Maize ribosome-inactivating proteins (RIPs) with distinct expression patterns have similar requirements for proenzyme activation

Journal of Experimental Botany

Volumn 55, Issue 406, 2004, Pages 2219-2233

  Bass, Hank W ^a   Krawetz, Julie E ^b   Obrian, Gregory R ^b   Zinselmeier, Christopher ^c   Habben, Jeffrey E ^c   Boston, Rebecca S ^b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c PIONEER HI BRED INTERNATIONAL INC   (United States)

Author keywords

Maize; Ribosome inactivating protein; Toxin; Translation; Water stress

Indexed keywords

BIOASSAY; BIODIVERSITY; ENZYME KINETICS; GENES; POLYPEPTIDES; PROTEINS; RNA;

ACIDIC RESIDUES; HOLOENZYMES; PROENZYME ACTIVATION; RIBOSOME-INACTIVATING PROTEINS (RIP);

CROPS;

ENZYME PRECURSOR; PLANT DNA; PLANT RNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; COMPARATIVE STUDY; ENZYME ACTIVATION; GENETICS; ISOLATION AND PURIFICATION; MAIZE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RESTRICTION MAPPING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DNA, PLANT; ENZYME ACTIVATION; ENZYME PRECURSORS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; RESTRICTION MAPPING; RNA, PLANT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; ZEA MAYS;

EMBRYOPHYTA; ZEA MAYS;

EID: 5144226834     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/erh243     Document Type: Article

References (94)

