Characterization of a gene encoding clathrin heavy chain in maize up-regulated by salicylic acid, abscisic acid and high boron supply

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 15179-15198

  Zeng, Mu Heng ^a   Liu, Sheng Hong ^a   Yang, Miao Xian ^a   Zhang, Ya Jun ^a   Liang, Jia Yong ^a   Wan, Xiao Rong ^a   Liang, Hong ^a  

^a ZHONGKAI UNIVERSITY OF AGRICULTURE AND ENGINEERING   (China)

Author keywords

Clathrin heavy chain; Gene cloning and expression; Maize (Zea mays L.); Salicylic acid and abiotic stresses

Indexed keywords

ABSCISIC ACID; BORON; CLATHRIN HEAVY CHAIN; SALICYLIC ACID; SODIUM AZIDE;

ABSCISIC ACID RESPONSIVE ELEMENT; ARABIDOPSIS; ARTICLE; CHC1 GENE; CHC2 GENE; COLD SENSITIVITY; COLD STRESS; CONTROLLED STUDY; DNA STRUCTURE; DOWN REGULATION; ENDOCYTOSIS; ENERGY METABOLISM; EXON; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC SIMILARITY; INTRON; MAIZE; MOLECULAR CLONING; MONOCOT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT DEFENSE; PLANT ROOT; PROMOTER REGION; PROTEIN FUNCTION; SALICYLIC ACID RESPONSIVE ELEMENT; SEEDLING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84880761230     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140715179     Document Type: Article

References (57)

1. Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature 2003, 422, 37-44.
2. Murphy, A.S.; Bandyopadhyay, A.; Holstein, S.E.; Peer, W.A. Endocytotic cycling of PM proteins. Annu. Rev. Plant Biol. 2005, 56, 221-251.
3. Wieffer, M.; Maritzen, T.; Haucke, V. SnapShot: Endocytic trafficking. Cell 2009, 137, e381-e383.
4. McMahon, H.T.; Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2011, 12, 517-533.
5. Chen, X.; Irani, N.G.; Friml, J. Clathrin-mediated endocytosis: The gateway into plant cells. Curr. Opin. Plant Biol. 2011, 14, 674-682.
6. Adam, T.; Bouhidel, K.; Der, C.; Robert, F.; Najid, A.; Simon-Plas, F.; Leborgne-Castel, N. Constitutive expression of clathrin hub hinders elicitor-induced clathrin-mediated endocytosis and defense gene expression in plant cells. FEBS Lett. 2012, 586, 3293-3298.
7. Pearse, B.M. Clathrin: A unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl. Acad. Sci. USA 1976, 73, 1255-1259.
8. Kirchhausen, T. Imaging endocytic clathrin structures in living cells. Trends Cell Biol. 2009, 19, 596-605.
9. Dhonukshe, P.; Aniento, F.; Hwang, I.; Robinson, D.G.; Mravec, J.; Stierhof, Y.D.; Friml, J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 2007, 17, 520-527.
10. Robert, S.; Kleine-Vehn, J.; Barbez, E.; Sauer, M.; Paciorek, T.; Baster, P.; Vanneste, S.; Zhang, J.; Simon, S.; Covanova, M. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 2010, 143, 111-121.
11. Kitakura, S.; Vanneste, S.; Robert, S.; Lofke, C.; Teichmann, T.; Tanaka, H.; Friml, J. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 2011, 23, 1920-1931.
12. Blackbourn, H.D.; Jackson, A.P. Plant clathrin heavy chain: Sequence analysis and restricted localisation in growing pollen tubes. J. Cell Sci. 1996, 109, 777-787.
13. Fujimoto, M.; Arimura, S.; Ueda, T.; Takanashi, H.; Hayashi, Y.; Nakano, A.; Tsutsumi, N. Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc. Natl. Acad. Sci. USA 2010, 107, 6094-6099.
14. Food and Agriculture Organization of the United Nations. Available online: http://faostat.fao.org (accessed on 31 December 2008).
15. Tester, M.; Langridge, P. Breeding technologies to increase crop production in a changing world. Science 2010, 327, 818-822.
16. Lescot, M.; Ddhais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; van de Peer, Y.; Rouzd, P.; Rombauts, S. PlantCARE: A database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002, 30, 325-327.
17. Kirchhausen, T.; Harrison, S.C.; Chow, E.P.; Mattaliano, R.J.; Ramachandran, K.L.; Smart, J.; Brosius, J. Clathrin heavy chain: Molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 1987, 84, 8805-8809.
18. Lemmon, S.K.; Pellicena-Palle, A.; Conley, K.; Freund, C.L. Sequence of the clathrin heavy chain from Saccharomyces cerevisiae and requirement of the COOH terminus for clathrin function. J. Cell Biol. 1991, 112, 65-80.
19. Doge, G.R.; Kovalszky, I.; McBride, O.W.; Yi, H.F.; Chu, M.; Saitta, B.; Stokes, D.; Iozzo, R.V. Human clathrin heavy chain (CLTL): Partial molecular cloning, expression, and mapping of the gene to human chromosome 17q11-qter. Genomics 1991, 11, 174-178.
20. Sirotkin, H.; Morrow, B.; DasGupta, R.; Goldberg, R.; Patanjali, S.R.; Shi, G.; Cannizzaro, L.; Shprintzen, R.; Weissman S.M.; Kucherlapati, R. Isolation of a new clathrin heavy chain gene with muscle-specific expression from the region commonly deleted in velo-cardio-facial syndrome. Hum. Mol. Genet. 1996, 5, 617-624.
21. Bazinet, C.; Katzen, A.L.; Morgan, M.; Mahowald, A.P.; Lemmon, S.K. The Drosophila clathrin heavy chain gene: Clathrin function is essential in a multicellular organism. Genetics 1993, 134, 1119-1134.
22. Wingen, C.; Stumpges, B.; Hoch, M.; Behr, M. Expression and localization of clathrin heavy chain in Drosophila melanogaster. Gene Expr. Patterns 2009, 9, 549-554.
23. Hölzenspies, J.J.; Roelen, B.A.J.; Colenbrander, B.; Romijn, R.A.P.; Hemrika, W.; Stoorvogel, W.; van Haeften, T. Clathrin is essential for meiotic spindle function in oocytes. Reproduction 2010, 140, 223-233.
24. Nathke, I.S.; Heuser, J.; Lupas, A.; Stockton, J.; Turck, C.W.; Brodsky, F.M. Folding and trimerisation of clathrin subunits at the triskelion hub. Cell 1992, 68, 899-910.
25. Tamura, K.; Dudley, J.; Nei, M.; Kumar, S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24, 1596-1599.
26. Bannai, H.; Tamada, Y.; Maruyama, O.; Nakai, K.; Miyano, S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 2002, 18, 298-305.
27. Bari, R.; Jones, J.D. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69, 473-488.
