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. 1996 Jun;8(6):971–983. doi: 10.1105/tpc.8.6.971

The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel.

W H Cheng 1, E W Taliercio 1, P S Chourey 1
PMCID: PMC161152  PMID: 12239408

Abstract

Collective evidence demonstrates that the Miniature1 (Mn1) seed locus in maize encodes an endosperm-specific isozyme of cell wall Invertase, CWI-2. The evidence includes (1) isolation and characterization of ethyl methanesulfonate-induced mn1 mutants with altered enzyme activity and (2) a near-linear relationship between gene/dose and invertase activity and the CWI-2 protein. In addition, molecular analyses showed that the cDNA clone incw2 maps to the Mn1 locus and differentiates the six ethyl methanesulfonate-induced mn1 mutants of independent origin into two classes when RNA gel blot analyses were used. We also report two unexpected observations that provide significant new insight into the physiological role of invertase and its regulation in a developing seed. First, a large proportion of total enzyme activity (~90%) was dispensable (i.e., nonlimiting). However, below the threshold level of ~6% of wild-type activity, the endosperm enzyme controlled both the sink strength of the developing endosperm as well as the developmental stability of maternal cells in the pedicel in a rate-limiting manner. Our data also suggest an unusually tight coordinate control between the cell wall-bound and the soluble forms of invertase, which are most likely encoded by two separate genes, presumably through metabolic controls mediated by the sugars.

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Selected References

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  1. Bartel B., Fink G. R. ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science. 1995 Jun 23;268(5218):1745–1748. doi: 10.1126/science.7792599. [DOI] [PubMed] [Google Scholar]
  2. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  3. Chourey P. S., Nelson O. E. Interallelic Complementation at the sh Locus in Maize at the Enzyme Level. Genetics. 1979 Feb;91(2):317–325. doi: 10.1093/genetics/91.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Doehlert D. C., Kuo T. M. Sugar metabolism in developing kernels of starch-deficient endosperm mutants of maize. Plant Physiol. 1990 Apr;92(4):990–994. doi: 10.1104/pp.92.4.990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Elliott K. J., Butler W. O., Dickinson C. D., Konno Y., Vedvick T. S., Fitzmaurice L., Mirkov T. E. Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Mol Biol. 1993 Feb;21(3):515–524. doi: 10.1007/BF00028808. [DOI] [PubMed] [Google Scholar]
  6. Gardiner J. M., Coe E. H., Melia-Hancock S., Hoisington D. A., Chao S. Development of a core RFLP map in maize using an immortalized F2 population. Genetics. 1993 Jul;134(3):917–930. doi: 10.1093/genetics/134.3.917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Greiner S., Weil M., Krausgrill S., Rausch T. A tobacco cDNA coding for cell-wall invertase. Plant Physiol. 1995 Jun;108(2):825–826. doi: 10.1104/pp.108.2.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  9. Miller M. E., Chourey P. S. The Maize Invertase-Deficient miniature-1 Seed Mutation Is Associated with Aberrant Pedicel and Endosperm Development. Plant Cell. 1992 Mar;4(3):297–305. doi: 10.1105/tpc.4.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Roitsch T., Bittner M., Godt D. E. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 1995 May;108(1):285–294. doi: 10.1104/pp.108.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Shanker S., Salazar R. W., Taliercio E. W., Chourey P. S. Cloning and characterization of full-length cDNA encoding cell-wall invertase from maize. Plant Physiol. 1995 Jun;108(2):873–874. doi: 10.1104/pp.108.2.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Sturm A., Chrispeels M. J. cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell. 1990 Nov;2(11):1107–1119. doi: 10.1105/tpc.2.11.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Thomas B. R., Rodriguez R. L. Metabolite Signals Regulate Gene Expression and Source/Sink Relations in Cereal Seedlings. Plant Physiol. 1994 Dec;106(4):1235–1239. doi: 10.1104/pp.106.4.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Tsai C. Y., Salamini F., Nelson O. E. Enzymes of carbohydrate metabolism in the developing endosperm of maize. Plant Physiol. 1970 Aug;46(2):299–306. doi: 10.1104/pp.46.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Unger C., Hofsteenge J., Sturm A. Purification and characterization of a soluble beta-fructofuranosidase from Daucus carota. Eur J Biochem. 1992 Mar 1;204(2):915–921. doi: 10.1111/j.1432-1033.1992.tb16712.x. [DOI] [PubMed] [Google Scholar]
  16. Wadsworth G. J., Redinbaugh M. G., Scandalios J. G. A procedure for the small-scale isolation of plant RNA suitable for RNA blot analysis. Anal Biochem. 1988 Jul;172(1):279–283. doi: 10.1016/0003-2697(88)90443-5. [DOI] [PubMed] [Google Scholar]
  17. Weil M., Krausgrill S., Schuster A., Rausch T. A 17-kDa Nicotiana tabacum cell-wall peptide acts as an in-vitro inhibitor of the cell-wall isoform of acid invertase. Planta. 1994;193(3):438–445. doi: 10.1007/BF00201824. [DOI] [PubMed] [Google Scholar]
  18. Zrenner R., Willmitzer L., Sonnewald U. Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta. 1993;190(2):247–252. doi: 10.1007/BF00196618. [DOI] [PubMed] [Google Scholar]

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