1. Ahn S, Tanksley SD. 1993. Comparative linkage maps of the rice and maize genomes. Proceedings of the National Academy of Sciences, USA 90, 7980-7984.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1992. Current protocols in molecular biology. New York: Greene Publishing Associates, Wiley-Interscience.
3. Barbieri L, Stirpe F. 1982. Ribosome-inactivating proteins from plants: properties and possible uses. Cancer Survey 1, 489-520.
4. Barbieri L, Aron GM, Irvin JD, Stirpe F. 1982. Purification and partial characterization of another form of the antiviral protein from the seeds of Phytolacca americana L. (pokeweed). Biochemical Journal 203, 55-59.
5. Bass HW, OBrian GR, Boston RS. 1995. Cloning and sequencing of a second ribosome-inactivating protein gene from maize (Zea mays L.). Plant Physiology 107, 661-662.
6. Bass HW, Goode JH, Greene TW, Boston RS. 1994. Control of ribosome-inactivating protein (RIP) RNA levels during maize seed development. Plant Science 101, 17-30.
7. Bass HW, Webster C, OBrian GR, Roberts JK, Boston RS. 1992. A maize ribosome-inactivating protein is controlled by the transcriptional activator Opaque-2. The Plant Cell 4, 225-234.
8. Becker W, Apel K. 1992. Isolation and characterization of a cDNA clone encoding a novel jasmonate-induced protein of barley (Hordeum vulgare L.). Plant Molecular Biology 19, 1065-1067.
9. Bonner TI, Brenner DJ, Neufeld BR, Britten RJ. 1973. Reduction in the rate of DNA reassociation by sequence divergence. Journal of Molecular Biology 81, 123-135.
10. Boston RS, Larkins BA. 1986. Specific transcription of a 15 kilodalton zein gene in HeLa cell extracts. Plant Molecular Biology 7, 71-79.
11. Burr B, Burr FA. 1991. Recombinant inbreds for molecular mapping in maize; theoretical and practical considerations. Trends in Genetics 7, 55-60.
12. Casey J, Davidson N. 1977. Rates of formation and thermal stabilities of RNA:DNA and DNA:DNA duplexes at high concentrations of formamide. Nucleic Acids Research 4, 1539-1552.
13. Chaudhry B, Muuler-Uri F, Cameron-Mills V, Gough S, Simpson D, Skriver K, Mundy J. 1994. The barley 60 kDa jasmonate-induced protein (JIP60) is a novel ribosome-inactivating protein. The Plant Journal 6, 815-824.
14. Chen Y, Peumans WJ, Van Damme EJ. 2002. The Sambucus nigra type-2 ribosome-inactivating protein SNA-I′ exhibits in planta antiviral activity in transgenic tobacco. FEBS Letters 516, 27-30.
15. Chevalier C, Bourgeois E, Pradet A, Raymond P. 1995. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Molecular Biology 28, 473-485.
16. Di Fonzo N, Manzocchi L, Salamini f, Soave C. 1986. Purification and properties of an endospermic protein of maize associated with the opaque-2 and opaque-6 genes. Planta 167, 587-594.
17. Di Fonzo N, Hartings H, Brembilla M, Motto M, Soave C, Navarro E, Palau J, Rhode W, Salamini F. 1988. The b-32 protein from maize endosperm, an albumin regulated by the O2 locus: nucleic acid (cDNA) and amino acid sequences. Molecular and General Genetics 212, 481-487.
18. Di Massimo AM, Di Loreto M, Pacilli A, Raucci G, D'Alatri L, Mele A, Bolognesi A, Polito L, Stirpe F, De Santis R. 1997. Immunoconjugates made of an anti-EGF receptor monoclonal antibody and type 1 ribosome-inactivating proteins from Saponaria ocymoides or Vaccaria pyramidata. British Journal of Cancer 75, 822-828.
19. Dowd PF, Mehta AD, Boston RS. 1998. Relative toxicitiy of the maize endosperm ribosome-inactivating protein to insects. Journal of Agricultural and Food Chemistry 46, 3775-3779.
20. Endo Y, Tsurugi K. 1987. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. Journal of Biological Chemistry 262, 8128-8130.
21. Endo Y, Mitsui K, Motizuki M, Tsurugi K. 1987. The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28S ribosomal RNA caused by the toxins. Journal of Biological Chemistry 262, 5908-5912.
22. Evensen G, Mathiesen A, Sundan A. 1991. Direct molecular cloning and expression of two distinct abrin A-chains. Journal of Biological Chemistry 266, 6848-6852.
23. Falasca A, Gasperi-Campani A, Abbondanza A, Barbieri L, Stirpe F. 1982. Properties of the ribosome-inactivating proteins gelonin, Momordica charantia inhibitor, and dianthins. Biochemistry Journal 207, 505-509.
