Genetic identification of a second site modifier of ctr1-1 that controls ethylene-responsive and gravitropic root growth in Arabidopsis thaliana

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• 作者：Kihye Shin (197)
  Rin-A Lee (197)
  Inhye Lee (197)
  Sumin Lee (197)
  Soon Ki Park (297)
  Moon-Soo Soh (197)
  
• 关键词：Arabidopsis ; auxin ; ctr1 ; 1 ; ethylene ; gravitropism
• 刊名：Molecules and Cells
• 出版年：2013
• 出版时间：July 2013
• 年：2013
• 卷：36
• 期：1
• 页码：88-96
• 全文大小：1172KB
• 参考文献：1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wi艡niewska, J., Moulinier-Anzola, J.C., Sieberer, T., Friml, J., and Luschnig, C. (2006). Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. / 8, 249. CrossRef
  2. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J.R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in / Arabidopsis. Science / 284, 2148鈥?152. CrossRef
  3. An, F., Zhao, Q., Ji, Y., Li, W., Jiang, Z., Yu, X., Zhang, C., Han, Y., He, W., Liu, Y., et al. (2010). Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell / 22, 2384鈥?401. CrossRef
  4. Barbez, E., Kubes, M., Rolcik, J., Beziat, C., Pencik, A., Wang, B., Rosquete, M.R., Zhu, J., Dobrev, P.I., Lee, Y., et al. (2012). A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature / 485, 119鈥?22. CrossRef
  5. Bleecker, A.B., and Kende, H. (2000). Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. / 16, 1鈥?8. CrossRef
  6. Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T., and Masson, P.H. (1998). The / Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA / 95, 15112鈥?5117. CrossRef
  7. Depuydt, S., and Hardtke Christian, S. (2011). Hormone signal-ling crosstalk in plant growth regulation. Curr. Biol. / 21, R365鈥揜373. CrossRef
  8. Ganguly, A., Sasayama, D., and Cho, H.-T. (2012). Regulation of the polarity of protein trafficking by phosphorylation. Mol. Cells / 33, 423鈥?30. CrossRef
  9. Grieneisen, V.A., Xu, J., Maree, A.F., Hogeweg, P., and Scheres, B. (2007). Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature / 449, 1008鈥?013. CrossRef
  10. Guo, H., and Ecker, J.R. (2003). Plant responses to ethylene gas are mediated by SCF EBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell / 115, 667鈥?77. CrossRef
  11. Guzman, P., and Ecker, J.R. (1990). Exploiting the triple res-ponse of Arabidopsis to identify ethylene-related mutants. Plant Cell / 2, 513鈥?23.
  12. He, W., Brumos, J., Li, H., Ji, Y., Ke, M., Gong, X., Zeng, Q., Li, W., Zhang, X., An, F., et al. (2011). A small-molecule screen identifies l-Kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in / Arabidopsis. Plant Cell / 23, 3944鈥?960. CrossRef
  13. Hua, J., and Meyerowitz, E.M. (1998). Ethylene responses are negatively regulated by a receptor gene family in / Arabidopsis thaliana. Cell / 94, 261鈥?71. CrossRef
  14. Huang, Y., Li, H., Hutchison, C.E., Laskey, J., and Kieber, J.J. (2003). Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. / 33, 221鈥?33. CrossRef
  15. Ju, C., and Chang, C. (2012). Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. AoB Plants 2012. pls031.
  16. Ju, C., Yoon, G.M., Shemansky, J.M., Lin, D.Y., Ying, Z.I., Chang, J., Garett, W.M., Kessenbrock, M., Groth, G., Tucker, M.L., et al. (2012). CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from ER membrane to the nucleus in / Arabidopsis. Proc. Natl. Acad. Sci. USA / 109, 19486鈥?9491. CrossRef
  17. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., and Ecker, J.R. (1993). CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases. Cell / 72, 427鈥?41. CrossRef
  18. Kleine-Vehn, J., and Friml, J. (2008). Polar targeting and endo-cytic recycling in auxin-dependent plant development. Annu. Rev. Cell Dev. Biol. / 24, 447鈥?73. CrossRef
  19. Kleine-Vehn, J., Ding, Z., Jones, A.R., Tasaka, M., Morita, M.T., and Friml, J. (2010). Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc. Natl. Acad. Sci. USA / 107, 22344鈥?2349. CrossRef
  20. Lehman, A., Black, R., and Ecker, J.R. (1996). HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the / Arabidopsis hypocotyl. Cell / 85, 183. CrossRef
  21. Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G., and Spalding, E.P. (2007). Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell / 19, 1838鈥?850. CrossRef
  22. Lewis, D.R., Negi, S., Sukumar, P., and Muday, G.K. (2011). Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development / 138, 3485鈥?495. CrossRef
  23. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in / Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. / 123, 795鈥?05. CrossRef
  24. Luschnig, C., Gaxiola, R.A., Grisafi, P., and Fink, G.R. (1998). EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in / Arabidopsis thaliana. Genes Dev. / 12, 2175鈥?187. CrossRef
  25. Muday, G.K., Rahman, A., and Binder, B.M. (2012). Auxin and ethylene: collaborators or competitors? Trends Plant Sci. / 17, 181鈥?95. CrossRef
  26. Muller, A., Guan, C., Galweier, L., Tanzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E., and Palme, K. (1998). / AtPIN2 defines a locus of / Arabidopsis for root gravitropism control. EMBO J. / 17, 6903鈥?911. CrossRef
