Home LiteratureArticle Details
PMID: 15031413 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis.

The Plant cell ·Vol. 16 ·No. 4 ·2004-04-00 ·Pages 1008-20

Nonomura K, Nakano M, Fukuda T, Eiguchi M, Miyao A, Hirochika H, Kurata N

Abstract

We have identified and characterized a novel gene, PAIR1 (HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1), required for homologous chromosome pairing and cytokinesis in male and female meiocytes of rice (Oryza sativa). The pair1 mutation, tagged by the endogenous retrotransposon Tos17, exhibited meiosis-specific defects and resulted in complete sterility in male and female gametes. The PAIR1 gene encodes a 492-amino acid protein, which contains putative coiled-coil motifs in the middle, two basic regions at both termini, and a potential nuclear localization signal at the C terminus. Expression of the PAIR1 gene was detected in the early stages of flower development, in which the majority of the sporocytes had not entered meiosis. During prophase I of the pair1 meiocyte, all the chromosomes became entangled to form a compact sphere adhered to a nucleolus, and homologous pairing failed. At anaphase I and telophase I, chromosome nondisjunction and degenerated spindle formation resulted in multiple uneven spore production. However, chromosomal fragmentation frequent in plant meiotic mutants was never observed in all of the pair1 meiocytes. These observations clarify that the PAIR1 protein plays an essential role in establishment of homologous chromosome pairing in rice meiosis.