24. Fordham-Skelton AP, Taylor PN, Hartley MR, Croy RR. 1991. Characterisation of saporin genes: in vitro expression and ribosome inactivation. Molecular and General Genetics 229, 460-466.
25. Frankel A, Schlossman D, Welsh P, Hertler A, Withers D, Johnston S. 1989. Selection and characterization of ricin toxin A-chain mutations in Saccharomyces cerevisiae. Molecular and Cellular Biology 9, 415-420.
26. French RR, Penney CA, Browning AC, Stirpe F, George AJ, Glennie MJ. 1995. Delivery of the ribosome-inactivating protein, gelonin, to lymphoma cells via CD22 and CD38 using bispecific antibodies. British Journal of Cancer 71, 986-994.
27. Funatsu G, Islam MR, Minami Y, Sung-Sil K, Kimura M. 1991. Conserved amino acid residues in ribosome-inactivating proteins from plants. Biochimie 73, 1157-1161.
28. Gale MD, Devos KM. 1998. Comparative genetics in the grasses. Proceedings of the National Academy of Sciences, USA 95, 1971-1974.
29. Gasperi-Campani A, Barbieri L, Battelli MG, Stirpe F. 1985. On the distribution of ribosome-inactivating proteins amongst plants. Journal of Natural Products (Lloydia) 48, 446-454.
30. Gaut BS. 2001. Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Research 11, 55-66.
31. Habuka N, Kataoka J, Miyano M, Tsuge H, Ago H, Noma M. 1993. Nucleotide sequence of a genomic gene encoding tritin, a ribosome-inactivating protein from Triticum aestivum. Plant Molecular Biology 22, 171-176.
32. Hao Q, Van Damme EJ, Hause B, Barre A, Chen Y, Rouge P, Peumans WJ. 2001. Iris bulbs express type 1 and type 2 ribosome-inactivating proteins with unusual properties. Plant Physiology 125, 866-876.
33. Hartings H, Lazzaroni N, Marsan PA, Aragay A, Thompson R, Salamini F, Di Fonzo N, Palau J, Motto M. 1990. The b-32 protein from maize endosperm: characterization of genomic sequences encoding two alternative central domains. Plant Molecular Biology 14, 1031-1040.
34. Hartley MR, Lord JM. 1993. Structure, function and applications of ricin and related cytotoxic proteins. In: Grierson D, ed. Biosynthesis and manipulation of plant products. Glasgow: Chapman and Hall, 210-239.
35. Hartley MR, Chaddock J, Bonness MS. 1996. The structure and function of ribosome-inactivating proteins. Trends in Plant Science 1, 254-260.
36. Helentjaris T, Weber D, Wright S. 1988. Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. Genetics 118, 353-364.
37. Henikoff S. 1991. Playing with blocks: some pitfalls of forcing multiple alignments. New Biology 3, 1148-1154.
38. Henikoff S, Henikoff JG. 1994. Protein family classification based on searching a database of blocks. Genomics 19, 97-107.
39. Hey TD, Hartley M, Walsh TA. 1995. Maize ribosome-inactivating protein (b-32). Homologs in related species, effects on maize ribosomes, and modulation of activity by pro-peptide deletions. Plant Physiology 107, 1323-1332.
40. Hong Y, Saunders K, Hartley MR, Stanley J. 1996. Resistance to geminivirus infection by virus-induced expression of dianthin in transgenic plants. Virology 220, 119-127.
41. Irvin JD, Kelly T, Robertus JD. 1980. Purification and properties of a second antiviral protein from Phytolacca americana which inactivates eukaryotic ribosomes. Archives of Biochemistry and Biophysics 200, 418-425.
42. Jach G, Gornhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C. 1995. Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. The Plant Journal 8, 97-109.
43. Katzin BJ, Collins EJ, Robertas JD. 1991. Structure of ricin A-chain at 2.5 Å. Proteins 10, 251-259.
44. Kim JK, Jang IC, Wu R, Zuo WN, Boston RS, Lee YH, Ahn IP, Nahm BH. 2003. Co-expression of a modified maize ribosome-inactivating protein and a rice basic chitinase gene in transgenic rice plants confers enhanced resistance to sheath blight. Transgenic Research 12, 475-484.
45. Krawetz JE, Boston RS. 2000. Substrate specificity of a maize ribosome-inactivating protein differs across diverse taxa. European Journal of Biochemistry 267, 1966-1974.
46. Krishnan R, McDonald KA, Dandekar AM, Jackman AP, Falk B. 2002. Expression of recombinant tricosanthin, a ribosome-inactivating protein, in transgenic tobacco. Journal of Biotechnology 97, 69-88.
47. Lamb FI, Roberts LM, Lord JM. 1985. Nucleotide sequence of cloned cDNA coding for preproricin. European Journal of Biochemistry 148, 265-270.
