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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

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