Overexpression of NtUBQ2 encoding Ub-extension protein enhances cadmium tolerance by activating 20S and 26S proteasome in tobacco (Nicotiana tabacum)

• Autorzy: Lee B.D. , Hwang S.
• Języki publikacji: EN

Abstrakty

EN

The Ub/26S proteasome system removes abnormal proteins and most short-lived regulatory proteins, thereby contributing to cell proliferation, hormone responses, development and resistance to abiotic and biotic stresses. Here we show that cadmium tolerance is related positively to the 20S proteasome (catalytic particle of 26S proteasome) activity in plants. By transforming WT yeast Y800 with a tobacco expression cDNA library, we isolated a tobacco cDNAs, NtUBQ2 (the Ub-extension protein) conferring cadmium tolerance. Overexpression of NtUBQ2 increased cadmium tolerance in transgenic tobacco; 20S proteasome activity was enhanced and ubiquitinated protein level was diminished in response to cadmium. In contrast, proteasome activity was reduced and ubiquitinated protein level was less decreased than transgenic tobacco by Cd treatment in control tobacco which is sensitive to Cd. These observations strongly suggest that plants acquire cadmium tolerance by removing cadmium-damaged proteins via Ub/ 26S proteasome-dependent proteolysis or Ub-independent 20S proteasome. This finding could be applied to engineering efficient metal phytoremediators.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 02
• Opis fizyczny: Article: 22 [8 p.], fig.,ref.

Twórcy

autor

Lee B.D.

• Department of Molecular Biology and Plant Engineering Research Institute, Sejong University, 98 Kunja-dong, Kwangjin-gu, Seoul, Korea

autor

Hwang S.

• Department of Molecular Biology and Plant Engineering Research Institute, Sejong University, 98 Kunja-dong, Kwangjin-gu, Seoul, Korea

