Home LiteratureArticle Details
PMID: 15377758 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis.

The Plant cell ·Vol. 16 ·No. 10 ·2004-10-00 ·Pages 2614-28

Acosta-García G, Vielle-Calzada JP

Abstract

Classical arabinogalactan proteins (AGPs) are an abundant class of cell surface proteoglycans widely distributed in flowering plants. We have used a combination of enhancer detection tagging and RNA interference (RNAi)-induced posttrancriptional silencing to demonstrate that AGP18, a gene encoding a classical arabinogalactan protein, is essential for female gametogenesis in Arabidopsis thaliana. AGP18 is expressed in cells that spatially and temporally define the sporophytic to gametophytic transition and during early stages of seed development. More than 75% of the T1 transformants resulted in T2 lines showing reduced seed set during at least three consecutive generations but no additional developmental defects. AGP18-silenced T2 lines showed reduced AGP18 transcript levels in female reproductive organs, the presence of 21-bp RNA fragments specific to the AGP18 gene, and the absence of in situ AGP18 mRNA localization in developing ovules. Reciprocal crosses to wild-type plants indicate that the defect is female specific. The genetic and molecular analysis of AGP18-silenced plants containing a single T-DNA RNAi insertion suggests that posttranscriptional silencing of AGP18 is acting both at the sporophytic and gametophytic levels. A cytological analysis of all defective AGP18-RNAi lines, combined with the analysis of molecular markers acting at key stages of female gametogenesis, showed that the functional megaspore fails to enlarge and mitotically divide, indicating that AGP18 is essential to initiate female gametogenesis in Arabidopsis. Our results assign a specific function in plant development to a gene encoding a classical AGP.

