DOI QR코드

DOI QR Code

Characterization of a Novel DWD Protein that Participates in Heat Stress Response in Arabidopsis

  • Kim, Soon-Hee (Department of Biology Education, Pusan National University) ;
  • Lee, Joon-Hyun (Department of Biology Education, Pusan National University) ;
  • Seo, Kyoung-In (Department of Biology Education, Pusan National University) ;
  • Ryu, Boyeong (Department of Biology Education, Pusan National University) ;
  • Sung, Yongju (Department of Biology Education, Pusan National University) ;
  • Chung, Taijoon (Department of Biological Sciences, Pusan National University) ;
  • Deng, Xing Wang (Department of Molecular, Cellular and Developmental Biology, Yale University) ;
  • Lee, Jae-Hoon (Department of Biology Education, Pusan National University)
  • Received : 2014.08.06
  • Accepted : 2014.09.03
  • Published : 2014.11.30

Abstract

Cullin4-RING ubiquitin ligase (CRL4) is a family of multi-subunit E3 ligases. To investigate the possible involvement of CRL4 in heat stress response, we screened T-DNA insertion mutants of putative CRL4 substrate receptors that exhibited altered patterns in response to heat stress. One of the mutants exhibited heat stress tolerance and was named heat stress tolerant DWD1 (htd1). Introduction of HTD1 gene into htd1-1 led to recovery of heat sensitivity to the wild type level, confirming that the decrease of HTD1 transcripts resulted in heat tolerance. Therefore, HTD1 plays a negative role in thermotolerance in Arabidopsis. Additionally, HTD1 directly interacted with DDB1a in yeast two-hybrid assays and associated with DDB1b in vivo, supporting that it could be a part of a CRL4 complex. Various heat-inducible genes such as HSP14.7, HSP21, At2g03020 and WRKY28 were hyper-induced in htd1-1, indicating that HTD1 could function as a negative regulator for the expression of such genes and that these genes might contribute to thermotolerance of htd1-1, at least in part. HTD1 was associated with HSP90-1, a crucial regulator of thermotolerance, in vivo, even though the decrease of HTD1 did not affect the accumulation pattern of HSP90-1 in Arabidopsis. These findings indicate that a negative role of HTD1 in thermotolerance might be achieved through its association with HSP90-1, possibly by disturbing the action of HSP90-1, not by the degradation of HSP90-1. This study will serve as an important step toward understanding of the functional connection between CRL4-mediated processes and plant heat stress signaling.

