Specific pools of endogenous peptides are present in gametophore, protonema, and protoplast cells of the moss Physcomitrella patens

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Fesenko, Igor A ^a   Arapidi, Georgij P ^a,c   Skripnikov, Alexander Yu ^a,e   Alexeev, Dmitry G ^b,c   Kostryukova, Elena S ^b   Manolov, Alexander I ^b,c   Altukhov, Ilya A ^b,c   Khazigaleeva, Regina A ^a   Seredina, Anna V ^a   Kovalchuk, Sergey I ^a,b   Ziganshin, Rustam H ^a   Zgoda, Viktor G ^d   Novikova, Svetlana E ^d   Semashko, Tatiana A ^b   Slizhikova, Darya K ^a   Ptushenko, Vasilij V ^e   Gorbachev, Alexey Y ^b   Govorun, Vadim M ^a,b,c   Ivanov, Vadim T ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b FEDERAL RESEARCH AND CLINICAL CENTER OF PHYSICAL CHEMICAL MEDICINE OF FEDERAL MEDICAL BIOLOGICAL AGENCY   (Russian Federation)

^c MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^d INSTITUTE OF BIOMEDICAL CHEMISTRY   (Russian Federation)

^e MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Endogenous peptides; LC MS MS; Physcomitrella patens; Proteome; Transcriptome profiling

Indexed keywords

BRYOPHYTA; PHYSCOMITRELLA PATENS;

PEPTIDE; PLANT PROTEIN; PROTEOME;

BRYOPSIDA; CYTOLOGY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PLANT CELL; PROTOPLAST; SEQUENCE ALIGNMENT;

BRYOPSIDA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GERM CELLS, PLANT; PEPTIDES; PHOTOSYNTHESIS; PLANT CELLS; PLANT PROTEINS; PROTEOME; PROTOPLASTS; SEQUENCE ALIGNMENT;

EID: 84928257276     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0468-7     Document Type: Article

References (97)