MeSH Terms
Arabidopsis/embryology,physiology Base Sequence DNA Primers Enhancer Elements, Genetic In Situ Hybridization Molecular Sequence Data Mucoproteins/genetics,physiology Plant Proteins RNA Interference Reproduction/physiology Seeds/growth & development
Chemicals
DNA Primers Mucoproteins Plant Proteins arabinogalactan proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Acosta-García Gerardo
Laboratory of Reproductive Development and Apomixis, Department of Genetic Engineering, Centro de Investigación y Estudios Avanzados, Unidad Irapuato, Irapuato Guanajuato, Mexico.
Vielle-Calzada Jean-Philippe
References (72)
72 references, click to expand
  1. The classical arabinogalactan protein gene family of arabidopsis.
    Plant Cell. 2000 Sep;12(9):1751-68 PMID: 11006345
  2. The Ovule and the Embryo Sac.
    Plant Cell. 1993 Oct;5(10):1291-1301 PMID: 12271029
  3. Glycosylation motifs that direct arabinogalactan addition to arabinogalactan-proteins.
    Plant Physiol. 2003 Jul;132(3):1362-9 PMID: 12857818
  4. N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis.
    Plant Physiol. 2001 Apr;125(4):1880-90 PMID: 11299367
  5. The molecular and genetic basis of ovule and megagametophyte development.
    Semin Cell Dev Biol. 1998 Apr;9(2):227-38 PMID: 9599420
  6. Isolation of the protein backbone of an arabinogalactan-protein from the styles of Nicotiana alata and characterization of a corresponding cDNA.
    Plant Cell. 1994 Nov;6(11):1643-53 PMID: 7827496
  7. A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower.
    Cell. 1995 Aug 11;82(3):395-403 PMID: 7634329
  8. Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube.
    Planta. 1998 Apr;204(4):450-8 PMID: 9684368
  9. Genetics of gametophyte biogenesis in Arabidopsis.
    Curr Opin Plant Biol. 2000 Feb;3(1):53-7 PMID: 10679449
  10. Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis.
    Electrophoresis. 1999 Jul;20(10):2027-35 PMID: 10451111
  11. Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11664-9 PMID: 10500234
  12. The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1.
    Genes Dev. 2003 Jun 15;17(12):1540-53 PMID: 12815071
  13. Transcriptional silencing and promoter methylation triggered by double-stranded RNA.
    EMBO J. 2000 Oct 2;19(19):5194-201 PMID: 11013221
  14. The complex structures of arabinogalactan-proteins and the journey towards understanding function.
    Plant Mol Biol. 2001 Sep;47(1-2):161-76 PMID: 11554470
  15. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity.
    Genes Dev. 1999 Nov 15;13(22):2971-82 PMID: 10580004
  16. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA.
    Science. 2002 Sep 20;297(5589):2053-6 PMID: 12242443
  17. A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of beta-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana.
    Plant J. 1996 Jun;9(6):919-25 PMID: 8696368
  18. Identification of a transitional cell state in the developmental pathway to carrot somatic embryogenesis.
    J Cell Biol. 1992 Dec;119(5):1371-80 PMID: 1280275
  19. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  20. Ten years of enhancer detection: lessons from the fly.
    Plant Cell. 1999 Dec;11(12):2271-81 PMID: 10590157
  21. Effectiveness of RNA interference in transgenic plants.
    FEBS Lett. 2004 May 21;566(1-3):223-8 PMID: 15147899
  22. Arabinogalactan-proteins: structure, expression and function.
    Cell Mol Life Sci. 2001 Sep;58(10):1399-417 PMID: 11693522
  23. Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):7921-6 PMID: 9653116
  24. Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana.
    Cold Spring Harb Symp Quant Biol. 1997;62:35-47 PMID: 9598334
  25. Incompatibility in Flowering Plants: Adaptation of an Ancient Response.
    Plant Cell. 1995 Jan;7(1):5-16 PMID: 12242348
  26. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR.
    Plant J. 1995 Sep;8(3):457-63 PMID: 7550382
  27. Arabinogalactan proteins and plant differentiation.
    Plant Mol Biol. 1996 Mar;30(6):1077-86 PMID: 8704120
  28. The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis.
    Plant J. 2003 Dec;36(6):853-66 PMID: 14675450
  29. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis.
    Genetics. 1998 Jun;149(2):621-31 PMID: 9611178
  30. Presence of a glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins.
    J Biol Chem. 1999 May 21;274(21):14724-33 PMID: 10329668
  31. The dyad gene is required for progression through female meiosis in Arabidopsis.
    Development. 2000 Jan;127(1):197-207 PMID: 10654613
  32. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein.
    Development. 2003 Dec;130(24):5975-87 PMID: 14573517
  33. Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis.
    Science. 1995 May 12;268(5212):877-80 PMID: 7754372
  34. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis.
    Dev Biol. 1998 Oct 1;202(1):136-51 PMID: 9758709
  35. Total silencing by intron-spliced hairpin RNAs.
    Nature. 2000 Sep 21;407(6802):319-20 PMID: 11014180
  36. Molecular cloning of a gene encoding an arabinogalactan-protein from pear (Pyrus communis) cell suspension culture.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10305-9 PMID: 7937945
