Caenorhabditis elegans embryonic axial patterning requires two recently discovered posterior-group Hox genes.

Hox genes encode highly conserved transcription factors that control regional identities of cells and tissues along the developing anterior-posterior axis, probably in all bilaterian metazoans. However, in invertebrate embryos other than Drosophila, Hox gene functions remain largely unknown except by inference from sequence similarities and expression patterns. Recent genomic sequencing has shown that Caenorhabditis elegans has three Hox genes of the posterior paralog group [Ruvkun, G. & Hobert, O. (1998) Science 282, 2033-2041]. However, only one has been previously identified genetically, and it is not required for embryonic development [Chisholm, A. (1991) Development (Cambridge, U.K.) 111, 921-932]. Herein, we report identification of the remaining two posterior paralogs as the nob-1 gene and the neighboring php-3 gene. Elimination of nob-1 and php-3 functions causes gross embryonic defects in both posterior patterning and morphogenetic movements of the posterior hypodermis, as well as posterior-to-anterior cell fate transformations and lethality. The only other Hox gene essential for embryogenesis is the labial/Hox1 homolog ceh-13, required for more anterior patterning [Brunschwig, K., Wittmann, C., Schnabel, R., Burglin, T. R., Tobler, H. & Muller, F. (1999) Development (Cambridge, U.K.) 126, 1537-1546]. Therefore, essential embryonic patterning in C. elegans requires only Hox genes of the anterior and posterior paralog groups, raising interesting questions about evolution of the medial-group genes.

[1]  C. Kenyon,et al.  A cluster of Antennapedia-class homeobox genes in a nonsegmented animal. , 1991, Science.

[2]  Andrew D. Chisholm,et al.  Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39 , 1993, Cell.

[3]  C. Huynh,et al.  A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. , 1992, Genetics.

[4]  S. Carroll,et al.  Early animal evolution: emerging views from comparative biology and geology. , 1999, Science.

[5]  J. Priess,et al.  Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. , 1986, Developmental biology.

[6]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[7]  C. Kenyon,et al.  The role of lin-22, a hairy/enhancer of split homolog, in patterning the peripheral nervous system of C. elegans. , 1997, Development.

[8]  A. Fire,et al.  Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans , 1998, Nature.

[9]  Andrew Smith Genome sequence of the nematode C-elegans: A platform for investigating biology , 1998 .

[10]  G. Ruvkun,et al.  The taxonomy of developmental control in Caenorhabditis elegans. , 1998, Science.

[11]  Henry F. Epstein,et al.  Caenorhabditis elegans : modern biological analysis of an organism , 1995 .

[12]  A. Fire,et al.  Double-stranded RNA as a mediator in sequence-specific genetic silencing and co-suppression. , 1998, Trends in genetics : TIG.

[13]  D. Martinez,et al.  Cnidarian homeoboxes and the zootype , 1998, Nature.

[14]  C. Hunter,et al.  Spatial and Temporal Controls Target pal-1 Blastomere-Specification Activity to a Single Blastomere Lineage in C. elegans Embryos , 1996, Cell.

[15]  J White,et al.  Four-Dimensional Imaging: Computer Visualization of 3D Movements in Living Specimens , 1996, Science.

[16]  C. Kenyon,et al.  A homeotic gene cluster patterns the anteroposterior body axis of C. elegans , 1993, Cell.

[17]  G. Ruvkun,et al.  Nematode homeobox cluster , 1991, Nature.

[18]  A. Fire,et al.  RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  A. Chisholm,et al.  Control of cell fate in the tail region of C. elegans by the gene egl-5. , 1991, Development.

[20]  M. Wigler,et al.  Cloning the differences between two complex genomes , 1993, Science.

[21]  Thomas Blumenthal,et al.  Operons as a common form of chromosomal organization in C. elegans , 1994, Nature.

[22]  S. Brenner The genetics of Caenorhabditis elegans. , 1974, Genetics.

[23]  R. Schnabel,et al.  Anterior organization of the Caenorhabditis elegans embryo by the labial-like Hox gene ceh-13. , 1999, Development.

[24]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[25]  David Hirsh,et al.  A trans-spliced leader sequence on actin mRNA in C. elegans , 1987, Cell.

[26]  W B Wood,et al.  Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Sean B. Carroll,et al.  Hox genes in brachiopods and priapulids and protostome evolution , 1999, Nature.

[28]  C. Mello,et al.  RNAi in C. elegans: Soaking in the Genome Sequence , 1998, Science.