Patterns and timing in expression of early auxin-induced genes imply involvement of phospholipases a (PPLAS) in the regulation of auxin responses

Molecular Plant

Volumn 6, Issue 5, 2013, Pages 1473-1486

  Labusch, Corinna ^a   Shishova, Maria ^b   Effendi, Yunus ^a   Li, Maoyin ^c,d   Wang, Xuemin ^c,d   Scherer, Günther F E ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^d DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

hormonal regulation; hormone biology; signal transduction

Indexed keywords

ARABIDOPSIS THALIANA;

INDOLEACETIC ACID DERIVATIVE; PHOSPHOLIPASE A;

ARABIDOPSIS; ARTICLE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORMONAL REGULATION; HORMONE BIOLOGY; LIGHT; METABOLISM; MUTATION; PHENOTYPE; PLANT GENE; PLANT ROOT; RADIATION EXPOSURE; SEEDLING; SIGNAL TRANSDUCTION.; TIME;

HORMONAL REGULATION; HORMONE BIOLOGY; SIGNAL TRANSDUCTION.;

ARABIDOPSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INDOLEACETIC ACIDS; LIGHT; MUTATION; PHENOTYPE; PHOSPHOLIPASES A; PLANT ROOTS; SEEDLING; TIME FACTORS;

EID: 84885064251     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst053     Document Type: Article

References (70)

