Abstract
The first step in sucrose use by maize kernels produces fructose, regardless of whether the initial reaction is catalyzed by an invertase or the reversible sucrose synthase. This fructose can enter subsequent metabolism via hexokinase, or in maize kernels, by a sorbitol dehydrogenase that reversibly converts fructose + NADH to sorbitol + NAD. High levels of SDH activity suggest that kernels synthesize considerable amounts of sorbitol, but the molecular mechanism and functional role for this process have remained equivocal. To gain insights on the role of sorbitol synthesis in maize endosperm we cloned and characterized the transcriptional control of the maize sorbitol dehydrogenase (Sdh1) gene. Data indicated that Sdh1 was essentially kernel- and endosperm-specific, with maximal expression at both the mRNA and enzyme activity levels during early kernel development. Expression was elevated in high-sugar mutants (sugary1, shrunken2), also by sugar injections, and was more pronounced when transfected tissues were incubated at low oxygen concentrations. Control of Sdh1 expression in our transient assays was largely dependent on the first intron of Sdh1. We speculate that SDH activity may represent an adaptation to the high-sugar/low-oxygen environment of the endosperm. Under these conditions, the NADH-dependent reduction of fructose to sorbitol would regenerate NAD[+], thus contributing to the maintenance of the redox and energy status of the cell.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aragão FJL, Barros LMG, Brasileiro ACM, Ribeiro G, Smith FD, Sanford JC et al (1995) Inheritance of foreign genes in transgenic bean (Phaseolus vulgaris L.) co-transformed via particle bombardment. Theor Appl Genet 93:142–150. doi:10.1007/BF00225739
Bieleski RL (1982) Sugar alcohols. In: Loewus F, Tanner W (eds) Encyclopedia of plant physiology, new series, vol 13A. Edited Springer-Verlag, Berlin, pp 158–192
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Callis J, Fromm M, Walbot V (1987) Introns increase gene expression in cultured maize cells. Genes Dev 1:1183–1200. doi:10.1101/gad.1.10.1183
Carey EE, Dickinson DB, Wei LY, Rhodes AM (1982) Occurrence of sorbitol in Zea mays. Phytochemistry 21:1909–1911. doi:10.1016/0031-9422(82)83013-6
Cheng L, Zhou R, Reidel EJ, Sharkey TD, Dandekar AM (2005) Antisense inhibition of sorbitol synthesis leads to up-regulation of starch synthesis without altering CO2 assimilation in apple leaves. Planta 220:767–776. doi:10.1007/s00425-004-1384-5
Clancy M, Hannah LC (2002) Splicing of the maize Sh1 first intron is essential for enhancement of gene expression, and a T-rich motif increases expression without affecting splicing. Plant Physiol 130:918–929. doi:10.1104/pp.008235
Cox EL, Dickinson DB (1973) Hexokinase from maize endosperm and scutellum. Plant Physiol 51:960–966
Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599. doi:10.1146/annurev.ph.54.030192.003051
Dinges JR, Colleoni C, Myers AM, James MG (2001) Molecular structures of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects. Plant Physiol 125:1406–1418. doi:10.1104/pp.125.3.1406
Doehlert DC (1987a) Ketose activity in developing maize endosperm. Plant Physiol 84:830–834
Doehlert DC (1987b) Substrate inhibition of maize endosperm sucrose synthase by fructose and its interaction with glucose inhibition. Plant Sci 52:153–157. doi:10.1016/0168-9452(87)90048-3
Doehlert DC, Kuo TM (1990) Sugar metabolism in developing kernels of starch deficient endosperm mutants of maize. Plant Physiol 92:990–994
Doehlert DC, Kuo TM (1994) Gene expression in developing kernels of some endosperm mutants of maize. Plant Cell Physiol 35:411–418
