Genetic Analysis of RpL38 and RpL5, Two Minute Genes Located in the Centric Heterochromatin of Chromosome 2 of Drosophila melanogaster

Abstract

The Minute mutations of Drosophila melanogaster are thought to disrupt genes that encode ribosomal proteins (RPs) and thus impair ribosome function and protein synthesis. However, relatively few Minutes have been tied to distinct RP genes and more Minute loci are likely to be discovered. We have identified point mutations in RpL38 and RpL5 in a screen for factors limiting for growth of the D. melanogaster wing. Here, we present the first genetic characterization of these loci. RpL38 is located in the centric heterochromatin of chromosome arm 2R and is identical to a previously identified Minute, M(2)41A, and also l(2)41Af. RpL5 is located in the 2L centric heterochromatin and defines a novel Minute gene. Both genes are haploinsufficient, as heterozygous mutations cause the classic Minute phenotypes of small bristles and delayed development. Surprisingly, we find that RpL38 Ϫ /ϩ and RpL5 Ϫ /ϩ adult flies have abnormally large wings as a result of increased cell size, emphasizing the importance of translational regulation in the control of growth. Taken together, our data provide new molecular and genetic information on two previously uncharacterized Minute/RP genes, the heterochromatic regions in which they reside, and the role of their protein products in the control of organ growth.

Drosophila melanogaster as a model for studying protein-encoding genes that are resident in constitutive heterochromatin

“…The expression of heterochromatic essential genes such as light, rolled, RpL5, RpL38, RpL15, Nipped-B and Parp is present throughout all developmental stages (Biggs et al, 1994;Rollins et al, 1999;Tulin et al, 2002;Marygold et al, 2005;Schulze et al, 2005). The same is true for fourteen predicted genes from chromosome 2 heterochromatin that we have recently analysed (F Rossi, N Corradini, R Moschetti, R Caizzi and P Dimitri, unpublished data).…”

“…Thus far, at least 32 essential genes are known to map to the mitotic heterochromatin of chromosomes 2 and 3. Only a few of these, however, are sufficiently defined at the molecular level: RpL5, light, concertina, rolled, RpL38, Nipped-B, Nipped-A, Parp and RpL15 (Hilliker, 1976;Devlin et al, 1990a, b;Parks and Wieschaus, 1991;Biggs et al, 1994;Rollins et al, 1999;Tulin et al, 2002;Myster et al, 2004;Marygold et al, 2005;Schulze et al, 2005).…”

“…Highly expressed genes tend to have substantially shorter introns than those expressed at low levels (Castillo-Davis et al, 2002). In this regard, it is worth noting that although RpL38, RpL5 and RpL15 -three highly expressed ribosomal protein-coding genes -are located in heterochromatin, they are all short and carry short introns (Marygold et al, 2005;Schulze et al, 2005).…”

Essential Loci in Centromeric Heterochromatin of Drosophila melanogaster. I: The Right Arm of Chromosome 2

“…The Nipped-B complementation group was identified by the eight Nipped-B alleles sequenced by Gause et al (2008) (see Table 1). Similarly, Marygold et al (2005) previously sequenced line NC21 showing that it is an allele of RpL38.…”

“…One of these heterochromatic loci was identified as the previously described rl gene. Two of the remaining vital loci have since been identified: Nipped-A is synonymous with the l(2) 41Ah complementation group (Rollins et al 1999) and RpL38 is synonymous with Minute(2)41A and Hilliker's (1976) l(2)41Af complementation group (Marygold et al 2005; also referred to as l(2)Ag in FlyBase). In addition, Rollins et al (1999) found the Nipped-B gene to be located in 2Rh, but how this locus fit into the data from Hilliker (1976) was unclear.…”