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Plant Physiol. (1999) 121: 1-8 UPDATE ON BIOCHEMISTRY Invertases. Primary Structures, Functions, and Roles in Plant Development and Sucrose Partitioning
Friedrich Miescher Institute, Maulbeerstrasse 66, CH-4058 Basel, Switzerland
One of the key features of plants is their ability
to reduce carbon dioxide in the presence of sunlight and water to
sugars, and the subsequent transport of assimilated carbon to the
nonphotosynthetic tissues (sink tissues). In most plants, the
transported sugar is Suc, a nonreducing disaccharide, in which Glc and
Fru are linked ( Utilization of Suc as a source of carbon and energy depends on its
cleavage into hexoses, and in plants either Suc synthase (EC 2.4.1.13)
or invertase (EC 3.2.1.26) catalyzes this reaction. Suc synthase is a
glycosyl transferase, which converts Suc in the presence of UDP into
UDP-Glc and Fru. Invertase is a hydrolase, cleaving Suc into the two
monosaccharides. Suc synthase is a cytoplasmic enzyme and, in most
plants, two closely related isoforms have been identified (for summary,
see Sturm et al., 1999 Most plant species contain at least two isoforms of vacuolar
invertase, which accumulate as soluble proteins (soluble acid invertases) in the lumen of this acidic compartment. Likewise, several
isoforms of extracellular invertase (cell wall invertases) that are
ionically bound to the cell wall have been detected. Vacuolar and cell
wall invertases share some biochemical properties, e.g. they cleave Suc
most efficiently between pH 4.5 and 5.0 and attack the disaccharide
from the Fru residue. Thus, these so-called acid invertases are
Acid invertases have been purified from several plant species (for
summary, see Unger et al., 1992 Like plant invertase, yeast invertase exists in different isoforms
with discrete subcellular locations (Carlson and Botstein, 1982
Because the plant invertases with pH optima between 7.0 and 7.8 are extremely labile and enzyme activity is rapidly lost after tissue
homogenization, their purification turned out to be very difficult.
Only in a few cases were polypetides of apparent electrophoretic homogeneity obtained (for summary, see Ross et al., 1996 Recently, a cDNA was obtained from poison rye grass (Lolium
temulentum) that codes for a polypeptide with neutral/alkaline invertase activity (Gallagher and Pollock, 1998 Genes for acid invertases have been isolated from tomato (Elliott
et al., 1993
During the purification of cell wall invertase from a suspension
culture of tobacco, a small polypeptide of 17 kD that inhibits enzyme
activity in a pH-dependent manner was identified (Weil et al., 1994 In connection with the various roles Suc plays in plants
(nutrient, osmoticum, and signal molecule), invertases may have several different functions (Fig. 3). Most
likely, invertases cleave Suc into hexoses to provide cells with fuel
for respiration and with carbon and energy for the synthesis of
numerous different compounds. Invertases may also be involved in the
long-distance transport of Suc by generating the necessary Suc
concentration gradient between sites of phloem loading and unloading
(Eschrich, 1980
A more controversial question is whether invertases are involved
in Suc metabolism in actively filling sink organs such as seeds,
tubers, or roots. In developing seeds of lima bean and tubers of
potato, Suc synthase was found to be the prominent Suc breakdown
activity, and sucrolysis via invertase was low and secondary (Sung et
al., 1989 Marked changes in the activity of acid and alkaline invertases
appear to be intimately related to the process of cell differentiation in carrot tissue cultures (Silva and Ricardo, 1992 During the past decade, great progress has been made in the
characterization and functional analysis of plant invertases. Despite
these accomplishments, numerous important questions still need to be
answered. Why are there invertases with different properties in
different subcellular compartments and how do these enzymes cooperate?
What is the function of neutral/alkaline invertase and why does it
exist only in photosynthetic organisms? Under what conditions do the
products of Suc hydrolysis regulate invertase gene expression and
enzyme activity? What other metabolites or effector molecules modulate
invertase expression? What is the role of the proteinaceous invertase
inhibitor (Greiner et al., 1998
Received May 20, 1999;
accepted June 1, 1999.
I thank my colleagues Guo-Qing Tang and Patrick J. King (Friedrich Miescher Institute) for critical reading of the manuscript and Thomas Rausch (University of Heidelberg) for helpful discussions.
