Home LiteratureArticle Details
PMID: 18667720 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Comparative transcriptomics of Arabidopsis sperm cells.

Plant physiology ·Vol. 148 ·No. 2 ·2008-10-00 ·Pages 1168-81

Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijó JA, Becker JD

Abstract

In flowering plants, the two sperm cells are embedded within the cytoplasm of the growing pollen tube and as such are passively transported to the embryo sac, wherein double fertilization occurs upon their release. Understanding the mechanisms and conditions by which male gametes mature and take part in fertilization are crucial goals in the study of plant reproduction. Studies of gene expression in male gametes of maize (Zea mays) and Plumbago and in lily (Lilium longiflorum) generative cells already showed that the previously held view of transcriptionally inert male gametes was not true, but genome-wide studies were lacking. Analyses in the model plant Arabidopsis (Arabidopsis thaliana) were hindered, because no method to isolate sperm cells was available. Here, we used fluorescence-activated cell sorting to isolate sperm cells from Arabidopsis, allowing GeneChip analysis of their transcriptome at a genome-wide level. Comparative analysis of the sperm cell transcriptome with those of representative sporophytic tissues and of pollen showed that sperm has a distinct and diverse transcriptional profile. Functional classifications of genes with enriched expression in sperm cells showed that DNA repair, ubiquitin-mediated proteolysis, and cell cycle progression are overrepresented Gene Ontology categories. Moreover, analysis of the small RNA and DNA methylation pathways suggests that distinct mechanisms might be involved in regulating the epigenetic state of the paternal genome. We identified numerous candidate genes whose involvement in sperm cell development and fertilization can now be directly tested in Arabidopsis. These results provide a roadmap to decipher the role of sperm-expressed proteins.

