The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Arabidopsis thaliana Remorins Interact with SnRK1 and Play a Role in Susceptibility to Beet Curly Top Virus and Beet Severe Curly Top Virus

  • Son, Seungmin (School of Biological Sciences, College of Natural Sciences, Seoul National University) ;
  • Oh, Chang Jae (School of Biological Sciences, College of Natural Sciences, Seoul National University) ;
  • An, Chung Sun (School of Biological Sciences, College of Natural Sciences, Seoul National University)
  • Received : 2014.06.17
  • Accepted : 2014.07.22
  • Published : 2014.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Remorins, a family of plant-specific proteins containing a variable N-terminal region and conserved C-terminal domain, play a role in various biotic and abiotic stresses, including host-microbe interactions. However, their functions remain to be completely elucidated, especially for the Arabidopsis thaliana remorin group 4 (AtREM4). To elucidate the role of remorins in Arabidopsis, we first showed that AtREM4s have typical molecular characteristics of the remorins, such as induction by various types of biotic and abiotic stresses, localization in plasma membrane and homo- and hetero-oligomeric interaction. Next, we showed that their loss-of-function mutants displayed reduced susceptibility to geminiviruses, Beet Curly Top Virus and Beet Severe Curly Top Virus, while overexpressors enhanced susceptibility. Moreover, we found that they interacted with SnRK1, which phosphorylated AtREM4.1, and were degraded by the 26S proteasome pathway. These results suggest that AtREM4s may be involved in the SnRK1-mediated signaling pathway and play a role as positive regulators of the cell cycle during geminivirus infection.

Keywords

References

  1. Alcaide-Loridan, C. and Jupin, I. 2012. Ubiquitin and plant viruses, let's play together! Plant Physiol. 160:72-82. https://doi.org/10.1104/pp.112.201905
  2. Aronson, M. N., Meyer, A. D., Gyorgyey, J., Katul, L., Vetten, H. J., Gronenborn, B. and Timchenko, T. 2000. Clink, a nanovirus- encoded protein, binds both pRB and SKP1. J. Virol. 74:2967-2972. https://doi.org/10.1128/JVI.74.7.2967-2972.2000
  3. Ascencio-Ibanez, J. T., Sozzani, R., Lee, T. J., Chu, T. M., Wolfinger, R. D., Cella, R. and Hanley-Bowdoin, L. 2008. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148:436-454. https://doi.org/10.1104/pp.108.121038
  4. Baena-Gonzalez, E., Rolland, F., Thevelein, J. M. and Sheen, J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938-942. https://doi.org/10.1038/nature06069
  5. Bariola, P. A., Retelska, D., Stasiak, A., Kammerer, R. A., Fleming, A., Hijri, M., Frank, S. and Farmer, E. E. 2004. Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants. Plant Mol. Biol. 55:579-594. https://doi.org/10.1007/s11103-004-1520-4
  6. Benschop, J. J., Mohammed, S., O'Flaherty, M., Heck, A. J., Slijper, M. and Menke, F. L. 2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell Proteomics 6:1198-1214. https://doi.org/10.1074/mcp.M600429-MCP200
  7. Bozkurt, T. O., Richardson, A., Dagdas, Y. F., Mongrand, S., Kamoun, S. and Raffaele, S. 2014. The plant membraneassociated REMORIN1.3 accumulates in discrete perihaustorial domains and enhances susceptibility to Phytophthora infestans. Plant Physiol. 165:1005-1018. https://doi.org/10.1104/pp.114.235804
  8. Coaker, G. L., Willard, B., Kinter, M., Stockinger, E. J. and Francis, D. M. 2004. Proteomic analysis of resistance mediated by Rcm 2.0 and Rcm 5.1, two loci controlling resistance to bacterial canker of tomato. Mol. Plant-Microbe Interact. 17:1019-1028. https://doi.org/10.1094/MPMI.2004.17.9.1019
  9. Desvoyes, B., Ramirez-Parra, E., Xie, Q., Chua, N. H. and Gutierrez, C. 2006. Cell type-specific role of the retinoblastoma/ E2F pathway during Arabidopsis leaf development. Plant Physiol. 140:67-80.