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P. Geigenberger Regulation of sucrose to starch conversion in growing potato tubers J. Exp. Bot., January 3, 2003; 54(382): 457 - 465. [Abstract] [Full Text] [PDF] |
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T. Roitsch, M. E. Balibrea, M. Hofmann, R. Proels, and A. K. Sinha Extracellular invertase: key metabolic enzyme and PR protein J. Exp. Bot., January 3, 2003; 54(382): 513 - 524. [Abstract] [Full Text] [PDF] |
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S. M. Sherson, H. L. Alford, S. M. Forbes, G. Wallace, and S. M. Smith Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis J. Exp. Bot., January 3, 2003; 54(382): 525 - 531. [Abstract] [Full Text] [PDF] |
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H. Rosenkranz, R. Vogel, S. Greiner, and T. Rausch In wounded sugar beet (Beta vulgaris L.) tap-root, hexose accumulation correlates with the induction of a vacuolar invertase isoform J. Exp. Bot., December 1, 2001; 52(365): 2381 - 2385. [Abstract] [Full Text] [PDF] |
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E. M. Farre, A. Tiessen, U. Roessner, P. Geigenberger, R. N. Trethewey, and L. Willmitzer Analysis of the Compartmentation of Glycolytic Intermediates, Nucleotides, Sugars, Organic Acids, Amino Acids, and Sugar Alcohols in Potato Tubers Using a Nonaqueous Fractionation Method Plant Physiology, October 1, 2001; 127(2): 685 - 700. [Abstract] [Full Text] [PDF] |
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W. Van den Ende, A. Michiels, D. Van Wonterghem, S. P. Clerens, J. De Roover, and A. J. Van Laere Defoliation Induces Fructan 1-Exohydrolase II in Witloof Chicory Roots. Cloning and Purification of Two Isoforms, Fructan 1-Exohydrolase IIa and Fructan 1-Exohydrolase IIb. Mass Fingerprint of the Fructan 1-Exohydrolase II Enzymes Plant Physiology, July 1, 2001; 126(3): 1186 - 1195. [Abstract] [Full Text] [PDF] |
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M. Goetz, D. E. Godt, A. Guivarc'h, U. Kahmann, D. Chriqui, and T. Roitsch Induction of male sterility in plants by metabolic engineering of the carbohydrate supply PNAS, May 22, 2001; 98(11): 6522 - 6527. [Abstract] [Full Text] [PDF] |
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R. Viola, A. G. Roberts, S. Haupt, S. Gazzani, R. D. Hancock, N. Marmiroli, G. C. Machray, and K. J. Oparka Tuberization in Potato Involves a Switch from Apoplastic to Symplastic Phloem Unloading PLANT CELL, February 1, 2001; 13(2): 385 - 398. [Abstract] [Full Text] |
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E. Gout, A.-M. Boisson, S. Aubert, R. Douce, and R. Bligny Origin of the Cytoplasmic pH Changes during Anaerobic Stress in Higher Plant Cells. Carbon-13 and Phosphorous-31 Nuclear Magnetic Resonance Studies Plant Physiology, February 1, 2001; 125(2): 912 - 925. [Abstract] [Full Text] |
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U. Roessner, A. Luedemann, D. Brust, O. Fiehn, T. Linke, L. Willmitzer, and A. R. Fernie Metabolic Profiling Allows Comprehensive Phenotyping of Genetically or Environmentally Modified Plant Systems PLANT CELL, January 1, 2001; 13(1): 11 - 29. [Abstract] [Full Text] |
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M. Lüscher, U. Hochstrasser, G. Vogel, R. Aeschbacher, V. Galati, C. J. Nelson, T. Boller, and A. Wiemken Cloning and Functional Analysis of Sucrose:Sucrose 1-Fructosyltransferase from Tall Fescue Plant Physiology, November 1, 2000; 124(3): 1217 - 1228. [Abstract] [Full Text] |
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A. F. López-Millán, F. Morales, A. Abadía, and J. Abadía Effects of Iron Deficiency on the Composition of the Leaf Apoplastic Fluid and Xylem Sap in Sugar Beet. Implications for Iron and Carbon Transport Plant Physiology, October 1, 2000; 124(2): 873 - 884. [Abstract] [Full Text] |
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E. M. Farré, P. Geigenberger, L. Willmitzer, and R. N. Trethewey A Possible Role for Pyrophosphate in the Coordination of Cytosolic and Plastidial Carbon Metabolism within the Potato Tuber Plant Physiology, June 1, 2000; 123(2): 681 - 688. [Abstract] [Full Text] |
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