Ubiquitous urease affects soybean susceptibility to fungi

Plant Molecular Biology

Volumn 79, Issue 1-2, 2012, Pages 75-87

  Wiebke Strohm, Beatriz ^a   Pasquali, Giancarlo ^a   Margis Pinheiro, Márcia ^a   Bencke, Marta ^a   Bücker Neto, Lauro ^a   Becker Ritt, Arlete B ^a   Martinelli, Anne H S ^a   Rechenmacher, Ciliana ^a   Polacco, Joseph C ^b   Stolf, Renata ^c   Marcelino, Francismar C ^c   Abdelnoor, Ricardo V ^c   Homrich, Milena S ^a   Del Ponte, Emerson M ^a   Carlini, Celia R ^a   de Carvalho, Mayra C C G ^c   Bodanese Zanettini, Maria Helena ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b University of Missouri   (United States)

^c EMBRAPA CERRADOS   (Brazil)

Author keywords

Co suppression; Functional analysis; Fungal resistance; Genetic transformation; Glycine max; Overexpression

Indexed keywords

BACTERIAL DNA; T DNA; T-DNA; UREA; UREASE; VEGETABLE PROTEIN;

ARTICLE; BASIDIOMYCETES; BIOASSAY; DISEASE RESISTANCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC RECOMBINATION; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT LEAF; SOYBEAN; TRANSGENE; TRANSGENIC PLANT;

BASIDIOMYCOTA; BIOLOGICAL ASSAY; DISEASE RESISTANCE; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENETIC VECTORS; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RECOMBINATION, GENETIC; SOYBEANS; TRANSFORMATION, GENETIC; TRANSGENES; UREA; UREASE;

FUNGI; GLYCINE MAX; HYPHOMYCETES; PENICILLIUM; PHAKOPSORA PACHYRHIZI; PHOMOPSIS; THANATEPHORUS CUCUMERIS;

EID: 84859988272     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-012-9894-1     Document Type: Article

References (56)