1. Abel, S., and Theologis, A. (1996). Early genes and auxin action. Plant Physiol. 111, 9-17.
2. Abel, S., Nguyen, M.D., and Theologis, A. (1995). The PS-IAA4/5- like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251, 533-549.
3. Abel, S., Oeller, P.W., and Theologis, A. (1994). Early auxin-induced genes encode short-lived nuclear proteins. Proc. Natl Acad. Sci. U S A. 91, 326-330.
4. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., Stevenson, D.K., Zimmerman, J., Barajas, P., Cheuk, R., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657.
5. Balsinde, J., and Balboa, M.A. (2005). Cellular regulation and proposed biological functions of group VIA calcium-independent phospholipase A2 in activated cells. Cell Signal. 17, 1052-1062.
6. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 115, 591-602.
7. Chae, K., Isaacs, C.G., Reeves, P.H., Maloney, G.S., Muday, G.K., Nagpal, P., and Reed, J.W. (2012). Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J. 71, 684-697.
8. Delker, C., Raschke, A., and Quint, M. (2008). Auxin dynamics: the dazzling complexity of a small molecule's message. Planta. 227, 929-941.
9. Dreher, K.A., Brown, J., Saw, R.E., and Callis, J. (2006). The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell. 18, 699-714.
10. Dubrovsky, J., and Forde, B.G. (2012). Quantitative analysis of lateral root development: pitfalls and how to avoid them. Plant Cell. 24, 4-14.
11. Effendi, Y., and Scherer, G.F.E. (2011). Auxin binding-protein1 (ABP1), a receptor to regulate auxin transport and early auxin genes in an interlocking system with PIN proteins and the receptor TIR1. Plant Signal Behav. 6, 1101-1103.
12. Effendi, Y., Rietz, S., Fischer, U., and Scherer, G.F.E. (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.
13. Estelle, M.A., and Somerville, C. (1987). Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206.
14. Franklin, K.A., Lee, S.H., Patel, D., Kumar, V., Spartz, A.K., Gu, C., Ye, S., Yu, P., Breen, G., Cohen, J.D., et al. (2011). PHYTOCHROME INTERACTING FACTOR 4 regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. U S A. 108, 2131-2135.
15. Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A., and Tasaka, M. (2005). Tissue-specific expression of stabilized SOLITARY-ROOT/ IAA14 alters lateral root development in Arabidopsis. Plant J. 44, 382-395.
16. Fukaki, H., Tameda, S., Masuda, H., and Tasaka, M. (2002). Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153-168.
17. Fukaki, H., Taniguchi, N., and Tasaka, M. (2006). PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J. 48, 380-389.
18. Guilfoyle, T.J., Hagen, G., Ulmasov, T., and Murfett, J. (1998b). How does auxin turn on genes? Plant Physiol. 118, 341-347.
19. Guilfoyle, T.J., Ulmasov, T., and Hagen, G. (1998a). The ARF family of transcription factors and their role in plant hormone responsive transcription. Cell Mol. Life Sci. 54, 619-627.
20. Hagen, G., and Guilfoyle, T. (2002). Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373-385.
21. Holk, A., Rietz, S., Zahn, M., Quader, H., and Scherer, G.F. (2002). Molecular identification of cytosolic, patatin-related phospholipases A from Arabidopsis with potential functions in plant signal transduction. Plant Physiol. 130, 90-101.
22. Huang, S., Cerny, R.E., Bhat, D.S., and Brown, S.M. (2001). Cloning of an Arabidopsis patatin-like gene, STURDY, by activation T-DNA tagging. Plant Physiol. 125, 573-584.
23. Jain, M., Tyagi, A.K., and Khurana, J.P. (2006). Genome-wide analysis, evolutionary expansion, and expression of early auxinresponsive SAUR gene family in rice (Oryza sativa). Genomics. 88, 360-371.
24. Kim, B.C., Soh, M.S., Kang, B.J., Furuya, M., and Nam, H.G. (1996). Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J. 9, 441-456.
25. La Camera, S., Geoffroy, P., Samaha, H., Ndiaye, A., Rahim, G., Legrand, M., and Heitz, T. (2005). A pathogen-inducible patatin- like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J. 44, 810-825.
26. Li, H., Cheng, Y., Murphy, A., Hagen, G., and Guilfoyle, T.J. (2009). Constitutive repression and activation of auxin signaling in Arabidopsis. Plant Physiol. 149, 1277-1288.
27. Li, M., Bahn, S.C., Guo, L., Musgrave, W., Berg, H., Welti, R., and Wang, X. (2011). Patatin-related phospholipase pPLAIIIβ- induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell. 23, 1107-1123.
28. Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Nieto-Jacobo, M.F., Simpson, J., and Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129, 244-256.
29. Mano, Y., and Nemoto, K. (2012). The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63, 2853-2872.
30. Mashiguchi, K., Tanaka, K., Sakai, T., Sugawara, S., Kawaide, H., Natsume, M., Hanada, A., Yaeno, T., Shirasu, K., Yao, H., et al. (2011). The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl Acad. Sci. U S A. 108, 18512-18517.
31. Matos, A.R., d'Arcy-Lameta, A., França, M., Pêtres, S., Edelman, L., Kader, J., Zuily-Fodil, Y., and Pham-Thi, A.T. (2001). A novel patatin-like gene stimulated by drought stress encodes a galactolipid acyl hydrolase. FEBS Lett. 491, 188-192.
32. Mockaitis, K., and Estelle, M. (2008). Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24, 55-80.
33. Napier, R.M., David, K.M., and Perrot-Rechenmann, C. (2002). A short history of auxin-binding proteins. Plant Mol. Biol. 49, 339-348.
34. Paponov, I.A., Paponov, M., Teale, W., Menges, M., Chakrabortee, S., Murray, J.A.H., and Palme, K. (2008). Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol. Plant. 1, 321-337.
35. Paul, R.U., Holk, A., and Scherer, G.F.E. (1998). Fatty acids and lysophospholipids as potential second messengers in auxin action: rapid activation of phospholipase A2 activity by auxin in suspension-cultured parsley and soybean cells. Plant J. 16, 601-611.