1. Matsubayashi Y, Sakagami Y. Peptide hormones in plants. Annu Rev Plant Biol. 2006;57:649-74.
2. Farrokhi N, Whitelegge JP, Brusslan JA. Plant peptides and peptidomics. Plant Biotechnol J. 2008;6(2):105-34.
3. Murphy E, Smith S, De Smet I. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell. 2012;24(8):3198-217.
4. Marmiroli N, Maestri E. Plant peptides in defense and signaling. Peptides. 2014;56C:30-44.
5. De Smet I, Voss U, Jurgens G, Beeckman T. Receptor-like kinases shape the plant. Nat Cell Biol. 2009;11(10):1166-73.
6. Lease KA, Walker JC. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol. 2006;142(3):831-8.
7. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. Plant peptides in signalling: looking for new partners. Trends Plant Sci. 2009;14(5):255-63.
8. Kondo T, Plaza S, Zanet J, Benrabah E, Valenti P, Hashimoto Y, et al. Small peptides switch the transcriptional activity of Shavenbaby during Drosophila embryogenesis. Science. 2010;329(5989):336-9.
9. Hanada K, Higuchi-Takeuchi M, Okamoto M, Yoshizumi T, Shimizu M, Nakaminami K, et al. Small open reading frames associated with morphogenesis are hidden in plant genomes. Proc Natl Acad Sci U S A. 2013;110(6):2395-400.
10. Slavoff SA, Mitchell AJ, Schwaid AG, Cabili MN, Ma J, Levin JZ, et al. Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat Chem Biol. 2013;9(1):59-64.
11. Ladoukakis E, Pereira V, Magny EG, Eyre-Walker A, Couso JP. Hundreds of putatively functional small open reading frames in Drosophila. Genome Biol. 2011;12(11):R118.
12. Ivanov VT, Yatskin ON. Peptidomics: a logical sequel to proteomics. Expert Rev Proteomics. 2005;2(4):463-73.
13. Iatskin ON, Karelin AA, Ivanov VT. Peptidomes of the brain, heart, lung, and spleen of a rat: similarity and differences. Bioorg Khim. 2009;35(4):471-82.
14. Blishchenko EY, Sazonova OV, Yatskin ON, Kalinina OA, Tolmazova AG, Philippova MM, et al. beta-Actin-derived peptides isolated from acidic extract of rat spleen suppress tumor cell growth. J Pept Sci. 2008;14(7):811-8.
15. Sasaki K, Takahashi N, Satoh M, Yamasaki M, Minamino N. A peptidomics strategy for discovering endogenous bioactive peptides. J Proteome Res. 2010;9(10):5047-52.
16. Brand GD, Magalhaes MT, Tinoco ML, Aragao FJ, Nicoli J, Kelly SM, et al. Probing protein sequences as sources for encrypted antimicrobial peptides. PLoS One. 2012;7(9):e45848.
17. Chen YL, Lee CY, Cheng KT, Chang WH, Huang RN, Nam HG, et al. Quantitative Peptidomics Study Reveals That a Wound-Induced Peptide from PR-1 Regulates Immune Signaling in Tomato. Plant Cell. 2014;26(10):4135-48.
18. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, et al. Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A. 2006;103(23):8894-9.
19. Pearce G, Munske G, Yamaguchi Y, Ryan CA. Structure-activity studies of GmSubPep, a soybean peptide defense signal derived from an extracellular protease. Peptides. 2010;31(12):2159-64.
20. Yamaguchi Y, Barona G, Ryan CA, Pearce G. GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol. 2011;156(2):932-42.
21. Kamisugi Y, Schlink K, Rensing SA, Schween G, Von Stackelberg M, Cuming AC, et al. The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res. 2006;34(21):6205-14.
22. Strepp R, Scholz S, Kruse S, Speth V, Reski R. Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci U S A. 1998;95(8):4368-73.
23. Decker EL, Frank W, Sarnighausen E, Reski R. Moss systems biology en route: phytohormones in Physcomitrella development. Plant Biol (Stuttg). 2006;8(3):397-405.
24. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science. 2008;319(5859):64-9.
25. Sarnighausen E, Wurtz V, Heintz D, Van Dorsselaer A, Reski R. Mapping of the Physcomitrella patens proteome. Phytochemistry. 2004;65(11):1589-607.
26. Cho SH, Hoang QT, Kim YY, Shin HY, Ok SH, Bae JM, et al. Proteome analysis of gametophores identified a metallothionein involved in various abiotic stress responses in Physcomitrella patens. Plant Cell Rep. 2006;25(5):475-88.
27. Skripnikov AY, Polyakov NB, Tolcheva EV, Velikodvorskaya VV, Dolgov SV, Demina IA, et al. Proteome analysis of the moss Physcomitrella patens (Hedw.) B.S.G. Biochemistry (Mosc). 2009;74(5):480-90.
28. Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, et al. Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta. 2008;228(1):167-77.
29. Wang X, Yang P, Zhang X, Xu Y, Kuang T, Shen S, et al. Proteomic analysis of the cold stress response in the moss. Physcomitrella patens. Proteomics. 2009;9(19):4529-38.
30. Cui S, Hu J, Guo S, Wang J, Cheng Y, Dang X, et al. Proteome analysis of Physcomitrella patens exposed to progressive dehydration and rehydration. J Exp Bot. 2012;63(2):711-26.
31. Lang EG, Mueller SJ, Hoernstein SN, Porankiewicz-Asplund J, Vervliet-Scheebaum M, Reski R. Simultaneous isolation of pure and intact chloroplasts and mitochondria from moss as the basis for sub-cellular proteomics. Plant Cell Rep. 2011;30(2):205-15.
