Opinion - Nickel and urease in plants: Still many knowledge gaps

Plant Science

Volumn 199-200, Issue , 2013, Pages 79-90

  Polacco, Joe C ^a   Mazzafera, Paulo ^b   Tezotto, Tiago ^c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Metalloenzyme; Micronutrient; Nitrogen metabolism; Urease

Indexed keywords

ARGININE; NICKEL; NITROGEN; TRACE ELEMENT; UREA; UREASE; VEGETABLE PROTEIN;

ENZYMOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; PLANT; PLANT IMMUNITY; REVIEW; SOYBEAN; SYMBIOSIS;

ARGININE; MICRONUTRIENTS; NICKEL; NITROGEN; PLANT IMMUNITY; PLANT PROTEINS; PLANTS; SOYBEANS; STRESS, PHYSIOLOGICAL; SYMBIOSIS; UREA; UREASE;

EID: 84875296729     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2012.10.010     Document Type: Review

References (178)

1. Dixon N.E., Gazzola C., Blakeley R.L., Zerner B. A metalloenzyme. A simple biological role for nickel. J. Am. Chem. Soc. 1975, 97:4131-4133.
2. Polacco J.C. Nitrogen metabolism in soybean tissue culture. I. Assimilation of urea. Plant Physiol. 1976, 58:350-357.
3. Polacco J.C. Nitrogen metabolism in soybean tissue culture: II. Urea utilization and urease synthesis require Ni. Plant Physiol. 1977, 59:827-830.
4. Eskew D.L., Welch R.M., Cary E.E. Nickel: an essential micronutrient for legumes and possibly all higher plants. Science 1983, 222:621-623.
5. Eskew D.L., Welch R.M., Norvell W.A. Nickel in higher plants: further evidence for an essential role. Plant Physiol. 1984, 76:691-693.
6. Bailey C.J., Boulter D. Urease a typical seed protein of the Leguminosae. The Chemotaxonomy of the Leguminosae 1971, 485-502. Academic Press, New York. J.B. Harborne, D. Boulter, B.L. Turner (Eds.).
7. Carlini C.R., Polacco J.C. Toxic properties of urease (Perspectives). Crop Sci. 2008, 48.
8. Hogan M.E., Swift I.E., Done J. Urease assay and ammonia release from leaf tissues. Phytochemistry 1983, 22:663-667.
9. Walker D.W., Graham R.D., Madison J.T., Cary E.E., Welch R.M. Effects of Ni deficiency on some nitrogen metabolites in cowpea (Vigna unguiculata L. Wap.). Plant Physiol. 1985, 79:474-479.
10. Wood B.W., Reilly C.C., Nyezepir A.P. Mouse-ear of pecan: I. Symptomatology and occurrence. HortScience 2004, 39:87-94.
11. Wood B.W., Reilly C.C., Nyezepir A.P. Mouse-ear of pecan: II. Influence of nutrient applications. HortScience 2004, 39:95-100.
12. Wood B.W., Reilly C.C., Nyezepir A.P. Mouse-ear of pecan: a nickel deficiency. HortScience 2004, 39:1238-1242.
13. Bai C., Reilly C.C., Wood B.W. Nickel deficiency disrupts metabolism of ureides, amino acids, and organic acids of young pecan foliage. Plant Physiol. 2006, 140:433-443.
14. P. Mazzafera, T. Tezotto, J.C. Polacco, Nickel in plants, in: V.N. Uversdy, R.H. Kretsinger, E.A. Permyakov (Eds.), Encylopedia of Metalloproteins, Springer, in press (upcoming in January 2013).
15. Brown P.H., Welch R.M., Cary E.E. Nickel: a micronutrient essential for higher plants. Plant Physiol. 1987, 85:801-803.
16. Brown P.H., Welch R.M., Cary E.E., Checkai R.T. Beneficial effects of nickel on plant growth. J. Plant Nutr. 1987, 10:2125-2135.
