A Novel RNA-Recognition-Motif Protein Is Required for Premeiotic G/S-Phase Transition in Rice ( L.)
The molecular mechanism for meiotic entry remains largely elusive in flowering plants. Only Arabidopsis SWI1/DYAD and maize AM1, both of which are the coiled-coil protein, are known to be required for the initiation of plant meiosis. The mechanism underlying the synchrony of male meiosis, characteristic to flowering plants, has also been unclear in the plant kingdom. In other eukaryotes, RNA-recognition-motif (RRM) proteins are known to play essential roles in germ-cell development and meiosis progression. Rice MEL2 protein discovered in this study shows partial similarity with human proline-rich RRM protein, deleted in Azoospermia-Associated Protein1 (DAZAP1), though MEL2 also possesses ankyrin repeats and a RING finger motif. Expression analyses of several cell-cycle markers revealed that, in mel2 mutant anthers, most germ cells failed to enter premeiotic S-phase and meiosis, and a part escaped from the defect and underwent meiosis with a significant delay or continued mitotic cycles. Immunofluorescent detection revealed that T7 peptide-tagged MEL2 localized at cytoplasmic perinuclear region of germ cells during premeiotic interphase in transgenic rice plants. This study is the first report of the plant RRM protein, which is required for regulating the premeiotic G1/S-phase transition of male and female germ cells and also establishing synchrony of male meiosis. This study will contribute to elucidation of similarities and diversities in reproduction system between plants and other species.
Vyšlo v časopise:
A Novel RNA-Recognition-Motif Protein Is Required for Premeiotic G/S-Phase Transition in Rice ( L.). PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001265
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001265
Souhrn
The molecular mechanism for meiotic entry remains largely elusive in flowering plants. Only Arabidopsis SWI1/DYAD and maize AM1, both of which are the coiled-coil protein, are known to be required for the initiation of plant meiosis. The mechanism underlying the synchrony of male meiosis, characteristic to flowering plants, has also been unclear in the plant kingdom. In other eukaryotes, RNA-recognition-motif (RRM) proteins are known to play essential roles in germ-cell development and meiosis progression. Rice MEL2 protein discovered in this study shows partial similarity with human proline-rich RRM protein, deleted in Azoospermia-Associated Protein1 (DAZAP1), though MEL2 also possesses ankyrin repeats and a RING finger motif. Expression analyses of several cell-cycle markers revealed that, in mel2 mutant anthers, most germ cells failed to enter premeiotic S-phase and meiosis, and a part escaped from the defect and underwent meiosis with a significant delay or continued mitotic cycles. Immunofluorescent detection revealed that T7 peptide-tagged MEL2 localized at cytoplasmic perinuclear region of germ cells during premeiotic interphase in transgenic rice plants. This study is the first report of the plant RRM protein, which is required for regulating the premeiotic G1/S-phase transition of male and female germ cells and also establishing synchrony of male meiosis. This study will contribute to elucidation of similarities and diversities in reproduction system between plants and other species.
