P granules are cytoplasmic structures of unknown function that are associated with germ nuclei in the C. elegans gonad, and are localized exclusively to germ cells, or germ cell precursors, throughout the life cycle. All the known protein components of P granules contain putative RNA-binding motifs, suggesting that RNA is involved in either the structure or function of the granules. However, no specific mRNAs have been identified within P granules in the gonad. We show here that P granules normally contain a low level of RNA, and describe conditions that increase this level. We present evidence that several, diverse mRNAs, including pos-1, mex-1, par-3, skn-1, nos-2 and gld-1 mRNA, are present at least transiently within P granules. In contrast, actin and tubulin mRNA and rRNA are either not present in P granules, or are present at relatively low levels. We show that pgl-1 and the glh (Vasa-related) gene family, which encode protein components of P granules, do not appear essential for RNA to concentrate in P granules; these proteins may instead function in events that are a prerequisite for RNAs to be transported efficiently from the nuclear surface.

Reference

Beams
H. W.
,
Kessel
R. G.
(
1974
)
The problem of germ cell determinants.
Int. Rev. Cytol
39
,
413
479
Braat
A. K.
,
van de Water
S.
,
Goos
H.
,
Bogerd
J.
,
Zivkovic
D.
(
2000
)
Vasa protein expression and localization in the zebrafish.
Mech. Dev
95
,
271
274
Bowerman
B.
,
Eaton
B. A.
,
Priess
J. R.
(
1992
)
skn-1, a maternallyexpressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo.
Cell
68
,
1061
1075
Castrillon
D. H.
,
Quade
B. J.
,
Wang
T. Y.
,
Quigley
C.
,
Crum
C. P.
(
2000
)
The human VASA gene is specifically expressed in the germ cell lineage.
Proc. Natl. Acad. Sci. USA
97
,
9585
9590
Draper
B. W.
,
Mello
C. C.
,
Bowerman
B.
,
Hardin
J.
,
Priess
J. R.
(
1996
)
MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos.
Cell
87
,
205
216
Eddy
E. M.
(
1975
)
Germ plasm and the differentiation of the germ cell line.
Int. Rev. Cytol
43
,
229
280
Eddy
E. M.
,
Ito
S.
(
1971
)
Fine structural and radioautographic observations on dense perinuclear cytoplasmic material in tadpole oocytes.
J. Cell Biol
49
,
90
108
Edwards
M. K.
,
Wood
W. B.
(
1983
)
Location of specific messenger RNAs in Caenorhabditis elegans by cytological hybridization.
Dev. Biol
97
,
375
390
Etemad-Moghadam
B.
,
Guo
S.
,
Kemphues
K. J.
(
1995
)
Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos.
Cell
83
,
743
752
Fire
A.
,
Xu
S.
,
Montgomery
M. K.
,
Kostas
S. A.
,
Driver
S. E.
,
Mello
C. C.
(
1998
)
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans [see comments].
Nature
391
,
806
811
Francis
R.
,
Maine
E.
,
Schedl
T.
(
1995
)
Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway.
Genetics
139
,
607
630
Frank
D. J.
,
Roth
M. B.
(
1998
)
ncl-1 is required for the regulation of cell size and ribosomal RNA synthesis in Caenorhabditis elegans.
J. Cell. Biol
140
,
1321
1329
Gibert
M.A.
,
Starck
J.
,
Beguet
B.
(
1984
)
Role of the gonad cytoplasmic core during oogenesis of the nematode Caenorhabditis elegans.
Biol. Cell
50
,
77
85
Gruidl
M. E.
,
Smith
P. A.
,
Kuznicki
K. A.
,
McCrone
J. S.
,
Kirchner
J.
,
Roussell
D. L.
,
Strome
S.
,
Bennett
K. L.
(
1996
)
Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans.
Proc. Natl. Acad. Sci. USA
93
,
13837
13842
Guedes
S.
,
Priess
J. R.
(
1997
)
The C. elegans MEX-1 protein is present in germline blastomeres and is a P granule component.
Development
124
,
731
739
Hird
S. N.
,
Paulsen
J. E.
,
Strome
S.
(
1996
)
Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation.
Development
122
,
1303
1312
Hay
B.
,
Ackerman
L.
,
Barbel
S.
