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First published online 18 February 2004
doi: 10.1242/dev.01002

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C. elegans pro-1 activity is required for soma/germline interactions that influence proliferation and differentiation in the germ line

Department of Biology New York University, New York, NY 10003, USA

View larger version (24K): [in a new window]   Fig. 1. Selected stages and lineages of hermaphrodite germline and somatic gonad development. Schematic diagram depicting four stages of gonadogenesis (left) and a corresponding abbreviated lineage (right). Yellow indicates germline proliferation; green indicates meiotic development. Somatic gonad lineages are coded: red, DTC; dark blue, SS cells; cyan, differentiated sheath cells; gray, spermatheca; white, uterus (Kimble and Hirsh, 1979); broken lines indicate additional cell divisions. The germ line is largely syncytial; `germ cell' refers to each nucleus and surrounding cytoplasm.

View larger version (70K): [in a new window]   Fig. 2. The pro-1(na48) Pro phenotype. One gonad arm of adult hermaphrodites under Nomarski optics (A,C) and in fixed DAPI-stained whole worms (B,D). A,B and C,D are the same wild-type and pro-1(na48) individuals, respectively. Arrowheads indicate the abnormal gametogenesis/proximal mitosis border. Scale bars: 25 µm. Asterisks indicate the distal end of the gonad arms.

View larger version (92K): [in a new window]   Fig. 3. Mitosis occurs within proximal undifferentiated germ cells in pro-1(na48) adults. Dissected gonad from adult wild-type (A-D) and pro-1(na48) (E-H) hermaphrodites labeled with DAPI (A,E), anti-phopho-histone H3 (B,F) and anti-MSP (C,G), and overlaid (D,H). Arrows (B,F) indicate M-phase mitotic nuclei (phospho-histone H3-positive/MSP-negative, non-oocyte). Arrowheads indicate the abnormal gametogenesis/proximal mitosis border. Scale bars: 25 µm. Asterisks indicate the distal end of the gonad arms.

View larger version (76K): [in a new window]   Fig. 4. Time-course analysis of the pro-1(na48) Pro phenotype. (A) Synchronized DAPI-stained animals (see Materials and methods) were scored for the presence of distal mitotic, transition, pachytene, gametogenic and proximal mitotic nuclei at indicated time points. Data are percent of gonad arms containing the indicated nuclei at a given time point. For each time point (46-70 hours at 2-hour intervals), n=62, 30, 66, 42, 58, 65, 38, 71, 60, 53, 80, 57 and 81 gonad arms, respectively. (B F) One characteristic gonad arm from selected time points. (B) 52 hours: all-proliferative; (C) 58 hours: distal mitosis, transition and proximal mitosis; (D) higher-magnification view (different focal plane) of C to show transition nuclei (left) distal to mitotic nuclei (right); (E) 64 hours: distal mitotic, transition, pachytene and proximal mitotic nuclei; (F) 66 hours: gametogenesis just distal to proximal mitosis. Arrowheads indicate the abnormal gametogenesis/proximal mitosis border. Asterisks indicate the distal end of the gonad arms. Scale bars: 10 µm in D; 25 µm in B,C,E,F.

View larger version (100K): [in a new window]   Fig. 5. PRO-1 is a member of a subfamily of WD-repeat proteins. Unbroken blue bars indicate WD-repeats in the underlying sequence (based on http://bmerc-www.bu.edu/wdrepeat/celegans/R166_CE_NEW.html); broken bars indicate possible degenerate repeats. The D211 residue is in red. Alignment from ClustalW (MacVector). Identical residues are boxed and shaded when present in more than four proteins; a consensus of these amino acids is given under the alignment. Sequences (NCBI locus names) are protozoan T. brucei (CAB95350), fission yeast S. pombe (NP_593710), budding yeast S. cerevisiae (NP_014217), plant A. thaliana (NP_190487), C. elegans (NP_496271), fly D. melanogaster (NP_569954) and H. sapiens (NP_077005). BLAST E-values against full-length PRO-1 range from 2.3x10-36 (human) to 1.9x10-10 (S. cerevisiase).

View larger version (100K): [in a new window]   Fig. 6. The pro-1(RNAi) somatic gonad phenotype. lim-7::GFP marks sheath pairs 1-4 in the adult hermaphrodite. Nomarski (A,D), GFP (B,E) and overlay (C,F) of one lim-7::GFP gonad arm in wild type (A-C) and pro-1(RNAi) (D-F). respectively. No GFP-positive sheath cells are visible in E; inset is the head of the same animal showing lim-7::GFP(+) head neurons (positive control for the transgene). (G) Nomarski image of a rare pro-1(RNAi) Pro germ line. Arrowheads indicate the abnormal gametogenesis/proximal mitosis border. Scale bars: 25 µm. Asterisks indicate the distal end of the gonad arms.

View larger version (19K): [in a new window]   Fig. 7. pro-1 mosaic analysis. Major embryonic lineages, somatic gonad lineages and the SS cells are shown. Broken lines indicate six divisions between MS and somatic gonad founders Z1 and Z4. Symbols are positioned at the youngest cell in which the transgenic array was lost, as indicated by GFP expression pattern (see text, and Materials and methods). Mosaic animals were scored wild type (circle), Pro (triangle) or Emo (square). For early losses, both gonad arms were scored. For losses within somatic gonad lineages, the phenotype of the gonad arm in which the array was lost is indicated.

View larger version (14K): [in a new window]   Fig. 8. Models for proposed SS lineage involvement in regulation of initial meiosis. All germ cells are mitotic in the L2 and meiotic onset occurs in the L3. See text for discussion of models depicted in A and B.

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