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Revisiting Apoplastic Auxin Signaling Mediated by AUXIN BINDING PROTEIN 1

  • Feng, Mingxiao (Division of Applied Life Science (BK21plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Kim, Jae-Yean (Division of Applied Life Science (BK21plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University)
  • 투고 : 2015.07.20
  • 심사 : 2015.10.05
  • 발행 : 2015.10.31

초록

It has been suggested that AUXIN BINDING PROTEIN 1 (ABP1) functions as an apoplastic auxin receptor, and is known to be involved in the post-transcriptional process, and largely independent of the already well-known SKP-cullin-F-box-transport inhibitor response (TIR1) /auxin signaling F-box (AFB) ($SCF^{TIR1/AFB}$) pathway. In the past 10 years, several key components downstream of ABP1 have been reported. After perceiving the auxin signal, ABP1 interacts, directly or indirectly, with plasma membrane (PM)-localized transmembrane proteins, transmembrane kinase (TMK) or SPIKE1 (SPK1), or other unidentified proteins, which transfer the signal into the cell to the Rho of plants (ROP). ROPs interact with their effectors, such as the ROP interactive CRIB motif-containing protein (RIC), to regulate the endocytosis/exocytosis of the auxin efflux carrier PIN-FORMED (PIN) proteins to mediate polar auxin transport across the PM. Additionally, ABP1 is a negative regulator of the traditional $SCF^{TIR1/AFB}$ auxin signaling pathway. However, Gao et al. (2015) very recently reported that ABP1 is not a key component in auxin signaling, and the famous abp1-1 and abp1-5 mutant Arabidopsis lines are being called into question because of possible additional mutantion sites, making it necessary to reevaluate ABP1. In this review, we will provide a brief overview of the history of ABP1 research.

