Yellow-e Determines the Color Pattern of Larval Head and Tail Spots of the Silkworm Bombyx mori

Abstract

Yellow proteins form a large family in insects. In Drosophila melanogaster, there are 14 yellow genes in the genome. Previous studies have shown that the yellow gene is necessary for normal pigmentation; however, the roles of other yellow genes in body coloration are not known. Here, we provide the first evidence that yellow-e is required for normal body color pattern in insect larvae. In two mutant strains, bts and its allele bts2, of the silkworm Bombyx mori, the larval head cuticle and anal plates are reddish brown instead of the white color found in the wild type. Positional cloning revealed that deletions in the Bombyx homolog of the Drosophila yellow-e gene (Bmyellow-e) were responsible for the bts/bts2 phenotype. Bmyellow-e mRNA was strongly expressed in the trachea, testis, and integument, and expression markedly increased at the molting stages. This profile is quite similar to that of Bmyellow, a regulator of neonatal body color and body markings in Bombyx. Quantitative reverse transcription-PCR analysis showed that Bmyellow-e mRNA was heavily expressed in the integument of the head and tail in which the bts phenotype is observed. The present results suggest that Yellow-e plays a crucial role in the pigmentation process of lepidopteran larvae.Major royal jelly proteins (MRJPs) 2 were initially identified as major constituents of royal jelly; they constitute 80 -90% of total royal jelly proteins, which play a central role in honeybee development (1). The yellow gene family of Drosophila melanogaster is known to encode the MRJP domain-containing protein (2) and to consist of 14 genes (3). The D. melanogaster yellow gene (Dmyellow) determines the degree and pattern of melanization by cooperating with the ebony gene (4). Dmyellow also controls male courtship behavior by its temporal expression in the brain (5). Furthermore, biochemical experiments revealed that the products of two other yellow genes, Dmyellow-f and Dmyellow-f2, have dopachrome-conversion enzyme activity (6). Despite the widespread use of the yellow gene as a visible genetic marker, there is little information regarding the functions of other members of the MRJP/YELLOW protein family in Drosophila and other organisms.Larval color variations are often observed in many lepidopteran insects. About 40 body color mutants have been reported in the silkworm, Bombyx mori (7,8). Recently, two mutants, chocolate (ch) and sooty (so), were characterized molecularly. In the ch mutants, the body color of neonatal larvae and the body markings of older instar larvae are reddish brown instead of normal black. Mutations at the so locus produce smoky larvae and black pupae. Linkage analysis and genomic studies revealed that Bombyx yellow and ebony are the genes responsible for the ch and so mutation, respectively (9). These results suggest that Yellow promotes and Ebony inhibits melanization in Lepidoptera and that melanin-synthesis enzymes play a critical role in the color pattern of lepidopteran larvae.In the bts (brown head and tail spot) body color mutant ...

Identification, mRNA expression and functional analysis of several yellow family genes in Tribolium castaneum

“…In P. xuthus and B. mori larvae, the expression of yellow-y genes, PxY-y and BmY-y, is also consistent with the appearance and patterning of black pigmentation. Very recently, Ito et al (2009) reported that BmY-e is also required for the normal larval body color pattern in B. mori. However, the exact physiological functions of most yellow genes are still little understood.…”

A major facilitator superfamily protein participates in the reddish brown pigmentation in Bombyx mori

“…Positional cloning revealed that yellow-e accounts for the phenotype of bts (brown tail spot, larval head cuticle and anal plates are reddish brown color instead of white) (Ito et al, 2010). A 126 bp deletion in the genome caused the loss of arylalkylamine N-acetyltransferase activity which is responsible for mln (melanism, black moth) Zhan et al, 2010).…”

“…Many body color mutants have been obtained in Bombyx mori, including lemon (lemon lethal) (Meng et al, 2009), ch, so , bts (Ito et al, 2010), mln Zhan et al, 2010), and sch , and have been characterized molecularly. It was found that mutations in the sepiapterin reductase (SPR) gene (Bmspr) are responsible for the yellow body coloration of the lemon and lemon lethal mutations (Meng et al, 2009).…”

Disruption of an N-acetyltransferase gene in the silkworm reveals a novel role in pigmentation

“…Thus, the independent and stable phenotypic defects are likely to be due to functional redundancy among the gene family members in insects. Recent research has shown that the yellow-e protein determines the silkworm bts mutant (Ito et al, 2010), which exhibits a similar…”

“…Within lepidopteran species, the silkworm is considered a suitable model for the genetic and molecular identification of traits owing to its substantial economic value (Fujii et al, 1998;Goldsmith et al, 2005), abundantly maintained variants and widely available genetic and genomic resources (Mita et al, 2004;Xia et al, 2004;Miao et al, 2005;International Silkworm Genome Consortium, 2008;Yamamoto et al, 2008;Zhan et al, 2009). Recently, several larval mutants have been identified for this well-studied model (Futahashi et al, 2008;Ito et al, 2009;Meng et al, 2009b;Ito et al, 2010), including novel models outside of the classical insect melanin synthesis pathway (Ito et al, 2009;Meng et al, 2009b).…”