1. Barros PR, Stassen H, Freitas MS, Carlini CR, Nascimento MAC, Follmer C (2009) Membrane-disruptive properties of the bioinsecticide Jaburetox-2Ec: implications to the mechanism of the action of insecticidal peptides derived from ureases. Biochim Biophys Acta 1794: 1848-1854.
2. Becker-Ritt AB, Martinelli AH, Mitidieri S, Feder V, Wassermann GE, Santi L, Vainstein MH, Oliveira JT, Fiuza LM, Pasquali G, Carlini CR (2007) Antifungal activity of plant and bacterial ureases. Toxicon 50: 971-983.
3. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
4. Camargo PO (2010) Estudo da herança de caracteres quali-quantitativos e mapeamento genético de alelos resistentes à Ferrugem Asiática da soja presentes nas PI561356 e PI594754. Dissertation, Universidade Estadual de Londrina.
5. Carlini CR, Polacco JC (2008) Toxic properties of urease. Crop Sci 48: 1665-1672.
6. Carlini CR, Oliveira AE, Azambuja P, Xavier-Filho J, Wells MA (1997) Biological effects of canatoxin in different insect models: evidence for a proteolytic activation of the toxin by insect cathepsinlike enzymes. J Econ Entomol 90: 340-348.
7. Choi JJ, Alkharouf NW, Schneider KT, Matthews BF, Frederick RD (2008) Expression patterns in soybean resistant to Phakopsora pachyrhizi reveal the importance of peroxidases and lipoxygenases. Funct Integr Genomics 8: 341-359.
8. Dixon NE, Gazzola TC, Blakeley RL, Zermer B (1975) Letter: Jack bean urease (EC 3. 5. 1. 5). A metalloenzyme. A simple biological role for nickel? J Am Chem Soc 97: 4131-4133.
9. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11-15.
10. Droste A, Pasquali G, Bodanese-Zanettini MH (2002) Transgenic fertile plants of soybean [Glycine max (L) Merrill] obtained from bombarded embryogenic tissue. Euphytica 127: 367-376.
11. El-Shemy HA, Khalafalla MM, Fujita K, Ishimoto M (2006) Molecular control of gene co-suppression in transgenic soybean via particle bombardment. J Biochem Mol Biol 39: 61-67.
12. Finer JJ, Vain P, Jones MW, McMullen MD (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep 11: 323-328.
13. Follmer C (2008) Insights into the role and structure of plant ureases. Phytochemistry 69: 18-28.
14. Follmer C, Wassermann GE, Carlini CR (2004a) Separation of jack bean (Canavalia ensiformis) urease isoforms by immobilized metal affinity chromatography and characterization of insecticidal properties unrelated to ureolytic activity. Plant Sci 167: 241-246.
15. Follmer C, Real-Guerra R, Wasserman GE, Olivera-Severo D, Carlini CR (2004b) Jackbean, soybean and Bacillus pasteurii ureases: biological effects unrelated to ureolytic activity. Eur J Biochem 271: 1357-1363.
16. Francis KE, Spiker S (2005) Identification of Arabidopsis thaliana transformants without selection reveals a high occurrence of silenced T-DNA integrations. Plant J 41: 464-477.
17. Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11: 169-177.
18. Goldraij A, Beamer LJ, Polacco JC (2003) Interallelic complementation at the ubiquitous urease coding locus of soybean. Plant Physiol 132: 1801-1810.
19. Graham MY, Weidner J, Wheeler K, Pelow MJ, Graham TL (2003) Induced expression of pathogenesis-related protein genes in soybean by wounding and the Phytophthora sojae cell wall glucan elicitor. Physiol Mol Plant Pathol 63: 141-149.
20. Homrich MS, Passaglia LMP, Pereira JF, Bertagnolli PF, Pasquali G, Zaidi MA, Altosaar I, Bodanese-Zanettini MH (2008) Resistance to Anticarsia gemmatalis Hübner (Lepidoptera, Noctuidae) in transgenic soybean (Glycine max (L.) Merrill, Fabales, Fabaceae) cultivar IAS5 expressing a modified Cry1Ac endotoxin. Gen Mol Biol 31: 522-531.
21. James VA, Avart C, Worland B, Snape JW, Vain P (2002) The relationship between homozygous and hemizygous transgene expression levels over generations in populations of transgenic rice plants. Theor Appl Genet 104: 553-561.
22. Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9: 1-14.
23. Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195.
24. Kohli A, Twyman RM, Abranches R, Wegel E, Stoger E, Christou P (2003) Transgene integration, organization and interaction in plants. Plant Mol Biol 52: 247-258.
25. Krajewska B (2009) Ureases I. Functional, catalytic and kinetic properties: a review. J Mol Catal B: Enzymatic 59: 9-21.
26. Lechtenberg B, Schuberty D, Forsbachz A, Gils M, Schmidt R (2003) Neither inverted repeat T-DNA configurations nor arrangements of tandemly repeated transgenes are sufficient to trigger transgene silencing. Plant J 34: 507-517.
27. Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, Clough SJ, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. Plant Genome 1: 44-54.
28. (-Delta Delta C(T)) method. Methods 25: 402-408.
29. Menegassi A, Wassermann GE, Olivera-Severo D, Becker-Ritt AB, Martinelli AH, Feder V, Carlini CR (2008) Urease from cotton (Gossypium hirsutum) seeds: isolation, physicochemical characterization, and antifungal properties of the protein. J Agric Food Chem 56: 4399-4405.
