A comparative glycoproteome study of developing endosperm in the hexose-deficient miniature1 (mn1) seed mutant and its wild type Mn1 in maize

Frontiers in Plant Science

Volumn 5, Issue FEB, 2014, Pages

  Silva Sanchez, Cecilia ^a   Chen, Sixue ^a   Li, Jinxi ^a   Chourey, Prem S ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b CENTER FOR MEDICAL   (United States)

Author keywords

Gene expression; Maize; Seed development; Sugar methabolism; Transfer cells

Indexed keywords

EID: 84901024552     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00063     Document Type: Article

References (71)

1. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Friedberg, I., Osterman, A., et al. (2004). Protein tyrosine phosphatases in the human genome. Cell 117, 699-711. doi: 10.1016/j.cell.2004.05.018
2. Arcalis, E., Stadlmann, J., Marcel, S., Drakakaki, G., Winter, V., Rodriguez, J., et al. (2010). The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol. 153, 693-702. doi: 10.1104/pp.109.152363
3. Barbazuk, W. B., Fu, Y., and McGinnis, K. M. (2008). Genome-wide analysis of alternative splicing in plants: opportunities and challenges. Genome Res. 18, 1381-1392. doi: 10.1101/gr.053678.106
4. Beránek, M., Drsata, J., and Palicka, V. (2001). Inhibitory effect of glycation on catalytic activity of alanine aminotransferase. Mol. Cell. Biochem. 218, 35-39. doi: 10.1023/A:1007280913732
5. Bernard, S. M., and Habash, D. Z. (2009). The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol. 182, 608-620. doi: 10.1111/j.1469-8137.2009.02823.x
6. Bernier, F., and Berna, A. (2001). Germins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiol. Biochem. 39, 545-554. doi: 10.1016/S0981-9428(01)01285-2
7. Boušová, I., Prùchová, Z., Trnková, L., and Dršata, J. (2011). Comparison of glycation of glutathione S-transferase by methylglyoxal, glucose or fructose. Mol. Cell. Biochem. 357, 323-330. doi: 10.1007/s11010-011-0903-5
8. Breen, J., and Bellgard, M. (2010). Germin-like proteins (GLPs) in cereal genomes: gene clustering and dynamic roles in plant defence. Funct. Integr. Genomics. 10, 463-476. doi: 10.1007/s10142-010-0184-1
9. Bykova, N. V., Rampitsch, C., Krokhin, O., Standing, K. G., and Ens, W. (2006). Determination and characterization of site-specific N-glycosylation using MALDI-Qq-TOF tandem mass spectrometry: case study with a plant protease. Anal. Chem. 78, 1093-1103. doi: 10.1021/ac0512711
10. Cheng, W. H., and Chourey, P. S. (1999). Genetic evidence that invertase-mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize. Theor. Appl. Genet. 98, 485-495. doi: 10.1007/s001220051096
11. Cheng, W. H., Taliercio, E. W., and Chourey, P. S. (1996). The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8, 971-983.
12. Chou, K. C., and Shen, H. B. (2010). Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5:e11335. doi: 10.1371/journal.pone.0011335
13. Chourey, P. S., Jain, M., Li, Q. B., and Carlson, S. J. (2006). Genetic control of cell wall invertase in developing endosperm of maize. Planta 223, 159-167. doi: 10.1007/s00425-005-0039-5
14. Chourey, P. S., Li, Q. B., and Cevallos-Cevallos, J. (2012). Pleiotropy and its dissection through a metabolic gene Miniature1 (Mn1) that encodes a cell wall invertase in developing seeds. Plant Sci. 184, 45-53. doi: 10.1016/j.plantsci.2011.12.011
15. Davis, R. W., Smith, J. D., and Cobb, B. G. (1990). A light and electron-microscope investigation of the transfer cell region of maize caryopses. Can. J. Bot. 68, 471-479. doi: 10.1139/b90-063
16. Denecke, J., Goldman, M. H., Demolder, J., Seurinck, J., and Botterman, J. (1991). The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3, 1025-1035.