Keywords

References

  1. Angers, S., Li, T., Yi, X., 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.
  2. Babitha, K.C., Ramu, S.V., Pruthvi, V., Mahesh, P., Nataraja, K.N., and Udayakumar, M. (2013). Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Res. 22, 327-341. https://doi.org/10.1007/s11248-012-9645-8
  3. Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, M., Ganguli, A., Kotak, S., Mishra, S.K., Nover, L., Port, M., Scharf, K.D., et al. (2004). Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29, 471-487. https://doi.org/10.1007/BF02712120
  4. Biedermann, S., and Hellmann, H. (2010). The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J. 62, 404-415. https://doi.org/10.1111/j.1365-313X.2010.04157.x
  5. Bohnert, H.J., Gong, Q., Li, P., and Ma, S. (2006). Unraveling abiotic stress tolerance mechanisms - Getting genomics going. Curr. Opin. Plant Biol. 9, 180-188. https://doi.org/10.1016/j.pbi.2006.01.003
  6. Boston, R.S., Viitanen, P.V., and Vierling, E. (1996). Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32, 191-222. https://doi.org/10.1007/BF00039383
  7. Botër, M., Amigues, B., Peart, J., Breuer, C., Kadota, Y., Casais, C., Moore, G., Kleanthous, C., Ochsenbein, F., Shirasu, K., and Guerois, R. (2007). Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell 19, 3791-3804. https://doi.org/10.1105/tpc.107.050427
  8. Chen, H., Shen, Y., Tang, X., Yu, L., Wang, J., Guo, L., Zhang, Y., Zhang, H., Feng, S., Strickland, E., et al. (2006). Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18, 1991-2004. https://doi.org/10.1105/tpc.106.043224
  9. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
  10. Dreher, K., and Callis, J. (2007). Ubiquitin, hormones and biotic stress in plants. Ann. Bot. 99, 787-822. https://doi.org/10.1093/aob/mcl255
  11. Gruber, H., Heijde, M., Heller, W., Albert, A., Seidlitz, H.K., and Ulm, R. (2010). Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc. Natl. Acad. Sci. USA 107, 20132-20137. https://doi.org/10.1073/pnas.0914532107
  12. He, Y.J., McCall, C.M., Hu, J., Zeng, Y., and Xiong, Y. (2006). DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 20, 2949-2954. https://doi.org/10.1101/gad.1483206
  13. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479. https://doi.org/10.1146/annurev.biochem.67.1.425
  14. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H., and Zhang, H. (2006). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 8, 1277-1283. https://doi.org/10.1038/ncb1490
  15. Hong, S.W., and Vierling, E. (2001). Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J. 27, 25-35. https://doi.org/10.1046/j.1365-313x.2001.01066.x
  16. Jin, J., Arias, E.E., Chen, J., Harper, J.W., and Walter, J.C. (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709-721. https://doi.org/10.1016/j.molcel.2006.08.010
  17. Kampinga, H.H., Brunsting, J.F., Stege, G.J., Burgman, P.W., and Konings, A.W. (1995). Thermal protein denaturation and protein aggregation in cells made thermotolerant by various chemicals: role of heat shock proteins. Exp. Cell Res. 219, 536-546. https://doi.org/10.1006/excr.1995.1262
  18. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., and Harter, K. (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. https://doi.org/10.1111/j.1365-313X.2007.03052.x
  19. Krishna, P., and Gloor, G. (2001). The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6, 238-246. https://doi.org/10.1379/1466-1268(2001)006<0238:THFOPI>2.0.CO;2
  20. Lee, J.H., and Schoffl, F. (1996). An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol. Gen. Genet. 252, 11-19.
  21. Lee, U., Wie, C., Escobar, M., Williams, B., Hong, S.W., and Vierling, E. (2005). Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell 17, 559-571. https://doi.org/10.1105/tpc.104.027540
  22. Lee, J.H., Terzaghi, W., Gusmaroli, G., Charron, J.B., Yoon, H.J., Chen, H., 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. https://doi.org/10.1105/tpc.107.055418
  23. Lee, J.H., Yoon, H.J., Terzaghi, W., Martinez, C., Dai, M., Li, J., 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. https://doi.org/10.1105/tpc.109.073783
  24. Li, S., Fu, Q., Chen, L., Huang, W., and Yu, D. (2011). Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233, 1237-1252. https://doi.org/10.1007/s00425-011-1375-2
  25. Meiri, D., and Breiman, A. (2009). Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J. 59, 387-399. https://doi.org/10.1111/j.1365-313X.2009.03878.x
  26. Meiri, D., Tazat, K., Cohen-Peer, R., Farchi-Pisanty, O., Aviezer-Hagai, K., Avni, A., and Breiman, A. (2010). Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol. Biol. 72, 191-203. https://doi.org/10.1007/s11103-009-9561-3
  27. Mittler, R., and Blumwald, E. (2010). Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 61, 443-462. https://doi.org/10.1146/annurev-arplant-042809-112116
