Recent advances in the study of prolamin storage protein organization and function

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Holding, David R ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Deletion_mutagenesis; Endosperm; Kafirin; Prolamin; Protein_body; QPM; Storage_protein; Zein

Indexed keywords

EID: 84979583951     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00276     Document Type: Review

References (60)

1. Aboubacar, A., Axtell, J. D., Huang, C. P., and Hamaker, B. R. (2001). A rapid protein digestibility assay for identifying highly digestible sorghum lines. Cereal Chem. 78, 160-165. doi:10.1094/Cchem.2001.78.2.160
2. Coleman, C. E., Clore, A. M., Ranch, J. P., Higgins, R., Lopes, M. A., and Larkins, B. A. (1997). Expression of a mutant alpha-zein creates the floury2 phenotype in transgenic maize. Proc. Natl. Acad. Sci. U.S.A. 94, 7094-7097. doi:10.1073/pnas.94.13.7094
3. Coleman, C. E., and Larkins, B. A. (1999). “The prolamins of maize,” in Seed Proteins, eds P. Shewry and R. Casey (Dordrecht: Kluwer Academic Publishers), 109-139. doi:10.1007/978-94-011-4431-5_6
4. Dannenhoffer, J. M., Bostwick, D. E., Or, E., and Larkins, B. A. (1995). Opaque-15, a maize mutation with properties of a defective opaque-2 modifier. Proc. Natl. Acad. Sci. U.S.A. 92, 1931-1935. doi:10.1073/pnas.92.6.1931
5. Duvick, D. N. (1961). Protein granules of maize endosperm cells. Cereal Chem. 38, 374-385.
6. Esen, A. (1987). A proposed nomenclature for the alcohol-soluble proteins (zeins) of maize (Zea-mays-L). J. Cereal Sci. 5, 117-128. doi:10.1016/S0733-5210(87)80015-2
7. Feng, L. N., Zhu, J., Wang, G., Tang, Y. P., Chen, H. J., Jin, W. B., et al. (2009). Expressional profiling study revealed unique expressional patterns and dramatic expressional divergence of maize alpha-zein super gene family. Plant Mol. Biol. 69, 649-659. doi:10.1007/s11103-008-9444-z
8. Geetha, K. B., Lending, C. R., Lopes, M. A., Wallace, J. C., and Larkins, B. A. (1991). Opaque-2 modifiers increase gamma-zein synthesis and alter its spatial-distribution in maize endosperm. Plant Cell 3, 1207-1219. doi:10.1105/tpc.3.11.1207
9. Geevers, H. O., and Lake, J. K. (1992). “Development of modified opaque-2 maize in South Africa,” in Quality Protein Maize, ed. E. T. Mertz (St. Paul, Minnesota: American Society of Cereal Chemists), 49-78.
10. Gillikin, J. W., Zhang, F., Coleman, C. E., Bass, H. W., Larkins, B. A., and Boston, R. S. (1997). A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane. Plant Physiol. 114, 345-352. doi:10.1104/pp.114.1.345
11. Guo, X., Ronhovde, K., Yuan, L. L., Yao, B., Soundararajan, M. P., Elthon, T., et al. (2012). Pyrophosphate-dependent fructose-6-phosphate 1-phosphotransferase induction and attenuation of hsp gene expression during endosperm modification in quality protein maize. Plant Physiol. 158, 917-929. doi:10.1104/pp.111.191163
12. Guo, X., Yuan, L., Chen, H., Sato, S. J., Clemente, T. E., and Holding, D. R. (2013). Nonredundant function of zeins and their correct stoichiometric ratio drive protein body formation in maize endosperm. Plant Physiol. 162, 1359-1369. doi:10.1104/pp.113.218941
13. Holding, D. R., Hunter, B. G., Chung, T., Gibbon, B. C., Ford, C. F., Bharti, A. K., et al. (2008). Genetic analysis of opaque2 modifier loci in quality protein maize. Theor. Appl. Genet. 117, 157-170. doi:10.1007/s00122-008-0762-y
14. Holding, D. R., Hunter, B. G., Klingler, J. P., Wu, S., Guo, X., Gibbon, B. C., et al. (2011). Characterization of opaque2 modifier QTLs and candidate genes in recombinant inbred lines derived from the K0326Y quality protein maize inbred. Theor. Appl. Gen. 122, 783-794. doi:10.1007/s00122-010-1486-3
15. Holding, D. R., and Larkins, B. A. (2008). Genetic engineering of seed storage proteins. Bioeng. Mol. Biol. Plant Pathw. 1, 107-133. doi:10.1016/S1755-0408(07)01005-3
16. Holding, D. R., Meeley, R. B., Hazebroek, J., Selinger, D., Gruis, F., Jung, R., et al. (2010). Identification and characterization of the maize arogenate dehydrogenase gene family. J. Exp. Bot. 61, 3663-3673. doi:10.1093/Jxb/Erq179
17. Holding, D. R., and Messing, J. (2013). “Evolution, structure, and function of prolamin storage proteins,” in Seed Genomics, ed. P. Becraft (New York: John Wiley & Sons), 139-158.
