Academic journal article Genetics

Autosomal Genes of Autosomal/X-Linked Duplicated Gene Pairs and Germ-Line Proliferation in Caenorhabditis Elegans

Academic journal article Genetics

Autosomal Genes of Autosomal/X-Linked Duplicated Gene Pairs and Germ-Line Proliferation in Caenorhabditis Elegans

Article excerpt

ABSTRACT

We report molecular genetic studies of three genes involved in early germ-line proliferation in Caenorhabditis elegans that lend unexpected insight into a germ-line/soma functional separation of autosomal/ X-linked duplicated gene pairs. In a genetic screen for germ-line proliferation-defective mutants, we identified mutations in rpl-11.1 (L11 protein of the large ribosomal subunit), pab-1 [a poly(A)-binding protein], and glp-3/eft-3 (an elongation factor 1-α homolog). All three are members of autosome/X gene pairs. Consistent with a germ-line-restricted function of rpl-11.1 and pab-1, mutations in these genes extend life span and cause gigantism. We further examined the RNAi phenotypes of the three sets of rpl genes (rpl-11, rpl-24, and rpl-25) and found that for the two rpl genes with autosomal/X-linked pairs (rpl-11 and rpl-25), zygotic germ-line function is carried by the autosomal copy. Available RNAi results for highly conserved autosomal/X-linked gene pairs suggest that other duplicated genes may follow a similar trend. The three rpl and the pab-1/2 duplications predate the divergence between C. elegans and C. briggsae, while the eft-3/4 duplication appears to have occurred in the lineage to C. elegans after it diverged from C. briggsae. The duplicated C. briggsae orthologs of the three C. elegans autosomal/X-linked gene pairs also display functional differences between paralogs. We present hypotheses for evolutionary mechanisms that may underlie germ-line/soma subfunctionalization of duplicated genes, taking into account the role of X chromosome silencing in the germ line and analogous mammalian phenomena.

GENOMES are shaped over evolution by a variety of forces, including gene duplication. The functions of duplicated genes can change over evolutionary time as well. One copy of a duplicated gene pair may acquire deleterious mutations, ultimately rendering it useless to the organism. Alternatively, both genes may remain functional. In the latter case, the duplicates may remain fully redundant or they may take on nonredundant roles. If the ancestral gene fulfilled multiple roles (e.g., was expressed in multiple regions of an organism), subfunctionalization can follow gene duplication such that the duplicated genes acquire different functional roles (THOMAS 1993; HUGHES 1994; LYNCH and CONERY 2000).

One potential factor postulated to influence the fate of duplicated genes is germ-line-specific X chromosome inactivation (McKEE and HANDEL 1993). This phenomenon occurs in the genomes of many organisms, including the nematodes Caenorhabditis elegans and C. briggsae and male mammals. In mammals, the XY body forms during spermatogenesis (see HANDEL 2004 and references therein). In the nematodes, repressing histone modifications have been observed on the X throughout much of hermaphrodite and all of male germ-line development (FONG et al 2002; KELLY et al 2002).

Silencing of the X chromosome during germ-line development could conceivably place constraints on genome organization. Taking cell-essential or housekeeping genes into account, this phenomenon suggests that (1) cell-essential genes are not located on the X; (2) if located on the X, these genes are not subject to inactivation; or (3) germ-line-active copies of these genes must be located in at least one additional place in the genome (i.e., on an autosome). The first possibility is suggested by functional-genomic and microarray studies that have demonstrated a dearth of essential genes (PiANO et al. 2002; KAMATH et al. 2003) and germ-line-enriched genes (REINKE et al. 2000) on the X of C. elegans and of late spermatogenesis-acting genes in mammals (KmL et al. 2004). The second possibility is still unresolved. The last possibility was suggested by McKEE and HANDEL (1993) and may be a determining factor for the existence of several autosomal intronless genes that function late in mouse spermatogenesis and that are closely related to intron-containing genes on the X (HANDEL 2004). …

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