  28. Mittler, R., Finka, A., and Goloubinoff, P. (2012). How do plants feel the heat? Trends Biochem. Sci. 37, 118-125. https://doi.org/10.1016/j.tibs.2011.11.007
  29. Murtagh, J., Lu, H., and Schwartz, E.L. (2006). Taxotere-induced inhibition of human endothelial cell migration is a result of heat shock protein 90 degradation. Cancer Res. 66, 8192-8199. https://doi.org/10.1158/0008-5472.CAN-06-0748
  30. Neuwald, A.F., Aravind, L., Spouge, J.L., and Koonin, E.V. (1999). AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43.
  31. Ono, K., Hibino, T., Kohinata, T., Suzuki, S., Tanaka, Y., Nakamura, T., Takabe, T., and Takabe, T. (2001). Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances the high temperature tolerance of tobacco during germination and early growth. Plant Sci. 160, 455-461. https://doi.org/10.1016/S0168-9452(00)00412-X
  32. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277. https://doi.org/10.1016/S0168-9525(00)02024-2
  33. Richter, K., and Buchner, J. (2001). Hsp90: chaperoning signal transduction. J. Cell. Physiol. 188, 281-290. https://doi.org/10.1002/jcp.1131
  34. Ruelland, E., and Zachowski, A. (2010). How plants sense temperature. Environ. Exp. Bot. 69, 225-232. https://doi.org/10.1016/j.envexpbot.2010.05.011
  35. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D., and von Koskull-Döring, P. (2006). The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 60, 759-772. https://doi.org/10.1007/s11103-005-5750-x
  36. 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. https://doi.org/10.1105/tpc.113.119974
  37. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590. https://doi.org/10.1146/annurev.arplant.55.031903.141801
  38. Sugino, M., Hibino, T., Tanaka, Y., Nii, N., Takabe, T., and Takabe, T. (1999). Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica acquires resistance to salt stress in transgenic tobacco plants. Plant Sci. 146, 81-88. https://doi.org/10.1016/S0168-9452(99)00086-2
  39. Sung, D.Y., Vierling, E., and Guy, C.L. (2001). Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126, 789-800. https://doi.org/10.1104/pp.126.2.789
  40. Todaka, D., Nakashima, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5, 6. https://doi.org/10.1186/1939-8433-5-6
  41. van Verk, M.C., Bol, J.F., and Linthorst, H.J. (2011). WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol. 11, 89. https://doi.org/10.1186/1471-2229-11-89
  42. Vierling, E. (1991). The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 579-620. https://doi.org/10.1146/annurev.pp.42.060191.003051
  43. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397. https://doi.org/10.1038/nrm2688
  44. von Koskull-Döring, P., Scharf, K.D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12, 452-457. https://doi.org/10.1016/j.tplants.2007.08.014
  45. Wang, W., Vinocur, B., Shoseyov, O., and Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252. https://doi.org/10.1016/j.tplants.2004.03.006
  46. Waters, E.R. (2013) The evolution, function, structure, and expression of the plant sHSPs. J. Exp. Bot. 64, 391-403. https://doi.org/10.1093/jxb/ers355
  47. Yabe, N., Takahashi, T., and Komeda, Y. (1994). Analysis of tissuespecific expression of Arabidopsis thaliana Hsp90-family gene HSP81. Plant Cell Physiol. 35, 1207-1219. https://doi.org/10.1093/oxfordjournals.pcp.a078715
  48. Zhang, Y., Feng, S., Chen, F., Chen, H., 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. https://doi.org/10.1105/tpc.108.058891
  49. Zhang, C., Guo, H., Zhang, J., Guo, G., Schumaker, K.S., and Guo, Y. (2010). Arabidopsis cockayne syndrome A-like proteins 1A and 1B form a complex with CULLIN4 and damage DNA binding protein 1A and regulate the response to UV irradiation. Plant Cell 22, 2353-2369. https://doi.org/10.1105/tpc.110.073973

Cited by

  1. Genome-wide analysis of DWD proteins in soybean (Glycine max): Significance of Gm08DWD and GmMYB176 interaction in isoflavonoid biosynthesis vol.12, pp.6, 2017, https://doi.org/10.1371/journal.pone.0178947
  2. Selection of reference genes suitable for normalization of qPCR data under abiotic stresses in bioenergy crop Arundo donax L. vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-11019-0
  3. The rolB plant oncogene affects multiple signaling protein modules related to hormone signaling and plant defense vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-20694-6
  4. Comparative transcriptome analysis reveals potential evolutionary differences in adaptation of temperature and body shape among four Percidae species vol.14, pp.5, 2014, https://doi.org/10.1371/journal.pone.0215933
  5. AtWAKL10, a Cell Wall Associated Receptor-Like Kinase, Negatively Regulates Leaf Senescence in Arabidopsis thaliana vol.22, pp.9, 2014, https://doi.org/10.3390/ijms22094885