18. Holding, D. R., Otegui, M. S., Li, B. L., Meeley, R. B., Dam, T., Hunter, B. G., et al. (2007). The maize floury1 gene encodes a novel endoplasmic reticulum protein involved in zein protein body formation. Plant Cell 19, 2569-2582. doi:10.1105/tpc.107/053538
19. Huang, S., Frizzi, A., Florida, C. A., Kruger, D. E., and Luethy, M. H. (2006). High lysine and high tryptophan transgenic maize resulting from the reduction of both 19-and 22-kD alpha-zeins. Plant Mol. Biol. 61, 525-535. doi:10.1007/s11103-006-0027-6
20. Hunter, B. G., Beatty, M. K., Singletary, G. W., Hamaker, B. R., Dilkes, B. P., Larkins, B. A., et al. (2002). Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14, 2591-2612. doi:10.1105/tpc.003905
21. Kim, C. S., Gibbon, B. C., Gillikin, J. W., Larkins, B. A., Boston, R. S., and Jung, R. (2006). The maize Mucronate mutation is a deletion in the 16-kDa gamma-zein gene that induces the unfolded protein response. Plant J. 48, 440-451. doi:10.1111/j.1365-313X.2006.02884.x
22. Kim, C. S., Hunter, B. G., Kraft, J., Boston, R. S., Yans, S., Jung, R., et al. (2004). A defective signal peptide in a 19-kD alpha-zein protein causes the unfolded protein response and an opaque endosperm phenotype in the maize De*-B30 mutant. Plant Physiol. 134, 380-387. doi:10.1104/pp.103.031310
23. Kim, C. S., Woo, Y. M., Clore, A. M., Burnett, R. J., Carneiro, N. P., and Larkins, B. A. (2002). Zein protein interactions, rather than the asymmetric distribution of zein mRNAs on endoplasmic reticulum membranes, influence protein body formation in maize endosperm. Plant Cell 14, 655-672. doi:10.1105/tpc.010431
24. Kriz, A. L. (2009). “Enhancement of amino acid availability in corn grain,” in Molecular Genetic Approaches to Maize Improvement, eds A. L. Kriz and B. A. Larkins (Heidelberg: Springer), 79-89. doi:10.1007/978-3-540-68922-5
25. Kumar, T., Dweikat, I., Sato, S., Ge, Z. X., Nersesian, N., Chen, H., et al. (2012). Modulation of kernel storage proteins in grain sorghum (Sorghum bicolor (L.) Moench). Plant Biotechnol. J. 10, 533-544. doi:10.1111/j.1467-7652.2012.00685.x
26. Lai, J. S., and Messing, J. (2002). Increasing maize seed methionine by mRNA stability. Plant J. 30, 395-402. doi:10.1046/j.1365-313X.2001.01285.x
27. Lending, C. R., and Larkins, B. A. (1989). Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell 1, 1011-1023. doi:10.1105/tpc.1.10.1011
28. Lending, C. R., and Larkins, B. A. (1992). Effect of the floury-2 locus on protein body formation during maize endosperm development. Protoplasma 171, 123-133. doi:10.1007/BF01403727
29. Lopes, M. A., and Larkins, B. A. (1991). Gamma-zein content is related to endosperm modification in Quality Protein Maize. Crop Sci. 31, 1655-1662. doi:10.2135/cropsci1991.0011183X003100060055x
30. Lopes, M. A., and Larkins, B. A. (1995). Genetic-analysis of opaque2 modifier gene activity in maize endosperm. Theor. Appl. Gen. 91, 274-281. doi:10.1007/BF00220889