17. Marschner H. Mineral Nutrition of Higher Plants 1995, Academic Press Inc., San Diego.
18. Todd C.D., Polacco J.C. Soybean cultivars 'Williams 82 and Maple Arrow produce both urea and ammonia uring ureide degradation. J. Exp. Bot. 2004, 398:867-877.
19. Brown P.H., Welch R.M., Madison J.T. Effect of nickel deficiency on soluble anion, amino acid and nitrogen levels in barley. Plant Soil 1990, 125:19-27.
20. Ma X., et al. OsARG encodes an arginase that plays critical roles in panicle development and grain production in rice. Plant J. 2012, 10.1111/j.1365-1313X.2012.05122.x.
21. Kutman B.Y., Kutman U.B., Cakmak I. Nickel-enriched seed and externally supplied nickel improve growth and alleviate foliar urea damage in soybean. Plant Soil 2012, 10.1007/s11104-012-1284-6.
22. Polacco J.C., Hyten D.L., Medeiros-Silva M., Sleper D.A., Bilyeu K.D. Mutational analysis of the major soybean UreF paralogue involved in urease activation. J. Exp. Bot. 2011, 62:3599-3608.
23. Yang X.E., Baligar V.C., Foster J.C., Martens D.C. Accumulation and transport of nickel in relation to organic acids in ryegrass and maize grown with different nickel levels. Plant Soil 1997, 196:271-276.
24. Stebbins N., Holland M.A., Cianzio S.R., Polacco J.C. Genetic tests of the roles of the embryonic ureases of soybean. Plant Physiol. 1991, 97:1004-1010.
25. 3) and Ni supply for growth, urease activity and nitrogen metabolism of zucchini (Cucurbita pepo convar. Giromontiina). Plant Soil 1997, 196:217-222.
26. 3 or urea as N source. Ann. Bot. 1999, 83:65-71.
27. Alcazar R., et al. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 2010, 231:1237-1249.
28. Szabados L., Savoure A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010, 15:89-97.
29. Chen H., Wilkerson C.G., Kuchar J.A., Phinney B.S., Howe G.A. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc. Natl. Acad. Sci U.S.A. 2005, 102:19237-19242.
30. Flores T., et al. Arginase-negative mutants exhibit increased NO signaling in root development. Plant Physiol. 2008, 147:1937-1946.
31. Brownfield D.L., Todd C.D., Deyholos M.K. Analysis of Arabidopsis arginase gene transcription patterns indicates specific biological functions for recently diverged paralogs. Plant Mol. Biol. 2008, 67:429-440.
32. Jenkinson C.P., Grody W.W., Cederbaum S.D. Comparative properties of arginases. Comp. Biochem. Phys. B 1996, 114:107-132.
33. Brauc S. Overexpression of arginase in Arabidopsis thaliana influences defence responses against Botrytis cinerea. Plant Biol. 2012, 14:39-45.
34. Gravot A. Arginase induction represses gall development during clubroot infection in Arabidopsis. Plant Cell Physiol. 2012, 53:901-911.
35. Wang B.-Q., Zhang Q.-F., Liu J.-H., Li G.-H. Overexpression of PtADC confers enhanced dehydration and drought tolerance in transgenic tobacco and tomato: effect on ROS elimination. Biochem. Biophys. Res. Commun. 2011, 413:10-16.
36. Wang J., et al. An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J. Exp. Bot. 2011, 62:2899-2914.
37. Hanfrey C., Sommer S., Mayer M.J., Burtin D., Michael A.J. Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J. 2001, 27:551-560.
38. Funck D., Stadelhofer B., Koch W. Orn-δ-aminotransferase is essential for Arg catabolism but not for proline biosynthesis. BMC Plant Biol. 2008, 8:40.
39. Stránská J., Kopečný D., Tylichová M., Snégaroff J., Šebela M. Orn δ-aminotransferase, an enzyme implicated in salt tolerance in higher plants. Plant Signal. Behav. 2008, 3:929-935.
40. Gravot A., et al. Arginase induction represses gall development during clubroot infection in Arabidopsis. Plant Cell Physiol. 2012, 53:901-911.