MeSH Terms
Amino Acid Sequence Base Sequence Chromosome Pairing Chromosomes, Plant/genetics DNA, Plant/genetics Genes, Plant Meiosis/genetics Molecular Sequence Data Mutation Oryza/cytology,genetics Phenotype Plant Proteins/chemistry,genetics Protein Structure, Secondary Spores/genetics
Chemicals
DNA, Plant Plant Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Nonomura Ken-Ichi
Experimental Farm/Plant Genetics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan. [email protected]
Nakano Mutsuko
Fukuda Toshiyuki
Eiguchi Mitsugu
Miyao Akio
Hirochika Hirohiko
Kurata Nori
References (67)
67 references, click to expand
  1. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis.
    Plant J. 1998 Aug;15(3):345-56 PMID: 9750346
  2. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica.
    J Cell Sci. 2002 Sep 15;115(Pt 18):3645-55 PMID: 12186950
  3. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1.
    Chromosoma. 2000;109(1-2):62-71 PMID: 10855496
  4. Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae.
    Genetics. 1998 Jun;149(2):817-32 PMID: 9611194
  5. AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis.
    Plant J. 2003 Oct;36(1):1-11 PMID: 12974806
  6. Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis.
    EMBO J. 2000 Jul 17;19(14):3831-40 PMID: 10899136
  7. The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets.
    Mol Genet Genomics. 2001 Apr;265(2):336-44 PMID: 11361345
  8. The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice.
    Plant Cell. 2003 Aug;15(8):1728-39 PMID: 12897248
  9. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing.
    J Cell Sci. 2003 Jul 15;116(Pt 14):2999-3007 PMID: 12783989
  10. Homologous chromosome pairing in wheat.
    J Cell Sci. 1999 Jun;112 ( Pt 11):1761-9 PMID: 10318768
  11. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis.
    Plant Cell. 1999 Sep;11(9):1623-34 PMID: 10488231
  12. The effect of colchicine on synaptonemal complex formation in Allium ursinum.
    Exp Cell Res. 1988 Sep;178(1):93-7 PMID: 3409980
  13. SPXX, a frequent sequence motif in gene regulatory proteins.
    J Mol Biol. 1989 May 5;207(1):61-84 PMID: 2500531
  14. AtSPO11-1 is necessary for efficient meiotic recombination in plants.
    EMBO J. 2001 Feb 1;20(3):589-600 PMID: 11157765
  15. S. pombe sporulation-specific coiled-coil protein Spo15p is localized to the spindle pole body and essential for its modification.
    J Cell Sci. 2000 Feb;113 ( Pt 3):545-54 PMID: 10639340
  16. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis.
    Genes Dev. 2001 Jul 15;15(14):1859-71 PMID: 11459834
  17. Coordination of meiotic recombination, pairing, and synapsis by PHS1.
    Science. 2004 Jan 2;303(5654):89-92 PMID: 14704428
  18. NPS@: network protein sequence analysis.
    Trends Biochem Sci. 2000 Mar;25(3):147-50 PMID: 10694887
  19. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana.
    J Cell Sci. 2001 Dec;114(Pt 23):4207-17 PMID: 11739653
  20. Microtubule-associated coiled-coil protein Ssm4 is involved in the meiotic development in fission yeast.
    Genes Cells. 1997 Feb;2(2):155-66 PMID: 9167972
  21. Retrotransposons of rice involved in mutations induced by tissue culture.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7783-8 PMID: 8755553
  22. Maize meiotic spindles assemble around chromatin and do not require paired chromosomes.
    J Cell Sci. 1998 Dec;111 ( Pt 23):3507-15 PMID: 9811565
  23. Telomere-led premeiotic chromosome movement in fission yeast.
    Science. 1994 Apr 8;264(5156):270-3 PMID: 8146661
  24. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family.
    Plant J. 1999 Aug;19(4):463-72 PMID: 10504568
  25. Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis.
    Plant Cell. 1999 Mar;11(3):417-30 PMID: 10072401
  26. A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant.
    Plant J. 1997 Apr;11(4):659-69 PMID: 9161029
  27. Multiple roles of Spo11 in meiotic chromosome behavior.
    EMBO J. 2000 Jun 1;19(11):2739-50 PMID: 10835371
  28. Meiotic telomeres: a matchmaker for homologous chromosomes.
    Genes Cells. 1998 Jul;3(7):405-13 PMID: 9753423
  29. An atypical topoisomerase II from Archaea with implications for meiotic recombination.
    Nature. 1997 Mar 27;386(6623):414-7 PMID: 9121560
  30. The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.).
    Genetics. 2002 Dec;162(4):1979-93 PMID: 12524364
  31. Synaptonemal complex and chromosome structure.
    Annu Rev Genet. 1975;9:91-109 PMID: 1108770
  32. The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo.
    J Cell Biol. 1998 Jul 27;142(2):331-9 PMID: 9679134
  33. The leptotene-zygotene transition of meiosis.
    Annu Rev Genet. 1998;32:619-97 PMID: 9928494
  34. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae.
    Cell. 1990 Jun 15;61(6):1089-101 PMID: 2190690
  35. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.
    J Cell Biol. 1997 Apr 7;137(1):5-18 PMID: 9105032
  36. Engineered GFP as a vital reporter in plants.
    Curr Biol. 1996 Mar 1;6(3):325-30 PMID: 8805250
  37. The Arabidopsis MEI1 gene encodes a protein with five BRCT domains that is involved in meiosis-specific DNA repair events independent of SPO11-induced DSBs.
    Plant J. 2003 Aug;35(4):465-75 PMID: 12904209
  38. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes.
    EMBO J. 1992 Dec;11(13):5091-100 PMID: 1464329
  39. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins.
    Science. 1988 Jun 24;240(4860):1759-64 PMID: 3289117
  40. CYTOKINESIS AND BUILDING OF THE CELL PLATE IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:751-784 PMID: 11337415
  41. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe.
    Nature. 1998 Apr 23;392(6678):825-8 PMID: 9572142
  42. The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes.
    Cell. 1998 Aug 7;94(3):375-86 PMID: 9708739
  43. The TATA-binding protein: a central role in transcription by RNA polymerases I, II and III.
    Trends Genet. 1992 Aug;8(8):284-8 PMID: 1509519
  44. Sequence requirements for synthetic peptide-mediated translocation to the nucleus.
    Mol Cell Biol. 1989 Jun;9(6):2487-92 PMID: 2668735
  45. The synaptonemal complex in genetic segregation.
    Annu Rev Genet. 1984;18:331-413 PMID: 6241453
  46. Chromosome cohesion, condensation, and separation.
    Annu Rev Biochem. 2000;69:115-44 PMID: 10966455
  47. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA.
    Plant J. 1994 Aug;6(2):271-82 PMID: 7920717
  48. Leucine is the most stabilizing aliphatic amino acid in the d position of a dimeric leucine zipper coiled coil.
    Biochemistry. 1997 Oct 14;36(41):12567-73 PMID: 9376362
  49. A novel fission yeast gene, kms1+, is required for the formation of meiotic prophase-specific nuclear architecture.
    Mol Gen Genet. 1997 Apr 16;254(3):238-49 PMID: 9150257
  50. Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination.
    Nature. 1998 Apr 23;392(6678):828-31 PMID: 9572143
  51. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes.
    Cell. 1990 Apr 6;61(1):73-84 PMID: 2107981
  52. SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat.
    Nucleic Acids Res. 1998 Jun 1;26(11):2572-9 PMID: 9592139
  53. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast.
    Cell. 1994 Jul 1;77(7):977-91 PMID: 8020104
  54. Genetic control of chromosome synapsis in yeast meiosis.
    Genome. 1989;31(1):88-94 PMID: 2687110
  55. B-ZIP proteins encoded by the Drosophila genome: evaluation of potential dimerization partners.
    Genome Res. 2002 Aug;12(8):1190-200 PMID: 12176927
  56. The fine structure of meiotic chromosome polarization and pairing in Locusta migratoria spermatocytes.
    Chromosoma. 1969;28(1):1-25 PMID: 5365542
  57. A novel meiosis-specific protein of fission yeast, Meu13p, promotes homologous pairing independently of homologous recombination.
    EMBO J. 2001 Jul 16;20(14):3871-81 PMID: 11447128
  58. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast.
    J Cell Biol. 1994 Jun;125(6):1191-200 PMID: 8207053
  59. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing.
    J Cell Biol. 1996 Sep;134(5):1109-25 PMID: 8794855
  60. Prediction of the secondary structure of proteins from their amino acid sequence.
    Adv Enzymol Relat Areas Mol Biol. 1978;47:45-148 PMID: 364941
  61. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis.
    Development. 2003 Jul;130(14):3309-18 PMID: 12783800
  62. How do meiotic chromosomes meet their homologous partners?: lessons from fission yeast.
    Bioessays. 2001 Jun;23(6):526-33 PMID: 11385632
  63. The synaptinemal complex.
    Annu Rev Genet. 1972;6:71-110 PMID: 4269097
  64. An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis.
    Mol Genet Genomics. 2004 Mar;271(2):121-9 PMID: 14758540
  65. The complete nucleotide sequence of a rice 25S.rRNA gene.
    Gene. 1985;37(1-3):255-9 PMID: 3902573
  66. Double-strand breaks at an initiation site for meiotic gene conversion.
    Nature. 1989 Mar 2;338(6210):87-90 PMID: 2645528
  67. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-04-00
Epub
2004-00-18
Pages
1008-20
Language
English
Region
England
NLM ID
9208688
PMCID
PMC412873
Subset
IM
Databases
GENBANK
AB158462, AC009273, AC107224
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: [email protected]