The Arabidopsis HEI10 is a new ZMM protein related to Zip3

PLoS Genetics

Volumn 8, Issue 7, 2012, Pages

  Chelysheva, Liudmila ^a   Vezon, Daniel ^a   Chambon, Aurélie ^a   Gendrot, Ghislaine ^b   Pereira, Lucie ^a   Lemhemdi, Afef ^a   Vrielynck, Nathalie ^a   Le Guin, Sylvia ^a   Novatchkova, Maria ^c,d   Grelon, Mathilde ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b UNIVERSITÉ DE LYON   (France)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^d ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; PROTEIN HEI10; PROTEIN MLH1; PROTEIN ZIP3; PROTEIN ZMM; REGULATOR PROTEIN; RING FINGER PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BUD; CHROMOSOME CHIASM; DNA FRAGMENTATION; FEMALE; FEMALE GAMETOPHYTE; MALE; MALE GAMETOPHYTE; MITOTIC RECOMBINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PLANT ROOT; PROPHASE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; VEGETATIVE GROWTH;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, PLANT; CROSSING OVER, GENETIC; FERTILITY; HOMOLOGOUS RECOMBINATION; MIOSIS; MOLECULAR SEQUENCE DATA; MUTATION; RING FINGER DOMAINS; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPTONEMAL COMPLEX; UBIQUITIN-PROTEIN LIGASES; YEASTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864587771     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002799     Document Type: Article

References (88)

1. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
2. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
3. Muller HJ, (1916) The mechanisms of crossing-over. American Naturalist 50: 193-221.
4. Whitby MC, (2005) Making crossovers during meiosis. Biochem Soc Trans 33: 1451-1455.
5. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC, (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523-544.
6. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP, (2007) The Role of AtMUS81 in Interference-Insensitive Crossovers in A. thaliana. PLoS Genet 3: e132 doi:10.1371/journal.pgen.0030132.
7. De Los Santos T, Hunter N, Lee C, Larkin B, Loidl J, et al. (2003) The mus81/mms4 endonuclease acts independently of double-holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164: 81-94.
8. Higgins JD, Buckling EF, Franklin FC, Jones GH, (2008) Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54: 152-162.
9. Lynn A, Soucek R, Borner GV, (2007) ZMM proteins during meiosis: Crossover artists at work. Chromosome Res 15: 591-605.
10. Higgins JD, Armstrong SJ, Franklin FC, Jones GH, (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18: 2557-2570.
11. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FC, et al. (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55: 28-39.
12. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, et al. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14: 1085-1097.
13. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, et al. (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. Faseb J 14: 1539-1547.
14. de Boer E, Stam P, Dietrich AJ, Pastink A, Heyting C, (2006) Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 103: 9607-9612.
15. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115: 1611-1622.
16. Neyton S, Lespinasse F, Moens PB, Paul R, Gaudray P, et al. (2004) Association between MSH4 (MutS homologue 4) and the DNA strand-exchange RAD51 and DMC1 proteins during mammalian meiosis. Mol Hum Reprod 10: 917-924.
17. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336-342.
18. Hunter N, Borts RH, (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11: 1573-1582.
19. Jackson N, Sanchez-Moran E, Buckling E, Armstrong SJ, Jones GH, et al. (2006) Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. Embo J 25: 1315-1323.
20. Kolas NK, Svetlanov A, Lenzi ML, Macaluso FP, Lipkin SM, et al. (2005) Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J Cell Biol 171: 447-458.
21. Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D, et al. (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31: 385-390.
22. Page SL, Hawley RS, (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-558.
23. de Boer E, Heyting C, (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115: 220-234.
24. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
25. Chua PR, Roeder GS, (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
26. Tsubouchi T, Zhao H, Roeder GS, (2006) The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev Cell 10: 809-819.
27. Shinohara M, Oh SD, Hunter N, Shinohara A, (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40: 299-309.
28. de Vries SS, Baart EB, Dekker M, Siezen A, de Rooij DG, et al. (1999) Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev 13: 523-531.
29. Chen C, Zhang W, Timofejeva L, Gerardin Y, Ma H, (2005) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J 43: 321-334.
30. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15: 692-701.
31. Wang K, Tang D, Wang M, Lu J, Yu H, et al. (2009) MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122: 2055-2063.
32. Chelysheva L, Gendrot G, Vezon D, Doutriaux MP, Mercier R, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3: e83 doi:10.1371/journal.pgen.0030083.
33. Mazina OM, Mazin AV, Nakagawa T, Kolodner RD, Kowalczykowski SC, (2004) Saccharomyces cerevisiae Mer3 helicase stimulates 3′-5′ heteroduplex extension by Rad51; implications for crossover control in meiotic recombination. Cell 117: 47-56.
34. Snowden T, Acharya S, Butz C, Berardini M, Fishel R, (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15: 437-451.
35. Macaisne N, Vignard J, Mercier R, (2011) SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J Cell Sci 124: 2687-2691.
36. Macaisne N, Novatchkova M, Peirera L, Vezon D, Jolivet S, et al. (2008) SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr Biol 18: 1432-1437.
37. Perry J, Kleckner N, Borner GV, (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102: 17594-17599.
38. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, et al. (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20: 2067-2081.
39. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, et al. (2007) Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 3: e139 doi:10.1371/journal.pgen.0030139.
40. Ross KJ, Fransz P, Jones GH, (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507-516.
41. Sanchez Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH, (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res 9: 121-128.
42. Berchowitz LE, Copenhaver GP, (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3: 41-50.
43. Perkins DD, (1949) Biochemical mutants in the smut fungus Ustilago maydis. Genetics 34: 607-626.
44. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A.
45. Armstrong SJ, Caryl AP, Jones GH, Franklin FC, (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645-3655.
46. Lhuissier FG, Offenberg HH, Wittich PE, Vischer NO, Heyting C, (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19: 862-876.
47. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, et al. (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res 129: 143-153.
48. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC, (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: 2488-2500.
49. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic acids research 40: D290-301.
50. Delorenzi M, Speed T, (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18: 617-625.
51. Altenhoff AM, Dessimoz C, (2009) Phylogenetic and functional assessment of orthologs inference projects and methods. PLoS Comput Biol 5: e1000262 doi:10.1371/journal.pcbi.1000262.
52. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, et al. (2012) Database resources of the National Center for Biotechnology Information. Nucleic acids research 40: D13-25.
53. Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, et al. (2010) PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic acids research 38: D204-210.
54. Wijeratne AJ, Chen C, Zhang W, Timofejeva L, Ma H, (2006) The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol Biol Cell 17: 1331-1343.
55. Singh MK, Nicolas E, Gherraby W, Dadke D, Lessin S, et al. (2007) HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26: 4825-4832.
56. Toby GG, Gherraby W, Coleman TR, Golemis EA, (2003) A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 23: 2109-2122.
57. Smith AP, Weeraratna AT, Spears JR, Meltzer PS, Becker D, (2004) SAGE identification and fluorescence imaging analysis of genes and transcripts in melanomas and precursor lesions. Cancer Biol Ther 3: 104-109.
58. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, et al. (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
59. Woods LM, Hodges CA, Baart E, Baker SM, Liskay M, et al. (1999) Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J Cell Biol 145: 1395-1406.
60. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, et al. (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21: 123-127.
61. Strong ER, Schimenti JC, (2010) Evidence Implicating CCNB1IP1, a RING Domain-Containing Protein Required for Meiotic Crossing Over in Mice, as an E3 SUMO Ligase. Genes (Basel) 1: 440-451.
62. Baudat F, de Massy B, (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565-577.
63. De Muyt A, Mercier R, Mezard C, Grelon M, (2009) Meiotic recombination and crossovers in plants. Genome Dyn 5: 14-25.
64. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, et al. (1997) Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106: 207-215.
65. Osman K, Sanchez-Moran E, Mann SC, Jones GH, Franklin FC, (2009) Replication protein A (AtRPA1a) is required for class I crossover formation but is dispensable for meiotic DNA break repair. Embo J 28: 394-404.
66. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94-106.
67. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF, (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4: e1000235 doi:10.1371/journal.pgen.1000235.
68. Tsubouchi T, Macqueen AJ, Roeder GS, (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217-3226.
69. Grelon M, Vezon D, Gendrot G, Pelletier G, (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20: 589-600.
70. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
71. Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, et al. (2008) Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319: 1398-1401.
72. Carpenter AT, (1975) Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule-a recombination-associated structure at pachytene? Proc Natl Acad Sci U S A 72: 3186-3189.
73. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.
74. Anderson LK, Stack SM, (2005) Recombination nodules in plants. Cytogenet Genome Res 109: 198-204.
75. Guillon H, de Massy B, (2002) An initiation site for meiotic crossing-over and gene conversion in the mouse. Nat Genet 32: 296-299.
76. Padmore R, Cao L, Kleckner N, (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239-1256.
77. Zickler D, (1977) Development of the synaptonemal complex and the "recombination nodules" during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw. Chromosoma 61: 289-316.
78. Gillies CB, (1979) The Relationship between Synaptinemal Complexes, Recombination Nodules and Crossing over in NEUROSPORA CRASSA Bivalents and Translocation Quadrivalents. Genetics 91: 1-17.
79. Leflon M, Grandont L, Eber F, Huteau V, Coriton O, et al. (2010) Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 22: 2253-2264.
80. Bechtold N, Ellis J, Pelletier G, (1993) In Planta, Agrobacterium mediated gene transfer by integration of adult Arabidopsis thaliana plants. C R Acad Sci Paris 316: 1194-1199.
81. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
82. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 doi:10.1371/journal.pgen.1000654.
83. De Muyt A, Vezon D, Gendrot G, Gallois JL, Stevens R, et al. (2007) AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. Embo J.
84. Moffatt BA, McWhinnie EA, Agarwal SK, Schaff DA, (1994) The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. Gene 143: 211-216.
85. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, et al. (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: 4621-4632.
86. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.
87. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
88. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, et al. (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24: 7998-8006.