The Monarch Butterfly Genome Yields Insights into Long-Distance Migration

Zhan, Shuai; Merlin, Christine; Boore, Jeffrey L.; Reppert, Steven M.

doi:10.1016/j.cell.2011.09.052

Cited by 504 publications

(568 citation statements)

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“…In addition to 1,683 Lepidoptera-specific genes (Supplementary Table 22 and Supplementary Note), we found 1,412 P. xylostella-specific genes (Supplementary Fig. 13), exceeding in number the 463 Bombyx mori-specific genes 13 and the 1,184 Danaus plexippus-specific genes 14 (Fig. 2).…”

Section: (Supplementarymentioning

confidence: 84%

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A heterozygous moth genome provides insights into herbivory and detoxification

et al. 2013

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l e t t e r sHow an insect evolves to become a successful herbivore is of profound biological and practical importance. Herbivores are often adapted to feed on a specific group of evolutionarily and biochemically related host plants 1 , but the genetic and molecular bases for adaptation to plant defense compounds remain poorly understood 2 . We report the first whole-genome sequence of a basal lepidopteran species, Plutella xylostella, which contains 18,071 protein-coding and 1,412 unique genes with an expansion of gene families associated with perception and the detoxification of plant defense compounds. A recent expansion of retrotransposons near detoxification-related genes and a wider system used in the metabolism of plant defense compounds are shown to also be involved in the development of insecticide resistance. This work shows the genetic and molecular bases for the evolutionary success of this worldwide herbivore and offers wider insights into insect adaptation to plant feeding, as well as opening avenues for more sustainable pest management.The global pest P. xylostella (Lepidoptera: Yponomeutidae) is thought to have coevolved with the crucifer plant family 3 ( Supplementary Fig. 1) and has become the most destructive pest of economically important food crops, including rapeseed, cauliflower and cabbage 4 . Recently, the total cost of damage and management worldwide was estimated at $4-5 billion per annum 5,6 . This insect is the first species to have evolved resistance to dichlorodiphenyltrichloroethane (DDT) in the 1950s 7 and to Bacillus thuringiensis (Bt) toxins in the 1990s 8 and has developed resistance to all classes of insecticide, making it increasingly difficult to control 9,10 . P. xylostella provides an exceptional system for understanding the genetic and molecular bases of how insect herbivores cope with the broad range of plant defenses and chemicals encountered in the environment (Supplementary Fig. 2).We used a P. xylostella strain (Fuzhou-S) collected from a field in Fuzhou in southeastern China (26.08 °N, 119.28 °E) for sequencing ( Supplementary Fig. 1). Whole-genome shotgun-based Illumina sequencing of single individuals (Supplementary Table 1), even after ten generations of laboratory inbreeding, resulted in a poor initial assembly (N50 = 2.4 kb, representing the size above which 50% of the total length of the sequences is included), owing to high levels of heterozygosity ( Supplementary Figs. 3 and 4 and Supplementary Table 2). Subsequently, we sequenced 100,800 fosmid clones (comprising ~10× the genome length) to a depth of 200× ( Supplementary Fig. 5 and Supplementary Tables 3-5), assembling the resulting sequence data into 1,819 scaffolds, with an N50 of 737 kb, spanning ~394 Mb of the genome sequence (version 1; Supplementary Fig. 6 and Supplementary Table 6). The assembly covered 85.5% of a set of protein-coding ESTs (Supplementary Tables 7 and 8) generated by transcriptome sequencing 11 . Alignment of a subject scaffold against a 126-kb BAC (GenBank GU058050) from an altern...

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Section: (Supplementarymentioning

confidence: 84%

“…The predicted proteomes in the DBM genome and those from the genomes of 11 insect species 13,14,[64][65][66][67][68][69][70][71] and 1 Arachnida outgroup species 72 were used in BLAST (1 × 10 −7 ). The fragmental alignments of HSPs were joined using Solar 36 .…”

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confidence: 99%

A heterozygous moth genome provides insights into herbivory and detoxification

et al. 2013

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“…Such a phylogenetic perspective is necessary to distinguish ancestral from derived states, but has until recently been limited by the availability of a single lepidopteran (B. mori) whole-genome reference sequence or comprehensive linkage map against which to make comparisons. (Two additional lepidopteran whole genomes are now available for H. melpomene (The Heliconius Genome Consortium, 2012) and D. plexippus (Zhan et al, 2011), although the latter's scaffolds are not assigned to chromosomes). A case in point is the reconstruction of the direction of a translocation event that led to rpl36 being Z linked in B. mori but autosomal in Ostrinia nubilalis.…”