31. Lopes, M. A., Takasaki, K., Bostwick, D. E., Helentjaris, T., and Larkins, B. A. (1995). Identification of opaque 2 modifier loci in quality protein maize. Mol. Gen. Genet. 247, 603-613. doi:10.1007/BF00290352
32. Maddaloni, M., Donini, G., Balconi, C., Rizzi, E., Gallusci, P., Forlani, F., et al. (1996). The transcriptional activator Opaque-2 controls the expression of a cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms. Mol. Gen. Genet. 250, 647-654. doi:10.1007/BF02174452
33. Mertz, E. T., Nelson, O. E., and Bates, L. S. (1964). Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145, 279-280. doi:10.1126/science.145.3629.279
34. Miclaus, M., Wu, Y. R., Xu, J. H., Dooner, H. K., and Messing, J. (2011a). The maize high-lysine mutant opaque7 Is defective in an acyl-CoA synthetase-like protein. Genetics 189, 1271-1280. doi:10.1534/genetics.111.133918
35. Miclaus, M., Xu, J. H., and Messing, J. (2011b). Differential gene expression and epiregulation of alpha zein gene copies in maize haplotypes. PLoS genetics 7:e1002131. doi:10.1371/journal.pgen.1002131
36. Myers, A. M., James, M. G., Lin, Q. H., Yi, G., Stinard, P. S., Hennen-Bierwagen, T. A., et al. (2011). Maize opaque5 encodes monogalactosyldiacylglycerol synthase and specifically affects galactolipids necessary for amyloplast and chloroplast function. Plant Cell 23, 2331-2347. doi:10.1105/tpc.111.087205
37. Oria, M. P., Hamaker, B. R., Axtell, J. D., and Huang, C. P. (2000). A highly digestible sorghum mutant cultivar exhibits a unique folded structure of endosperm protein bodies. Proc. Natl. Acad. Sci. U.S.A. 97, 5065-5070. doi:10.1073/pnas.080076297
38. Osborne, T. B. (1897). Amount and properties of the proteins of the maize kernel. J. Am. Chem. Soc. 19, 525-532. doi:10.1021/ja02081a002
39. Pastorello, E. A., Farioli, L., Pravettoni, V., Scibilia, J., Conti, A., Fortunato, D., et al. (2009). Maize food allergy: lipid-transfer proteins, endochitinases, and alpha-zein precursor are relevant maize allergens in double-blind placebo-controlled maize-challenge-positive patients. Anal. Bioanal. Chem. 395, 93-102. doi:10.1007/s00216-009-2945-z
40. Peremyslov, V. V., Morgun, E. A., Kurth, E. G., Makarova, K. S., Koonin, E. V., and Dolja, V. V. (2013). Identification of myosin XI receptors in arabidopsis defines a distinct class of transport vesicles. Plant Cell 25, 3022-3038. doi:10.1105/tpc.113.113704
41. Poethig, R. S., Coe, E. H., and Johri, M. M. (1986). Cell lineage patterns in maize embryogenesis-a clonal analysis. Dev. Biol. 117, 392-404. doi:10.1016/0012-1606(86)90308-90308
42. Schmidt, R. J., Burr, F. A., Aukerman, M. J., and Burr, B. (1990). Maize regulatory gene opaque-2 encodes a protein with a leucine-zipper motif that binds to zein DNA. Proc. Natl. Acad. Sci. U.S.A 87, 46-50. doi:10.1073/pnas.87.1.46