  10. Dyson, H. J. and Wright, P. E. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6:197-208. https://doi.org/10.1038/nrm1589
  11. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C. S. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45:616-629. https://doi.org/10.1111/j.1365-313X.2005.02617.x
  12. Farmer, E. E., Pearce, G. and Ryan, C. A. 1989. In vitro phosphorylation of plant plasma membrane proteins in response to the proteinase inhibitor inducing factor. Proc. Natl. Acad. Sci. USA 86:1539-1542. https://doi.org/10.1073/pnas.86.5.1539
  13. Gutzat, R., Borghi, L. and Gruissem, W. 2012. Emerging roles of RETINOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci. 17:139-148. https://doi.org/10.1016/j.tplants.2011.12.001
  14. Hao, L., Wang, H., Sunter, G. and Bisaro, D.M. 2003. Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15:1034-1048. https://doi.org/10.1105/tpc.009530
  15. Jarsch, I. K. and Ott, T. 2011. Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol. Plant-Microbe Interact. 24:7-12. https://doi.org/10.1094/MPMI-07-10-0166
  16. Jefferson, R. A., Kavanagh, T. A. and Bevan, M. W. 1987. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:3901-3907.
  17. Kong, L. J. and Hanley-Bowdoin, L. 2002. A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14:1817-1832. https://doi.org/10.1105/tpc.003681
  18. Kong, L. J., Orozco, B. M., Roe, J. L., Nagar, S., Ou, S., Feiler, H. S., Durfee, T., Miller, A. B., Gruissem, W., Robertson, D. and Hanley-Bowdoin, L. 2000. A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J. 19:3485-3495. https://doi.org/10.1093/emboj/19.13.3485
  19. Lai, J., Chen, H., Teng, K., Zhao, Q., Zhang, Z., Li, Y., Liang, L., Xia, R., Wu, Y., Guo, H. and Xie, Q. 2009. RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle. Plant J. 57:905-917. https://doi.org/10.1111/j.1365-313X.2008.03737.x
  20. Laloi, M., Perret, A. M., Chatre, L., Melser, S., Cantrel, C., Vaultier, M. N., Zachowski, A., Bathany, K., Schmitter, J. M., Vallet, M., Lessire, R., Hartmann, M. A. and Moreau, P. 2007. Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol. 143:461-472.
  21. Latham, J. R., Saunders, K., Pinner, M. S. and Stanley, J. 1997. Induction of plant cell division by beet curly top virus gene C4. Plant J. 11:1273-1283. https://doi.org/10.1046/j.1365-313X.1997.11061273.x
  22. Lee, S., Stenger, D. C., Bisaro, D. M. and Davis, K. R. 1994. Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J. 6:525-535. https://doi.org/10.1046/j.1365-313X.1994.6040525.x
  23. Lefebvre, B., Furt, F., Hartmann, M. A., Michaelson, L. V., Carde, J. P., Sargueil-Boiron, F., Rossignol, M., Napier, J. A., Cullimore, J., Bessoule, J. J. and Mongrand, S. 2007. Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raftassociated redox system. Plant Physiol. 144:402-418. https://doi.org/10.1104/pp.106.094102
  24. Lefebvre, B., Timmers, T., Mbengue, M., Moreau, S., Herve, C., Toth, K., Bittencourt-Silvestre, J., Klaus, D., Deslandes, L., Godiard, L., Murray, J. D., Udvardi, M. K., Raffaele, S., Mongrand, S., Cullimore, J., Gamas, P., Niebel, A. and Ott, T. 2010. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl. Acad. Sci. USA 107:2343-2348. https://doi.org/10.1073/pnas.0913320107
  25. Li, B., Zhang, C., Cao, B., Qin, G., Wang, W. and Tian, S. 2012. Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. Amino Acids 43:2469-2480. https://doi.org/10.1007/s00726-012-1327-6
  26. Liu, J., Elmore, J. M., Fuglsang, A. T., Palmgren, M. G., Staskawicz, B. J. and Coaker, G. 2009. RIN4 functions with plasma membrane $H^{+}$-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7:e1000139. https://doi.org/10.1371/journal.pbio.1000139
  27. Lozano-Duran, R., Rosas-Diaz, T., Gusmaroli, G., Luna, A. P., Taconnat, L., Deng, X. W. and Bejarano, E. R. 2011. Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23:1014-1032. https://doi.org/10.1105/tpc.110.080267