17. Deng, Z. Y., Gong, C. Y., and Wang, T. (2013). Use of proteomics to understand seed development in rice. Proteomics 13, 1784-1800. doi: 10.1002/pmic.201200389
18. Eimert, K., Villand, P., Kilian, A., and Kleczkowski, L. A. (1996). Cloning and characterization of several cDNAs for UDP-glucose pyrophosphorylase from barley (Hordeum vulgare) tissues. Gene 170, 227-232. doi: 10.1016/0378-1119(95)00873-X
19. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016. doi: 10.1006/jmbi.2000.3903
20. Grevesse, C., Lepoivre, P., and Jijakli, M. H. (2003). Characterization of the exoglucanase-encoding gene PaEXG2 and study of its role in the biocontrol activity of Pichia anomala strain K. Phytopathology 93, 1145-1152. doi: 10.1094/PHYTO.2003.93.9.1145
21. Gucciardo, S., Wisniewski, J. P., Brewin, N. J., and Bornemann, S. (2007). A germin-like protein with superoxide dismutase activity in pea nodules with high protein sequence identity to a putative rhicadhesin receptor. J. Exp. Bot. 58, 1161-1171. doi: 10.1093/jxb/erl282
22. Haltiwanger, R. S., Kelly, W. G., Roquemore, E. P., Blomberg, M. A., Dong, L. Y., Kreppel, L., et al. (1992). Glycosylation of nuclear and cytoplasmic proteins is ubiquitous and dynamic. Biochem. Soc. Trans. 20, 264-269.
23. Howell, S. H. (2013). Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64, 477-499. doi: 10.1146/annurev-arplant-050312-120053
24. Hurkman, W. J., and Tanaka, C. K. (1986). Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol. 81, 802-806. doi: 10.1104/pp.81.3.802
25. Kang, B. H., Xiong, Y., Williams, D. S., Pozueta-Romero, D., and Chourey, P. S. (2009). Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Physiol. 151, 1366-1376. doi: 10.1104/pp.109.142331
26. Kleczkowski, L. A., Geisler, M., Ciereszko, I., and Johansson, H. (2004). UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol. 134, 912-918. doi: 10.1104/pp.103.036053
27. Koles, K., Lim, J. M., Aoki, K., Porterfield, M., Tiemeyer, M., Wells, L., et al. (2007). Identification of N-glycosylated proteins from the central nervous system of Drosophila melanogaster. Glycobiology 17, 1388-1403. doi: 10.1093/glycob/cwm097
28. Kornfeld, R., and Kornfeld, S. (1985). Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 631-664. doi: 10.1146/annurev.bi.54.070185.003215
29. Koseki, T., Miwa, Y., Mese, Y., Miyanaga, A., Fushinobu, S., Wakagi, T., et al. (2006). Mutational analysis of N-glycosylation recognition sites on the biochemical properties of Aspergillus kawachii alpha-L-arabinofuranosidase 54. Biochim. Biophys. Acta 1760, 1458-1464. doi: 10.1016/j.bbagen.2006.04.009
30. Kriechbaumer, V., von Löffelholz, O., and Abell, B. M. (2012). Chaperone receptors: guiding proteins to intracellular compartments. Protoplasma 249, 21-30. doi: 10.1007/s00709-011-0270-9
31. LeClere, S., Schmelz, E. A., and Chourey, P. S. (2008). Cell wall invertase-deficient miniature 1 kernels have altered phytohormone levels. Phytochemistry 69, 692-699. doi: 10.1016/j.phytochem.2007.09.011
32. LeClere, S., Schmelz, E. A., and Chourey, P. S. (2010). Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol. 153, 306-318. doi: 10.1104/pp.110.155226
33. Li, J., Ferraris, J. D., Yu, D., Singh, T., Izumi, Y., Wang, G., et al. (2012a). Proteomic analysis of high NaCl-induced changes in abundance of nuclear proteins. Physiol. Genomics 44, 1063-1071. doi: 10.1152/physiolgenomics.00068.2012
34. Li, W., Gao, Y., Xu, H., Zhang, Y., and Wang, J. (2012b). A proteomic analysis of seed development in Brassica campestri L. PLoS ONE 7:e50290. doi: 10.1371/journal.pone.0050290
35. Liu, J. X., and Howell, S. H. (2010). Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22, 2930-2942. doi: 10.1105/tpc.110.078154
36. Love, D. C., and Hanover, J. A. (2005). The hexosamine signaling pathway: deciphering the "O-GlcNAc code. " Sci. STKE 2005, re13. doi: 10.1126/stke.3122005re13
