A mutation in the essential and widely conserved DAMAGED DNA BINDING1-Cullin4 ASSOCIATED FACTOR gene OZS3 causes hypersensitivity to zinc excess, cold and UV stress in Arabidopsis thaliana.
Arabidopsis thaliana
E3 ligases
WDR70
cold sensitivity
metal tolerance
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
02
05
2018
revised:
18
02
2020
accepted:
01
04
2020
pubmed:
22
4
2020
medline:
2
3
2021
entrez:
22
4
2020
Statut:
ppublish
Résumé
The overly zinc sensitive Arabidopsis thaliana mutant ozs3 shows reduced growth of the primary root, which is exacerbated by an excess specifically of Zn ions. In addition, ozs3 plants display various subtle developmental phenotypes, such as longer petioles and early flowering. Also, ozs3 seedlings are completely but reversibly growth-arrested when shifted to 4°C. The causal mutation was mapped to a gene encoding a putative substrate-recognition receptor of cullin4 E3 ligases. OZS3 orthologous genes can be found in almost all eukaryotic genomes. Most species from Schizosaccharomyces pombe to Homo sapiens, and including A. thaliana, possess one ortholog. No functional data are available for these genes in any of the multicellular model systems. CRISPR-Cas9-mediated knockout demonstrated that a complete loss of OZS3 function is embryo-lethal, indicating essentiality of OZS3 and its orthologs. The OZS3 protein interacts with the adaptor protein DAMAGED DNA BINDING1 (DDB1) in the nucleus. Thus, it is indeed a member of the large yet poorly characterized family of DDB1-cullin4 associated factors in plants. Mutant phenotypes of ozs3 plants are apparently caused by the weakened DDB1-OZS3 interaction as a result of the exchange of a conserved amino acid near the conserved WDxR motif.
Substances chimiques
Arabidopsis Proteins
0
CULLIN4 protein, Arabidopsis
0
Cullin Proteins
0
DDA1 (DDB1-ASSOCIATED1) protein, Arabidopsis
0
Zinc
J41CSQ7QDS
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
995-1009Informations de copyright
© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Alloway, B.J. (2008) Zinc in Soils and Crop Nutrition, 2nd ed. Brussels/Paris: IZA and IFA.
Andreini, C., Banci, L., Bertini, I. and Rosato, A. (2006) Zinc through the three domains of life. J. Proteome Res. 5, 3173-3178.
Angelé-Martínez, C., Goodman, C. and Brumaghim, J. (2014) Metal-mediated DNA damage and cell death: mechanisms, detection methods, and cellular consequences. Metallomics, 6, 1358-1381.
Angers, S., Li, T., Yi, X.H., Maccoss, M.J., Moon, R.T. and Zheng, N. (2006) Molecular architecture and assembly of the DDB1-CUL4a ubiquitin ligase machinery. Nature, 443, 590-593.
Arrivault, S., Senger, T. and Krämer, U. (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. 46, 861-879.
Assuncao, A.G.L., Herrero, E., Lin, Y.F. et al. (2010) Arabidopsis thaliana transcription factors bzip19 and bzip23 regulate the adaptation to zinc deficiency. Proc. Natl Acad. Sci. USA, 107, 10296-10301.
Beine-Golovchuk, O., Firmino, A.A.P., Dąbrowska, A., Schmidt, S., Erban, A., Walther, D., Zuther, E., Hincha, D.K. and Kopka, J. (2018) Plant temperature acclimation and growth rely on cytosolic ribosome biogenesis factor homologs. Plant Physiol. 176, 2251-2276.
Bernhardt, A., Mooney, S. and Hellmann, H. (2010) Arabidopsis DDB1a and DDB1b are critical for embryo development. Planta, 232, 555-566.
Biedermann, S. and Hellmann, H. (2011) WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci. 16, 38-46.
Bjerkan, K.N. and Grini, P.E. (2013) The Arabidopsis DDB1 interacting protein WDR55 is required for vegetative development. Plant Signal. Behav. 8, e25347.