  28. Marin, M., Thallmair, V. and Ott, T. 2012. The intrinsically disordered N-terminal region of AtREM1.3 remorin protein mediates protein-protein interactions. J. Biol. Chem. 287:39982-39991. https://doi.org/10.1074/jbc.M112.414292
  29. Mongrand, S., Morel, J., Laroche, J., Claverol, S., Carde, J. P., Hartmann, M. A., Bonneu, M., Simon-Plas, F., Lessire, R. and Bessoule, J. J. 2004. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J. Biol. Chem. 279:36277-36286. https://doi.org/10.1074/jbc.M403440200
  30. Nohzadeh Malakshah, S., Habibi Rezaei, M., Heidari, M. and Salekdeh, G. H. 2007. Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci. Biotechnol. Biochem. 71:2144-2154. https://doi.org/10.1271/bbb.70027
  31. Park, J., Lee, H. J., Cheon, C. I., Kim, S. H., Hur, Y. S., Auh, C. K., Im, K. H., Yun, D. J., Lee, S. and Davis, K. R. 2011. The Arabidopsis thaliana homeobox gene ATHB12 is involved in symptom development caused by geminivirus infection. PLoS ONE 6:e20054. https://doi.org/10.1371/journal.pone.0020054
  32. Perraki, A., Cacas, J. L., Crowet, J. M., Lins, L., Castroviejo, M., German-Retana, S., Mongrand, S. and Raffaele, S. 2012. Plasma membrane localization of Solanum tuberosum remorin from group 1, homolog 3 is mediated by conformational changes in a novel C-terminal anchor and required for the restriction of Potato Virus X movement. Plant Physiol. 160:624-637. https://doi.org/10.1104/pp.112.200519
  33. Raffaele, S., Bayer, E., Lafarge, D., Cluzet, S., German Retana, S., Boubekeur, T., Leborgne-Castel, N., Carde, J. P., Lherminier, J., Noirot, E., Satiat-Jeunemaitre, B., Laroche-Traineau, J., Moreau, P., Ott, T., Maule, A. J., Reymond, P., Simon-Plas, F., Farmer, E. E., Bessoule, J. J. and Mongrand, S. 2009a. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541-1555. https://doi.org/10.1105/tpc.108.064279
  34. Raffaele, S., Bayer, E. and Mongrand, S. 2009b. Upregulation of the plant protein remorin correlates with dehiscence and cell maturation: a link with the maturation of plasmodesmata? Plant Signal. Behav. 4:915-919. https://doi.org/10.4161/psb.4.10.9661
  35. Raffaele, S., Mongrand, S., Gamas, P., Niebel, A. and Ott. T. 2007. Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol. 145:593-600. https://doi.org/10.1104/pp.107.108639
  36. Rechsteiner, M. and Rogers, S. W. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267-271. https://doi.org/10.1016/0968-0004(96)10031-1
  37. Reymond, P., Kunz, B., Paul-Pletzer, K., Grimm, R., Eckerskorn, C. and Farmer, E. E. 1996. Cloning of a cDNA encoding a plasma membrane-associated, uronide binding phosphoprotein with physical properties similar to viral movement proteins. Plant Cell 8:2265-2276. https://doi.org/10.1105/tpc.8.12.2265
  38. Rogers, S., Wells, R. and Rechsteiner, M. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364-368. https://doi.org/10.1126/science.2876518
  39. Shen, Q., Liu, Z., Song, F., Xie, Q., Hanley-Bowdoin, L. and Zhou, X. 2011. Tomato SlSnRK1 protein interacts with and phosphorylates betaC1, a pathogenesis protein encoded by a geminivirus beta-satellite. Plant Physiol. 157:1394-1406. https://doi.org/10.1104/pp.111.184648
  40. Shen, W. and Hanley-Bowdoin, L. 2006. Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1- and mammalian AMPK-activating kinases. Plant Physiol. 142:1642-1655. https://doi.org/10.1104/pp.106.088476
  41. Shen, W., Reyes, M. I. and Hanley-Bowdoin, L. 2009. Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol. 150:996-1005. https://doi.org/10.1104/pp.108.132787
  42. Toth, K., Stratil, T. F., Madsen, E. B., Ye, J., Popp, C., Antolin- Llovera, M., Grossmann, C., Jensen, O. N., Schussler, A., Parniske, M. and Ott, T. 2012. Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicus. PLoS One 7:e30817. https://doi.org/10.1371/journal.pone.0030817
  43. Vanderschuren, H., Stupak, M., Futterer, J., Gruissem, W. and Zhang, P. 2007. Engineering resistance to geminiviruses- -review and perspectives. Plant Biotechnol. J. 5:207-220. https://doi.org/10.1111/j.1467-7652.2006.00217.x