,
Jan
L. Y.
,
Jan
Y. N.
(
1988
)
Identification of a component of Drosophila polar granules.
Development
103
,
625
640
Hirsh
D.
,
Oppenheim
D.
,
Klass
M.
(
1976
)
Development of the reproductive system of Caenorhabditis elegans.
Dev. Biol
49
,
200
219
Ikenishi
K.
(
1987
)
Functional gametes derived from explants of single blastomeres containing the ‘germ plasm’ in Xenopus laevis: a genetic marker study.
Dev. Biol
122
,
35
38
Ikenishi
K.
(
1998
)
Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus.
Dev. Growth Differ
40
,
1
10
Illmensee
K.
,
Mahowald
A. P.
(
1974
)
Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg.
Proc. Natl. Acad. Sci. USA
71
,
1016
1020
Illmensee
K.
,
Mahowald
A. P.
(
1976
)
The autonomous function of germ plasm in a somatic region of the Drosophila egg.
Exp. Cell Res
97
,
127
140
Iwasaki
K.
,
McCarter
J.
,
Francis
R.
,
Schedl
T.
(
1996
)
emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation.
J. Cell Biol
134
,
699
714
Jones
A. R.
,
Francis
R.
,
Schedl
T.
(
1996
)
GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage-and sex-specific expression during Caenorhabditis elegans germline development.
Dev. Biol
180
,
165
183
Kawasaki
I.
,
Shim
Y. H.
,
Kirchner
J.
,
Kaminker
J.
,
Wood
W. B.
,
Strome
S.
(
1998
)
PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans.
Cell
94
,
635
645
Kimble
J.
,
Hirsh
D.
(
1979
)
The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans.
Dev. Biol
70
,
396
417
Knaut
H.
,
Pelegri
F.
,
Bohmann
K.
,
Schwarz
H.
,
Nusslein-Volhard
C.
(
2000
)
Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification.
J. Cell Biol
149
,
875
888
Knowles
R. B.
,
Sabry
J. H.
,
Martone
M. E.
,
Deerinck
T. J.
,
Ellisman
M. H.
,
Bassell
G. J.
,
Kosik
K. S.
(
1996
)
Translocation of RNA granules in living neurons.
J. Neurosci
16
,
7812
7820
Kobayashi
S.
,
Amikura
R.
,
Mukai
M.
(
1998
)
Localization of mitochondrial large ribosomal RNA in germ plasm of Xenopus embryos.
Curr. Biol
8
,
1117
1120
Kobayashi
S.
,
Amikura
R.
,
Okada
M.
(
1993
)
Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster.
Science
260
,
1521
1524
Komiya
T.
,
Itoh
K.
,
Ikenishi
K.
,
Furusawa
M.
(
1994
)
Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed in germ cells of Xenopus laevis.
Dev. Biol
162
,
354
363
Kornhauser
G. V.
,
Krum
J. M.
,
Rosenstein
J. M.
(
1992
)
An innovative coating technique for light and electron microscopic autoradiography.
J. Histochem. Cytochem
40
,
879
882
Kraemer
B.
,
Crittenden
S.
,
Gallegos
M.
,
Moulder
G.
,
Barstead
R.
,
Kimble
J.
,
Wickens
M.
(
1999
)
NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans.
Curr. Biol
9
,
1009
1018
Krause
M.
,
Hirsh
D.
(
1987
)
A trans-spliced leader sequence on actin mRNA in C. elegans.
Cell
49
,
753
761
Kuznicki
K. A.
,
Smith
P. A.
,
Leung-Chiu
W. M.
,
Estevez
A. O.
,
Scott
H. C.
,
Bennett
K. L.
(
2000
)
Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans.
Development
127
,
2907
2916
Mahowald
A. P.
(
1971
)
Polar granules of drosophila. IV. Cytochemical studies showing loss of RNA from polar granules during early stages of embryogenesis.
J. Exp. Zool
176
,
345
352
Mahowald
A. P.
,
Hennen
S.
(
1971
)
Ultrastructure of the ‘germ plasm’ in eggs and embryos of Rana pipiens.
Dev. Biol
24
,
37
53
McCarter
J.
,
Bartlett
B.
,
Dang
T.
,
Schedl
T.
(
1999
)
On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans.
Dev. Biol
205
,
111
128
Mello
C. C.
,
Draper
B. W.
,
Krause
M.