Bjerkan, K.N., Jung-Roméo, S., Jürgens, G., Genschik, P. and Grini, P.E. (2012) Arabidopsis WD REPEAT DOMAIN55 interacts with DNA DAMAGED BINDING PROTEIN1 and is required for apical patterning in the embryo. Plant Cell, 24, 1013-1033.
Chen, P., Sjogren, C.A., Larsen, P.B. and Schnittger, A. (2019) A multi-level response to DNA damage induced by aluminium. Plant J. 98, 479-491.
Choi, C.M., Gray, W.M., Mooney, S. and Hellmann, H. (2014) Composition, roles, and regulation of cullin-based ubiquitin e3 ligases. Arabidopsis Book, 12, e0175.
Clemens, S. (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie, 88, 1707-1719.
Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
Deinlein, U., Weber, M., Schmidt, H. et al. (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell, 24, 708-723.
Deshaies, R.J. and Joazeiro, C.A.P. (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
Dumbliauskas, E., Lechner, E., Jaciubek, M. et al. (2011) The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J. 30, 731-743.
Guo, L., Nezames, C.D., Sheng, L., Deng, X. and Wei, N. (2013) Cullin-RING Ubiquitin ligase family in plant abiotic stress pathways. J. Integr. Plant Biol. 55, 21-30.
Haydon, M.J. and Cobbett, C.S. (2007) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol. 143, 1705-1719.
He, Y.Z.J., Mccall, C.M., Hu, J., Zeng, Y.X. and Xiong, Y. (2006) DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 20, 2949-2954.
Hong, J.H., Savina, M., Du, J., Devendran, A., Kannivadi Ramakanth, K., Tian, X., Sim, W.S., Mironova, V.V. and Xu, J. (2017) A sacrifice-for-survival mechanism protects root stem cell niche from chilling stress. Cell, 170, 102-113.
Hua, Z. and Vierstra, R.D. (2011) The Cullin-RING Ubiquitin-Protein Ligases. Annu. Rev. Plant Biol. 62, 299-334.
Huang, X., Li, J., Bao, F., Zhang, X. and Yang, S. (2010) A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol. 154, 796-809.
Hugly, S., McCourt, P., Browse, J., Patterson, G.W. and Somerville, C. (1990) A chilling sensitive mutant of Arabidopsis with altered steryl-ester metabolism. Plant Physiol. 93, 1053-1062.
Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F. and Cobbett, C.S. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell, 16, 1327-1339.
Jackson, S. and Xiong, Y. (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci. 34, 562-570.
Kambe, T., Tsuji, T., Hashimoto, A. and Itsumura, N. (2015) The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol. Rev. 95, 749-784.
Kawachi, M., Kobae, Y., Mori, H., Tomioka, R., Lee, Y. and Maeshima, M. (2009) A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant Cell Physiol. 50, 1156-1170.
Kilian, J., Whitehead, D., Horak, J. et al. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363.
Knight, J.K. and Wood, W.B. (1998) Gastrulation initiation in Caenorhabditis elegans requires the function of gad-1, which encodes a protein with WD repeats. Develop. Biol. 198, 253-265.
Kopittke, P.M., Blamey, F.P.C., Asher, C.J. and Menzies, N.W. (2010) Trace metal phytotoxicity in solution culture: a review. J. Exp. Bot. 61, 945-954.
Krężel, A. and Maret, W. (2016) The biological inorganic chemistry of zinc ions. Arch. Biochem. Biophys. 611, 3-19.
Kühnlenz, T., Hofmann, C., Uraguchi, S., Schmidt, H., Schempp, S., Weber, M., Lahner, B., Salt, D.E. and Clemens, S. (2016) Phytochelatin synthesis promotes leaf Zn accumulation of Arabidopsis thaliana plants grown in soil with adequate Zn supply and is essential for survival on Zn-contaminated soil. Plant Cell Physiol. 57, 2342-2352.
Lanquar, V., Grossmann, G., Vinkenborg, J.L., Merkx, M., Thomine, S. and Frommer, W.B. (2014) Dynamic imaging of cytosolic zinc in Arabidopsis roots combining FRET sensors and RootChip technology. New Phytol. 202, 198-208.