Zdroje
1. PawlowskiWP
SheehanMJ
RonceretA
2007 In the beginning: the initiation of meiosis. BioEssays 29 511 514
2. ItoM
TakegamiMH
1982 Commitment of mitotic cells to meiosis during the G2 phase of premeiosis. Plant Cell Physiol 23 943 952
3. HamantO
MaH
CandeWZ
2006 Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57 267 302
4. MercierR
VezonD
BullierE
MotamayorJC
SellierA
2001 SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev 15 1859 1871
5. AgasheB
PrasadCK
SiddiqiI
2002 Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development 129 3935 3943
6. PawlowskiWP
WangCJ
GolubovskayaIN
SzymaniakJM
ShiL
2009 Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc Natl Acad Sci USA 106 3603 3608
7. PalmerRG
1971 Cytological studies of ameiotic and normal maize with reference to premeiotic pairing. Chromosoma 35 233 246
8. StaigerCJ
CandeWZ
1992 Ameiotic, a gene that controls meiotic chromosome and cytoskeletal behavior in maize. Dev Biol 154 226 230
9. GolubovskayaI
GrebennikovaZK
AvalkinaNA
SheridanWF
1993 The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135 1151 1166
10. SchmitzRJ
AmasinoRM
2007 Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim Biophys Acta 1769 269 275
11. ArmstrongSJ
FranklinFCH
JonesGH
2003 A meiotic time-course for Arabidopsis thaliana. Sex Plant Reprod 16 141 149
12. NonomuraKI
NakanoM
MurataK
MiyoshiK
EiguchiM
2004 An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Gen Genomics 271 121 129
13. MagnardJL
YangM
ChenYC
LearyM
McCormickS
2001 The Arabidopsis gene tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiol 127 1157 1166
14. WangY
MagnardJL
McCormickS
YangM
2004 Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol 136 4127 4135
15. SiomiH
DreyfussG
1997 RNA-binding proteins as regulators of gene expression. Curr Opin Genet Dev 7 345 353
16. HarigayaY
TanakaH
YamanakaS
TanakaK
WatanabeY
2006 Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442 45 50
17. CaraniC
GromollJ
BrinkworthMH
SimoniM
WeinbauerGF
1997 cynDAZLA: a cynomolgus monkey homologue of the human autosomal DAZ gene. Mol Hum Reprod 3 479 483
18. MainesJZ
WassermanSA
1999 Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule. Nat Cell Biol 1 171 174
19. KarashimaT
SugimotoA
YamamotoM
2000 Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127 1069 1079
20. ChenCY
ShyuAB
1995 AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20 465 470
21. CollierB
GorgoniB
LoveridgeC
CookeHJ
GrayNK
2005 The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J 24 2656 2666
22. ReynoldsN
CollierB
BinghamV
GrayNK
CookeHJ
2007 Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA 13 974 981
23. KaurJ
SebastianJ
SiddiqiI
2006 The Arabidopsis-mei2-like genes play a role in meiosis and vegetative growth in Arabidopsis. Plant Cell 18 545 559
24. TsuiS
DaiT
RoettgerS
SchemppW
SalidoEC
2000 Identification of two novel proteins that interact with germ-cell-specific RNA-binding proteins DAZ and DAZL1. Genomics 65 266 273
25. NonomuraKI
MiyoshiK
EiguchiM
SuzukiT
MiyaoA
2003 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 15 1728 1739
26. NonomuraKI
MorohoshiA
NakanoM
EiguchiM
MiyaoA
2007 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 19 2583 2594
27. ChenR
ZhaoX
ShaoZ
WeiZ
WangY
2007 Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19 847 861
28. KarbowskiM
KuronoC
WozniakM
OstrowskiM
Teranishi, YM
1999 Free radical-induced megamitochondria formation and apoptosis. Free Radic Biol Med 26 396 409
29. ReshMD
1999 Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451 1 16
30. SedgwickSG
SmerdonSJ
1999 The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24 311 316
31. KenanDJ
QueryCC
KeeneJD
1991 RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16 214 220
32. BirneyE
KumarS
KrainerAR
1993 Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res 21 5803 5816
33. BurdCG
DreyfussG
1994 RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J 13 1197 1204
34. AltschulSF
MaddenTL
SchafferAA
ZhangJ
ZhangZ
1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402
35. KawabataT
FukuchiS
HommaK
OtaM
ArakiJ
2002 GTOP: a database of protein structures predicted from genome sequences. Nucleic Acids Res 30 294 298
36. FukuchiS
HommaK
SakamotoS
SugawaraH