43. Segal, G., Song, R. T., and Messing, J. (2003). A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165, 387-397.
44. Shull, J. M., Watterson, J. J., and Kirleis, A. W. (1991). Proposed nomenclature for the alcohol-soluble proteins (Kafirins) of Sorghum bicolor (L Moench) based on molecular-weight, solubility, and structure. J. Agric. Food Chem. 39, 83-87. doi:10.1021/Jf00001a015
45. Soave, C., and Salamini, F. (1984). Organization and regulation of zein genes in maize endosperm. Philos. Trans. R. Soc. Lond. Series B Biol. Sci. 304, 341-343. doi:10.1098/rstb.1984.0029
46. Song, R., Llaca, V., Linton, E., and Messing, J. (2001). Sequence, regulation, and evolution of the maize 22-kD alpha zein gene family. Genome Res. 11, 1817-1825. doi:10.1101/gr.197301
47. Song, R., and Messing, J. (2002). Contiguous genomic DNA sequence comprising the 19-kD zein gene family from maize. Plant Physiol. 130, 1626-1635. doi:10.1104/pp.012179
48. Torrent, M., Alvarez, I., Geli, M. I., Dalcol, I., and Ludevid, D. (1997). Lysine-rich modified gamma-zeins accumulate in protein bodies of transiently transformed maize endosperms. Plant Mol. Biol. 34, 139-149. doi:10.1023/A:1005889314967
49. Tsai, C. Y., Huber, D. M., and Warren, H. L. (1978). Relationship of kernel sink for N to maize productivity. Crop Sci. 18, 399-404. doi:10.2135/cropsci1978.0011183X001800030011x
50. Vasal, S. K., Villegas, E., Bjarnason, M., Gela, W., and Goertz, P. (1980). “Genetic modifiers and breeding strategies in developing hard endosperm opaque2 materials,” in Quality Traits of Maize for Grain and Silage Use, eds W. G. Pollmer and R. H. Phillips (London: Martinus Nijhoff), 37-73.
51. Wallace, J. C., Lopes, M. A., Paiva, E., and Larkins, B. A. (1990). New methods for extraction and quantitation of zeins reveal a high content of gamma-zein in modified ppaque-2 maize. Plant Physiol. 92, 191-196. doi:10.1104/pp.92.1.191
52. Wang, G. F., Wang, F., Wang, G., Wang, F., Zhang, X. W., Zhong, M. Y., et al. (2012). Opaque1 encodes a myosin XI motor protein that is required for endoplasmic reticulum motility and protein body formation in maize endosperm. Plant Cell 24, 3447-3462. doi:10.1105/tpc.112.101360
53. Woo, Y. M., Hu, D. W. N., Larkins, B. A., and Jung, R. (2001). Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13, 2297-2317. doi:10.1105/tpc.13.10.2297
54. Wu, Y., Holding, D. R., and Messing, J. (2010). Gamma-zein is essential for endosperm modification in quality protein maize. Proc. Natl. Acad. Sci. U.S.A. 107, 12810-12815. doi:10.1073/pnas.1004721107
55. Wu, Y., and Messing, J. (2010). RNA interference-mediated change in protein body morphology and seed opacity through loss of different zein proteins. Plant Physiol. 153, 337-347. doi:10.1104/pp.110.154690
56. Wu, Y. R., and Messing, J. (2011). Novel genetic selection system for quantitative trait loci of quality protein maize. Genetics 188, 1019-1022. doi:10.1534/genetics.111.131078
57. Wu, Y., Yuan, L., Guo, X., Holding, D. R., and Messing, J. (2013). Mutation in the seed storage protein kafirin creates a high-value food trait in sorghum. Nat. Commun. 4:2217. doi:10.1038/ncomms3217
58. Xu, J. H., and Messing, J. (2008). Organization of the prolamin gene family provides insight into the evolution of the maize genome and gene duplications in grass species. Proc. Natl. Acad. Sci. U.S.A 105, 14330-14335. doi:10.1073/pnas.0807026105
59. Xu, J. H., and Messing, J. (2009). Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor. Appl. Genet. 119, 1397-1412. doi:10.1007/s00122-009-1143-x
60. Yuan, L., Dou, Y., Kianian, S. F., Zhang, C., and Holding, D. R. (2014). Deletion mutagenesis identifies a haploinsufficient role for γ-zein in opaque2 endosperm modification. Plant Physiol. 164, 119-130. doi:10.1104/pp.113.230961