37. Lu, G. (2008). Regulation of Local Signaling by Type 2c Protein Phosphatases. Dissertations, Academic, UCLA, Molecular Cellular, and Integrative Physiology, 66-67.
38. Matsushita-Morita, M., Tada, S., Suzuki, S., Hattori, R., Marui, J., Furukawa, I., et al. (2011). Overexpression and characterization of an extracellular leucine aminopeptidase from Aspergillus oryzae. Curr. Microbiol. 62, 557-564. doi: 10.1007/s00284-010-9744-9
39. Miller, M. E., and Chourey, P. S. (1992). The maize invertase-deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell. 4, 297-305.
40. Müntz, K. (1996). Proteases and proteolytic cleavage of storage proteins in developing and germinating dicotyledonous seeds. J. Exp. Botany. 47, 605-622. doi: 10.1093/jxb/47.5.605
41. Offler, C. E., McCurdy, D. W., Patrick, J. W., and Talbot, M. J. (2003). Transfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54, 431-454. doi: 10.1146/annurev.arplant.54.031902.134812
42. Overath, T., Kuckelkorn, U., Henklein, P., Strehl, B., Bonar, D., Kloss, A., et al. (2012). Mapping of O-GlcNAc sites of 20 s proteasome subunits and Hsp90 by a novel biotin-cystamine tag. Mol. Cell Proteomics 11, 467-477. doi: 10.1074/mcp.M111.015966
43. Porras, F., Urrea, F., Ortiz, B., Martínez-Cairo, S., Bouquelet, S., Martínez, G., et al. (2005). Isolation of the receptor for the Amaranthus leucocarpus lectin from human T lymphocytes. Biochim. Biophys. Acta 1724, 155-162. doi: 10.1016/j.bbagen.2005.03.014
44. Radhamony, R. N., and Theg, S. M. (2006). Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell. Biol. 16, 385-387. doi: 10.1016/j.tcb.2006.06.003
45. Rodríguez-López, M., Baroja-Fernández, E., Zandueta-Criado, A., Moreno-Bruna, B., Muñoz, F. J., Akazawa, T., et al. (2001). Two isoforms of a nucleotide-sugar pyrophosphatase/phosphodiesterase from barley leaves (Hordeum vulgare l.) are distinct oligomers of hvglp1, a germin-like protein. FEBS Lett. 490, 44-48.
46. Romdhan, I. B., Fendri, A., Frikha, F., Gargouri, A., and Belghith, H. (2012). Purification, physico-chemical and kinetic properties of the deglycosylated Talaromyces thermophilus lipase. Int. J. Biol. Macromol. 51, 892-900. doi: 10.1016/j.ijbiomac.2012.06.034
47. Ruan, Y. L., Jin, Y., Yang, Y. J., Li, G. J., and Boyer, J. S. (2010). Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant. 3, 942-955. doi: 10.1093/mp/ssq044
48. Ruiz-May, E., Thannhauser, T. W., Zhang, S., and Rose, J. K. C. (2012). Analytical technologies for identification and characterization of the plant N-glycoproteome. Front. Plant Sci. 3:150. doi: 10.3389/fpls.2012.00150
49. Sadanandom, A., Bailey, M., Ewan, R., Lee, J., and Nelis, S. (2012). The ubiquitin-proteasome system: central modifier of plant signalling. New Phytol. 196, 13-28. doi: 10.1111/j.1469-8137.2012.04266.x
50. Satoh, K., Takeuchi, M., Oda, Y., Deguchi-Tawarada, M., Sakamoto, Y., Matsubara, K., et al. (2002). Identification of activity-regulated proteins in the postsynaptic density fraction. Genes Cells 7, 187-197. doi: 10.1046/j.1356-9597.2001.00505.x
51. Sheffield, J., Taylor, N., Fauquet, C., and Chen, S. (2006). The cassava (Manihot esculenta Crantz) root proteome: protein identification and differential expression. Proteomics 6, 1588-1598. doi: 10.1002/pmic.200500503
52. Shin, D., and Park, C. (2004). N-terminal extension of canine glutamine synthetase created by splicing alters its enzymatic property. J. Biol. Chem. 279, 1184-1190. doi: 10.1074/jbc.M309940200
53. Silva-Sanchez, C., Chen, S., Zhu, N., Li, Q.-B., and Chourey, P. S. (2013). Proteomic comparison of basal endosperm in maize miniature1 mutant and its wild-type Mn1. Front. Plant Sci. 4:211. doi: 10.3389/fpls.2013.00211