TatenoY
2009 The GTOP database in 2009: updated content and novel features to expand and deepen insights into protein structures and functions. Nucleic Acids Res (Database issue) 37 D333 337
37. UmedaM
Umeda-HaraC
YamaguchiM
HashimotoJ
UchimiyaH
1999 Differential expression of genes for cyclin-dependent protein kinases in rice plants. Plant Physiol 119 31 40
38. BassHW
MarshallWF
SedatJW
AgardDA
CandeWZ
1997 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 137 5 18
39. NonomuraKI
NakanoM
EiguchiM
SuzukiT
KurataN
2006 PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119 217 225
40. WangM
WangK
TangD
WeiC
LiM
2010 The Central Element Protein ZEP1 of the Synaptonemal Complex Regulates the Number of Crossovers during Meiosis in Rice. Plant Cell, tpc.109.070789
41. PodellS
GribskovM
2004 Predicting N-terminal myristoylation sites in plant proteins. BMC Genomics 5 37
42. LiXC
BarringerBC
BarbashDA
2009 The pachytene checkpoint and its relationship to evolutionary patterns of polyploidization and hybrid sterility. Heredity 102 24 30
43. CarylAP
JonesGH
FranklinFC
2003 Dissecting plant meiosis using Arabidopsis thaliana mutants. J Exp Bot 54 25 38
44. DreyfussG
MatunisMJ
Pinol-RomaS
BurdCG
1993 hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62 289 321
45. VeraY
DaiT
HikimAP
LueY
SalidoEC
2002 Deleted in azoospermia associated protein 1 shuttles between nucleus and cytoplasm during normal germ cell maturation. J Androl 23 622 628
46. LinYT
YenPH
2006 A novel nucleocytoplasmic shuttling sequence of DAZAP1, a testis-abundant RNA-binding protein. RNA 12 1486 1493
47. KuriharaY
WatanabeH
KawaguchiA
HoriT
MishiroK
2004 Dynamic changes in intranuclear and subcellular localizations of mouse Prrp/DAZAP1 during spermatogenesis: the necessity of the C-terminal proline-rich region for nuclear import and localization. Arch Histol Cytol 67 325 333
48. HsuLC
ChenHY
LinYW
ChuWC
LinMJ
2008 DAZAP1, an hnRNP protein, is required for normal growth and spermatogenesis in mice. RNA 14 1814 1822
49. MooreFL
JaruzelskaJ
FoxMS
UranoJ
FirpoMT
2003 Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci USA 100 538 543
50. UranoJ
FoxMS
Reijo PeraRA
2005 Interaction of the conserved meiotic regulators, BOULE (BOL) and PUMILIO-2 (PUM2). Mol Reprod Dev 71 290 298
51. KreftSG
NassalM
2003 hRUL138, a novel human RNA-binding RING-H2 ubiquitin-protein ligase. J Cell Sci 116 605 616
52. NodzonLA
XuWH
WangY
PiLY
ChakrabartyPK
2004 The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40 996 1006
53. PrasadME
SchofieldA
LyzengaW
LiuH
StoneSL
2010 Arabidopsis RING E3 ligase XBAT32 Regulates Lateral Root Production through its Role in Ethylene Biosynthesis. Plant Physiol DOI:10.1104/pp.110.156976
54. WolfeKH
GouyM
YangYW
SharpPM
LiWH
1989 Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86 6201 6205
55. Heslop-HarrisonJ
1966 Cytoplasmic connexions between angiosperm meiocytes. Annals Bot 30 221 230
56. LiN
ZhangDS
LiuHS
YinCS
LiXX
2006 The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18 2999 3014
57. AyaK
Ueguchi-TanakaM
KondoM
HamadaK
YanoK
2009 Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21 1453 1472
58. WeissH
MaluszynskaJ
2001 Molecular cytogenetic analysis of polyploidization in the anther tapetum of diploid and autotetraploid Arabidopsis thaliana. Annals Botany 87 729 735
59. ItohJ
NonomuraKI
IkedaK
YamakiS
InukaiY
2005 Rice plant development: from zygote to spikelet. Plant Cell Physiol 46 23 47
60. FuseT
SasakiT
YanoM
2001 Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotech 18 219 222
61. HieiY
OhtaS
KomariT
KumashiroT
1994 Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6 271 282
62. StadenR
1982 An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10 2951 2961
63. ImaiY
MatsushimaY
SugimuraT
TeradaM
1991 A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res 19 2785
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 1
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- H3K9me-Independent Gene Silencing in Fission Yeast Heterochromatin by Clr5 and Histone Deacetylases
- Rnf12—A Jack of All Trades in X Inactivation?
- Joint Genetic Analysis of Gene Expression Data with Inferred Cellular Phenotypes
- Evolutionary Conserved Regulation of HIF-1β by NF-κB