키워드

참고문헌

  1. Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Maurel., C, Palme, K., Schell, J., and Guern, J. (1991). Perception of the auxin signal at the plasma membrane of tobacco mesophyll protoplasts. Plant J. 1, 83-93. https://doi.org/10.1111/j.1365-313X.1991.00083.x
  2. Bauly, J.M., Sealy, I.M., Macdonald, H., Brearley, J., Droge, S., Hillmer, S., Robinson, D.G., Venis, M.A., Blatt, M.R., Lazarus, C.M., et al. (2000). Overexpression of auxin-binding protein enhances the sensitivity of guard cells to auxin. Plant Physiol. 12, 1299-1238.
  3. Bertosa, B., Kojic-Prodic, B., Wade, R.C., and Tomic, S. (2008). Mechanism of auxin interaction with auxin binding protein (ABP1): a molecular dynamics simulation study. Biophys. J. 94, 27-37. https://doi.org/10.1529/biophysj.107.109025
  4. Braun, N., Wyrzykowska, J., Muller, P., David, K., Couch, D., Perrot- Rechenmann, C., and Fleming, A.J. (2008). Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordiates cell division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell 20, 2746-2762. https://doi.org/10.1105/tpc.108.059048
  5. Brown, J.C., and Jones, A.M. (1994). Mapping the auxin-binding site of auxin-binding protein 1. J. Biol. Chem. 269, 21136-21140.
  6. Chen, J.G., Ullah, H., Young, J.C., Sussman, M.R., and Jones, A.M. (2001). ABP1 is required for organized cell elongation and division in Arabidopsis. Genes Dev. 15, 902-911. https://doi.org/10.1101/gad.866201
  7. Chen, X., Naramoto, S., Robert, S., Tejos, R., Lofke, C., Lin, D., Yang, Z., and Friml, J. (2012). ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr. Biol. 22, 1326-1332. https://doi.org/10.1016/j.cub.2012.05.020
  8. Chen, X., Grandont, L., Li, H., Hauschild, R., Paque, S., Abuzeineh, A., Rakusová, H., Benkova, E., Perrot-Rechenmann, C., and Friml, J. (2014). Inhibition of cell expansion by rapid ABP1- mediated auxin effect on microtubules. Nature 516, 90-93.
  9. Cross, J.W., and Briggs, W.R. (1978). Auxin receptors of maize coleoptile membranes do not have ATPase activity. Plant Physiol. 61, 581-584. https://doi.org/10.1104/pp.61.4.581
  10. Dai, N., Wang, W., Patterson, S.E., and Bleecker, A.B. (2013). The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLoS One 8, e60990. https://doi.org/10.1371/journal.pone.0060990
  11. David, K.M., Couch, D., Braun, N., Brown, S., Grosclaude, J., and Perrot-Rechenmann, C. (2007). The auxin-binding protein 1 is essential for the control of cell cycle. Plant J. 50, 197-206. https://doi.org/10.1111/j.1365-313X.2007.03038.x
  12. Dunwell, J.M., Gibbings, J.G., Mahmood, T., and Naqvi, S.M.S. (2008). Germin and germin-like proteins: evolution, structure, and function. Crit. Rev. Plant Sci. 27, 342-375. https://doi.org/10.1080/07352680802333938
  13. de Jager, S.M., Scofield, S., Huntley, R.P., Robinson, A.S., den Boer, B.G., and Murray, J.A. (2009). Dissecting regulatory pathways of G1/S control in Arabidopsis: common and distinct targets of CYCD3;1, E2Fa and E2Fc. Plant Mol. Biol. 71, 345-365. https://doi.org/10.1007/s11103-009-9527-5
  14. Effendi, Y., Rietz, S., Fischer, U., and Scherer, G.F. (2011). The heterozygous abp1/ABP1 insertional mutant has defects in functions requiring polar auxin transport and in regulation of early auxin-regulated genes. Plant J. 65, 282-294. https://doi.org/10.1111/j.1365-313X.2010.04420.x
  15. Effendi, Y., Jones, A.M., and Scherer, G.F. (2013). AUXIN-BINDINGPROTEIN1 (ABP1) in phytochrome-B-controlled response. J. Exp. Bot. 64, 5065-5074. https://doi.org/10.1093/jxb/ert294
  16. Effendi, Y., Ferro, N., Labusch, C., Geisler, M., and Scherer, G.F. (2015). Complementation of the embryo-lethal T-DNA insertion mutant of AUXIN-BINDING PROTEIN 1 (ABP1) with abp1 point mutated versions reveals crosstalk of ABP1 and phytochromes. J. Exp. Bot. 66, 403-418. https://doi.org/10.1093/jxb/eru433
  17. Enders, T.A., Oh, S., Yang, Z., Montgomery, B.L., and Strader, L.C. (2015). Genome sequencing of Arabidopsis abp1-5 reveals second-site mutations that may affect phenotypes. Plant Cell pii: tpc.15.00214.
  18. Fu, Y., Xu, T., Zhu, L., Wen, M., and Yang, Z. (2009). A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr. Biol. 19, 1827-1832. https://doi.org/10.1016/j.cub.2009.08.052
  19. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R., and Scheres, B. (2007). PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053-1057. https://doi.org/10.1038/nature06206
  20. Gao, Y., Zhang, Y., Zhang, D., Dai, X., Estelle, M., and Zhao, Y. (2015). Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc. Natl. Acad. Sci. USA 112, 2275-2280. https://doi.org/10.1073/pnas.1500365112
  21. Grones, P., and Friml., J. (2015). ABP1: finally docking. Mol. Plant. 8, 356-358. https://doi.org/10.1016/j.molp.2014.12.013