32. Cuming AC, Cho SH, Kamisugi Y, Graham H, Quatrano RS. Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss. Physcomitrella patens. New Phytol. 2007;176(2):275-87.
33. Richardt S, Timmerhaus G, Lang D, Qudeimat E, Correa LGG, Reski R, et al. Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol. 2010;72(1-2):27-45.
34. Xiao L, Wang H, Wan P, Kuang T, He Y. Genome-wide transcriptome analysis of gametophyte development in Physcomitrella patens. BMC Plant Biol. 2011;11:177.
35. Xiao L, Zhang L, Yang G, Zhu H, He Y. Transcriptome of protoplasts reprogrammed into stem cells in Physcomitrella patens. PLoS One. 2012;7(4):e35961.
36. Nishiyama T, Miyawaki K, Ohshima M, Thompson K, Nagashima A, Hasebe M, et al. Digital gene expression profiling by 5'-end sequencing of cDNAs during reprogramming in the moss Physcomitrella patens. PLoS One. 2012;7(5):e36471.
37. Erxleben A, Gessler A, Vervliet-Scheebaum M, Reski R. Metabolite profiling of the moss Physcomitrella patens reveals evolutionary conservation of osmoprotective substances. Plant Cell Rep. 2012;31(2):427-36.
38. Skripnikov A, Anikanov NA, Kazakov VS, Dolgov SV, Ziganshin R, Govorun VM, et al. Exploration and identification of Physcomitrella patens moss peptides. Bioorg Khim. 2011;37(1):108-18.
39. Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007;2(8):1896-906.
40. Faurobert M, Pelpoir E, Chaib J. Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol Biol. 2007;355:9-14.
41. Torrent M, Di Tommaso P, Pulido D, Nogues MV, Notredame C, Boix E, et al. AMPA: an automated web server for prediction of protein antimicrobial regions. Bioinformatics. 2012;28(1):130-1.
42. Cove DJ, Perroud PF, Charron AJ, McDaniel SF, Khandelwal A, Quatrano RS. Isolation of DNA, RNA, and protein from the moss Physcomitrella patens gametophytes. Cold Spring Harb Protoc. 2009;2009(2):prot5146.
43. Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, et al. Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genomics. 2013;14:498.
44. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-11.
45. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5.
46. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-40.
47. Hindson BJ, Ness KD, Masquelier DA, Belgrader P, Heredia NJ, Makarewicz AJ, et al. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal Chem. 2011;83(22):8604-10.
48. Blowers DP, Boss WF, Trewavas AJ. Rapid Changes in Plasma Membrane Protein Phosphorylation during Initiation of Cell Wall Digestion. Plant Physiol. 1988;86(2):505-9.
49. Prins A, Van Heerden PD, Olmos E, Kunert KJ, Foyer CH. Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: a model for dynamic interactions with ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. J Exp Bot. 2008;59(7):1935-50.
50. Rushton PJ, Somssich IE, Ringler P, Shen QJ. WRKY transcription factors. Trends Plant Sci. 2010;15(5):247-58.
51. Ramos MS, Abele R, Nagy R, Grotemeyer MS, Tampe R, Rentsch D, et al. Characterization of a transport activity for long-chain peptides in barley mesophyll vacuoles. J Exp Bot. 2011;62(7):2403-10.
52. Khanna-Chopra R. Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma. 2012;249(3):469-81.
53. Nelson CJ, Alexova R, Jacoby RP, Millar AH. Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiol. 2014;166(1):91-108.
54. Widiez T, Symeonidi A, Luo C, Lam E, Lawton M, Rensing SA. The chromatin landscape of the moss Physcomitrella patens and its dynamics during development and drought stress. Plant J. 2014;79(1):67-81.
55. Dure L, Galau GA. Developmental Biochemistry of Cottonseed Embryogenesis and Germination: XIII. Regulation of biosynthesis of principal storage proteins. Plant Physiol. 1981;68(1):187-94.
56. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 2008;148(1):6-24.
57. Wise MJ, Tunnacliffe A. POPP the question: what do LEA proteins do? Trends Plant Sci. 2004;9(1):13-7.
58. Chakrabortee S, Meersman F, Kaminski Schierle GS, Bertoncini CW, McGee B, Kaminski CF, et al. Catalytic and chaperone-like functions in an intrinsically disordered protein associated with desiccation tolerance. Proc Natl Acad Sci U S A. 2010;107(37):16084-9.
59. Furuki T, Shimizu T, Chakrabortee S, Yamakawa K, Hatanaka R, Takahashi T, et al. Effects of Group 3 LEA protein model peptides on desiccation-induced protein aggregation. Biochim Biophys Acta. 2012;1824(7):891-7.
60. Lienard D, Durambur G, Kiefer-Meyer MC, Nogue F, Menu-Bouaouiche L, Charlot F, et al. Water transport by aquaporins in the extant plant Physcomitrella patens. Plant Physiol. 2008;146(3):1207-18.
61. Heil M, Ibarra-Laclette E, Adame-Alvarez RM, Martinez O, Ramirez-Chavez E, Molina-Torres J, et al. How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLoS One. 2012;7(2):e30537.
62. Feussner I, Wasternack C. The lipoxygenase pathway. Annu Rev Plant Biol. 2002;53:275-97.
63. Stumpe M, Gobel C, Faltin B, Beike AK, Hause B, Himmelsbach K, et al. The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol. 2010;188(3):740-9.
