Calmodulin-related CML24 interacts with ATG4b and affects autophagy progression in Arabidopsis

Plant Journal

Volumn 73, Issue 2, 2013, Pages 325-335

  Tsai, Yu Chang ^a   Koo, Yeonjong ^a   Delk, Nikkí A ^a   Gehl, Bernadette ^a   Braam, Janet ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

Abiotic stress; Calcium signaling; Calmodulin like; Darkness; Environmental stress; Macroautophagy; Protein protein interaction; Starvation

Indexed keywords

ABIOTIC STRESS; CALCIUM SIGNALING; CALMODULIN-LIKE; DARKNESS; ENVIRONMENTAL STRESS; MACROAUTOPHAGY; PROTEIN-PROTEIN INTERACTIONS; STARVATION;

MOLECULAR BIOLOGY; TISSUE CULTURE; CALCIUM; PROTEINS;

CALMODULIN;

ARABIDOPSIS; EUKARYOTA; NICOTIANA TABACUM;

ARABIDOPSIS PROTEIN; ATG4 PROTEIN, ARABIDOPSIS; ATG4B PROTEIN, ARABIDOPSIS; CALCIUM BINDING PROTEIN; CYSTEINE PROTEINASE; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; RECOMBINANT PROTEIN; TCH2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLASMID; TWO HYBRID SYSTEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM-BINDING PROTEINS; CYSTEINE PROTEASES; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; PLASMIDS; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84872501497     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12043     Document Type: Article

References (43)

1. Bassham, D.C., Laport, M., Marty, F., Moriyasu, Y., Ohsumi, Y., Olsen, L.J. and Yoshimoto, K. (2006) Autophagy in development and stress responses of plants. Autophagy, 2, 2-11.
2. Braam, J. (1992a) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc. Natl Acad. Sci. USA, 89, 3213-3216.
3. Braam, J. (1992b) Regulation of expression of calmodulin and calmodulin-related genes by environmental stimuli in plants. Cell Calcium, 13, 457-463.
4. Braam, J. and Davis, R.W. (1990) Rain-, wind-and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell, 60, 357-364.
5. Brouquisse, R., Gaudillere, J.P. and Raymond, P. (1998) Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol. 117, 1281-1291.
6. Chin, D. and Means, A.R. (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10, 322-328.
7. Chung, T., Phillips, A.R. and Vierstra, R.D. (2010) ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. Plant J. 62, 483-493.
8. Contento, A.L., Xiong, Y. and Bassham, D.C. (2005) Visualization of auto-phagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J. 42, 598-608.
9. 2+ sensor that functions in responses to ABA, day length and ion stress. Plant Physiol. 139, 240-253.
10. James, P., Halladay, J. and Craig, E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
11. Kang, H.-G. and Klessig, D.F. (2005) Salicylic acid-inducible Arabidopsis CK2-like activity phosphorylates TGA2. Plant Mol. Biol. 57, 541-557.
12. Kang, H.-G., Kuhl, J.C., Kachroo, P. and Klessig, D.F. (2008) CRT1, an Ara-bidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to turnip crinkle virus. Cell Host Microbe, 3, 48-57.
13. Khan, A.R., Johnson, K.A., Braam, J. and James, M.N.G. (1997) Comparative modeling of the three-dimensional structure of the calmodulin-related TCH2 protein from Arabidopsis. Proteins, 27, 144-153.
14. Klionsky, D.J. (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8, 931-937.
15. Krisako, T., Ichimura, Y., Okada, H., Kabeya, Y., Mizushima, N., Yoshimori, T., Ohsumi, M., Takao, T., Noda, T. and Ohsumi, Y. (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 151, 263-276.
16. Kumanomidou, T., Mizushima, T., Komatsu, M., Suzuki, A., Tanida, I., Sou, Y.S., Ueno, T., Kominami, E., Tanaka, K. and Yamane, T. (2006) The crystal structure of human ATG4b, a processing and de-conjugating enzymes for autophagosome-forming modifiers. J. Mol. Biol. 355, 612-618.
17. Lee, D., Polisensky, D.H. and Braam, J. (2005) Genome-wide identification of touch-and darkness-regulated Arabidopsis genes: a focus on calmod-ulin-like and XTH genes. New Phytol. 165, 429-444.
18. Martínez-Priego, L., Donaire, L., Barajas, D. and Llave, C. (2008) Silencing suppressor activity of the Tobacco rattle virus-encoded 16-kDa protein and interference with endogenous small RNA-guided regulatory pathways. Virology. 376, 346-356.
19. McCormack, E. and Braam, J. (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol. 159, 585-598.
20. McCormack, E., Tsai, Y.-C. and Braam, J. (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci. 10, 383-389.
21. Michael, T.P., Mockler, T.C., Breton, G. et al. (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet. 4, e14.
22. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497.
23. Nakatogawa, H., Ichimura, Y. and Ohsumi, Y. (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell, 130, 165-178.
24. Nakatogawa, H., Suzuki, K., Kamada, Y. and Ohsumi, Y. (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10, 458-467.
25. Noda, T., Fujita, N. and Yoshimori, T. (2009) The late stages of autophagy: how does the end begin? Cell Death Differ. 16, 984-990.
26. Ohsumi, M. (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. 2, 211-216.
27. Phillips, A.R., Suttangkakul, A. and Vierstra, R.D. (2008) The ATG12-conju-gating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics, 178, 1339-1353.
28. Polisensky, D.H. and Braam, J. (1996) Cold-shock regulation of the Arabid-opsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol. 111, 1271-1279.
29. Rose, T.L., Bonneau, L., Der, C., Marty-Mazars, D. and Marty, F. (2006) Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol. Cell, 98, 53-67.
30. Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L. and Elazar, Z. (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 26, 1749-1760.
31. Sou, Y.S., Waguri, S., Iwata, J. et al. (2008) The Atg8 conjugation system is indispensable for proper development of autophagosome membranes in mice. Mol. Biol. Cell, 19, 4762-4775.
32. A receptor-associated protein-phospholipid conjugates. J. Cell Biol. 279, 36268-36276.
33. Thompson, A.R. and Vierstra, R.D. (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr. Opin. Plant Biol. 8, 165-173.
34. Thompson, A.R., Doelling, J.H., Suttangkakul, A. and Vierstra, R.D. (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138, 2097-2110.
35. Tsai, Y.-C., Delk, N., Chowdhury, N.I. and Braam, J. (2007) Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering. Plant Signal. Behav. 2, 446-454.
36. 13C nuclear magnetic resonance study. Planta, 231, 1495-1504.
37. Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T. and Mak-ino, A. (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol. 149, 885-893.
38. Wang, Y., Wang, B., Gilroy, S., Chehab, E.W. and Braam, J. (2011) CML24 is involved in root mechanoresponses and cortical microtubule orientation in Arabidopsis. J. Plant Growth Regul. 30, 467-479.
39. Xiao, S., Gao, W., Chen, Q.-F., Chan, S.-W., Zheng, S.-X., Ma, J., Wang, M., Welti, R. and Chye, M.-L. (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell, 22, 1463-1482.
40. Xie, Z., Nair, U. and Klionsky, D.J. (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol. Biol. Cell, 19, 3290-3298.
41. Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T. and Ohsumi, Y. (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjuga-tion by ATG4s are essential for plant autophagy. Plant Cell, 16, 2967-2983.
42. Zimmermann, P., Hennig, L. and Gruissem, W. (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci. 10, 407-409.
43. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.