  22. Grones, P., Chen, X., Simon, S., Kaufmann, W.A., De Rycke, R., Nodzynski, T., Zazimalova, E., and Friml, J. (2015). Auxinbinding pocket of ABP1 is crucial for its gain-of-function cellular and developmental roles. J. Exp. Bot. pii: erv177.
  23. Habets M.E.J., and Offringa, R. (2015). Auxin Binding Protein 1: a red herring after all? Mol. Plant 8, 1131-1134. https://doi.org/10.1016/j.molp.2015.04.010
  24. Hazak, O., Bloch, D., Poraty, L., Sternberg, H., Zhang, J., Friml, J., and Yalovsky, S. (2010). A Rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLOS Biol. 8, e1000282. https://doi.org/10.1371/journal.pbio.1000282
  25. Hertel, R., Thomson, K.S., and Russo, V.E.A. (1972). In-vitro auxin binding to particulate cell frations from corn coleoptiles. Planta 107, 325-340. https://doi.org/10.1007/BF00386394
  26. Huang, J.B., Liu, H., Chen, M., Li, X., Wang, M., Yang, Y., Wang, C., Huang, J., Liu, G., Liu, Y., et al. (2014). ROP3 GTPase contributes to polar auxin transport and auxin responses and is important for embryogenesis and seedling growth in Arabidopsis. Plant Cell 26, 3501-3518. https://doi.org/10.1105/tpc.114.127902
  27. Inohara, N., Shimomura, S., Fukui, T., and Futai, M. (1989). Auxinbinding protein located in the endoplasmic reticulum of maize shoots: Molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 86, 3564-3568. https://doi.org/10.1073/pnas.86.10.3564
  28. Jones, AM. (1994). Auxin binding proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 393-420. https://doi.org/10.1146/annurev.pp.45.060194.002141
  29. Jones, A.M., and Venis, M.A. (1989). Photoaffinity labeling of indole- 3-acetic acid-binding proteins in maize. Proc. Natl. Acad. Sci. USA 86, 6153-6156. https://doi.org/10.1073/pnas.86.16.6153
  30. Jones, A.M., and Herman, E.M. (1993). KDEL-containing auxinbinding protein is secreted to the plasma membrane and cell wall. Plant Physiol. 101, 595-606. https://doi.org/10.1104/pp.101.2.595
  31. Jones, A.M., Lamerson, P., and Venis, M.A. (1989). Comparison of Site I auxin binding and a 22-kilodalton auxin-binding protein in maize. Planta 179, 409-413. https://doi.org/10.1007/BF00391088
  32. Jones, A.M., Im, K.H., Savka, M.A., Wu, M.J., DeWitt, N.G., Shillito, R., and Binns, A.N. (1998). Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282, 1114-1117. https://doi.org/10.1126/science.282.5391.1114
  33. Lavy, M., Bloch, D., Hazak, O., Gutman, I., Poraty, L., Sorek, N., Sternberg, H., and Yalovsky, S. (2007). A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 17, 947-952. https://doi.org/10.1016/j.cub.2007.04.038
  34. Lin, D., Nagawa, S., Chen, J., Cao, L., Chen, X., Xu, T., Li, H., Dhonukshe, P., Yamamuro, C., Friml, J., et al. (2012). A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distriction of PIN2 in Arabidopsis roots. Curr. Biol. 22, 1319-1325. https://doi.org/10.1016/j.cub.2012.05.019
  35. Lin, D., Cao, L., Zhou, Z., Zhu, L., Ehrhardt, D., Yang, Z., and Fu, Y. (2013). Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr. Biol. 23, 290-297. https://doi.org/10.1016/j.cub.2013.01.022
  36. Liu, C.M. (2015). AUXIN BINDING PROTEIN 1 (ABP1): a matter of fact. J.Integr. Plant Biol. 57, 234-235. https://doi.org/10.1111/jipb.12339
  37. Lobler, M. and Klambt, D. (1985). Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. purification by immunological methods and characterization. J. Biol. Chem. 260, 9848-9853.
  38. Miyawaki, K. N., and Yang, Z. (2014). Extracellular signals and receptor-like kinases regulating ROP GTPases in plants. Front Plant Sci. 5, 449.
  39. Mockaitis, K., and Estelle, M. (2008). Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55-80. https://doi.org/10.1146/annurev.cellbio.23.090506.123214
  40. Mravec, J., Skupa, P., Bailly, A., Hoyerova, K., Krecek, P., Bielach, A., Petrasek, J., Zhang, J., Gaykova, V., Stierhof, YD., et al. (2009). Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136-1140. https://doi.org/10.1038/nature08066
  41. Nagawa, S., and Yang, Z. (2014). The regulation of cell shape formation by ROP-dependent auxin signaling. Plant Cell Wall Patterning and Cell Shape. H. Fukuda. ed. (Hoboken, New Jersey, USA: John wiley & Sons, Inc.), pp. 164-189.
  42. Nagawa, S., Xu, T., Lin, D., Dhonukshe, P., Zhang, X., Frimi, J., Scheres, B., Fu, Y., and Yang, Z. (2012). ROP GTPasedependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 10, e1001299. https://doi.org/10.1371/journal.pbio.1001299
  43. Napier, R.M., David, K.M., and Perrot-Rechenmann, C. (2002). A short history of auxin-binding proteins. Plant Mol. Biol. 49, 339-348. https://doi.org/10.1023/A:1015259130955