MeSH Terms
Arabidopsis/cytology,genetics,metabolism Arabidopsis Proteins/genetics,metabolism Cell Cycle/genetics DNA Methylation DNA Repair/genetics Expressed Sequence Tags Flow Cytometry Gene Expression Profiling Gene Library Genes, Plant Genome, Plant Plants, Genetically Modified/cytology,genetics,metabolism Pollen/cytology,genetics,metabolism Principal Component Analysis RNA, Messenger/genetics RNA, Plant/genetics Reverse Transcriptase Polymerase Chain Reaction Ubiquitination/genetics
Chemicals
Arabidopsis Proteins RNA, Messenger RNA, Plant
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Borges Filipe
Instituto Gulbenkian de Ciência, Centro de Biologia do Desenvolvimento, Oeiras, Portugal.
Gomes Gabriela
Gardner Rui
Moreno Nuno
McCormick Sheila
Feijó José A
Becker Jörg D
References (62)
62 references, click to expand
  1. Comparative analysis of the Arabidopsis pollen transcriptome.
    Plant Physiol. 2003 Jun;132(2):640-52 PMID: 12805594
  2. A gene expression map of Arabidopsis thaliana development.
    Nat Genet. 2005 May;37(5):501-6 PMID: 15806101
  3. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel.
    Nature. 2006 Feb 9;439(7077):737-40 PMID: 16467839
  4. AtTPK4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner.
    Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15621-6 PMID: 15505206
  5. GEX3, expressed in the male gametophyte and in the egg cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early embryogenesis.
    Mol Plant. 2008 Jul;1(4):586-98 PMID: 19825564
  6. The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway.
    Plant Mol Biol. 2007 Apr;63(6):777-85 PMID: 17221360
  7. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization.
    Development. 2006 Dec;133(23):4761-9 PMID: 17079265
  8. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants.
    Curr Biol. 2007 Jun 19;17(12):1032-7 PMID: 17555967
  9. Arabidopsis endogenous small RNAs: highways and byways.
    Trends Plant Sci. 2006 Sep;11(9):460-8 PMID: 16893673
  10. Transcriptome profiling of Lilium longiflorum generative cells by cDNA microarray.
    Plant Cell Rep. 2007 Jul;26(7):1045-52 PMID: 17245599
  11. Male gametic cell-specific gene expression in flowering plants.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2554-8 PMID: 10051681
  12. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing.
    EMBO J. 2007 Mar 21;26(6):1691-701 PMID: 17332757
  13. A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis.
    Nat Genet. 2006 Jan;38(1):63-7 PMID: 16311592
  14. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase.
    Plant Cell. 2006 May;18(5):1166-76 PMID: 16582009
  15. Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3.
    Plant J. 2005 Nov;44(4):557-68 PMID: 16262706
  16. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization.
    Nat Cell Biol. 2006 Jan;8(1):64-71 PMID: 16378100
  17. Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana.
    Development. 2008 Jan;135(1):65-73 PMID: 18045841
  18. MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis.
    EMBO Rep. 2006 Dec;7(12):1273-8 PMID: 17082821
  19. Male gametic cell-specific expression of H2A and H3 histone genes.
    Plant Mol Biol. 1999 Feb;39(3):607-14 PMID: 10092186
  20. Two regulatory levels of transcriptional gene silencing in Arabidopsis.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13659-62 PMID: 12370435
  21. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation.
    Plant Physiol. 2005 Jun;138(2):744-56 PMID: 15908605
  22. Reproductive biology: delivering spermatozoan RNA to the oocyte.
    Nature. 2004 May 13;429(6988):154 PMID: 15141202
  23. Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate.
    Stain Technol. 1970 May;45(3):115-20 PMID: 4192549
  24. Expressed sequence tag analysis of Lilium longiflorum generative cells.
    Plant Cell Physiol. 2006 Jun;47(6):698-705 PMID: 16571618
  25. Comparison of Petunia inflata S-Locus F-box protein (Pi SLF) with Pi SLF like proteins reveals its unique function in S-RNase based self-incompatibility.
    Plant Cell. 2007 Nov;19(11):3593-609 PMID: 18024566
  26. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
    Plant J. 2004 Mar;37(6):914-39 PMID: 14996223
  27. Spermatozoal RNA profiles of normal fertile men.
    Lancet. 2002 Sep 7;360(9335):772-7 PMID: 12241836
  28. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes.
    Plant Cell. 2006 Nov;18(11):3033-46 PMID: 17098809
  29. Arabidopsis vacuolar H-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis.
    Plant J. 2005 Jan;41(1):125-32 PMID: 15610355
  30. Targets of RNA-directed DNA methylation.
    Curr Opin Plant Biol. 2007 Oct;10(5):512-9 PMID: 17702644
  31. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis.
    Dev Biol. 1999 Mar 15;207(2):322-33 PMID: 10068466
  32. Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression.
    Plant Physiol. 2005 Jan;137(1):297-307 PMID: 15618418
  33. How many genes are needed to make a pollen tube? Lessons from transcriptomics.
    Ann Bot. 2007 Dec;100(6):1117-23 PMID: 17951360
  34. Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes.
    Development. 1999 Feb;126(5):1065-75 PMID: 9927606
  35. MscS-like proteins control plastid size and shape in Arabidopsis thaliana.
    Curr Biol. 2006 Jan 10;16(1):1-11 PMID: 16401419
  36. RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants.
    Trends Plant Sci. 2006 Jun;11(6):309-15 PMID: 16737841
  37. KSper, a pH-sensitive K+ current that controls sperm membrane potential.
    Proc Natl Acad Sci U S A. 2007 May 1;104(18):7688-92 PMID: 17460039
  38. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  39. Non-traditional roles of ubiquitin-proteasome system in fertilization and gametogenesis.
    Int J Biochem Cell Biol. 2004 May;36(5):776-84 PMID: 15006630
  40. Plant homologue of human excision repair gene ERCC1 points to conservation of DNA repair mechanisms.
    Plant J. 1998 Mar;13(6):823-9 PMID: 9681020
  41. Gametophyte interaction and sexual reproduction: how plants make a zygote.
    Int J Dev Biol. 2005;49(5-6):615-32 PMID: 16096969
  42. Identification of the pollen determinant of S-RNase-mediated self-incompatibility.
    Nature. 2004 May 20;429(6989):302-5 PMID: 15152253
  43. F-box proteins in Arabidopsis.
    Trends Plant Sci. 2000 Nov;5(11):454-7 PMID: 11077244
  44. Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development.
    Plant Cell. 2007 Apr;19(4):1163-78 PMID: 17435085
  45. The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes.
    Genes Dev. 2008 Apr 15;22(8):1051-68 PMID: 18367645
  46. cDNA cloning reveals the molecular structure of a sperm surface protein, PH-20, involved in sperm-egg adhesion and the wide distribution of its gene among mammals.
    J Cell Biol. 1990 Dec;111(6 Pt 2):2939-49 PMID: 2269661
  47. The making of gametes in higher plants.
    Int J Dev Biol. 2005;49(5-6):595-614 PMID: 16096968
  48. Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis.
    Trends Genet. 1998 Jun;14(6):236-43 PMID: 9635407
  49. The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis.
    Plant Physiol. 2007 Nov;145(3):801-13 PMID: 17905865
  50. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists.
    Genome Biol. 2007;8(9):R183 PMID: 17784955
  51. A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice.
    Plant Cell. 2007 Aug;19(8):2583-94 PMID: 17675402
  52. Green sperm. Identification of male gamete promoters in Arabidopsis.
    Plant Physiol. 2005 Aug;138(4):2124-33 PMID: 16055690
  53. The Arabidopsis basic/helix-loop-helix transcription factor family.
    Plant Cell. 2003 Aug;15(8):1749-70 PMID: 12897250
  54. Members of the Arabidopsis AtTPK/KCO family form homomeric vacuolar channels in planta.
    Plant J. 2006 Oct;48(2):296-306 PMID: 16984403
  55. Sperm cells of Zea mays have a complex complement of mRNAs.
    Plant J. 2003 Jun;34(5):697-707 PMID: 12787250
  56. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes.
    Plant J. 2006 Jun;46(6):1018-31 PMID: 16805734
  57. A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis.
    Science. 2006 Apr 14;312(5771):264-6 PMID: 16614222
  58. Arabidopsis hapless mutations define essential gametophytic functions.
    Genetics. 2004 Oct;168(2):971-82 PMID: 15514068
  59. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome.
    Plant Physiol. 2003 Oct;133(2):713-25 PMID: 14500793
  60. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18830-5 PMID: 18000057
  61. A novel class of MYB factors controls sperm-cell formation in plants.
    Curr Biol. 2005 Feb 8;15(3):244-8 PMID: 15694308
  62. F-box proteins and protein degradation: an emerging theme in cellular regulation.
    Plant Mol Biol. 2000 Sep;44(2):123-8 PMID: 11117256
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2008-10-00
Epub
2008-00-30
Pages
1168-81
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2556834
Subset
IM
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