Doehlert DC, Kuo TM, Felker FC (1988) Enzymes of sucrose and hexose metabolism in developing kernels of two inbreds of maize. Plant Physiol 86:1013–1019
Duncan KA, Hardin SC, Huber ST (2006) The three maize sucrose synthase isoforms differ in distribution, localization, and phosphorilation. Plant Cell Physiol 47:959–971. doi:10.1093/pcp/pcj068
Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194
Freitas FA, Yunes JA, da Silva MJ, Arruda P, Leite A (1994) Structural characterization and promoter activity analysis of the γ-kafirin gene from sorghum. Mol Gen Genet 245:177–186. doi:10.1007/BF00283265
Halperin SJ, Koster KL (2006) Sugar effects on membrane damage during desiccation of pea embryo protoplasts. J Exp Bot 57:2303–2311. doi:10.1093/jxb/erj208
Ho L (1988) Metabolism and compartmentalization of imported sugars in sink organs in relation to sink strength. Annu Rev Plant Physiol Plant Mol Biol 39:355–378. doi:10.1146/annurev.pp.39.060188.002035
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–872. doi:10.1101/gr.9.9.868
Igamberdiev AU, Hill RD (2004) Nitrate, NO and hemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482. doi:10.1093/jxb/erh272
Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol 5:387–405. doi:10.1007/BF02667740
Jeong YM, Mun JH, Lee I, Woo JC, Hong CB, Kim SG (2006) Distinct roles of the first introns on the expression of Arabidopsis profiling gene family members. Plant Physiol 140:196–209. doi:10.1104/pp.105.071316
Kemper EL, da Silva MJ, Arruda P (1996) Effect of microprojectile bomb. parameters and osmotic treatment on particle penetration and tissue damage in transiently transformed cultured immature maize (Zea mays L.) embryos. Plant Sci 121:85–93. doi:10.1016/S0168-9452(96)04500-1
Kiyota E, de Sousa SM, Santos ML, Lima AC, Menossi M, Yunes JA et al (2007) Crystallization and preliminary X-ray diffraction analysis of maize aldose reductase. Acta Crystallogr Sect F Struct Biol Cryst Commun 63:990–992. doi:10.1107/S1744309107052670
Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540. doi:10.1146/annurev.arplant.47.1.509
Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246. doi:10.1016/j.pbi.2004.03.014
Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 2:59–69
Koch KE, Ying Z, Wu Y, Avigne WT (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51:417–427. doi:10.1093/jexbot/51.suppl_1.417
Kosugi S, Ohashi Y, Nakajima K, Arai Y (1990) An improved assay for β-glucoronidase in transformed cells: methanol almost completely suppresses a putative endogenous β-glucoronidase activity. Plant Sci 70:133–140. doi:10.1016/0168-9452(90)90042-M
Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiol Plant 70:553–557. doi:10.1111/j.1399-3054.1987.tb02857.x
Manning K (1991) Isolation of nucleic acids from plants by differential solvent precipitation. Anal Biochem 195:45–50. doi:10.1016/0003-2697(91)90292-2
Nosarszewski M, Clements AM, Downie B, Archbold DD (2004) Sorbitol dehydrogenase expression and activity during apple fruit set and early development. Physiol Plant 121:391–398. doi:10.1111/j.1399-3054.2004.00344.x
Ohta K, Moriguchi R, Kanahama K, Yamaki S, Kanayama Y (2005) Molecular evidence of sorbitol dehydrogenase in tomato, a non-Rosaceae plant. Phytochemistry 66:2822–2828. doi:10.1016/j.phytochem.2005.09.033
Pauly TA, Elkstrom JL, Beebe DA, Chrunyk B, Cunningham D, Griffor M et al (2003) X-ray crystallographic and kinetic studies of human sorbitol dehydrogenase. Structure 11:1071–1085. doi:10.1016/S0969-2126(03)00167-9
Rolland F, Moorem B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205