30. Meyer-Bothling LE, Polacco JC (1987) Mutational analysis of the embryo-specific urease locus of soybean. Mol Gen Genet 209: 439-444.
31. Miles MR, Levy C, Morel W, Mueller T, Steinlage T, van Rij N, Frederick RD, Hartman GL (2007) International fungicide efficacy trials for the management of soybean rust. Plant Dis 91: 1450-1458.
32. Mulinari F, Staniscuaski F, Bertholdo-Vargas LR, Postal M, Oliveira-Neto OB, Rigden DJ, Grossi-de-Sa MF, Carlini CR (2007) Jaburetox-2Ec: an insecticidal peptide derived from an isoform of urease from the plant Canavalia ensiformis. Peptides 28: 2042-2050.
33. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2: 279-289.
34. Panthee DR, Yuan JS, Wright DL, Marois JJ, Mailhot D, Stewart CN Jr (2007) Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Funct Integr Genomics 7: 291-301.
35. Panthee DR, Marois JJ, Wright DL, Narvaez D, Yuan JS, Stewart CN Jr (2009) Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific. Theor Appl Genet 118: 359-370.
36. Polacco JC, Havir EA (1979) Comparisons of soybean urease isolated from seed and tissue culture. J Biol Chem 254: 1707-1715.
37. Polacco JC, Holland MA (1993) Roles of urease in plant cells. Int Rev Cytol 145: 65-103.
38. Polacco JC, Winkler RG (1984) Soybean leaf urease: a seed enzyme? Plant Physiol 74: 800-803.
39. Polacco JC, Krueger RW, Winkler RG (1985) Structure and possible ureide degrading function of the ubiquitous urease of soybean. Plant Physiol 79: 794-800.
40. Schmidt M, Parrott W (2001) Quantitative detection of transgenes in soybean [Glycine max (L.) Merrill] and peanut (Arachis hypogaea L.) by real-time polymerase chain reaction. Plant Cell Rep 20: 422-428.
41. Schmidt MA, Lafayette PR, Artelt BA, Parrott WA (2008) A comparison of strategies for transformation with multiple genes via microprojectile-mediate bombardment. In Vitro Cell Dev Biol 44: 162-168.
42. Shou H, Frame BR, Whitham SA, Wang K (2004) Assessment of transgenic maize events produced by particle bombardment or Agrobacterium-mediated transformation. Mol Breed 13: 201-208.
43. Sinclair JB, Hartman GL (1999) Soybean diseases. In: Hartman GL, Sinclair JB, Rupe JC (eds) Compendium of soybean diseases, 4th edn. American Phytopathological Society, St. Paul, pp 3-4.
44. Soria-Guerra RE, Rosales-Mendoza S, Chang S, Haudenshield JS, Padmanaban A, Rodriguez-Zas S, Hartman GL, Ghabrial SA, Korban SS (2010a) Transcriptome analysis of resistant and susceptible genotypes of Glycine tomentella during Phakopsora pachyrhizi infection reveals novel rust resistance genes. Theor Appl Genet 120: 1315-1333.
45. Soria-Guerra RE, Rosales-Mendoza S, Chang S, Haudenshield JS, Zheng D, Rao SS, Hartman GL, Ghabrial SA, Korban SS (2010b) Identifying differentially expressed genes in leaves of Glycine tomentella in the presence of the fungal pathogen Phakopsora pachyrhizi. Planta 232: 1181-1189.
46. Stebbins NE, Polacco JC (1995) Urease is not essential for ureide degradation in soybean. Plant Physiol 109: 169-175.
47. Tang W, Newton RJ, Weidner DA (2007) Genetic transformation and gene silencing mediated by multiple copies of a transgene in eastern white pine. J Exp Bot 58: 545-554.
48. Thibaud-Nissen F, Wu H, Richmond T, Redman JC, Johnson C, Green R, Arias J, Town CD (2006) Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J 45: 152-162.
49. Torisky RS, Griffin JD, Yenofsky RL, Polacco JC (1994) A single gene (Eu4) encodes the tissue-ubiquitous urease of soybean. Mol Gen Genet 242: 404-414.
50. Twizeyimana M, Bandyopadhyay R, Ojiambo P, Paul C, Hartman GL (2006) A detached leaf method to evaluate soybean for resistance to rust National Soybean. Rust symposium. In: Proceedings of 2006 National Soybean rust symposium, Saint Louis.
51. van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida AM, Baum TJ, Whitham SA (2007) Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol Plant Microbe Interact 20: 887-899.
52. Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39: 971-974.
53. Wiebke-Strohm B, Droste A, Pasquali G, Osorio MB, Bücker-Neto L, Passaglia LMP, Bencke M, Homrich MS, Margis-Pinheiro M, Bodanese-Zanettini MH (2011) Transgenic fertile soybean plants derived from somatic embryos transformed via the combined DNA-free particle bombardment and Agrobacterium system. Euphytica 177: 343-354.
54. Witte CP, Tiller SA, Taylor MA, Davies HV (2002) Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of (15)N after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiol 128: 1129-1136.
55. Yin Z, Plader W, Malepszy S (2004) Transgene inheritance in plants. J Appl Genet 45: 127-144.
56. Yuan JS, Burris J, Stewart NR, Mentewab AC, Stewart N Jr (2007) Statistical tools for transgene copy number estimation based on real-time PCR. BMC Bioinform 8: S6.