Lee, J. and Zhou, P.B. (2007) DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol. Cell, 26, 775-780.
Lee, J.H., Terzaghi, W., Gusmaroli, G., Charron, J.B.F., Yoon, H.J., Chen, H.D., He, Y.J., Xiong, Y. and Deng, X.W. (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell, 20, 152-167.
Lee, J.H., Yoon, H.J., Terzaghi, W., Martinez, C., Dai, M.Q., Li, J.G., Byun, M.O. and Deng, X.W. (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell, 22, 1716-1732.
Maret, W. (2017) Zinc in cellular regulation: the nature and significance of “zinc signals”. Int. J. Mol. Sci. 18, 2285.
Mi, H., Muruganujan, A., Huang, X., Ebert, D., Mills, C., Guo, X. and Thomas, P.D. (2019) Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat. Protoc. 14, 703-721.
Molinier, J., Lechner, E., Dumbliauskas, E. and Genschik, P. (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet. 4, e1000093.
Nagajyoti, P.C., Lee, K.D. and Sreekanth, T.V.M. (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199-216.
Nezames, C.D., Sjogren, C.A., Barajas, J.F. and Larsen, P.B. (2012) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell, 24, 608-621.
van Nocker, S. and Ludwig, P. (2003) The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genom. 4, 50.
Pazhouhandeh, M., Molinier, J., Berr, A. and Genschik, P. (2011) MSI4/FVE interacts with CUL4G-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc. Natl. Acad. Sci. USA, 108, 3430-3435.
Penkett, C.J., Morris, J.A., Wood, V. and Bähler, J. (2006) YOGY: a web-based, integrated database to retrieve protein orthologs and associated Gene Ontology terms. Nucleic Acids Res. 34, W330-W334.
Rapić-Otrin, V., Navazza, V., Nardo, T., Botta, E., McLenigan, M., Bisi, D.C., Levine, A.S. and Stefanini, M. (2003) True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum. Mol. Genet. 12, 1507-1522.
Remans, T., Opdenakker, K., Guisez, Y., Carleer, R., Schat, H., Vangronsveld, J. and Cuypers, A. (2012) Exposure of Arabidopsis thaliana to excess Zn reveals a Zn-specific oxidative stress signature. Environ. Exp. Bot. 84, 61-71.
Ren, H., Han, J., Yang, P. et al. (2019) Two E3 ligases antagonistically regulate the UV-B response in Arabidopsis. Proc. Natl. Acad. Sci. USA, 116, 4722-4731.
Schneider, J., Hugly, S. and Somerville, C. (1995) Chilling-sensitive mutants of Arabidopsis. Plant Mol. Biol. Rep. 13, 11-17.
Schroeder, D.F., Gahrtz, M., Maxwell, B.B., Cook, R.K., Kan, J.M., Alonso, J.M., Ecker, J.R. and Chory, J. (2002) De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 12, 1462-1472.
Schuler, M., Rellán-Álvarez, R., Fink-Straube, C., Abadía, J. and Bauer, P. (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell, 24, 2380-2400.
Seo, K.-I., Lee, J.-H., Nezames, C.D., Zhong, S., Song, E., Byun, M.-O. and Deng, X.W. (2014) ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell, 26, 695-711.
Serrano, I., Campos, L. and Rivas, S. (2018) Roles of E3 ubiquitin-ligases in nuclear protein homeostasis during plant stress responses. Front. Plant Sci. 9, 139.
Shu, K. and Yang, W. (2017) E3 ubiquitin ligases: Ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol. 58, 1461-1476.
Sinclair, S.A. and Krämer, U. (2012) The zinc homeostasis network of land plants. Biochim. Biophys. Acta, 1823, 1553-1567.
Sinclair, S.A., Larue, C., Bonk, L. et al. (2017) Etiolated seedling development requires repression of photomorphogenesis by a small cell-wall-derived dark signal. Curr. Biol. 27, 3403-3418.