28. An, C.; Mou, Z. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 2011, 53, 412-428.
29. Vernooij, B.; Friedrich, L.; Morse, A.; Rest, R.; Kolditz-Jawahar, R.; Ward, E.; Uknef, S.; Kessmann H.; Ryalf, J. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required for signal transduction. Plant Cell 1994, 6, 959-965.
30. Pérez-Gómez, J.; Moore I. Plant endocytosis: It is clathrin after all. Curr. Biol. 2007, 17, R217-R219.
31. Geldner, N.; Jurgens, G. Endocytosis in signalling and development. Curr. Opin. Plant Biol. 2006, 9, 589-594.
32. Holstein, S.E. Clathrin and plant endocytosis. Traffic 2002, 3, 614-620.
33. Dhonukshe, P.; Tanaka, H.; Goh, T.; Ebine, K.; Mähönen, A.P.; Prasad, K.; Blilou, I.; Geldner, N.; Xu, J.; Uemura, T.; et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 2008, 456, 962-966.
34. Boutté, Y.; Frescatada-Rosa, M.; Men, S.; Chow, C.M.; Ebine, K.; Gustavsson, A.; Johansson, L.; Ueda, T.; Moore, I.; Jurgens, G.; et al. Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J. 2010, 29, 546-558.
35. Takeda, S.; Gapper, C.; Kaya, H.; Bell, E.; Kuchitsu, K.; Dolan, L. Local positive feedback regulation determines cell shape in root hair cells. Science 2008, 319, 1241-1244.
36. Zhao, Y.; Yan, A.; Feijó, J.A.; Furutani, M.; Takenawa, T.; Hwang, I.; Fu, Y.; Yang, Z. Phosphoinositides regulate clathrindependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. Plant Cell 2010, 22, 4031-4044.
37. Ivanov, R.; Gaude, T. Endocytosis and endosomal regulation of the S-receptor kinase during the self-incompatibility response in Brassica oleracea. Plant Cell 2009, 21, 2107-2117.
38. Robatzek, S.; Chinchilla, D.; Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 2006, 20, 537-542.
39. + channel and its recycling to the plasma membrane. Curr. Biol. 2007, 17, 1396-1402.
40. Takano, J.; Miwa, K.; Yuan, L.; von Wirén, N.; Fujiwara, T. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl. Acad. Sci. USA 2005, 102, 12276-12281.
41. Takano, J.; Tanaka, M.; Toyoda, A.; Miwa, K.; Kasai, K.; Fuji, K.; Onouchi, H.; Naito, S.; Fujiwara, T. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. USA 2010, 107, 5220-5225.
42. Onelli, E.; Prescianotto-Baschong, C.; Caccianiga, M.; Moscatelli, A. Clathrin-dependent and independent endocytic pathways in tobacco protoplasts revealed by labeling with charged nanogold. J. Exp. Bot. 2008, 59, 3051-3068.
43. Prescianotto-Baschong, C.; Riezman, H. Morphology of the yeast endocytic pathway. Mol. Biol. Cell 1998, 9, 173-189.
44. Baluska, F.; Hlavacka, A.; Samaj, J.; Palme, K.; Robinson, D.G.; Matoh, T.; McCurdy, D.; Menzel, D.; Volkmann, D. F-actin dependent endocytosis of cell wall pectins in meristematic root cells. Insights from Brefeldin A-induced compartments. Plant Physiol. 2002, 130, 422-431.
45. Koornnef, A.; Pieterse, C.M. Cross talk in defence signaling. Plant Physiol. 2008, 146, 839-844.
46. Mika, A.; Boenisch, M.J.; Hopff, D.; Luthje S. Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors. J. Exp. Bot. 2010, 61, 831-841.
47. Leborgne-Castel, N.; Adam, T.; Bouhidel, K. Endocytosis in plant-microbe interactions. Protoplasma 2010, 247, 177-193.
48. Leborgne-Castel, N.; Lherminier, J.; Der, C.; Fromentin, J.; Houot, V.; Simon-Plas, F. The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in Bright Yellow-2 tobacco cells. Plant Physiol. 2008, 146, 1255-1266.
49. Banbury, D.N.; Oakley, J.D.; Sessions, R.B.; Banting, G. Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. J. Biol. Chem. 2003, 278, 12022-12028.
50. Murashige, T.; Skoog, F. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant. 1962, 15, 473-497.
51. Wan, X.R.; Li, L. Molecular cloning and characterization of a dehydration-inducible cDNA encoding a putative 9-cis-epoxycarotenoid dioxygenase in Arachis hypogaea L. DNA Seq. 2005, 16, 217-223.
52. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215: 403-410.
53. Schwede, T.; Kopp, J.; Guex, N.; Peitsch, M.C. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 2003, 31, 3381-3385.
54. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modeling. Bioinformatics 2006, 22, 195-201.
55. Muller, P.Y.; Janovjak, H.; Miserez, A.R.; Dobbie, Z. Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 2002, 32, 1372-1379.
56. Jahn, R.; Lang, T.; Sudhof, T.C. Membrane fusion. Cell 2003, 112, 519-533.
57. Surpin, M.; Raikhel, N. Traffic jams affect plant development and signal transduction. Nat. Rev. Mol. Cell Biol. 2004, 5, 100-109.