36. Péret, B., De Rybel, B., Casimiro, I., Benokvá, E., Swarup, R., Laplaze, L., Beekman, T., and Bennet, M.J. (2009). Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14, 399-408.
37. Pérez-Torres, C.A., López-Bucio, J., Cruz-Ramírez, A., Ibarra- Laclette, E., Dharmasiri, S., Estelle, M., and Herrera-Estrella, L. (2008). Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell. 20, 3258-3272.
38. Pfaffl, M.W., Horgan, G.W., and Dempfle, L. (2002). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
39. Quint, M., and Gray, W.M. (2006). Auxin signalling. Curr. Opin. Plant Biol. 9, 448-453.
40. Quint, M., Barkawi, L.S., Fan, K.-T., Cohen, J.D., and Gray, W.M. (2009). Arabidopsis IAR4 modulates auxin response by regulating auxin homeostasis. Plant Physiol. 150, 748-758.
41. Reed, J.W. (2001). Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420-425.
42. Rietz, S., Dermendjiev, G., Oppermann, E., Tafesse, F.G., Effendi, Y., Holk, A., Parker, J.E., Teige, M., and Scherer, G.F.E. (2010). Roles of Arabidopsis patatin-related phospholipases A in root development are related to auxin responses and phosphate deficiency. Mol. Plant. 3, 534-538.
43. Rietz, S., Holk, A., and Scherer, G.F. (2004). Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta. 219, 743-753.
44. Robert, S., Kleine-Vehn, J., Barbez, E., Sauer, M., Paciorek, T., Baster, P., Vanneste, S., Zhang, J., Simon, S., Čovanová, M., et al. (2010). ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell. 143, 111-121.
45. Ruiz Rosquete, M., Barbez, E., and Kleine-Vehn, J. (2012). Cellular auxin homeostasis: gatekeeping is housekeeping. Mol. Plant. 5, 772-786.
46. Ryu, S.B. (2004). Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci. 9, 229-235.
47. Sauer, M., and Kleine-Vehn, J. (2011). AUXIN BINDING PROTEIN1: the outsider. Plant Cell. 23, 2033-2043.
48. Scherer, G.F.E. (2011). AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J. Exp. Bot. 62, 3339-3357.
49. Scherer, G.F.E., and André, B. (1989). A rapid response to a plant hormone auxin stimulates phospholipase-A2 enzymes in vivo and in vitro. Biochem. Biophys. Res. Commun. 163, 111-117.
50. Scherer, G.F.E., and Arnold, B. (1997). Auxin-induced growth is inhibited by phospholipase A2 inhibitors: implications for auxin-induced signal transduction. Planta. 202, 462-469.
51. Scherer, G.F.E., Labusch, C., and Effendi, Y. (2012). Phospholipases and the network of auxin signal transduction with ABP1 and TIR1 as two receptors: a comprehensive and provocative model. Front Plant Sci. 3, 56.
52. Scherer, G.F.E., Ryu, S.B., Wang, X., Matos, A.R., and Heitz, T. (2010). Patatin-related phospholipase A: nomenclature, subfamilies, and functions in plants. Trends Plant Sci. 15, 693-700.
53. Scherer, G.F.E., Zahn, M., Callis, J., and Jones, A.M. (2007). A role for phospholipase A in auxin-regulated gene expression. FEBS Lett. 581, 4205-4211.
54. Shi, J.-H., and Yang, Z.-B. (2011). Is ABP1 an auxin receptor yet? Mol. Plant. 4, 635-640.
55. Soh, M.S., Hong, S.H., Kim, B.C., Vizir, I., Park, D.H., Choi, G., Hong, M.Y., Chung, Y.Y., Furuya, M., and Nam, H.G. (1999). Regulation of both light- and auxin-mediated development by the Arabidopsis IAA3/SHY2 gene. J. Plant Biol. 42, 239-246.
56. Spartz, A.K., Lee, S.H., Wenger, J.P., Gonzalez, N., Itoh, H., Inze, D., Peer, W.A., Murphy, A.S., Overvoorde, P., and Gray, W.M. (2012). The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J. 70, 978-990.
57. Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M.T., Maldonado, M.C., and Suza, W. (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 17, 616-627.
58. Sussman, M.R., Amasino, R.M., Young, J.C., Krysan, P.J., and Austin-Phillips, S. (2000). The Arabidopsis T-DNA insertion facility at the University of Wisconsin-Madison. Plant Physiol. 124, 1465-1467.
59. Tatematsu, K., Kumagai, S., Muto, H., Sato, A., Watahiki, M.K., Harper, R.M., Liscum, E., and Yamamoto, K.T. (2004). MASSUGU2 encodes AUX/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NHP4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell. 16, 379-393.
60. Terrile, M.C., París, R., Calderón-Villalobos, L.I., Iglesias, M.J., Lamattina, L., Estelle, M., and Casalongué, C.A. (2012). Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J. 70, 492-500.
61. Tian, Q., and Reed, J.W. (1999). Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development. 126, 711-721.
62. Tian, Q., Nagpal, P., and Reed, J.W. (2003). Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J. 36, 643-651.
63. Vanneste, S., De Rybel, B., Beemster, G.T., Ljung, K., De Smet, I., Van Isterdael, G., Naudts, M., Iida, R., Gruissem, W., Tasaka, M., et al. (2005). Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell. 17, 3035-3050.
64. Vieten, A., Vanneste, S., Wisniewska, J., Benková, E., Benjamins, R., Luschnig, C., and Friml, J. (2005). Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development. 132, 4521-4531.
65. Wang, J.-R., Hu, H., Wang, G.-H., Li, J., Chen, J.-Y., and Wu, P. (2009). Expression of PIN Genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. Mol. Plant. 2, 823-831.
66. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J.G., Wu, M.J., Perrot- Rechenmann, C., Friml, 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.
67. Xu, T., Nagawa, S., and Yang, Z. (2011). Uniform auxin triggers the Rho GTPase-dependent formation of interdigitation patterns in pavement cells. Small Gtpases. 2, 227-232.
68. Yang, T., and Poovaiah, B.W. (2000). Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J. Biol. Chem. 275, 3137-3143.
69. Yang, W., Devaiah, S.P., Pan, X., Isaac, X., Welti, R., and Wang, X. (2007). AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea. J. Biol. Chem. 282, 18116-18128.
70. Zenser, N., Ellsmore, A., Leasure, C., and Callis, J. (2001). Auxin modulates the degradation rate of Aux/IAA proteins. Proc. Natl Acad. Sci. U S A. 98, 11795-11800.