41. Flores T., et al. Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiol. 2008, 147:1936-1946.
42. Lanfranco L., Guether M., Bonfante P. Arbuscular mycorrhizas and N acquisition by plants. Ecological Aspects of Nitrogen Metabolism in Plants 2011, John Wiley & Sons, Inc., pp. 52-68.
43. de Faria S.M., Resende A.S., Júnior O.J.S., Boddey R.M. Exploiting mycorrhizae and rhizobium symbioses to recover seriously degraded soils. Ecological Aspects of Nitrogen Metabolism in Plants 2011, John Wiley & Sons, Inc., pp. 195-215.
44. Brito B. Rhizobium leguminosarum hupE encodes a nickel transporter required for hydrogenase activity. J. Bacteriol. 2010, 192:925-935.
45. Brito Lopez M.B., et al. Diversity of nickel ligands in nodule cytosol, nickel transport, and expression of a nickel-dependent enzyme in endosymbiotic bacteria as affected by the legume host. XIII National Meeting of the Spanish Society of Nitrogen Fixation and II Portuguese-Spanish Congress on Nitrogen Fixation 2010, Universidad Politécnica de Madrid, Zaragoza, Spain, pp. 159-160.
46. Cacho C., Brito B., Palacios J., Pérez-Conde C., Cámara C. Speciation of nickel by HPLC-UV/MS in pea nodules. Talanta 2010, 83:78-83.
47. Lundberg D.S., et al. Defining the core Arabidopsis thaliana root microbiome. Nature 2012, 488:86-90.
48. Weng J.-K., Phillipe R.N., Noel J.P. The rise of chemodiversity in plants. Science 2012, 336:1667-1670.
49. Milo R., Last R.L.L. Achieving diversity in the face of constraints: lessons from metabolism. Science 2012, 336:1663-1667.
50. Holland M.A., Polacco J.C. Urease-null and hydrogenase-null phenotypes of a phylloplane bacterium reveal altered nickel metabolism in two soybean mutants. Plant Physiol. 1992, 98:942-948.
51. Splittstoesser W.E. Metabolism of Arg by aging and 7 day old pumpkin seedling. Plant Physiol. 1969, 44:361-366.
52. Kollöffel C., Van Dijke H.D. Mitochondrial arginase activity from cotyledons of developing and germinating seeds of Vicia faba L. Plant Physiol. 1975, 55:507-510.
53. Matsubara S., Suzuki Y. Arginase activity in the cotyledons of soybean seedlings. Physiol. Plant 1984, 62:309-314.
54. Kang J.H., Cho Y.D. Purification and properties of arginase from soybean (Glycine max) axes. Plant Physiol. 1990, 93:1230-1234.
55. Goldraij A., Polacco J.C. Arginase is inoperative in developing soybean seeds. Plant Physiol. 1999, 119:297-304.
56. Zonia L.E., Stebbins N.E., Polacco J.C. Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol. 1995, 107:1097-1103.
57. King J.E., Gifford D.J. Amino acid utilization in seeds of loblolly pine during germination and early seedling growth. I. Arginine and arginase activity. Plant Physiol. 1997, 113:1125-1135.
58. Mishra D., Kar M. Nickel in plant growth and metabolism. Bot. Rev. 1974, 40:395-452.
59. Graham R.D., Welch R.M., A role for nickel in the resistance of plants to rust. Australian Agronomy Conference 1985, 337. Australian Society of Agronomy, Hobart. A. Agronomy (Ed.).
60. Freyermuth S.K., Bacanamwo M., Polacco J.C. The soybean Eu3 gene encodes a Ni-binding protein necessary for urease activity. Plant J. 2000, 21:53-60.
61. Wood B.W., Reilly C.C. Interaction of nickel and plant disease. Mineral Nutrition and Plant Disease 2007, 217-247. American Phytopathological Society Press, Minneapolis. L.E. Datnoff, W.H. Elmer, D.M. Huber (Eds.).
