The homeotic gene lin-39 and the evolution of nematode epidermal cell fates

Science

Volumn 278, Issue 5337, 1997, Pages 452-455

  Eizinger, Andreas ^a   Sommer, Ralf J ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; EPIDERMIS CELL; HOMEOBOX; MOLECULAR EVOLUTION; NEMATODE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CELL FUSION; CELL LINEAGE; EPIDERMIS; EVOLUTION; EXONS; FEMALE; GENES, HELMINTH; GENES, HOMEOBOX; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; RHABDITIDA; STEM CELLS; VULVA;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; PRISTIONCHUS; PRISTIONCHUS PACIFICUS;

EID: 0030661822     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.278.5337.452     Document Type: Article

References (20)

1. J. E. Sulston and H. R. Horvitz, Dev. Biol. 56, 110 (1977).
2. R. J. Sommer and P. W. Sternberg, Curr. Biol. 6, 52 (1996).
3. R. J. Sommer, Development 124, 243 (1997); Bioessays 19, 225 (1997).
4. R. J. Sommer, Development 124, 243 (1997); Bioessays 19, 225 (1997).
5. We would argue that the fusion of nonvulval cells that is seen in Caenorhabditis is ancestral, as this cell fate is observed in species of many different families. In particular, Strongyloides ratti, a species of the order Strongylida that can be considered as an outgroup for both Caenorhabditis and Pristionchus [V. V. Malakhov, Nematodes (Smithsonian Institution Press, Washington, DC, 1994)] displays fusion of nonvulval epidermal cells (R. J. Sommer, unpublished observation).
6. B. B. Wang et al., Cell 74, 29 (1993); S. G. Clark, A. D. Chisholm, H. R. Horvitz, ibid., p. 43; S. J. Salser, C. M. Loer, C. Kenyon, Genes Dev. 7, 1714 1993); T. R. Clandinin, W. S. Katz, P. W. Sternberg, Dev. Biol. 182, 150 (1997).
7. B. B. Wang et al., Cell 74, 29 (1993); S. G. Clark, A. D. Chisholm, H. R. Horvitz, ibid., p. 43; S. J. Salser, C. M. Loer, C. Kenyon, Genes Dev. 7, 1714 1993); T. R. Clandinin, W. S. Katz, P. W. Sternberg, Dev. Biol. 182, 150 (1997).
8. B. B. Wang et al., Cell 74, 29 (1993); S. G. Clark, A. D. Chisholm, H. R. Horvitz, ibid., p. 43; S. J. Salser, C. M. Loer, C. Kenyon, Genes Dev. 7, 1714 1993); T. R. Clandinin, W. S. Katz, P. W. Sternberg, Dev. Biol. 182, 150 (1997).
9. B. B. Wang et al., Cell 74, 29 (1993); S. G. Clark, A. D. Chisholm, H. R. Horvitz, ibid., p. 43; S. J. Salser, C. M. Loer, C. Kenyon, Genes Dev. 7, 1714 1993); T. R. Clandinin, W. S. Katz, P. W. Sternberg, Dev. Biol. 182, 150 (1997).
10. Ppa-lin-39 was cloned by PCR using degenerate primers in the homeodomain. The primers were 5′-CGTCAGMGTACTGCNTAYAC-3′ and 5′-CATGCKACKRTTYTGRAACCA-3′.
11. Mutagenesis screens were carried out as described (2).
12. Hermaphrodites of the fifth mutant, sy319, never form ventral protrusions or vulvae and thus, cannot be mated.
13. First genetic characterization of these mutants indicates that they belong to several genes. None of the mutants is linked to Ppa-dpy-1 (C. Weise and R. J. Sommer, unpublished observation).
14. DNA was isolated from two independent batches of mutant animals, amplified by three independent PCR reactions, and sequenced in both directions. Although the mutant sy319 cannot be tested genetically, the molecular analysis suggests that the mutant is an allele of Ppa-lin-39. The molecular lesion introduces a stop codon into the hexapeptide, removing the complete homeodomain. The strong vulvaless phenotype of sy319 mutant animals is consistent with the more severe molecular truncation in comparison to the three other alleles (Figs. 3 and 4; Table 1). However, we cannot rule out that a second background mutation is involved in generating the strong vulvaless phenotype of sy319 mutant animals.
15. D. M. Bird and D. L. Riddle, J. Nematol. 26, 138 (1994).
16. The three alleles tu2, tu29, and sy374 were all marked with the linked recessive visible mutation Ppa-dpy-1. Crossed progeny from a mating of such marked vulvaless homozygous hermaphrodites with wild-type males are wild type for the visible marker (being Ppa-dpy-1/+) and wild type for the vulva phenotype scored under Nomarski optics (10/10 for each allele). Such heterozygous hermaphrodites segregated one-quarter vulvaless animals, all of which are also homozygous mutant for the visible marker. Segregants that are wild type for the visible marker are also wild type for the vulva phenotype scored under Nomarski optics (25/25 for each allele).
17. J. Yuan, J. Cell. Biochem. 60, 4 (1996).
18. K.-Z. Lee and R. J. Sommer, unpublished observation.
19. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
20. We thank C. Kenyon and C. Hunter for a Caenorhabditis lin-39 cDNA clone used in the original hybridization experiments; D. Gilmour, S. Jesuthasan, T. Nicolson, and S. Roth for critical reading of the manuscript; and members of the laboratory for discussion. R.J.S. is a Young investigator with the Max-Planck Society.