48. Langridge P, Pintor-Toro JA, Feix G. 1982. Transcriptional effects of the opaque-2 mutation of Zea mays L. Planta 156, 166-170.
49. Lappi DA, Esch FS, Barbieri L, Stirpe F, Soria M. 1985. Characterization of a Saponaria officinalis seed ribosome-inactivating protein: immunoreactivity and sequence homologies. Biochemistry and Biophysics Research Communications 129, 934-942.
50. Leah R, Tommerup H, Svendsen I, Mundy J. 1991. Biochemical and molecular characterization of three barley seed proteins with antifungal properties. Journal of Biological Chemistry 266, 1564-1573.
51. Legname G, Bellosta P, Gromo G, Modena D, Keen JN, Roberts LM, Lord JM. 1991. Nucleotide sequence of cDNA coding for dianthin 30, a ribosome inactivating protein from Dianthus caryophyllus. Biochimica et Biophysica Acta 1090, 119-122.
52. Lin Q, Chen ZC, Antoniw JF, White RF. 1991. Isolation and characterization of a cDNA clone encoding the anti-viral protein from Phytolacca americana. Plant Molecular Biology 17, 609-614.
53. Lodge JK, Kaniewski WK, Turner NE. 1993. Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proceedings of the National Academy of Sciences, USA 90, 7089-7093.
54. Logeman J, Jach G, Tommerup H, Mundy J, Schell J. 1992. Expression of a barley ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Biol Technology 10, 305-308.
55. Lohmer S, Maddaloni M, Motto M, Di Fonzo N, Hartings H, Salamini F, Thompson RD. 1991. The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. The EMBO Journal 10, 617-624.
56. Maddaloni M, Forlani F, Balmas V, Donini G, Stasse L, Corazza L, Motto M. 1997. Tolerance to the fungal pathogen Rhizoctonia solani AG4 of transgenic tobacco expressing the maize ribosome-inactivating protein b-32. Transgenic Research 6, 393-402.
57. Maniatis T, Fritsch EF, Sambrook J. 1982. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
58. Massiah AJ, Hartley MR. 1995. Wheat ribosome-inactivating proteins: seed and leaf forms with different specificities and cofactor requirements. Planta 197, 633-640.
59. May MJ, Hartley MR, Roberts LM, Krieg PA, Osborn RW, Lord JM. 1989. Ribosome inactivation by ricin A chain: a sensitive method to assess the activity of wild-type and mutant polypeptides. EMBO Journal 8, 301-308.
60. Montfort W, Villafranca JE, Monzingo AF, Ernst SR, Katzin B, Rutenber E, Xuong NH, Hamlin R, Robertus JD. 1987. The three-dimensional structure of ricin at 2.8 Å. Journal of Biological Chemistry 262, 5398-5403.
61. Muller M, Dues G, Balconi C, Salamini F, Thompson RD. 1997. Nitrogen and hormonal responsiveness of the 22 kDa alpha-zein and b-32 genes in maize endosperm is displayed in the absence of the transcriptional regulator Opaque-2. The Plant Journal 12, 281-291.
62. Mundy J, Leah R, Boston RS, Endo Y, Stirpe F. 1994. Genes encoding ribosome-inactivating proteins. Plant Molecular Biology Reports (Commission on Plant Gene Nomenclature Supplement) 12, S60-S62.
63. Neale AD, Wahleithner JA, Lund M, Bonnett HT, Kelly A, Meeks-Wagner DR, Peacock WJ, Dennis ES. 1990. Chitinase, beta-1,3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. The Plant Cell 2, 673-684.
64. Nielsen K, Boston RS. 2001. Ribosome-inactivating proteins: a plant perspective. Annual Review of Plant Physiology and Plant Molecular Biology 52, 785-816.
65. Nielsen K, Payne GA, Boston RS. 2001. Maize ribosome-inactivating protein inhibits normal development of Aspergillus nidulans and Aspergillus flavus. Molecular Plant-Microbe Interactions 14, 164-172.
66. Park SW, Lawrence CB, Linden JC, Vivanco JM. 2002. Isolation and characterization of a novel ribosome-inactivating protein from root cultures of pokeweed and its mechanism of secretion from roots. Plant Physiology 130, 164-178.
67. Peattie DA. 1979. Direct chemical method for sequencing RNA. Proceedings of the National Academy of Sciences, USA 76, 1760-1764.
68. Poyet J-L, Radom J, Hoeveler A. 1994. Isolation and characterization of a cDNA clone encoding the pokeweed antiviral protein II from Phytolacca americana and its expression in E. coli. FEBS Letters 347, 268-272.
69. Ready MP, Kim Y, Robertus JD. 1991. Site-directed mutagenesis of ricin A-chain and implications for the mechanism of action. Proteins 10, 270-278.
70. Reinbothe S, Mollenhauer B, Reinbothe C. 1994b. JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. The Plant Cell 6, 1197-1209.