62. Boyd R.S. The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 2007, 293:153-176.
63. Wiebke-Ströhm B., et al. Ubiquitious urease affects soybean susceptibility to fungi. Plant Mol. Biol. 2012, 79:75-87.
64. Martens S.N., Boyd R.S. The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 1994, 98:379-384.
65. Boyd R.S. Elemental defenses of plants by metals. Nat. Educ. Knowl. 2010, 1:6.
66. Boyd R.S. Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci. 2012, 195:88-95.
67. Davis M.A., Boyd R.S. Dynamics of Ni-based defense and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae). New Phytol. 2000, 146:211-217.
68. Brooks R.R. Serpentine and its Vegetation. A Multidisciplinary Approach 1987, Dioscorides Press, Inc., Portland, OR.
69. Coleman C.M., Boyd R.S., Eubanks M.D. Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. J. Chem. Ecol. 2005, 31:1669-1681.
70. Davis M.A., Murphy J.F., Boyd R.S. Nickel increases susceptibility of a nickel hyperaccumulator to Turnip mosaic virus. J. Environ. Qual. 2001, 40:85-90.
71. Wang D., Wang Y. Nickel sulfate induces numerous defects in Caenorhabditis elegans that can also be transferred to progeny. Environ. Pollut. 2008, 151:585-592.
72. Duxbury T. Toxicity of heavy metals to soil bacteria. FEMS Microbiol. Lett. 1981, 11:217-220.
73. Babich H., Stotzky G. Toxicity of nickel to microorganisms in soil: Influence of some physicochemical characteristics. Environ. Pollut. A 1982, 29:303-315.
74. Wang K.L.-C., Li H., Ecker J.R. Ethylene biosynthesis and signaling networks. Plant Cell 2002, 14:S131-S151.
75. Brown P.H. Nickel. Handbook of Plant Nutrition 2007, 395-409. CRC Press, Boca Raton, FL. A.V. Barker, D.J. Pilbeam (Eds.).
76. Lau O.L., Yang S.F. Inhibition of ethylene production by cobaltous ion. Plant Physiol. 1976, 58:114-117.
77. McGarvey D.J., Christoffersen R.E. Characterization and kinetic parameters of ethylene-forming enzyme from avocado fruit. J. Biol. Chem. 1992, 267:5964-5967.
78. Carter E.L., Tronrud D.E., Taber S.R., Karplus P.A., Hausinger R.P. Iron-containing urease in a pathogenic bacterium. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:13095-13099.
79. Itamura H., Ohno Y., Yamamura H. Characteristics of fruit softening in Japanese persimmon. Acta Horticult. 1997, 685:37-44.
80. Zheng Q.L., Nakatsuka A., Itamura H. Extraction and characterization of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase from wounded persimmon fruit. J. Jap. Soc. Horticult. Sci. 2005, 74:159-166.
81. Zheng Q.L., Nakatsuka A., Matsumoto T., Itamura H. Pre-harvest nickel application to the calyx of Saijo persimmon fruit prolongs postharvest shelf-life. Postharv. Biol. Technol. 2006, 42:98-103.
82. Tezotto T., Favarin J.L., Azevedo R.A., Alleoni L.R.F., Mazzafera P. Coffee is highly tolerant to cadmium, nickel and zinc: plant and soil nutritional status, metal distribution and bean yield. Field Crops Res. 2012, 125:25-34.
83. Mazzafera P. Chemical composition of defective coffee beans. Food Chem. 1999, 64:547-554.
84. Bari R., Jones J. Role of plant hormones in plant defence responses. Plant Mol. Biol. 2009, 69:473-488.
85. Gerendás J., Polacco J.C., Freyermuth S.K., Sattelmacher B. Significance of nickel for plant growth and metabolism. J. Plant Nutr. Soil Sci. 1999, 162:241-256.
86. Winkler R.G., Polacco J.C., Eskew D.L., Welch R.M. Nickel is not required for apourease synthesis in soybean seeds. Plant Physiol. 1983, 72:262-263.
