Abstract
Expression of the maize (Zea mays L.) starch branching enzyme (SBE) genes Sbe1 and Sbe2 were characterized during kernel development and in vegetative tissues. The onset of Sbe1 and Sbe2 expression during endosperm development was similar to that of other genes involved in starch biosynthesis (Wx, Sh2 and Bt2). However, the expression of Sbe2 peaked earlier than that of Sbe1 in developing endosperm and embryos resulting in a shift in the ratio of Sbe1 to Sbe2 relative message levels during kernel and embryo development. Transcripts hybridizing to the Sbe2 probe were not detectable in leaves or roots which nonetheless have SBEII enzymatic activity, suggesting that there may be another divergent SBEII-like gene(s) in maize. A similar expression pattern is shared between the maize genes and related genes in pea, which together with their evolutionary conservation, suggests that the SBE isoforms may play unique roles in starch biosynthesis during plant development.
Similar content being viewed by others
References
Baba T, Arai Y, Amano E, Itoh T: Role of the recessive amylose-extender allele in starch biosynthesis of maize. Starch/Starke 33: 79–83 (1981).
Baba T, Kimura K, Mizuno K, Etoh H, Ishida Y, Shida O, Arai Y: Sequence conservation of the catalytic regions of amylolytic enzymes in maize branching enzyme-I. Biochem Biophys Res Commun 181: 87–94 (1991).
Bae JM, Giroux M, Hannah LC: Cloning and characterization of the Brittle-2 gene of maize. Maydica 35: 317–322 (1990).
Bhattacharyya MK, Martin C, Smith A: The importance of starch biosynthesis in the wrinkled seed shape character of peas studied by Mendel. Plant Mol Biol 22: 525–531 (1993).
Bhattacharyya MK, Smith AM, Ellis THN, Hedley C, Martin C: The wrinkled-seed character of pea described by Mendel is caused by a transponson-like insertion in a gene encoding starch-branching enzyme. Cell 60: 115–122 (1990).
Bhave MR, Lawrence S, Barton C, Hannah LC: Identification and molecular characterization of Shrunken-2 cDNA clones of maize. Plant Cell 2: 581–588 (1990).
Boyer CD, Preiss J: Multiple forms of (1,4)-α-D-glucan, (1,4)-α-D-glucan-6-glycosyl transferase from developing Zea mays L. kernels. Carbohydr. Res. 61: 321–334 (1978).
Boyer CD, Preiss J: Multiple forms of starch branching enzyme of maize: evidence for independent genetic control. Biochem Biophys Res Comm 80: 169–175 (1978).
Burton RA, Bewley J, Smith AM, Bhattacharyya MK, Tatge H, Ring S, Bull V, Hamilton WDO, Martin C: Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 7: 3–15 (1995).
Commission on Plant Gene Nomenclature: Nomenclature of sequenced plant genes. Plant Mol Biol Rep 12: S1-S109 (1994).
Dang PL, Boyer CD: Maize leaf and kernel starch synthases and branching enzymes. Phytochemistry 27: 1255–1259 (1988).
Dang PL, Boyer CD: Comparison of soluble starch synthases and branching enzymes from leaves and kernels of normal and amylose extender maize. Biochem Genet 27: 521–532 (1989).
Fisher DK, Boyer CD, Hannah LC: Starch branching enzyme II from maize endosperm. Plant Physiol 102: 1045–1046 (1993).
Fisher DK, Gao M, Kim K-N, Boyer CD, Guiltinan MJ: Allelic analysis of the maize (Zea mays L.) amylose-extender locus suggests that independent genes encode starch branching enzymes IIa and IIb. Plant Physiol 110: 611–619 (1996).
Fisher DK, Gao M, Kim K-N, Boyer CD, Guiltinan MJ: Two closely related cDNAs encoding starch branching enzyme from Arabidopsis thaliana. Plant Mol Biol 30: 97–108 (1996).
Fisher DK, Kim KN, Gao M, Boyer CD, Guiltinan MJ: A cDNA encoding starch branching enzyme I from maize endosperm. Plant Physiol 108: 1313–1314 (1995).