  37. A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth.
    Cell. 1995 Aug 11;82(3):383-93 PMID: 7634328
  38. Chemical and physical properties of an arabinogalactan-peptide from wheat endosperm.
    Biochem J. 1974 Jun;139(3):535-45 PMID: 4850989
  39. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes.
    Cell. 2004 Feb 20;116(4):577-89 PMID: 14980224
  40. Soluble Signals from Cells Identified at the Cell Wall Establish a Developmental Pathway in Carrot.
    Plant Cell. 1997 Dec;9(12):2225-2241 PMID: 12237357
  41. Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case.
    Plant Physiol. 2002 Aug;129(4):1448-63 PMID: 12177459
  42. An Arabidopsis histidine kinase is essential for megagametogenesis.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15800-5 PMID: 12426401
  43. The multiple roles of arabinogalactan proteins in plant development.
    Plant Physiol. 2000 Jan;122(1):3-10 PMID: 10631243
  44. Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana.
    Development. 1997 Apr;124(7):1367-76 PMID: 9118807
  45. Development and function of the angiosperm female gametophyte.
    Annu Rev Genet. 2002;36:99-124 PMID: 12429688
  46. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13959-64 PMID: 9811908
  47. Delayed activation of the paternal genome during seed development.
    Nature. 2000 Mar 2;404(6773):91-4 PMID: 10716449
  48. AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression.
    Plant J. 1997 Jan;11(1):1-14 PMID: 9025299
  49. Developmental Regulation of a Plasma Membrane Arabinogalactan Protein Epitope in Oilseed Rape Flowers.
    Plant Cell. 1991 Dec;3(12):1317-1326 PMID: 12324592
  50. Fucosylated arabinogalactan-proteins are required for full root cell elongation in arabidopsis.
    Plant J. 2002 Oct;32(1):105-13 PMID: 12366804
  51. NaAGP4 is an arabinogalactan protein whose expression is suppressed by wounding and fungal infection in Nicotiana alata.
    Protoplasma. 2001;215(1-4):128-39 PMID: 11732052
  52. Detection of glycosyl-phosphatidylinositol-anchored proteins on the surface of Nicotiana tabacum protoplasts.
    FEBS Lett. 1997 Mar 17;405(1):1-4 PMID: 9094413
  53. Glycosyl-phosphatidylinositol-anchor addition signals are processed in Nicotiana tabacum.
    Plant J. 2000 Jan;21(1):43-52 PMID: 10652149
  54. Proteoglycans and related components in plant cells.
    Int Rev Cytol. 1997;174:195-291 PMID: 9161008
  55. The maternal chromosome set is the target of the T-DNA in the in planta transformation of Arabidopsis thaliana.
    Genetics. 2000 Aug;155(4):1875-87 PMID: 10924482
  56. Apomixis: seasonal and population differences in a grass.
    Science. 1967 Jul 21;157(3786):325-6 PMID: 6028403
  57. Gene traps: tools for plant development and genomics.
    Plant Cell. 2000 Jul;12(7):1007-20 PMID: 10899970
  58. A species of small antisense RNA in posttranscriptional gene silencing in plants.
    Science. 1999 Oct 29;286(5441):950-2 PMID: 10542148
  59. The molecular and genetic control of ovule development.
    Curr Opin Plant Biol. 1999 Feb;2(1):13-7 PMID: 10047571
  60. Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A genomic analysis.
    Plant Physiol. 2002 Jun;129(2):486-99 PMID: 12068095
  61. Isolation of ethyl methanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1.
    Genetics. 1999 Feb;151(2):849-63 PMID: 9927475
  62. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein.
    Genes Dev. 1999 Aug 15;13(16):2108-17 PMID: 10465788
  63. AtAGP30, an arabinogalactan-protein in the cell walls of the primary root, plays a role in root regeneration and seed germination.
    Plant J. 2003 Oct;36(2):256-70 PMID: 14535889
  64. Tomato LeAGP-1 is a plasma membrane-bound, glycosylphosphatidylinositol-anchored arabinogalactan-protein.
    Physiol Plant. 2004 Feb;120(2):319-327 PMID: 15032867
  65. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements.
    Genes Dev. 1995 Jul 15;9(14):1797-810 PMID: 7622040
  66. Molecular cloning of cDNAs encoding the protein backbones of arabinogalactan-proteins from the filtrate of suspension-cultured cells of Pyrus communis and Nicotiana alata.
    Plant J. 1995 Aug;8(2):269-81 PMID: 7670506
  67. COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis.
    Genes Dev. 2001 May 1;15(9):1115-27 PMID: 11331607
  68. A proteoglycan mediates inductive interaction during plant vascular development.
    Nature. 2004 Jun 24;429(6994):873-8 PMID: 15215864
  69. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots.
    EMBO J. 1989 Feb;8(2):335-41 PMID: 16453870
  70. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4985-90 PMID: 10781109
  71. RNA interference is mediated by 21- and 22-nucleotide RNAs.
    Genes Dev. 2001 Jan 15;15(2):188-200 PMID: 11157775
  72. Identification of T-DNA tagged Arabidopsis mutants that are resistant to transformation by Agrobacterium.
    Mol Gen Genet. 1999 Apr;261(3):429-38 PMID: 10323222
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-10-00
Epub
2004-00-17
Pages
2614-28
Language
English
Region
England
NLM ID
9208688
PMCID
PMC520959
Subset
IM
Databases
RefSeq
NM_119909
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com