87. Cataldo D.A., Garland T.R., Wildung R.E. Nickel in plants II. Distribution and chemical form in soybean plants. Plant Physiol. 1978, 62:566-570.
88. Checkai R.T., Norvell W.A. A recirculating resin-buffered hydroponic system for controlling nutrient ion activities. J. Plant Nutr. 1992, 15:871-892.
89. + symporter in Arabidopsis. Plant Cell 2003, 15:790-800.
90. Kojima S., Bohner A., Gassert B., Yuan L., Wirén N.v. AtDUR3 represents the major transporter for high-affinity urea transport across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J. 2007, 52:30-40.
91. Shima S., et al. The crystal structure of [Fe]-hydrogenase reveals the geometry of the active site. Science 2008, 321:572-575.
92. Sumner J.B. The isolation and crystallization of the enzyme urease. J. Biol. Chem. 1926, 69:435-441.
93. Wöhler F. Ueber künstliche Bildung des Harnstoffs. Ann. Phys. 1828, 88:253-256.
94. Zerner B. Recent advances in the chemistry of an old enzyme, urease. Bioinorg. Chem. 1991, 19:116-131.
95. Krajewska B., Ureases I. Functional, catalytic and kinetic properties: a review. J. Mol. Catal. B: Enzym. 2009, 59:9-21.
96. Park I.-S., Hausinger R.P. Site-directed mutagenesis of Klebsiella aerogenes urease: identification of histidine residues that appear to function in nickel ligation, substrate binding, and catalysis. Protein Sci. 1993, 2:1034-1041.
97. Radzicka A., Wolfenden R. A proficient enzyme. Science 1995, 267:90-93.
98. Karplus P.A., Pearson M.A., Hausinger R.P. 70 years of crystalline urease: what have we learned?. ChemInform 1997, 28:330-337.
99. Van Etten C.H., Kwolek W.F., Peters J.E., Barclary A.S. Plant seeds as protein sources of food or feed. Evaluation based on amino acid composition of 379 species. J. Agric. Food Chem. 1967, 15:1077-1089.
100. Goldraij A., Polacco J.C. Arginine degradation by arginase in mitochondria of soybean seedling cotyledons. Planta 2000, 210:652-658.
101. Polacco J.C., Holland M.A. Roles of urease in plant cells. International Review of Cytology 1993, 65-103. Academic Press, San Diego. W.J. Kwang, J. Jonathan (Eds.).
102. Faye L., Greenwood J.S., Chrispeels M.J. Urease in jack bean (Canavalia ensiformis [L.] DC) seeds is a cytosolic protein. Planta 1986, 168:579-585.
103. Holland M.A., Griffin J.D., Elise Meyer-Bothling L., Polacco J.C. Developmental genetics of the soybean urease isozymes. Dev. Genet. 1987, 8:375-387.
104. Witte C.-P., Tiller S., Isidore E., Davies H.V., Taylor M.A. Analysis of two alleles of the urease gene from potato: polymorphisms, expression, and extensive alternative splicing of the corresponding mRNA. J. Exp. Bot. 2005, 56:91-99.
105. Lee E.J., Yoo K.S., Jifon J., Patil B.S. Characterization of shortday onion cultivars of 3 pungency levels with flavor precursor, free amino acid, sulfur, and sugar contents. J. Food Sci. 2009, 74:475-480.
106. Ninomiya A., Murata Y., Tada M., Shimoishi Y. Change in allantoin and arginine contents in Dioscorea opposita 'Tsukuneimo' during the growth. J. Jap. Soc. Horticult. Sci. 2004, 73:546-551.
107. Nordin A., Näsholm T. Nitrogen storage forms in nine boreal understorey plant species. Oecologia 1997, 110:487-492.
108. Bausenwein U., Millard P., Thornton B., Raven J.A. Seasonal nitrogen storage and remobilization in the forb Rumex acetosa. Funct. Ecol. 2001, 15:370-377.