  44. Voinnet, O., Rivas, S., Mestre, P. and Baulcombe, D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33:949-956. https://doi.org/10.1046/j.1365-313X.2003.01676.x
  45. 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. https://doi.org/10.1111/j.1365-313X.2008.03612.x
  46. Wang, F., Zhu, D., Huang, X., Li, S., Gong, Y., Yao, Q., Fu, X., Fan, L. M. and Deng, X. W. 2009. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21:2378-2390. https://doi.org/10.1105/tpc.108.065433
  47. Wang, H., Buckley, K. J., Yang, X., Buchmann, R. C. and Bisaro, D. M. 2005. Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79:7410-7418. https://doi.org/10.1128/JVI.79.12.7410-7418.2005
  48. Widjaja, I., Naumann, K., Roth, U., Wolf, N., Mackey, D., Dangl, J. L., Scheel, D. and Lee, J. 2009. Combining subproteome enrichment and Rubisco depletion enables identification of low abundance proteins differentially regulated during plant defense. Proteomics 9:138-147. https://doi.org/10.1002/pmic.200800293
  49. Yang, J. Y., Iwasaki, M., Machida, C., Machida, Y., Zhou, X. and Chua, N. H. 2008. betaC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev. 22:2564-2577. https://doi.org/10.1101/gad.1682208
  50. Zhang, X. R., Henriques, R., Lin, S. S., Niu, Q. W. and Chua, N. H. 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1:641-646. https://doi.org/10.1038/nprot.2006.97
  51. Zhang, Z., Chen, H., Huang, X., Xia, R., Zhao, Q., Lai, J., Teng, K., Li, Y., Liang, L., Du, Q., Zhou, X., Guo, H. and Xie, Q. 2011. BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273-288. https://doi.org/10.1105/tpc.110.081695

Cited by

  1. Heat-Shock Protein 90 (Hsp90) as Anticancer Target for Drug Discovery: An Ample Computational Perspective vol.86, pp.5, 2015, https://doi.org/10.1111/cbdd.12582
  2. Identification of lipopolysaccharide-interacting plasma membrane-type proteins in Arabidopsis thaliana vol.111, 2017, https://doi.org/10.1016/j.plaphy.2016.11.025
  3. The cladistic analysis of serine/threonine protein kinase KIN10 and peculiarities of its expression in different organs of Arabidopsis thaliana pp.1, 2016, https://doi.org/10.15407/dopovidi2016.01.081
  4. OsREM4.1 Interacts with OsSERK1 to Coordinate the Interlinking between Abscisic Acid and Brassinosteroid Signaling in Rice vol.38, pp.2, 2016, https://doi.org/10.1016/j.devcel.2016.06.011
  5. AKIN10, a representative Arabidopsis SNF1-related protein kinase 1 (SnRK1), phosphorylates and downregulates plant HMG-CoA reductase vol.591, pp.8, 2017, https://doi.org/10.1002/1873-3468.12618
  6. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains vol.6, 2017, https://doi.org/10.7554/eLife.26404
  7. In situ localization and changes in the expression level of transcripts related to intercellular transport and phloem loading in leaves of maize (Zea mays L.) treated with low temperature vol.38, pp.5, 2016, https://doi.org/10.1007/s11738-016-2151-5
  8. Influence of protein kinase KIN10 gene expression on root phenotype of Arabidopsis thaliana root system under condition of energy stress vol.50, pp.4, 2016, https://doi.org/10.3103/S009545271604006X
  9. The SnRK1 Energy Sensor in Plant Biotic Interactions vol.21, pp.8, 2016, https://doi.org/10.1016/j.tplants.2016.04.008
  10. Potato remorin gene StREMa4 cloning and its spatiotemporal expression pattern under Ralstonia solanacearum and plant hormones treatment vol.44, pp.4, 2016, https://doi.org/10.1007/s12600-016-0536-z
  11. Grain setting defect1 (GSD1) function in rice depends on S-acylation and interacts with actin 1 (OsACT1) at its C-terminal vol.6, 2015, https://doi.org/10.3389/fpls.2015.00804
  12. REM1.3's phospho-status defines its plasma membrane nanodomain organization and activity in restricting PVX cell-to-cell movement vol.14, pp.11, 2018, https://doi.org/10.1371/journal.ppat.1007378
  13. Altered Subcellular Localization of a Tobacco Membrane Raft-Associated Remorin Protein by Tobamovirus Infection and Transient Expression of Viral Replication and Movement Proteins vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.00619