Analysis of the role of arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development

Frontiers in Plant Science

Volumn 4, Issue OCT, 2013, Pages

  Aguilar Martlnez, Jose A ^a   Sinha, Neelima ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arabidopsis; Leaf development; SRDX construct; TCP; Transcription factor

Indexed keywords

EID: 84901002675     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00406     Document Type: Article

References (68)

1. Aggarwal, P., Das Gupta, M., Joseph, A.P., Chatterjee, N., Srinivasan, N., and Nath, U. (2010). Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22, 1174-1189. doi: 10.1105/tpc.109.066647
2. Aguilar-Martmez, J. A., Poza-Carrion, C., and Cubas, P. (2007). Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19, 458-472. doi: 10.1105/tpc.106.048934
3. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., et al. (2003). Genome-Wide inser- tional mutagenesis of Arabidopsis thaliana. Science 301, 653-657. doi: 10.1126/science.1086391
4. Alonso-Blanco, C., El-Assal, S. E., Coupland, G., and Koornneef, M. (1998). Analysis of natural allelic variation at flowering time loci in the landsberg erecta and cape verde islands ecotypes ofArabidopsis thaliana. Genetics 149, 749-764.
5. Babu, M. M., van der Lee, R., de Groot, N. S., and Gsponer, J. (2011). Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 21, 432-440. doi: 10.1016/j.sbi.2011.03.011
6. Beschtold, N., Ellis, J., and Pelletier, G. (1993). In planta Agrobacterium- mediated gene transfer by filtration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. (Paris) 316, 1194-1199.
7. Busch, A., and Zachgo, S. (2009). Flower symmetry evolution: towards understanding the abominable mystery of angiosperm radiation. Bioessays 31, 1181-1190. doi: 10.1002/bies.200900081
8. Byrne, M. E., Barley, R., Curtis, M., Arroyo, J. M., Dunham, M., Hudson, A., et al. (2000). Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967-971. doi: 10.1038/35050091
9. Chuck, G., Lincoln, C., and Hake, S. (1996). KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8, 1277-1289. doi: 10.2307/3870301
10. Clough, S. J., and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. PlantJ. 16, 735-743. doi: 10.1046/j. 1365-313x.1998.00343.x
11. Cubas, P. (2002). Role ofTCP genes in the evolution of key morphological characters in angiosperms in Developmental Genetics and Plant Evolution, eds Q. Cronk, J. Hawkins, and R. M. Bateman (London: Taylor and Francis), 247-266. doi: 10.1201/9781420024982.ch13
12. Cubas, P., Coen, E., and Zapater, J. (2001). Ancient asymmetries in the evolution of flowers. Curr. Biol. 11, 1050-1052. doi: 10.1016/S0960- 9822(01)00295-0
13. Cubas, P., Lauter, N., Doebley, J., and Coen, E. (1999). The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18, 215-222. doi: 10.1046/j.1365-313X.1999.00444.x
14. Danisman, S., Wal, F., Dhondt, S., Waites, R., Folter, S., Bimbo, A., et al. (2012). Arabidopsis Class I and Class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically. Plant Physiol. 159, 1511-1523. doi: 10.1104/pp.112.200303
15. Doebley, J., Stec, A., and Hubbard, L. (1997). The evolution of apical dominance in maize. Nature 386, 485-488. doi: 10.1038/ 386485a0
16. Finlayson, S. A. (2007). Arabidopsis TEOSINTE BRANCHED 1 -LIKE 1 regulates axillary bud outgrowth and is homologous to monocot teosinte branched1. Plant Cell Physiol. 48, 667-677. doi: 10.1093/pcp/pcm044
17. Giraud, E., Ng, S., Carrie, C., Duncan, O., Low, J., Lee, C. P., et al. (2010). TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22, 3921-3934. doi: 10.1105/tpc.110.074518
18. Guo, M., Thomas, J., Collins, G., and Timmermans, M. (2008). Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20, 48-58. doi: 10.1105/tpc.107.056127
19. Guo, Z., Fujioka, S., Blancaflor, E. B., Miao, S., Gou, X., and Li, J. (2010). TCP1 modulates brassinos- teroid biosynthesis by regulating the expression of the key biosynthetic gene DWARF4 in Arabidopsis thaliana. Plant Cell 22, 1161-1173. doi: 10.1105/tpc.109.069203
20. Hammani, K., Gobert, A., Hleibieh, K., Choulier, L., Small, I., and Giege, P. (2011). An Arabidopsis duallocalized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23, 730-740. doi: 10.1105/tpc.110.081638
21. Herve, C., Dabos, P., Bardet, C., Jauneau, A., Auriac, M. C., Ramboer, A., et al. (2009). In Vivo Interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol. 149, 1462-1477. doi: 10.1104/pp.108.126136
22. Hiratsu, K., Matsui, K., Koyama, T., and Ohme-Takagi, M. (2003). Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 34, 733-739. doi: 10.1046/j.1365-313X.2003.01759.x
23. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., et al. (2008). Genevestigator V3: a reference expression database for the meta-analysis oftranscriptomes. Adv. Bioinformatics 2008, 420-747. doi: 10.1155/2008/420747
24. Ingram, G. C., and Waites, R. (2006). Keeping it together: coordinating plant growth. Curr. Opin. Plant Biol. 9, 12-20. doi: 10.1016/j.pbi.2005.11.007
25. Itoh, J. I., Hasegawa, A., Kitano, H., and Nagato, Y. (1998). A recessive heterochronic mutation, plas- tochron1, shortens the plastochron and elongates the vegetative phase in rice. Plant Cell 10, 1511-1522. doi: 10.2307/3870615
26. Kagan, M. L., Novoplansky, N., and Sachs, T. (1992). Variable cell lineages form the functional pea epidermis. Ann. Bot. 69, 303-312.
27. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. doi: 10.1016/S1360-1385 (02)02251-3
28. Kieffer, M., Master, V., Waites, R., and Davies, B. (2011). TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 68, 147-158. doi: 10.1111/j.1365- 313X.2011.04674.x
29. Koncz, C., and Schell, J. (1986). The promoter of TL -DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type ofAgrobacterium binaryvector. Mol. Gen. Genet. 204, 383-396. doi: 10.1007/BF00331014
30. Kosugi, S., and Ohashi, Y. (1997). PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9, 1607-1619. doi: 10.2307/3870447
31. Kosugi, S., and Ohashi, Y. (2002). DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J. 30, 337-348. doi: 10.1046/j.1365- 313X.2002.01294.x
32. Koyama, T., Furutani, M., Tasaka, M., and Ohme-Takagi, M. (2007). TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary- specific genes in Arabidopsis. Plant Cell 19, 473-484. doi: 10.1105/tpc.106.044792
33. Koyama, T., Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2010). TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22, 3574-3588. doi: 10.1105/tpc.110. 075598
34. Li, C., Potuschak, T., Colon-Carmona, A., Gutierrez, R. A., and Doerner, P. (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc. Natl. Acad. Sci. U.S.A. 102, 2978-12983. doi: 10.1073/pnas.0504039102
35. Li, Y., Rosso, M. G., Viehoever, P., and Weisshaar, B. (2007). GABI- Kat SimpleSearch: an Arabidopsis thaliana T-DNA mutant database with detailed information for confirmed insertions. Nucleic Acids Res. 35, D874-D878. doi: 10.1093/nar/gkl753
36. Li, Z., Li, B., and Dong, A. (2012a). The Arabidopsis transcription factor AtTCP15 regulates endoredu- plication by modulating expression of key cell-cycle genes. Mol. Plant 5, 270-280. doi: 10.1093/mp/ ssr086
37. Li, Z., Li, B., Shen, W. H., Huang, H., and Dong, A. (2012b). TCP transcription factors interact with AS2 in the repression of class-I KNOX genes in Arabidopsis thaliana. Plant J. 71, 99-107. doi: 10.1111/j.1365- 313X.2012.04973.x
38. Maloof, J. N., Nozue, K., Mumbach, M. R., and Palmer, C. M. (2013). LeafJ: an imagej plugin for semiautomated leaf shape measurement. J. Vis. Exp. 71, e50028. doi: 10.3791/50028
39. Martin-Trillo, M., and Cubas, P. (2010). TCP genes: a family snapshot ten years later. Trends Plant Sci. 15, 31-39. doi: 10.1016/j.tplants.2009.11.003
40. Mutwil, M., Obro, J., Willats, W. G., and Persson, S. (2008). GeneCAT: novel webtools that combine BLAST and co-expression analyses. Nucleic Acids Res 36, W320-W326. doi: 10.1093/nar/gkn292
41. Nag, A., King, S., and Jack, T. (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 22534-22539. doi: 10.1073/ pnas.0908718106
42. Nath, U., Crawford, B. C. W., Carpenter, R., and Coen, E. (2003). Genetic control of surface curvature. Science 299, 1404-1407. doi: 10.1126/ science.1079354
43. Navaud, O., Dabos, P., Carnus, E., Tremousaygue, D., and Herve, C. (2007). TCP transcription factors predate the emergence of land plants. J. Mol. Evol. 65, 23-33. doi: 10.1007/s00239-006-0174-z
44. Niwa, M., Daimon, Y., Kurotani, K., Higo, A., Pruneda-Paz, J. L., Breton, G., et al. (2013). BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25, 1228-1242. doi: 10.1105/tpc.112.109090
45. Ori, N., Cohen, A. R., Etzioni, A., Brand, A., Yanai, O., Shleizer, S., et al. (2007). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39, 787-791. doi: 10.1038/ng2036
46. Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C., et al. (2003). Control of leaf morphogenesis by microRNAs. Nature 425, 257-263. doi: 10.1038/nature01958
47. Pruneda-Paz, J. L., Breton, G., Para, A., and Kay, S. A. (2009). A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323, 1481-1485. doi: 10.1126/science.1167206