,
Weintraub
H.
,
Priess
J. R.
(
1992
)
The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos.
Cell
70
,
163
176
Mello
C. C.
,
Schubert
C.
,
Draper
B.
,
Zhang
W.
,
Lobel
R.
,
Priess
J.R.
(
1996
)
The PIE-1 protein and germline specification in C. elegans embryos [letter].
Nature
382
,
710
712
Nakamura
A.
,
Amikura
R.
,
Mukai
M.
,
Kobayashi
S.
,
Lasko
P. F.
(
1996
)
Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment.
Science
274
,
2075
2079
Nelson
G. A.
,
Lew
K. K.
,
Ward
S.
(
1978
)
Intersex, a temperature-sensitive mutant of the nematode Caenorhabditis elegans.
Dev. Biol
66
,
386
409
Olsen
L. C.
,
Aasland
R.
,
Fjose
A.
(
1997
)
A vasa-like gene in zebrafish identifies putative primordial germ cells.
Mech. Dev
66
,
95
105
Pitt
J. N.
,
Schisa
J. A.
,
Priess
J. R.
(
2000
)
P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA.
Dev. Biol
219
,
315
333
Savage
R. M.
,
Danilchik
M.V.
(
1993
)
Dynamics of germ plasm localization and its inhibition by ultraviolet irradiation in early cleavage Xenopus embryos.
Dev. Biol
157
,
371
382
Schnabel
R.
,
Weigner
C.
,
Hutter
H.
,
Feichtinger
R.
,
Schnabel
H.
(
1996
)
mex-1 and the general partitioning of cell fate in the early C. elegans embryo.
Mech. Dev
54
,
133
147
Starck
J.
(
1977
)
Radioautographic study of RNA synthesis in Caenorhabditis elegans (Bergerac variety) oogenesis.
Biol. Cell
30
,
181
182
Starck
J.
,
Gibert
M.
,
Brun
J.
,
Bosch
C.
(
1982
)
Ribosomal RNA synthesis and processing during oogenesis of the free living nematode Caenorhabditis elegans.
Comp. Biochem. Physiol
75
,
475
480
Sträβer
K.
,
Baβler
J.
,
Hurt
E.
(
2000
)
Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG, and FG repeat nucleoporins is essential for nuclear mRNA export.
J. Cell. Biol
150
,
695
706
Strome
S.
,
Wood
W. B.
(
1982
)
Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans.
Proc. Natl. Acad. Sci. USA
79
,
1558
1562
Subramaniam
K.
,
Seydoux
G.
(
1999
)
nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans.
Development
126
,
4861
4871
Tabara
H.
,
Hill
R. J.
,
Mello
C. C.
,
Priess
J. R.
,
Kohara
Y.
(
1999
)
pos-1 encodes a cytoplasmic zinc-finger protein essential for germline specification in C. elegans.
Development
126
,
1
11
Tenenhaus
C.
,
Schubert
C.
,
Seydoux
G.
(
1998
)
Genetic requirements for PIE-1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans.
Dev. Biol
200
,
212
224
Tsunekawa
N.
,
Naito
M.
,
Sakai
Y.
,
Nishida
T.
,
Noce
T.
(
2000
)
Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells.
Development
127
,
2741
2750
Wang
C.
,
Lehmann
R.
(
1991
)
Nanos is the localized posterior determinant in Drosophila [published erratum appears in Cell 1992 Mar 20;68(6):1177].
Cell
66
,
637
647
Wilsch-Brauninger
M.
,
Schwarz
H.
,
Nusslein-Volhard
C.
(
1997
)
A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis.
J. Cell Biol
139
,
817
829
Wylie
C.
(
1999
)
Germ cells.
Cell
96
,
165
174
Yoon
C.
,
Kawakami
K.
,
Hopkins
N.
(
1997
)
Zebrafish vasa homologue RNA is localized to the cleavage planes of 2-and 4-cell-stage embryos and is expressed in the primordial germ cells.
Development
124
,
3157
3165
Zorio
D. A.
,
Cheng
N. N.
,
Blumenthal
T.
,
Spieth
J.
(
1994
)
Operons as a common form of chromosomal organization in C. elegans [see comments].
Nature
372
,
270
272
This content is only available via PDF.