Stemmer, M., Thumberger, T., Del Sol Keyer, M., Wittbrodt, J. and Mateo, J.L. (2015) CCTop: an intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS ONE, 10, e0124633.
Stirnimann, C.U., Petsalaki, E., Russell, R.B. and Müller, C.W. (2010) WD40 proteins propel cellular networks. Trends Biochem. Sci. 35, 565-574.
Suryawanshi, V., Talke, I.N., Weber, M., Eils, R., Brors, B., Clemens, S. and Krämer, U. (2016) Between-species differences in gene copy number are enriched among functions critical for adaptive evolution in Arabidopsis halleri. BMC Genom. 17, 3319.
Vogel, J.T., Zarka, D.G., Van Buskirk, H.A., Fowler, S.G. and Thomashow, M.F. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 41, 195-211.
Waadt, R. and Kudla, J. (2008) In planta visualization of protein interactions using bimolecular fluorescence complementation (BiFC). Cold Spring Harbor Protoc. 2008(5), pdb.prot4995. https://doi.org/10.1101/pdb.prot4995
Waadt, R., Schmidt, L.K., Lohse, M., Hashimoto, K., Bock, R. and Kudla, J. (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505-516.
Wang, Y., Hu, X.-J., Zou, X.-D., Wu, X.-H., Ye, Z.-Q. and Wu, Y.-D. (2015) WDSPdb: a database for WD40-repeat proteins. Nucleic Acids Res. 43, D339-D344.
Wang, Y., Zhang, Y., Wang, Z., Zhang, X. and Yang, S. (2013) A missense mutation in CHS1, a TIR-NB protein, induces chilling sensitivity in Arabidopsis. Plant J. 75, 553-565.
Weber, M., Deinlein, U., Fischer, S., Rogowski, M., Geimer, S., Tenhaken, R. and Clemens, S. (2013) A mutation in the Arabidopsis thaliana cell wall biosynthesis gene pectin methylesterase 3 as well as its aberrant expression cause hypersensitivity specifically to Zn. Plant J. 76, 151-164.
Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T. and Lin, C.S. (2009) Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method. Plant Methods, 5, 16. https://doi.org/10.1186/1746-4811-5-16.
Xing, H.-L., Dong, L., Wang, Z.-P., Zhang, H.-Y., Han, C.-Y., Liu, B., Wang, X.-C. and Chen, Q.-J. (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.
Yang, H., Shi, Y., Liu, J., Guo, L., Zhang, X. and Yang, S. (2010) A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J. 63, 283-296.
Youngren, K.K., Coveney, D. and Peng, X. et al. (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature, 435, 360-364.
Zbierzak, A.M., Porfirova, S., Griebel, T., Melzer, M., Parker, J.E. and Dörmann, P. (2013) A TIR-NBS protein encoded by Arabidopsis Chilling Sensitive 1 (CHS1) limits chloroplast damage and cell death at low temperature. Plant J. 75, 539-552.
Zeng, M., Ren, L., Mizuno, K. et al. (2016) CRL4(Wdr70) regulates H2B monoubiquitination and facilitates Exo1-dependent resection. Nature Commun. 7, 11364.
Zhang, Y., Feng, S.H., Chen, F.F., Chen, H.D., Wang, J., Mccall, C., Xiong, Y. and Deng, X.W. (2008) Arabidopsis DDB1-CUL4 associated factor1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell, 20, 1437-1455.
Zhao, F.-J., Ma, Y., Zhu, Y.-G., Tang, Z. and McGrath, S.P. (2015a) Soil contamination in China: current status and mitigation strategies. Environ. Sci. Technol. 49, 750-759.
Zhao, L., Oliver, E., Maratou, K. et al. (2015b) The zinc transporter ZIP12 regulates the pulmonary vascular response to chronic hypoxia. Nature, 524, 356-360.
Zlobin, I.E., Kartashov, A.V., Nosov, A.V., Fomenkov, A.A. and Kuznetsov, V.V. (2019) The labile zinc pool in plant cells. Funct. Plant Biol. 46(9), 796. https://doi.org/10.1071/FP19064