54. Solórzano, C., Angel Mayoral. M., de los Angeles, C. M., Berumen, J., Guevara, J., Raúl Chávez, F., et al. (2012). Overexpression of glycosylated proteins in cervical cancer recognized by the Machaerocereus eruca agglutinin. Folia Histochem. Cytobiol. 50, 398-406. doi: 10.5603/FHC.2012.0054
55. Spadiut, O., Rossetti, L., Dietzsch, C., and Herwig, C. (2012). Purification of a recombinant plant peroxidase produced in Pichia pastoris by a simple 2-step strategy. Protein Expr. Purif. 86, 89-97. doi: 10.1016/j.pep.2012.09.008
56. Spielbauer, G., Li, L., Romisch-Margl, L., Do, T., Fouquet, R., Fernie, A. R., et al. (2013). Chlorplast-localized 6-phosphogluconate dehydrogensae is critical for maize starch accumulation. J. Exp. Bot. 64, 2231-2242. doi: 10.1093/jxb/ert082
57. Spiro, R. G. (2002). Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R-56R. doi: 10.1093/glycob/12.4.43R
58. Spiro, R. G., Spiro, M. J., and Bhoyroo, V. D. (1983). Studies on the regulation of the biosynthesis of glucose-containing oligosaccharide-lipids. Effect of energy deprivation. J. Biol. Chem. 258, 9469-9476.
59. Tatusov, R. L., Fedorova, N. D., Jackson, J. D., Jacobs, A. R., Kiryutin, B., Koonin, E. V., et al. (2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. doi: 10.1186/1471-2105-4-41
60. Tawde, M. D., and Freimuth, P. (2012). Toxic misfolding of Arabidopsis cellulases in the secretory pathway of Pichia pastoris. Protein Expr. Purif. 85, 211-217. doi: 10.1016/j.pep.2012.08.009
61. Thornton, T. M., Swain, S. M., and Olszewski, N. E. (1999). Gibberellin signal transduction presents ellipsisthe SPY who O-GlcNAc'd me. Trends Plant Sci. 4, 424-428. doi: 10.1016/S1360-1385(99)01485-5
62. Vartapetian, A. B., Tuzhikov, A. I., Chichkova, N. V., Taliansky, M., and Wolpert, T. J. (2011). A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ. 18, 1289-1297. doi: 10.1038/cdd.2011.49
63. Vaughn, K. C., Talbot, M. J., Offler, C. E., and McCurdy, D. W. (2007). Wall ingrowths in epidermal transfer cells of Vicia faba cotyledons are modified primary walls marked by localized accumulations of arabinogalactan proteins. Plant Cell Physiol. 48, 159-168. doi: 10.1093/pcp/pcl047
64. Vitale, A., and Boston, R. S. (2008). Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9, 1581-1588. doi: 10.1111/j.1600-0854.2008.00780.x
65. Xue, Y. L., Miyakawa, T., Sawano, Y., and Tanokura, M. (2012). Cloning of genes and enzymatic characterizations of novel dioscorin isoforms from Dioscorea japonica. Plant Sci. 183, 14-19. doi: 10.1016/j.plantsci.2011.10.021
66. Zhang, M., Gaschen, B., Blay, W., Foley, B., Haigwood, N., Kuiken, C., et al. (2004). Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14, 1229-1246. doi: 10.1093/glycob/cwh106
67. Zhang, M., and Schekman, R. (2013). Unconventional secretion, unconventional solutions. Scie 340, 559-561. doi: 10.1126/science.1234740
68. Zhou, H., Liu, Y., Chui, J., Guo, K., Shun, Q., Lu, W., et al. (2007). Investigation on glycosylation patterns of proteins from human liver cancer cell lines based on the multiplexed proteomics technology. Arch. Biochem. Biophys. 459, 70-78. doi: 10.1016/j.abb.2006.10.027
69. Zhu, J., Chen, S., Alvarez, S., Asirvatham, V. S., Schachtman, D. P., Wu, Y., et al. (2006). Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol. 140, 311-325. doi: 10.1104/pp.105.070219
70. Zhu, M., Simons, B., Zhu, N., Oppenheimer, D. G., and Chen, S. (2010). Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging. J. Proteomics 73, 790-805. doi: 10.1016/j.jprot.2009.11.002
71. Zuppini, A., Navazio, L., and Mariani, P. (2004). Endoplasmic reticulum stress-induced programmed cell death in soybean cells. J. Cell Sci. 117, 2591-2598. doi: 10.1242/jcs.01126