109. Rennenberg H., Wildhagen H., Ehlting B. Nitrogen nutrition of poplar trees. Plant Biol. 2010, 12:275-291.
110. Elser J.J., Fagan W.F., Subramanian S., Kumar S. Signature of ecological resource availability in the animal and plant proteomes. Mol. Biol. Evol. 2006, 23:1946-1951.
111. Amarante L., Lima J.D., Sodek L. Growth and stress conditions cause similar changes in xylem amino acids for different legume species. Environ. Exp. Bot. 2006, 58:123-129.
112. Brychkova G., Alikulov Z., Fluhr R., Sagi M. A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant J. 2008, 54:496-509.
113. Vogels G.D., Drift C.v.d. Degradation of purines and pyrimidines by microorganisms. Bacteriol. Rev. 1976, 40:403-468.
114. Marzluf G.A. Regulation of nitrogen metabolism and gene expression in fungi. Microbiol. Rev. 1981, 45:437-461.
115. Cooper T.G. Nitrogen metabolism in Saccharomyces cerevisiae. The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression 1982, 39-99. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. J.N. Strathern, E.W. Jones, J.R. Broach (Eds.).
116. Kinghorn J.R., Fluri R. Genetic studies of purine breakdown in the fission yeast Schizosaccharomyces pombe. Curr. Genet. 1984, 8:99-105.
117. Piedras P., Muñoz A., Aguilar M., Pineda M. Allantoate amidinohydrolase (allantoicase) from Chlamydomonas reinhardtii: its purification and catalytic and molecular characterization. Arch. Biochem. Biophys. 2000, 378:340-348.
118. Winkler R.G., Polacco J.C., Blevins D.G., Randall D.D. Enzymic degradation of allantoate in developing soybeans. Plant Physiol. 1985, 79:787-793.
119. Winkler R.G., Blevins D.G., Polacco J.C., Randall D.D. Ureide catabolism of soybeans. II. Pathway of catabolism in intact leaf tissue. Plant Physiol. 1987, 83:585-591.
120. Winkler R.G., Blevins D.G., Randall D.D. Ureide catabolism in soybeans. III. Ureidoglycolate amidohydrolase and allantoate amidohydrolase are activities of an allantoate degrading enzyme complex. Plant Physiol. 1988, 86:1084-1088.
121. Werner A.K., Sparkes I.A., Romeis T., Witte C.-P. Identification, biochemical characterization, and subcellular localization of allantoate amidohydrolases from Arabidopsis and soybean. Plant Physiol. 2008, 146:418-430.
122. Todd C.D., Polacco J.C. AtAAH encodes a protein with allantoate amidohydrolase activity from Arabidopsis thaliana. Planta 2006, 223:1108-1113.
123. Werner A.K., Romeis T., Witte C.-P. Ureide catabolism in Arabidopsis thaliana and Escherichia coli. Nat. Chem. Biol. 2009, 6:19-21.
124. Stahlhut R.W., Widholm J.M. Ureide catabolism by soybean [Glycine-Max (L) Merrill] cell-suspension cultures. I. Urea is not an intermediate in allantoin degradation. J. Plant Physiol. 1989, 134:85-89.
125. Díaz-Leal J.L., Gálvez-Valdivieso G., Fernández J., Pineda M., Alamillo J.M. Developmental effects on ureide levels are mediated by tissue-specific regulation of allantoinase in Phaseolus vulgaris L. J. Exp. Bot. 2012, 10.1093/jxb/ers090.
126. Sagers C.L. Nutrient acquisition and concentration by ant symbionts: the incidence and importance of biological interactions to plant nutrition. Ecological Aspects of Nitrogen Metabolism in Plants 2011, 308-329. John Wiley & Sons, Inc., Hoboken, NJ. J.C. Polacco, C.D. Todd (Eds.).
127. Tao L., Hunter M.D. Effects of insect herbivores on the nitrogen economy of plants. Environmental Aspects of Nitrogen Metabolism in Plants 2011, 255-279. John Wiley & Sons, Inc., Hoboken, NJ, (Chapter 12). J.C. Polacco, C.D. Todd (Eds.).