  44. Palme, K., Hesse, T., Campos, N., Garbers, C., Yanofsky, M.F., and Schell, J. (1992). Molecular analysis of an auxin binding protein gene located on chromosome 4 of Arabidopsis. Plant Cell 4, 193-201. https://doi.org/10.1105/tpc.4.2.193
  45. Paque, S., Mouille, G., Grandont, L., Alabadí, D., Gaertner, C., Goyallon, A., Muller, P., Primard-Brisset, C., Sormani, R., Blazquez, M.A., et al. (2014). AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling and cell expression in Arabidopsis. Plant Cell 26, 280-295. https://doi.org/10.1105/tpc.113.120048
  46. Paulick, M.G., and Bertozzi, C.R. (2008). The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochem. 47, 6991-7000. https://doi.org/10.1021/bi8006324
  47. Pelham, H.R. (1989). Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 1-23. https://doi.org/10.1146/annurev.cb.05.110189.000245
  48. Qiu, J.L., Jilk, R., Marks, M.D., and Szymanski, D.B. (2002). The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14, 101-118. https://doi.org/10.1105/tpc.010346
  49. Ren, H., and Lin, D. (2015). ROP GTPase regulation of auxin transport in Arabidopsis. Mol. Plant 8, 193-195. https://doi.org/10.1016/j.molp.2014.11.011
  50. Rescher, U., Walther, A., Schiebl, C., and Klambt, D. (1996). In vitro binding affinities of 4-chloro-, 2-methyl-, 4-methyl-, and 4- ethylindoleacetic acid to auxin-binding protein 1 (ABP1) correlate with their growth-stimulating activities. J. Plant Growth Regul. 15, 1-3. https://doi.org/10.1007/BF00213127
  51. Robert, S., Kleine-Vehn, J., Barbez, E., Sauer, M., Paciorek, T., Baster, P., Vanneste, S., Zhang, J., Simon, S., Covanova, M., et al. (2010). ABP1 mediates auxin inhibition of clathrindependent endocytosis in Arabidopsis. Cell 143, 111-121. https://doi.org/10.1016/j.cell.2010.09.027
  52. Shimomura, S. (2006). Identification of a glycosylphosphatidylinostiol- anchored plasma membrane protein interacting with the Cterminus of auxin-binding protein 1: a photoaffinity crosslinking study. Plant Mol. Biol. 60, 663-677. https://doi.org/10.1007/s11103-005-5471-1
  53. Shimomura, S., Sotobayashi, T., Futai, M., and Fukui, T. (1986). Purification and properties of an auxin-binding protein from maize shoot membranes. J. Biochem. 99, 1513-1524. https://doi.org/10.1093/oxfordjournals.jbchem.a135621
  54. Tejos, R., and Friml, J. (2012). Cell polarity and endocytosis. In Endocytosis in Plants. J Samaj. ed. (Berlin, Germany: Springer-Verlag), pp. 63-80.
  55. Tian, H., Klämbt, D., and Jones, A.M. (1995). Auxin-binding protein 1 does not bind auxin within the endoplasmic reticulum despite this being the predominant subcellular localization for this hormone receptor. J. Biol. Chem. 270, 26962-26969. https://doi.org/10.1074/jbc.270.45.26962
  56. Tillmann, U., Viola, G., Kayser, B., Siemeister, G., Hesse, T., Palme, K., Lobler, M., and Klambt, D. (1989). cDNA clones of the auxin- binding protein from corn coleptiles (Zea mays L.): Isolation and characterization by immunological methods. EMBO J. 8, 2463-2467.
  57. Tromas, A., Braun, N., Muller, P., Khodus, T., Paponov, I.A., Palme, K., Ljung, K., Lee, J.Y., Benfey, P., Murray, J.A., et al. (2009). The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth. PLoS One 4, e6648. https://doi.org/10.1371/journal.pone.0006648
  58. Tromas, A., Paponov, I., and Perrot-Rechenmann, C. (2010). AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends Plant Sci. 15, 436-446. https://doi.org/10.1016/j.tplants.2010.05.001
  59. Tromas, A., Paque, S., Stierle, V., Quettier, A.L., Muller, P., Lechner, E., Genschik, P., and Perrot-Rechenmann, C. (2013). Auxinbinding protein 1 is a negative regulator of the SCFTIR1/AFB pathway. Nat. Comm. 4, 2496.
  60. Venis, M.A., Napier, R.M., Barbier-Brygoo, H., Maurel, C., Perrot- Rechenmann, C., and Guern, J. (1992). Antibodies to a peptide from the maize auxin-binding protein have auxin agonist activity. Proc. Natl. Acad. Sci. USA 89, 7208-7212. https://doi.org/10.1073/pnas.89.15.7208
  61. Woo, E.J., Marshall, J., Bauly, J., Chen, J.G., Venis, M., Napier, R.M., and Pickersgill, R.W. (2002). Crystal structure of auxinbinding protein 1 in complex with auxin. EMBO J. 21, 2877-2885. https://doi.org/10.1093/emboj/cdf291
  62. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J.G., Wu, M.J., Perrot- Rechenmann, C., Frimi, J., Jones, A.M., and Yang, Z. (2010). Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110. https://doi.org/10.1016/j.cell.2010.09.003
  63. Xu, T., Dai, N., Chen, J., Nagawa, S., Cao, M., Li, H., Zhou, Z., Chen, X., De Rycke, R., Rakusová, H., et al. (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343, 1025-1028. https://doi.org/10.1126/science.1245125

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