64. Ponce De Leon I, Schmelz EA, Gaggero C, Castro A, Alvarez A, Montesano M. Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol. 2012;13(8):960-74.
65. Pollier J, Moses T, Gonzalez-Guzman M, De Geyter N, Lippens S, Vanden Bossche R, et al. The protein quality control system manages plant defence compound synthesis. Nature. 2013;504(7478):148-52.
66. Yamaguchi Y, Huffaker A. Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol. 2011;14(4):351-7.
67. Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, et al. Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling. Plant Physiol. 2014;165(3):1302-14.
68. Pearce G, Yamaguchi Y, Barona G, Ryan CA. A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci U S A. 2010;107(33):14921-5.
69. Moreno J, Garcia-Murria MJ, Marin-Navarro J. Redox modulation of Rubisco conformation and activity through its cysteine residues. J Exp Bot. 2008;59(7):1605-14.
70. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, et al. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 2009;149(2):885-93.
71. Kwon KC, Verma D, Jin S, Singh ND, Daniell H. Release of proteins from intact chloroplasts induced by reactive oxygen species during biotic and abiotic stress. PLoS One. 2013;8(6):e67106.
72. Coll NS, Epple P, Dangl JL. Programmed cell death in the plant immune system. Cell Death Differ. 2011;18(8):1247-56.
73. Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ. A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ. 2011;18(8):1289-97.
74. Van Doorn WG. Classes of programmed cell death in plants, compared to those in animals. J Exp Bot. 2011;62(14):4749-61.
75. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G. Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun. 2001;286(3):433-42.
76. Lanneau D, Brunet M, Frisan E, Solary E, Fontenay M, Garrido C. Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med. 2008;12(3):743-61.
77. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. Protein degradation - an alternative respiratory substrate for stressed plants. Trends Plant Sci. 2011;16(9):489-98.
78. Kurepa J, Wang S, Li Y, Smalle J. Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav. 2009;4(10):924-7.
79. Saric T, Graef CI, Goldberg AL. Pathway for degradation of peptides generated by proteasomes: a key role for thimet oligopeptidase and other metallopeptidases. J Biol Chem. 2004;279(45):46723-32.
80. Reits E, Neijssen J, Herberts C, Benckhuijsen W, Janssen L, Drijfhout JW, et al. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity. 2004;20(4):495-506.
81. Chao WS, Pautot V, Holzer FM, Walling LL. Leucine aminopeptidases: the ubiquity of LAP-N and the specificity of LAP-A. Planta. 2000;210(4):563-73.
82. Book AJ, Yang P, Scalf M, Smith LM, Vierstra RD. Tripeptidyl peptidase II. An oligomeric protease complex from Arabidopsis. Plant Physiol. 2005;138(2):1046-57.
83. Polge C, Jaquinod M, Holzer F, Bourguignon J, Walling L, Brouquisse R. Evidence for the Existence in Arabidopsis thaliana of the Proteasome Proteolytic Pathway: ACTIVATION IN RESPONSE TO CADMIUM. J Biol Chem. 2009;284(51):35412-24.
84. Beninga J, Rock KL, Goldberg AL. Interferon-gamma can stimulate post-proteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J Biol Chem. 1998;273(30):18734-42.
85. Hughes E, Burke RM, Doig AJ. Inhibition of toxicity in the beta-amyloid peptide fragment beta -(25-35) using N-methylated derivatives: a general strategy to prevent amyloid formation. J Biol Chem. 2000;275(33):25109-15.
86. Tenidis K, Waldner M, Bernhagen J, Fischle W, Bergmann M, Weber M, et al. Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J Mol Biol. 2000;295(4):1055-71.
87. van der Hoorn RA. Plant proteases: from phenotypes to molecular mechanisms. Annu Rev Plant Biol. 2008;59:191-223.
88. Xiong Y, Contento AL, Nguyen PQ, Bassham DC. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 2007;143(1):291-9.
89. Davies KJ. Degradation of oxidized proteins by the 20S proteasome. Biochimie. 2001;83(3-4):301-10.
90. Asher G, Reuven N, Shaul Y. 20S proteasomes and protein degradation "by default". Bioessays. 2006;28(8):844-9.
91. Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J. 1998;335(Pt 3):637-42.
92. Savulescu AF, Glickman MH. Proteasome activator 200: the heat is on. Mol Cell Proteomics. 2011;10(5):R110-R006890.
93. Stone SL. The role of ubiquitin and the 26S proteasome in plant abiotic stress signaling. Frontiers Plant Sci. 2014;5:135.
94. Marino D, Peeters N, Rivas S. Ubiquitination during plant immune signaling. Plant Physiol. 2012;160(1):15-27.
95. Gfeller A, Baerenfaller K, Loscos J, Chetelat A, Baginsky S, Farmer EE. Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol. 2011;156(4):1797-807.
96. Golldack D, Vera P, Dietz KJ. Expression of subtilisin-like serine proteases in Arabidopsis thaliana is cell-specific and responds to jasmonic acid and heavy metals with developmental differences. Physiol Plant. 2003;118(1):64-73.
97. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013;41(Database issue):D1063-9.