Rolletschek H, Koch K, Wobus U, Borisjuk L (2005) Positional cues for starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J 42:69–83. doi:10.1111/j.1365-313X.2005.02352.x
Rose AB (2002) Requirements for intron-mediated enhancement of gene expression in Arabidopsis. RNA 8:1444–1453. doi:10.1017/S1355838202020551
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor
Sergeeva LI, Vreugdenhil D (2002) In situ staining of activities of enzymes involved in carbohydrate metabolism in plant tissues. J Exp Bot 53:361–370. doi:10.1093/jexbot/53.367.361
Shaw JR, Dickinson DB (1984) Studies of sugars and sorbitol in developing corn kernels. Plant Physiol 75:207–211
Spielbauer G, Margl L, Hannah LC, Romisch W, Ettenhuber C, Bacher A et al (2006) Robustness of central carbohydrate metabolism in developing maize kernels. Phytochemistry 67:1460–1475. doi:10.1016/j.phytochem.2006.05.035
Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407. doi:10.1016/S1360-1385(99)01470-3
Teo G, Suzuki Y, Uratsu SL, Lampinen B, Ormonde N, Hu WK et al (2006) Silencing leaf sorbitol synthesis alters long-distance partitioning and apple fruit quality. Proc Natl Acad Sci USA 103:18842–18847. doi:10.1073/pnas.0605873103
Tomkins JP, Davis G, Main D, Duru N, Musket T, Goicoechea JL et al (2002) Construction and characterization of a deep-coverage bacterial artificial chromosome library for maize. Crop Sci 42:928–933
Tsai CY, Salamini F, Nelson OE (1970) Enzymes of carbohydrate metabolism in the developing endosperm of maize. Plant Physiol 46:299–306
Verza NC, Silva TR, Cord Neto G, Nogueira FTS, deBrito PHF, de Rosa VEJ et al (2005) Endosperm-preferred expression of maize genes as revealed by transcriptome-wide analysis of expressed sequence tags. Plant Mol Biol 59:363–374. doi:10.1007/s11103-005-8924-7
Werr W, Frommer W-B, Maas C, Starlinger P (1985) Structure of the sucrose synthase gene on chromosome 9 of Zea mays L. EMBO J 4:1373–1380
Young TE, Gallie DR, DeMason DA (1997) Ethylene mediated programmed cell death during maize endosperm development of su1 and sh2 genotypes. Plant Physiol 115:737–751
Xu J, Avigne WT, McCarty DR, Koch KE (1996) A similar dichotomy of sugar modulation and developmental expression affects both paths of sucrose metabolism: evidence from a maize invertase gene family. Plant Cell 8:1209–1220
Zeng Y, Wu Y, Avigne WT, Koch KE (1998) Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional response. Plant Physiol 116:1573–1583. doi:10.1104/pp.116.4.1573
Zimmermann MH, Ziegler H (1975) List of sugars and sugar alcohols in sieve-tube exudates. In: Transport in plants I: phloem transport. Springer-Verlag, Berlin
Acknowledgments
The authors wish to thank the Structural Molecular Biology Center (CEBIME) researchers from the National Synchrotron Light Laboratory (LNLS) for technical expertise in MS/MS experiments. We thank Karen E. Koch for critical reading of the manuscript. This work was supported by CNPq. S.M.S. was recipient of a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). M.D.G.P was recipient of fellowship from FAPESP.
Author information
Authors and Affiliations
Corresponding author
Additional information
Accession numbers
Sequence data from this article can be found in the GenBank/EMBL data libraries under the following accession numbers: DQ191049 (SDH) and DU132578 to DU133156.
Rights and permissions
About this article
Cite this article
de Sousa, S.M., Paniago, M.d.G., Arruda, P. et al. Sugar levels modulate sorbitol dehydrogenase expression in maize. Plant Mol Biol 68, 203–213 (2008). https://doi.org/10.1007/s11103-008-9362-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-008-9362-0