128. Wright P.A. Nitrogen excretion: three end products, many physiological roles. J. Exp. Biol. 1995, 198:273-281.
129. Witte C.P. Urea metabolism in plants. Plant Sci. 2011, 180:431-438.
130. Mérigout P., et al. Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiol. 2008, 147:1225-1238.
131. Sumrada R.A., Cooper T.G. Urea carboxylase and allophanate hydrolase are components of a multifunctional protein in yeast. J. Biol. Chem. 1982, 257:9119-9127.
132. Dhammika H.M., et al. Dur3 is the major urea transporter in Candida albicans and is co-regulated with the urea amidolyase. Microbiology 2011, 157:270-279.
133. Thompson J.F., Muenster A.-M.E. Separation of the chlorella ATP: urea amido-lyase into two components. Biochem. Biophys. Res. Commun. 1971, 43:1049-1055.
134. Kanamori T., Kanou N., Atomi H., Imanaka T. Enzymatic characterization of a prokaryotic urea carboxylase. J. Bacteriol. 2004, 186:2532-2539.
135. Witte C.-P., Rosso M.G., Romeis T. Identification of three urease accessory proteins that are required for urease activation in Arabidopsis. Plant Physiol. 2005, 139:1155-1162.
136. Gerendás J., Zhu Z., Sattelmacher B. Influence of N and Ni supply on nitrogen metabolism and urease activity in rice (Oryza sativa L.). J. Exp. Bot. 1998, 49:1545-1554.
137. van Beusichem M.L., Neeteson J.J. Urea nutrition of young maize and sugar-beet plants with emphasis on ionic balance and vascular transport of nitrogenous compounds. Neth. J. Agric. Sci. 1982, 30:317-330.
138. Bradley D.P., Morgan M.A., O'Toole P. Uptake and apparent utilization of urea and ammonium nitrate in wheat seedlings. Nutr. Cycl. Agroecosys. 1989, 20:41-49.
139. Allen A.E., et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 2011, 473:203-207.
140. Witte C.-P., Tiller S.A., Taylor M.A., Davies H.V. Addition of nickel to Murashige and Skoog medium in plant tissue culture activates urease and may reduce metabolic stress. Plant Cell Tiss. Org. Cult. 2002, 68:103-104.
141. Murashige C., Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 1962, 15:473-497.
142. Tan X.W., Ikeda H., Oda M. Effects of nickel concentration in the nutrient solution on the nitrogen assimilation and growth of tomato seedlings in hydroponic culture supplied with urea or nitrate as the sole nitrogen source. Sci. Hortic. 2000, 84:265-273.
143. Cao F.-Q., et al. Identification and characterization of proteins involved in rice urea and arginine catabolism. Plant Physiol. 2010, 154:98-108.
144. Krouk G., et al. A framework integrating plant growth with hormones and nutrients. Trends Plant Sci. 2011, 16:178-182.
145. Krouk G., et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 2010, 18:927-937.
146. Malamy J.E. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 2005, 28:67-77.
147. --induced stimulation of leaf growth. J. Exp. Bot. 2005, 56:1143-1152.
148. Wang W.-H., Köhler B., Cao F.-Q., Liu L.-H., Molecular physiological aspects of urea transport in higher plants. Plant Sci. 2008, 175:467-477.
149. Soto G., et al. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J. 2010, 64:1038-1047.
150. Carter E.L., Flugga N., Boer J.L., Mulrooney S.B., Hausinger R.P. Interplay of metal ions and urease. Metallomics 2009, 1:207-221.
151. Mobley H., Island M., Hausinger R. Molecular biology of microbial ureases. Microbiol. Rev. 1995, 59:451-480.
152. Balasubramanian A., Ponnuraj K. Crystal structure of the first plant urease from jackbean: 83 years of journey from its first crystal to molecular structure. J. Mol. Biol. 2010, 400:274-283.
153. Sirko A., Brodzik R. Plant ureases: roles and regulation. Acta Biochim. Pol. 2000, 47:1189-1195.
154. Goldraij A., Beamer L.J., Polacco J.C. Interallelic complementation at the ubiquitous urease coding locus of soybean. Plant Physiol. 2003, 132:1801-1810.