Hedman KD, Boyer CD: Gene dosage at the amylose-extender locus of maize: effects on the level of starch branching enzymes. Biochem Genet 20: 483–492 (1982).
James MG, Robertson DS, Myers AM: Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7: 417–429 (1995).
Kawasaki T, Mizuno K, Baba T, Shimada H: Molecular analysis of the gene encoding a rice starch branching enzyme. Mol Gen Genet 237: 10–16 (1993).
Kossmann J, Visser RGF, Müller-Röber B, Willmitzer L, Sonnewald U: Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthetic genes. Mol Gen Genet 230: 39–44 (1991).
McCarty D: A simple method for extraction of RNA from maize tissue. Maize Gen Coop Newsl 60: 61 (1986).
Mendel G: Versuche uber Pflanzen-Hybriden. Verh Naturforsch Ver Brunn 4: 3–47 (1865).
Mizuno K, Kawasaki T, Shimada H, Satoh H, Kobayashi E, Okumura S, Arai Y, Baba T: Alteration of the structural properties of starch components by the lack of an isoform of starch branching enzyme in rice seeds. J Biol Chem 268: 19084–19091 (1993).
Mizuno K, Kimura K, Arai Y, Kawasaki T, Shimada H, Baba T: Starch branching enzymes from immature rice seeds. J Biochem 112: 643–651 (1992).
Nakamura Y, Takeichi T, Kawaguchi K, Yamanouchi H: Purification of two forms of starch branching enzyme (Q-enzyme) from developing rice endosperm. Physiol Plant 84: 329–335 (1992).
Nakamura Y, Yamanouchi H: Nucleotide sequence of cDNA encoding starch-branching enzyme, or Q-enzyme, from rice endosperm. Plant Physiol 99: 1265–1266 (1992).
Nelson O, Pan D: Starch synthesis in maize endosperms. Annu Rev Plant Physiol Plant Mol Biol 46: 475–496 (1995).
Poulsen P, Kreiberg JD: Starch branching enzyme cDNA from Solanum tuberosum. Plant Physiol 102: 1053–1054 (1993).
Preiss J: Biosynthesis of starch and its regulation. In: J.P. Preiss (ed) The Biochemistry of Plants, pp. 181–254. Academic Press Inc., New York (1980).
Preiss J: Biology and molecular biology of starch synthesis and its regulation. Oxf Surv Plant Mol Cell Biol 7: 59–114 (1991).
Salehuzzaman SNIM, Jacobsen E, Visser RGF: Cloning, partial sequencing and expression of a cDNA coding for branching enzyme in cassava. Plant Mol Biol 20: 809–819 (1992).
Sambrook J, Fritsch E, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Shure M, Wessler S, Fedoroff N: Molecular identification and isolation of the Waxy locus in maize. Cell 35: 225–233 (1983).
Smith AM: Major differences in isoforms of starch-branching enzyme between developing embryos of round and wrinkled-seeded peas (Pisum sativum L.). Planta 175: 270–279 (1988).
Smith AM, Denyer K, Martin CR: What controls the amount and structure of starch in storage organs. Plant Physiol 107: 673–677 (1995).
Stinard PS, Robertson DS, Schnable PS: Genetic isolation, cloning, and analysis of Mutator-induced, dominant antimorph of the maize Amylose Extenderl locus. Plant Cell 5: 1555–1566 (1993).
Takeda Y, Guan HP, Preiss J: Branching of amyloseby the branching isoenzymes of maize endosperm. Carbohydr Res 240: 253–263 (1993).
Visser RGF, Vreugdenhil D, Hendriks T, Jacobsen E: Gene expression and carbohydrate content during stolon to tuber transition in potatoes (Solanum tuberosum). Physiol Plant 90: 75–84 (1994).
Vos-Scheperkeuter GH, de Wit JG, Ponstein AS, Feestra WJ, Witholt B: Immunological comparison of the starch branching enzymes from potato tubers and maize kernels. Plant Physiol 90: 75–84 (1989).
Yamanouchi H, Nakamura Y: Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in 1-ice. Plant Cell Physiol 33: 985–991 (1992).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gao, M., Fisher, D.K., Kim, KN. et al. Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol Biol 30, 1223–1232 (1996). https://doi.org/10.1007/BF00019554
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019554