  27. Peer, W.A., Blakeslee, J.J., Yang, H., and Murphy, A.S. (2011). Seven things we think we know about auxin transport. Mol. Plant / 4, 487鈥?04. CrossRef
  28. Pickett, F.B., Wilson, A.K., and Estelle, M. (1990). The / aux1 mutation of / Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. / 94, 1462鈥?466. CrossRef
  29. Potuschak, T. (2003). EIN3-dependent regulation of plant ethylene hormone signalling by two / Arabidopsis F box proteins: EBF1 and EBF2. Cell / 115, 679鈥?89. CrossRef
  30. Qiao, H., Shen, Z., Huang, S.S., Schmitz, R.J., Urich, M.A., Briggs, S.P., and Ecker, J.R. (2012). Processing and subcell-ular trafficking of ER-tethered EIN2 control response to ethylene gas. Science / 338, 390鈥?93. CrossRef
  31. Rahman, A., Takahashi, M., Shibasaki, K., Wu, S., Inaba, T., Tsurumi, S., and Baskin, T.I. (2010). Gravitropism of / Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell / 22, 1762鈥?776. CrossRef
  32. Rashotte, A.M., DeLong, A., and Muday, G.K. (2001). Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell / 13, 1683鈥?697.
  33. Rosquete, M.R., Barbez, E., and Kleine-Vehn, J. (2012). Cellular auxin homeostasis: Gatekeeping is housekeeping. Mol. Plant / 5, 772鈥?86. CrossRef
  34. Ruzicka, K., Ljung, K., Vanneste, S., Podhorska, R., Beeckman, T., Friml, J., and Benkova, E. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell / 19, 2197鈥?212. CrossRef
  35. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., et al. (1999). An auxin-dependent distal organizer of pattern and polarity in the / Arabidopsis root. Cell / 99, 463鈥?72. CrossRef
  36. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. / 3, 1101鈥?108. CrossRef
  37. Sedbrook, J., Boonsirichai, K., Chen, R., Hilson, P., Pearlman, R., Rosen, E., Rutherford, R., Batiza, A., Carroll, K., Schulz, T., et al. (1998). Molecular genetics of root gravitropism and waving in / Arabidopsis thaliana. Gravit. Space Biol. Bull. / 11, 71鈥?8.
  38. Stepanova, A.N., Hoyt, J.M., Hamilton A.A., and Alonso, J.M. (2005). A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell / 17, 2230鈥?242. CrossRef
  39. Stepanova, A.N., Yun, J., Likhacheva, A.V., and Alonso, J.M. (2007). Multilevel interactions between ethylene and auxin in / Arabidopsis roots. Plant Cell / 19, 2169鈥?185. CrossRef
  40. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., Dolezal, K., Schlereth, A., Jurgens, G., and Alonso, J.M. (2008). TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell / 133, 177鈥?91. CrossRef
  41. Swarup, R., Kramer, E.M., Perry, P., Knox, K., Leyser, H.M.O., Haseloff, J., Beemster, G.T.S., Bhalerao, R., and Bennett, M.J. (2005). Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. / 7, 1057鈥?065. CrossRef
  42. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J. (2007). Ethylene upregulates auxin biosynthesis in / Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell / 19, 2186鈥?196. CrossRef
  43. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell / 9, 1963鈥?971.
  44. Utsuno, K., Shikanai, T., Yamada, Y., and Hashimoto, T. (1998). AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. / 39, 1111鈥?118. CrossRef
  45. Vandenbussche, F., Petr谩拧ek, J., 沤谩dn铆kov盲, P., Hoyerov谩, K., Pe拧ek, B., Raz, V., Swarup, R., Bennett, M., Za啪铆malov谩, E., Benkov谩, E., et al. (2010). The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in / Arabidopsis thaliana seedlings. Development / 137, 597鈥?06. CrossRef
  46. Vanstraelen, M., and Benkov谩, E. (2012). Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. / 28, 463鈥?87. CrossRef
  47. Wen, X., Zhang, C., Ji, Y., Zhao, Q., He, W., An, F., Jiang, L., and Guo, H. (2012). Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxy terminus. Cell Res. / 22, 1613鈥?616. CrossRef
  48. Willemsen, V., Wolkenfelt, H., de Vrieze, G., Weisbeek, P., and Scheres, B. (1998). The / HOBBIT gene is required for forma-tion of the root meristem in the / Arabidopsis embryo. Develop-ment / 125, 521鈥?31.
  49. Xu, J., and Scheres, B. (2005). Dissection of Arabidopsis ADPRIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell / 17, 525鈥?36. CrossRef
  50. Yanagisawa, S., Yoo, S.D., and Sheen, J. (2003). Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature / 425, 521鈥?25. CrossRef
  51. Yoo, S.D., Cho, Y.H., Tena, G., Xiong, Y., and Sheen, J. (2008). Dual control of nuclear EIN3 by bifurcate MAPK cascades in ethylene signalling. Nature / 451, 789鈥?95. CrossRef
  52. 沤谩dn铆kiov谩, P, Petr谩拧ek, J., Marhav媒, P., Raz, V., Vanden-bussche, F., Ding, Z., Schwarzerov谩, K., Morita, M.T., Tasaka, M., Hej谩tko, J., et al. (2010). Role of PIN-mediated auxin efflux in apical hook development of / Arabidopsis thaliana. Development / 137, 607鈥?17. CrossRef
  53. Za啪铆alov谩, E., Murphy, A.S., Yang, H., Hoyerov谩, K., and Ho拧ek, P. (2010). Auxin transporters-why so many? Cold Spring Harb. Perspect. Biol. / 2, a001552. CrossRef
  54. Zhang, W., and Wen, C.K. (2010). Preparation of ethylene gas and comparison of ethylene responses induced by ethylene, ACC, and ethephon. Plant Physiol. Biochem. / 48, 45鈥?3. CrossRef
  