71. Reinbothe S, Reinbothe C, Lehmann J, Becker W, Apel K, Parthier B. 1994a. JIP60, a methyl jasmonate-induced ribosome-inactivating protein involved in plant stress reactions. Proceedings of the National Academy of Sciences, USA 91, 7012-7016.
72. Reisbig RR, Bruland O. 1983a. Dianthin 30 and 32 from Dianthus caryophyllus: two inhibitors of plant protein synthesis and their tissue distribution. Archives of Biochemistry and Biophysics 224, 700-706.
73. Reisbig RR, Bruland O. 1983b. The protein synthesis inhibitors from wheat, barley, and rye have identical antigenic determinants. Biochemistry and Biophysics Research Communications 114, 190-196.
74. Schmidt RJ, Ketudat M, Aukerman MJ, Hoschek G. 1992. Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. The Plant Cell 4, 689-700.
75. Soave C, Tardani L, Di Fonzo N, Salamini F. 1981. Zein level in maize endosperm depends on a protein under control of the opaque-2 and opaque-6 loci. Cell 27, 403-410.
76. Southern EM. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503-517.
77. Stirpe F, Barbieri L. 1986. Ribosome-inactivating proteins up to date. FEBS Letters 195, 1-8.
78. Stirpe F, Barbieri L, Battelli MG, Soria M, Lappi DA. 1992. Ribosome-inactivating proteins from plants: present status and future prospects. Biol/Technology 10, 405-412.
79. Strockbine NA, Jackson MP, Sung LM, Holmes RK, O'Brien AD. 1988. Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1. Journal of Bacteriology 170, 1116-1122.
80. van Damme EJ, Hao Q, Chen Y, Barre A, Vandenbussche F, Desmyter S, Rouge P, Peumans WJ. 2001. Ribosome-inactivating Proteins: a family of plant proteins that do more than inactivate ribosomes. Critical Reviews in Plant Sciences 20, 395-465.
81. Veronese P, Ruiz MT, Coca MA, et al. 2003. In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiology 131, 1580-1590.
82. Vilardell J, Goday A, Freire MA, Torrent M, Martinez MC, Torne JM, Pages M. 1990. Gene sequence, developmental expression, and protein phosphorylation of RAB-17 in maize. Plant Molecular Biology 14, 423-432.
83. Vivanco JM, Savary BJ, Flores HE. 1999. Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the Andean crop Mirabilis expansa. Plant Physiology 119, 1447-1456.
84. Wallace JC, Galili G, Kawata EE, Cuellar RE, Shotwell MA, Larkins BA. 1988. Aggregation of lysine-containing zeins into protein bodies in Xenopus oocytes. Science 240, 662-664.
85. Walsh TA, Morgan AE, Hey TD. 1991. Characterization and molecular cloning of a proenzyme form of a ribosome-inactivating protein from maize. Novel mechanism of proenzyme activation by proteolytic removal of a 2.8-kilodalton internal peptide segment. Journal of Biological Chemistry 266, 23422-23427.
86. Weston SA, Tucker AD, Thatcher DR, Derbyshire DJ, Pauptit RA. 1994. X-ray structure of recombinant ricin A-chain at 1.8 A resolution. Journal of Molecular Biology 244, 410-422.
87. Wetmur JG, Davidson N. 1968. Kinetics of renaturation of DNA. Journal of Molecular Biology 31, 349-370.
88. Whitkus R, Doebley J, Lee M. 1992. Comparative genome mapping of sorghum and maize. Genetics 132, 1119-1130.
89. Wilson WA, Harrington SE, Woodman WL, Lee M, Sorrells ME, McCouch SR. 1999. Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated panicoids. Genetics 153, 453-473.
90. Wool IG, Gluck A, Endo Y. 1992. Ribotoxin recognition of ribosomal RNA and a proposal for the mechanism of translocation. Trends in Biochemical Science 17, 266-269.
91. Xiong J-P, Xia, Z-X, Wang Y. 1994. Crystal structure of trichosanthin-NADPH complex at 1.7 Å resolution reveals active-site architecture. Nature Structural and Molecular Biology 1, 695-700.
92. Yuan H, Ming X, Wang L, Hu P, An C, Chen Z. 2002. Expression of a gene encoding tricosanthin in transgenic rice plants enhances resistance to fungus blast disease. Plant Cell Reports 20, 992-998.
93. Zimmer EA, Newton KJ. 1982. A simple method for the isolation of high molecular weight DNA from individual maize seedlings and tissues. In: Sherdian WF, ed. Maize for biological research. Grand Forks, ND: North Dakota Press.
94. Zoubenko O, Hudak K, Tumer NE. 2000. A non-toxic pokeweed antiviral protein mutant inhibits pathogen infection via a novel salicylic acid-independent pathway. Plant Molecular Biology 44, 219-229.