Abstract
The gene encoding hydroxyisourate hydrolase, a novel ureide-metabolizing enzyme, has been cloned from soybean (Glycine max). The gene encodes a protein that is 560 amino acids in length and contains a 31-amino acid signal sequence at the N terminus that is not present in the mature protein. The presence of two SKL motifs near the C terminus suggests that the protein resides in the peroxisome. This expectation is borne out by results from immunogold electron microscopy, which revealed that hydroxyisourate hydrolase was localized in the peroxisomes of uninfected root nodules. The gene encoding hydroxyisourate hydrolase was expressed in Escherichia coli, and soluble, catalytically active enzyme was purified to homogeneity. Sequence analysis revealed considerable homology with members of the beta-glucosidase family of enzymes. Two glutamate residues, E199 and E408, align with the conserved glutamates that play catalytic roles in the beta-glucosidases. However, the other residues that have been identified by crystallography to interact directly with the substrates in beta-glucosidases are not conserved in hydroxyisourate hydrolase. The E199A and E408A hydroxyisourate hydrolase mutants were devoid of detectable catalytic activity. Analysis of transcripts for hydroxyisourate hydrolase demonstrated that its level of expression was highest in the nodule; mRNA was detectable 12 d after infection and increased until 21 d postinfection, then declined. In a similar manner, immunodetection of hydroxyisourate hydrolase indicated preferential localization in the nodule; the amount of protein detected was maximal at 21 d postinfection. The pattern of expression of hydroxyisourate hydrolase matched that of urate oxidase, and supports the hypothesis that hydroxyisourate hydrolase plays a role in ureide metabolism.
MeSH Terms
Amidohydrolases/genetics,metabolism
Amino Acid Sequence
Cloning, Molecular
DNA, Complementary/chemistry,genetics
Escherichia coli/genetics,metabolism
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Microscopy, Immunoelectron
Molecular Sequence Data
Peroxisomes/metabolism
Plant Roots/enzymology,genetics,ultrastructure
Sequence Analysis, DNA
Sequence Homology, Amino Acid
Soybean Proteins/genetics,metabolism
Soybeans/enzymology,genetics
beta-Glucosidase/genetics,metabolism
Chemicals
DNA, Complementary
Soybean Proteins
beta-Glucosidase
Amidohydrolases
hydroxyisourate hydrolase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Raychaudhuri Aniruddha
Department of Biochemistry, University of Missouri, Columbia, Missouri 65211, USA.
Tipton Peter A
References (28)
28 references, click to expand
-
Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation.
Plant Physiol. 2002 Mar;128(3):793-802
PMID: 11891236
-
A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions.
Plant Mol Biol. 1994 Mar;24(6):853-62
PMID: 8204823
-
Expression and Localization of Plant Protein Disulfide Isomerase.
Plant Physiol. 1993 Nov;103(3):719-726
PMID: 12231974
-
Identification and purification of hydroxyisourate hydrolase, a novel ureide-metabolizing enzyme.
J Biol Chem. 1999 Nov 26;274(48):33863-5
PMID: 10567345
-
Crystal structure of a monocotyledon (maize ZMGlu1) beta-glucosidase and a model of its complex with p-nitrophenyl beta-D-thioglucoside.
Biochem J. 2001 Feb 15;354(Pt 1):37-46
PMID: 11171077
-
A new hemoglobin gene from soybean: a role for hemoglobin in all plants.
Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5682-7
PMID: 8650152
-
Two distinct uricase II (nodulin 35) genes are differentially expressed in soybean plants.
Mol Plant Microbe Interact. 1997 Aug;10(6):735-41
PMID: 9245835
-
Enzymes of Purine Biosynthesis and Catabolism in Glycine max: I. COMPARISON OF ACTIVITIES WITH N(2) FIXATION AND COMPOSITION OF XYLEM EXUDATE DURING NODULE DEVELOPMENT.
Plant Physiol. 1981 Nov;68(5):1115-22
PMID: 16662061
-
Localization of enzymes of ureide biosynthesis in peroxisomes and microsomes of nodules.
Plant Physiol. 1981 Jul;68(1):65-9
PMID: 16661891
-
Uninfected cells of soybean root nodules: ultrastructure suggests key role in ureide production.
Science. 1981 Jun 19;212(4501):1394-6
PMID: 17746261
-
Lipo-oligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs.
Plant J. 1993 Oct;4(4):727-33
PMID: 8252073
-
Developmental regulation of enzymes of sucrose and hexose metabolism in effective and ineffective soybean nodules.
Plant Physiol. 1990 Feb;92(2):346-51
PMID: 16667280
-
Enzymes of the Poly-beta-Hydroxybutyrate and Citric Acid Cycles of Rhizobium japonicum Bacteroids.
Plant Physiol. 1984 Aug;75(4):1158-62
PMID: 16663750
-
Isolation and characterization of infected and uninfected cells from soybean nodules : role of uninfected cells in ureide synthesis.
Plant Physiol. 1983 Apr;71(4):869-73
PMID: 16662921
-
Immunogold localization of nodule-specific uricase in developing soybean root nodules.
Planta. 1986 Apr;167(4):425-36
PMID: 24240357
-
Cellular compartmentation of ureide biogenesis in root nodules of cowpea (Vigna unguiculata (L.) Walp.).
Planta. 1987 Oct;172(2):162-75
PMID: 24225867
-
Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants.
Plant Cell. 1993 Jul;5(7):781-94
PMID: 7689881
-
Structural and expression analysis of uricase mRNA from Lotus japonicus.
Mol Plant Microbe Interact. 2000 Oct;13(10):1156-60
PMID: 11043477
-
Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
Protein Eng. 1997 Jan;10(1):1-6
PMID: 9051728
-
Snapshots along an enzymatic reaction coordinate: analysis of a retaining beta-glycoside hydrolase.
Biochemistry. 1998 Aug 25;37(34):11707-13
PMID: 9718293
-
Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002
PMID: 2461560
-
Salt Stress Increases the Level of Translatable mRNA for Phosphoenolpyruvate Carboxylase in Mesembryanthemum crystallinum.
Plant Physiol. 1987 Aug;84(4):1270-5
PMID: 16665596
-
Spectroscopic characterization of intermediates in the urate oxidase reaction.
Biochemistry. 1998 Aug 18;37(33):11651-9
PMID: 9709003
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca.
Plant Cell. 1995 Feb;7(2):213-23
PMID: 7756831
-
Building new models for peroxisome biogenesis.
Plant Physiol. 2001 Nov;127(3):731-9
PMID: 11706158
-
Human immunodeficiency virus-1 protease. 1. Initial velocity studies and kinetic characterization of reaction intermediates by 18O isotope exchange.
Biochemistry. 1991 Aug 27;30(34):8441-53
PMID: 1883830
-
Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume.
Science. 1996 Jul 19;273(5273):370-3
PMID: 8662527