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PMID: 16025339 Published · ppublish English Journal Article

Genetic control of cell wall invertases in developing endosperm of maize.

Planta ·Vol. 223 ·No. 2 ·2006-01-00 ·Pages 159-67

Chourey PS, Jain M, Li QB, Carlson SJ

Abstract

We show here that the total invertase activity in developing seeds of maize is due to two cell wall invertase (CWI) genes, Incw1 and Incw2 (Mn1). Our previous results have shown that loss-of-function mutations at the Mn1 locus lead to the miniature-1 (mn1) seed phenotype, marked by a loss of >70% of seed weight at maturity. The mn1 seed mutant is, however, non-lethal presumably because it retains a residual low level, approximately 1%, of the total CWI activity relative to the Mn1 endosperm throughout seed development. Evidence here shows that the residual activity in the mn1 mutant is encoded by the Incw1 gene. RNA level analyses, especially quantitative real-time PCR studies, showed significant spatial and temporal heterogeneity in the expression of the two CWI genes in the developing endosperm. The Mn1-encoded Incw2 transcripts were seen at the highest levels in the basal region (the sugar unloading zone) during the early phase of cell division and elongation in the endosperm. In contrast, the highest levels of Incw1 transcripts were seen in the storage phase in both the upper (storage cells) and the lower parts of the endosperm. Protein and enzyme level analyses, however, appeared to show a lack of concordance with the RNA level of expression in both the Mn1 and mn1 endosperms, indicating a possibility of post-transcriptional control in the expression of these two genes. Collectively, the data suggest an important role for apoplastic cleavage of sucrose throughout the duration of seed development; and, of the two isoforms, the INCW2 appears to control metabolic flux of sugar utilization in the developing endosperm.

MeSH Terms
Cell Wall/enzymology,genetics Gene Expression Regulation, Developmental Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Immunohistochemistry Plant Proteins/genetics,metabolism RNA, Plant/metabolism Reverse Transcriptase Polymerase Chain Reaction Seeds/enzymology,genetics,growth & development Zea mays/enzymology,genetics,growth & development beta-Fructofuranosidase/genetics,metabolism
Chemicals
Plant Proteins RNA, Plant beta-Fructofuranosidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chourey Prem S
U. S. Department of Agriculture, Agricultural Research Service, CMAVE, Gainesville, FL 32611-0680, USA. [email protected]
Jain Mukesh
Li Qin-Bao
Carlson Susan J
References (31)
31 references, click to expand
  1. Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning.
    Plant Cell. 1999 Feb;11(2):177-89 PMID: 9927637
  2. A procedure for the small-scale isolation of plant RNA suitable for RNA blot analysis.
    Anal Biochem. 1988 Jul;172(1):279-83 PMID: 2461112
  3. The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel.
    Plant Cell. 1996 Jun;8(6):971-983 PMID: 12239408
  4. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  5. Increased potato tuber size resulting from apoplastic expression of a yeast invertase.
    Nat Biotechnol. 1997 Aug;15(8):794-7 PMID: 9255797
  6. Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.).
    Plant Cell Rep. 2005 Jun;24(4):225-36 PMID: 15759120
  7. Characterization of two members of the maize gene family, Incw3 and Incw4, encoding cell-wall invertases.
    Gene. 2000 Mar 7;245(1):89-102 PMID: 10713449
  8. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  9. The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development.
    Plant J. 2003 Jan;33(2):395-411 PMID: 12535352
  10. Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling.
    Plant Cell Physiol. 2002 Apr;43(4):452-9 PMID: 11978873
  11. An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development.
    Plant Physiol. 2004 Jan;134(1):246-54 PMID: 14657403
  12. Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials.
    Ann Bot. 2004 Nov;94(5):675-89 PMID: 15355866
  13. Cloning and characterization of full-length cDNA encoding cell-wall invertase from maize.
    Plant Physiol. 1995 Jun;108(2):873-4 PMID: 7610195
  14. Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains.
    Plant J. 2004 Feb;37(4):539-53 PMID: 14756762
  15. Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize.
    Plant Physiol. 2002 Oct;130(2):591-604 PMID: 12376627
  16. Sucrose metabolism during cotyledon development of Vicia faba L. is controlled by the concerted action of both sucrose-phosphate synthase and sucrose synthase: expression patterns, metabolic regulation and implications for seed development.
    Plant J. 1996 Jun;9(6):841-50 PMID: 8696364
  17. Enzymes of carbohydrate metabolism in the developing endosperm of maize.
    Plant Physiol. 1970 Aug;46(2):299-306 PMID: 16657454
  18. Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism.
    Plant Physiol. 1997 Sep;115(1):273-82 PMID: 9306701
  19. Control of seed mass by APETALA2.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3123-8 PMID: 15708976
  20. Sugars modulate an unusual mode of control of the cell-wall invertase gene (Incw1) through its 3' untranslated region in a cell suspension culture of maize.
    Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10512-7 PMID: 10468640
  21. Cloning of a tobacco apoplasmic invertase inhibitor. Proof of function of the recombinant protein and expression analysis during plant development.
    Plant Physiol. 1998 Feb;116(2):733-42 PMID: 9489020
  22. Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene.
    Plant Mol Biol. 2002 May;49(1):15-29 PMID: 12008896
  23. A Re-Evaluation of the Relative Roles of Two Invertases, INCW2 and IVR1, in Developing Maize Kernels and Other Tissues.
    Plant Physiol. 1999 Nov;121(3):1025-1035 PMID: 10557252
  24. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds.
    Plant Cell. 1997 Jun;9(6):895-908 PMID: 9212465
  25. Epistatic interaction and functional compensation between the two tissue- and cell-specific sucrose synthase genes in maize.
    Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):7917-21 PMID: 8058735
  26. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence.
    Plant Cell. 2004 May;16(5):1276-87 PMID: 15100396
  27. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning.
    Plant Physiol. 1999 Sep;121(1):1-8 PMID: 10482654
  28. The Maize Invertase-Deficient miniature-1 Seed Mutation Is Associated with Aberrant Pedicel and Endosperm Development.
    Plant Cell. 1992 Mar;4(3):297-305 PMID: 12297647
  29. Cytometrical evidence that the loss of seed weight in the miniature1 seed mutant of maize is associated with reduced mitotic activity in the developing endosperm.
    Plant Physiol. 2002 May;129(1):23-30 PMID: 12011334
  30. A Similar Dichotomy of Sugar Modulation and Developmental Expression Affects Both Paths of Sucrose Metabolism: Evidence from a Maize Invertase Gene Family.
    Plant Cell. 1996 Jul;8(7):1209-1220 PMID: 12239414
  31. Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana.
    Plant J. 2004 Jul;39(2):161-9 PMID: 15225282
Article Info
Journal
Planta
Abbr.
Planta
ISSN
0032-0935
Published
2006-01-00
Epub
2005-00-15
Pages
159-67
Language
English
Region
Germany
NLM ID
1250576
Subset
IM
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