48. Rueda-Romero, P., Barrero-Sicilia, C., Gomez-Cadenas, A. Carbonero, P., Onate-Sanchez, L. (2012). Arabidopsis thaliana DOF6 negatively affects germination in non-after-ripened seeds and interacts with TCP14. J. Exp. Bot. 63, 1937-1949. doi: 10.1093/ jxb/err388
49. Salome, P. A., Bomblies, K., Laitinen, R. A., Yant, L., Mott, R., and Weigel, D. (2011). Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188, 421-433. doi: 10.1534/genet- ics.111.126607
50. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., et al. (2005). A gene expression map of Arabidopsis development. Nat. Genet. 37, 501-506. doi: 10.1038/ng1543
51. Schommer, C., Palatnik, J. F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E. E., et al. (2008). Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 6:e230. doi: 10.1371/journal.pbio.0060230
52. Sessions, A., Burke, E., Presting, G., Aux, G., McElver, J., Patton, D., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14, 2985-2994. doi: 10.1105/tpc.004630
53. Steiner, E., Efroni, I., Gopalraj, M., Saathoff, K., Tseng, T.-S., Kieffer, M., et al. (2012a). The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with Class I TCPs to facilitate cytokinin responses in leaves and flowers. Plant Cell 24, 96-108. doi: 10.1105/tpc.111.093518
54. Steiner, E., Yanai, O., Efroni, I., Ori, N., Eshed, Y., and Weiss, D. (2012b). Class I TCPs modulate cytokinin-induced branching and meristematic activity in tomato. PlantSignal. Behav. 7, 807-810. doi: 10.4161/psb.20606
55. Takeda, T., Amano, K., Ohto, M.- A., Nakamura, K., Sato, S., Kato, T., et al. (2006). RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development. Plant Mol. Biol. 61, 165-177. doi: 10.1007/s11103-006- 6265-9
56. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using likelihood, distance, and parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
57. Tatematsu, K., Nakabayashi, K., Kamiya, Y., and Nambara, E. (2008). Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J. 53, 42-52. doi: 10.1111/j.1365-313X.2007.03308.x
58. Tokunaga, H., Kojima, M., Kuroha, T., Ishida, T., Sugimoto, K., Kiba, T., et al. (2012). Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG- dependent pathway in cytokinin activation. Plant J. 69, 355-365. doi: 10.1111/j.1365-313X.2011.04795.x
59. Uberti-Manassero, N. G., Lucero, L. E., Viola, I. L., Vegetti, A. C., and Gonzalez, D. H. (2012). The class I protein AtTCP15 modulates plant development through a pathway that overlaps with the one affected by CIN-like TCP proteins. J. Exp. Bot. 63, 809-823. doi: 10.1093/jxb/err305
60. Uberti Manassero, N. G., Viola, I. L., Welchen, E., and Gonzalez, D. H.(2013). TCP transcription factors: architectures of plant form. Biomol. Concepts 4, 111-127. doi: 10.1515/bmc-2012-0051
61. Uchida, N., Townsley, B., Chung, K., and Sinha, N. (2007). Regulation of SHOOT MERISEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proc. Natl. Acad. Sci. U.S.A. 104, 15953-15958. doi: 10.1073/pnas.0707577104
62. Valsecchi, I., Guittard-Crilat, E., Maldiney, R., Habricot, Y., Lignon, S., Lebrun, R., et al. (2013). The intrinsically disordered C-terminal region of Arabidopsis thaliana TCP8 transcription factor acts both as a transactivation and self-assembly domain. Mol. BioSyst. 9, 2282-2295. doi: 10.1039/C3MB70128J
63. Viola, I., Uberti-Manassero, N., Ripoll, R., and Gonzalez, D. (2011). The Arabidopsis class I TCP transcription factor AtTCP11 is a developmental regulator with distinct DNA-binding properties due to the presence of a threonine residue at position 15 of the TCP domain. Biochem. J. 435, 143-155. doi: 10.1042/BJ20101019
64. Wang, J.-W., Schwab, R., Czech, B., Mica, E., and Weigel, D. (2008). Dual effects of miR156-targeted SPL genes andCYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20, 1231-1243. doi: 10.1105/tpc.108.058180
65. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G. V., and Provart, N. J. (2007). An 'Electronic Fluorescent Pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718. doi: 10.1371/journal.pone.0000718
66. Woody, S., Austin-Phillips, S., Amasino, R., and Krysan, P. (2007). The WiscDsLox T-DNA collection: an Arabidopsis community resource generated by using an improved high-throughput T-DNA sequencing pipeline. J. Plant Res. 120, 157-165. doi: 10.1007/s10265-006-0048-x
67. Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Xu, Y., et al. (2003). Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130, 4097-4107. doi: 10.1242/ dev.00622
68. Yanai, O., Shani, E., Russ, D., and Ori, N. (2011). Gibberellin partly mediates LANCEOLATE activity in tomato. Plant J. 68, 571-582. doi: 10.1111/j.1365-313X.2011.04716.x