microalgae. In: C. Gonzalez & R. Munoz (Eds.), Microalgal-based biofuels and bioproducts. From Feedstock cultivation to end products. (1st ed., pp. 461–483). Woodhead publishing Elsevier. https://doi.org/10.1016/B978-0-08-101023-5.00019-4
Voigt J (1985) Extraction by lithium chloride of hydroxyproline-rich glycoproteins from intact cells of Chlamydomonas reinhardii. Planta 164(3):379–389. https://doi.org/10.1007/BF00402950
doi: 10.1007/BF00402950
pubmed: 24249608
Voigt J (1988) The lithium-chloride-soluble cell-wall layers of Chlamydomonas reinhardii contain several immunologically related glycoproteins. Planta 173(3):373–384. https://doi.org/10.1007/BF00401024
doi: 10.1007/BF00401024
pubmed: 24226544
Voigt J, Wrann D, Vogeler HP, Koenig WA, Mix M (1994) Hydroxyproline-containing and glycine-rich cell-wall polypeptides are widespread in the green algae. Microbiol Res 149(3):223–229. https://doi.org/10.1016/S0944-5013(11)80062-5
doi: 10.1016/S0944-5013(11)80062-5
Voigt J, Frank R, Wöstemeyer J (2009) The chaotrope-soluble glycoprotein GP1 is a constituent of the insoluble glycoprotein framework of the Chlamydomonas cell wall: research letter. FEMS Microbiol Lett 291(2):209–215. https://doi.org/10.1111/J.1574-6968.2008.01456.X
doi: 10.1111/J.1574-6968.2008.01456.X
pubmed: 19146575
Voigt J, Stolarczyk A, Zych M, Malec P, Burczyk J (2014) The cell-wall glycoproteins of the green alga Scenedesmus obliquus. The predominant cell-wall polypeptide of Scenedesmus obliquus is related to the cell-wall glycoprotein gp3 of Chlamydomonas reinhardtii. Plant Sci 215–216:39–47. https://doi.org/10.1016/j.plantsci.2013.10.011
doi: 10.1016/j.plantsci.2013.10.011
pubmed: 24388513
Wang L, Liu J, Filipiak M, Mungunkhuyag K, Jedynak P, Burczyk J, Fu P, Malec P (2021) Fast and efficient cadmium biosorption by Chlorella vulgaris K-01 strain: the role of cell walls in metal sequestration. Algal Res 60:102497. https://doi.org/10.1016/j.algal.2021.102497
doi: 10.1016/j.algal.2021.102497
Wettern M, Parag HA, Pollmann L, Ohad I, Kulka RG (1990) Ubiquitin in Chlamydomonas reinhardii. Eur J Biochem 191(3):571–576. https://doi.org/10.1111/J.1432-1033.1990.TB19159.X
doi: 10.1111/J.1432-1033.1990.TB19159.X
pubmed: 2167845
Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362. https://doi.org/10.1038/nmeth.1322
doi: 10.1038/nmeth.1322
pubmed: 19377485
Wohlert M, Benselfelt T, Wågberg L, Furó I, Berglund LA, Wohlert J (2022) Cellulose and the role of hydrogen bonds: not in charge of everything. Cellulose 29:1–23. https://doi.org/10.1007/S10570-021-04325-4
doi: 10.1007/S10570-021-04325-4
Xu FQ, Xue HW (2019) The ubiquitin-proteasome system in plant responses to environments. Plant Cell Environ 42(10):2931–2944. https://doi.org/10.1111/PCE.13633
doi: 10.1111/PCE.13633
pubmed: 31364170
Yamamoto M, Nozaki H, Miyazawa Y, Koide T, Kawano S (2003) Relationship between presence of a mother cell wall and speciation in the unicellular microalga Nannochloris (Chlorophyta). J Phycol 39(1):172–184. https://doi.org/10.1046/j.1529-8817.2003.02052.x
doi: 10.1046/j.1529-8817.2003.02052.x
Zhang K, McKinlay C, Hocart CH, Djordjevic MA (2006) The Medicago truncatula small protein proteome and peptidome. J Proteome Res 5(12):3355–3367. https://doi.org/10.1021/pr060336t
doi: 10.1021/pr060336t
pubmed: 17137337
Zhang J, Chen S, Yan Y, Zhu X, Qi Q, Zhang Y, Zhang Q, Xia R (2019) Extracellular ubiquitin is the causal link between stored blood transfusion therapy and tumor progression in a melanoma mouse model. J Cancer 10(12):2822–2835. https://doi.org/10.7150/JCA.31360
doi: 10.7150/JCA.31360
pubmed: 31258790
pmcid: 6584930
Zheng N, Shabek N (2017) Ubiquitin ligases: structure, function, and regulation. Annu Rev Biochem 86:129–157. https://doi.org/10.1146/annurev-biochem-060815-014922
doi: 10.1146/annurev-biochem-060815-014922
pubmed: 28375744
Zhou Y, Li M, Zhao F, Zha H, Yang L, Lu Y, Wang G, Shi J, Chen J (2016) Floral nectary morphology and proteomic analysis of nectar of Liriodendron tulipifera Linn. Front Plant Sci 7:826. https://doi.org/10.3389/FPLS.2016.00826
doi: 10.3389/FPLS.2016.00826
pubmed: 27379122
pmcid: 4905952
Zych M, Burczyk J, Borymska W, Kaczmarczyk-Sedlak I (2022) Accumulation of proteins in the medium of the various naturally occurring Chlorella and Scenedesmus microalgae containing and not-containing algaenan. Algal Res 62:102598. https://doi.org/10.1016/j.algal.2021.102598
doi: 10.1016/j.algal.2021.102598
Zych M (2001) Cell wall proteins of green algae from the order Chlorococcales, with special emphasis on ubiquitin. Doctoral Dissertation (in Polish). Silesian Medical University. Katowice, Poland