• 作者单位：Kihye Shin (197)
  Rin-A Lee (197)
  Inhye Lee (197)
  Sumin Lee (197)
  Soon Ki Park (297)
  Moon-Soo Soh (197)
  
  197. Department of Molecular Biology, College of Life Science, Sejong University, Seoul, 143-747, Korea
  297. School of Applied Biosciences, Kyungpook National University, Daegu, 702-701, Korea
  
• ISSN：0219-1032

文摘

Ethylene controls myriad aspects of plant growth throughout developmental stages in higher plants. It has been well established that ethylene-responsive growth entails extensive crosstalk with other plant hormones, particularly auxin. Here, we report a genetic mutation, named 1-aminocyclopropane carboxylic acid (ACC) resistant root1-1 (are1-1) in Arabidopsis thaliana (L.) Heynh. The CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) encodes a Raf-related protein, functioning as an upstream negative regulator of ethylene signaling in Arabidopsis thaliana. We found that the ctr1-1, a kinase-inactive allele exhibited slightly, but significantly, longer root length, compared to ACC-treated wild-type or ctr1-3, a null allele. Our genetic studies unveiled the existence of are1-1 mutation in the ctr1-1 mutant, as a second-site modifier which confers root-specific ethylene-resistance. Based on well-characterized crosstalk between ethylene and auxin during ethylene-responsive root growth, we performed various physiological analyses. Whereas are1-1 displayed normal sensitivity to synthetic auxins, it showed modest resistance to an auxin transport inhibitor, 1-Nnaphthylphthalamic acid. In addition, are1-1 mutant exhibited ectopically altered DR5:GUS activity upon ethylenetreatment. The results implicated the involvement of are1-1 in auxin-distribution, but not in auxin-biosynthesis, -uptake, or -sensitivity. In agreement, are1-1 mutant exhibited reduced gravitropic root growth and defective redistribution of DR5:GUS activity upon gravi-stimulation. Taken together with genetic and molecular analysis, our results suggest that ARE1 defines a novel locus to control ethylene-responsive root growth as well as gravitropic root growth presumably through auxin distribution in Arabidopsis thaliana.