155. Buttery B.R., Buzzell R.I. Properties and inheritance of urease isozymes in soybean seeds. Can. J. Bot. 1971, 49:1101-1105.
156. Kloth R.H., Hymowitz T. Re-evaluation of the inheritance of urease in soybean seed. Crop Sci. 1985, 25:352-354.
157. Meyer-Bothling L.E., Polacco J.C., Cianzio S.R. Pleiotropic soybean mutants defective in both urease isozymes. Mol. Gen. Genet. 1987, 209:432-438.
158. Kim J.K., Mulrooney S.B., Hausinger R.P. Biosynthesis of active Bacillus subtilis urease in the absence of known urease accessory proteins. J. Bacteriol. 2005, 187:7150-7154.
159. Park I.S., Carr M.B., Hausinger R.P. In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:3233-3237.
160. Carter E.L., Hausinger R.P. Characterization of the Klebsiella aerogenes urease accessory protein UreD in fusion with the maltose binding protein. J. Bacteriol. 2010, 192:2294-2304.
161. Moncrief M., Hausinger R. Purification and activation properties of UreD-UreF-urease apoprotein complexes. J. Bacteriol. 1996, 178:5417-5421.
162. Salomone-Stagni M., Zambelli B., Musiani F., Ciurli S. A model-based proposal for the role of UreF as a GTPase-activating protein in the urease active site biosynthesis. Proteins Struct. Funct. Bioinform. 2007, 68:749-761.
163. Lam R., et al. Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori. Proteins Struct. Funct. Bioinform. 2010, 78:2839-2848.
164. Moncrief M.B., Hausinger R.P. Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease. J. Bacteriol. 1997, 179:4081-4086.
165. Boer J.L., Quiroz-Valenzuela S., Anderson K.L., Hausinger R.P. Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins. Biochemistry 2010, 49:5859-5869.
166. Jabri E., Carr M.B., Hausinger R.P., Karplus P.A. The crystal structure of urease from Klebsiella aerogenes. Science 1995, 268:998-1004.
167. Fahmy A.S., Mohamed M.A., Kamel M.Y. Ureases in the Cucurbitaceae, distribution and properties. Phytochemistry 1994, 35:151-154.
168. Schlueter J., et al. Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. BMC Genom. 2007, 8:330.
169. Brayman T., Hausinger R. Purification, characterization, and functional analysis of a truncated Klebsiella aerogenes UreE urease accessory protein lacking the histidine-rich carboxyl terminus. J. Bacteriol. 1996, 178:5410-5416.
170. Gerendás J., Polacco J.C., Freyermuth S.K., Sattelmacher B. Co does not replace Ni with respect to urease activity in zucchini (Cucurbita pepo convar. giromontiina) and soybean (Glycine max). Plant Soil 1998, 203:127-135.
171. Schlueter J.A., et al. Mining EST databases to resolve evolutionary events in major crop species. Genome 2004, 47:868-876.
172. Schmutz J., et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463:178-183.
173. Bacanamwo M., Witte C.-P., Lubbers M.W., Polacco J.C. Activation of the urease of Schizosaccharomyces pombe by the UreF accessory protein from soybean. Mol. Gen. Genom. 2002, 268:525-534.
174. Polacco J.C., Freyermuth S.K., Gerendás J., Cianzio S.R. Soybean genes involved in nickel insertion into urease. J. Exp. Bot. 1999, 50:1149-1156.
175. Lee M.H., Mulrooney S.B., Renner M.J., Markowicz Y., Hausinger R.P. Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureD, ureE, ureF, and ureG) are involved in nickel metallocenter biosynthesis. J. Bacteriol. 1992, 174:4324-4330.
176. Uraguchi S., et al. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J. Exp. Bot. 2009, 60:2677-2688.
177. Fujimaki S., et al. Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol. 2010, 152:1796-1806.
178. Uraguchi S., et al. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20959-20964.