Bibliografia

• Basset G, Raymond P, Malek L, Brouquisse R (2002) Changes in the expression and the enzymatic properties of the 20S proteasome in sugar-starved maize roots. Evidence for an in vivo oxidation of the proteasome. Plant Physiol 128:1149–1162
• Chen KQ, Rubenstein I (1991) Characterization of the structure and transcription of an ubiquitin fusion gene from maize. Gene 107:205–212
• Di Y, Tamás MJ (2007) Regulation of the arsenic-responsive transcription factor Yap8p involves the ubiquitin-proteasome pathway. J Cell Sci 120:256–264
• Djebali W, Gallusci P, Polge C, Boulila L, Galtier N, Raymond P, Chaibi W, Brouquisse R (2008) Modifications in endopeptidase and 20S proteasome expression and activities in cadmium treated tomato (Solanum lycopersicum L.) plants. Planta 227:625–639
• Farras R, Ferrando A, Jasik J, Kleinow T, OkreszL Tiburcio A, Salchert K, del Pozo C, Schell J, Koncz C (2001) SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 20:2742–2756
• Figueiredo-Pereira ME, Cohen G (1999) The ubiquitin/proteasome pathway: friend or foe in zinc-, cadmium-, and H2O2-induced neuronal oxidative stress. Mol Biol Rep 26:65–69
• Finley D, Bartel B, Varshavsky A (1989) The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosomal biogenesis. Nature 338:394–401
• Forzani C, Lobreaux S, Mari S, Briat JF, Lebrun M (2002) Metal resistance in yeast mediated by the expression of a maize 20S proteasome subunit. Gene 293:199–204
• Garbarino JE, Rockhold DR, Belknap WR (1992) Expression of stress-responsive ubiquitin genes in potato tubers. Plant Mol Biol 20:235–244
• Genschik P, Parmentier Y, Durr A, Marbach J, Criqui MC, Jamet E, Fleck J (1992) Ubiquitin genes are differentially regulated in protoplast-derived cultures of Nicotiana sylvestris and in response to various stresses. Plant Mol Biol 20:897–910
• Goller SP, Gorfer M, Kubicek CP (1998) Trichodermareesei prs12 encodes a stress- and unfolded-protein-response-inducible regulatory subunit of the fungal 26S proteasome. Curr Genet 33:284–290
• Harrison C, Katayama S, Dhut S, Chen D, Jones N, Ba¨hler J, Toda T (2005) SCFPof1-ubiquitin and its target Zip1 transcription factor mediate cadmium response in fission yeast. EMBO J 24(3): 599–610
• Hartmann-Petersen R, Seeger M, Gordon C (2003) Transferring substrates to the 26S proteasome. Trends Biochem Sci 28:26–31
• Horsch RB, Klee HJ, Stachel S, Winans SC, Nester EW, Rogers SG, Fraley RT (1986) Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs. Proc Natl Acad Sci USA 83:2571–2575
• Ingvardsen C, Veierskov B (2001) Ubiquitin- and proteasomedependent proteolysis in plants. Physiol Plant 112(4):451–459
• Jungmann J, Reins HA, Schobert C, Jentsch S (1993) Resistance to cadmium mediated by ubiquitin-dependent proteolysis. Nature 361:369–371
• Kirkpatrick DS, Dale KV, Catania JM, Gandolfi AJ (2003) Low-level arsenite causes accumulation of ubiquitinated proteins in rabbit renal cortical slices and HEK293 cells. Toxicol Appl Pharmacol 186:101–109
• Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol 115:1641–1650
• Kwok SF, Staub JM, Deng XW (1999) Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex. J Mol Biol 285:85–95
• Lee M, Hwang S (2012) Cyc07 enhances arsenite tolerance by reducing As levels in Nicotiana tabacum and Arabidopsis thaliana. Plant Biotechnol Rep 6:391–395
• Lee SS, Cho HS, Yoon GM, Ahn JW, Kim HH, Pai HS (2003) Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J 33:825–840
• Mao C, Yi K, Yang L, Zheng B, Wu Y, Liu F, Wu P (2004) Identification of aluminum-regulated genes by cDNA-AFLP in rice (Oryza sativa L.): aluminum-regulated genes for the metabolism of cell wall components. J Exp Bot 55:137–143
• Milla MA, Butler E, Huete AR, Wilson CF, Anderson O, Gustafson JP (2002) Expressed sequence tag-based gene expression analysis under aluminum stress in rye. Plant Physiol 130: 1706–1716
• Park SM, Kim JH, Lee YK, Pyee JH, Cheon CI, Hong CB (1997) Nucleotide sequence of a ubiquitin-extension protein gene in Nicotiana tabacum and its expression pattern upon heat shock. Mol Cells 7:125–130
• Pena LB, Pasquini LA, Tomaro ML, Gallego SM (2006) Proteolytic system in sunflower (Helianthus annuus L.) leaves under cadmium stress. Plant Sci 171:531–537
• Pena LB, Pasquini LA, Tomaro ML, Gallego SM (2007) 20S proteasome and accumulation of oxidized and ubiquitinated proteins in maize leaves subjected to cadmium stress. Phytochemistry 68:1139–1146
• Polge C, Jaquinod M, Holzer F, Bourguignon J, Walling L, Brouquisse R (2009) Evidence for the existence in Arabidopsis thaliana of the proteasome proteolytic pathway: activation in response to cadmium. J Biol Chem 284(51):35412–35424
• Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226
• Ross-Macdonald P, Sheehan A, Roeder GS, Snyder M (1997) A multipurpose transposon system for analyzing protein production, localization, and function in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94:190–195
• Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6(7):2180–2198
• Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590
• Sung DY, Kim TH, Komives EA, Mendoza-Co´zatl DG, Schroeder JI (2009) ARS5 is a component of the 26S proteasome complex, and negatively regulates thiol biosynthesis and arsenic tolerance in Arabidopsis. Plant J 59(5):802–812
• Tsirigotis M, Zhang M, Chiu RK, Wouters BG, Gray DA (2001) Sensitivity of mammalian cells expressing mutant ubiquitin to protein-damaging agents. J Biol Chem 276:46073–46078
• Van Nocker S, Vierstra RD (1993) Multiubiquitin chains linked through lysine 48 are abundant in vivo and are competent intermediates in the ubiquitin proteolytic pathway. J Biol Chem 268:24766–24773
• Vido K, Spector D, Lagniel G, Lopez S, Toledano MB (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J Biol Chem 276:8469–8474
• Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015–1068

Identyfikatory

DOI

10.1007/s11738-015-1774-2