Section: Discussionmentioning

confidence: 99%

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

et al. 2012

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We have constructed a linkage map for the peppered moth (Biston betularia), the classical ecological genetics model of industrial melanism, aimed both at localizing the network of loci controlling melanism and making inferences about chromosome dynamics. The linkage map, which is based primarily on amplified fragment length polymorphisms (AFLPs) and genes, consists of 31 linkage groups (LGs; consistent with the karyotype). Comparison with the evolutionarily distant Bombyx mori suggests that the gene content of chromosomes is highly conserved. Gene order is conserved on the autosomes, but noticeably less so on the Z chromosome, as confirmed by physical mapping using bacterial artificial chromosome fluorescence in situ hybridization (BAC-FISH). Synteny mapping identified three pairs of B. betularia LGs (11/29, 23/30 and 24/31) as being orthologous to three B. mori chromosomes (11, 23 and 24, respectively). A similar finding in an outgroup moth (Plutella xylostella) indicates that the B. mori karyotype (n ¼ 28) is a phylogenetically derived state resulting from three chromosome fusions. As with other Lepidoptera, the B. betularia W chromosome consists largely of repetitive sequence, but exceptionally we found a W homolog of a Z-linked gene (laminin A), possibly resulting from ectopic recombination between the sex chromosomes. The B. betularia linkage map, featuring the network of known melanization genes, serves as a resource for melanism research in Lepidoptera. Moreover, its close resemblance to the ancestral lepidopteran karyotype (n ¼ 31) makes it a useful reference point for reconstructing chromosome dynamic events and ancestral genome architectures. Our study highlights the unusual evolutionary stability of lepidopteran autosomes; in contrast, higher rates of intrachromosomal rearrangements support a special role of the Z chromosome in adaptive evolution and speciation.

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“…sequenced (Honeybee Genome Sequencing Consortium 2006; Xia et al 2008;Bonasio et al 2010;Werren et al 2010;Nygaard et al 2011;Zhan et al 2011). Thus, we speculated that the insertion was acquired by MyoIB relatively recently during insect evolution.…”

Section: Drosophila Myo95e Is a Myosin Ib Isoformmentioning

confidence: 98%

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

et al. 2015

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The class I myosin genes are conserved in diverse organisms, and their gene products are involved in actin dynamics, endocytosis, and signal transduction. Drosophila melanogaster has three class I myosin genes, Myosin 31DF (Myo31DF), Myosin 61F (Myo61F), and Myosin 95E (Myo95E). Myo31DF, Myo61F, and Myo95E belong to the Myosin ID, Myosin IC, and Myosin IB families, respectively. Previous loss-of-function analyses of Myo31DF and Myo61F revealed important roles in left-right (LR) asymmetric development and enterocyte maintenance, respectively. However, it was difficult to elucidate their roles in vivo, because of potential redundant activities. Here we generated class I myosin double and triple mutants to address this issue. We found that the triple mutant was viable and fertile, indicating that all three class I myosins were dispensable for survival. A loss-of-function analysis revealed further that Myo31DF and Myo61F, but not Myo95E, had redundant functions in promoting the dextral LR asymmetric development of the male genitalia. Myo61F overexpression is known to antagonize the dextral activity of Myo31DF in various Drosophila organs. Thus, the LR-reversing activity of overexpressed Myo61F may not reflect its physiological function. The endogenous activity of Myo61F in promoting dextral LR asymmetric development was observed in the male genitalia, but not the embryonic gut, another LR asymmetric organ. Thus, Myo61F and Myo31DF, but not Myo95E, play tissue-specific, redundant roles in LR asymmetric development. Our studies also revealed differential colocalization of the class I myosins with filamentous (F)-actin in the brush border of intestinal enterocytes.KEYWORDS myosin I; Myosin 31DF; Myosin 61F; Myosin 95E; left-right asymmetry T HE class I myosin genes encode myosin heavy chains, which are conserved in phylogenetically diverse organisms (Sellers 2000;Krendel and Mooseker 2005). The class I myosins are nonfilamentous, actin-based motor proteins and were the first discovered unconventional myosin proteins. These myosins are involved in a variety of cellular processes, such as cell migration, cell adhesion, and cell growth, through their regulation of actin dynamics, endocytosis, and signal transduction (Osherov and May 2000;Krendel and Mooseker 2005;Kim and Flavell 2008;McConnell and Tyska 2010).The structure of the myosin I heavy chains is evolutionarily conserved and composed of head (or motor), neck, and tail domains ( Figure 1A) (Coluccio 1997;Barylko et al. 2000). The head domain binds to filamentous (F)-actin and adenosine triphosphate (ATP), a common feature of myosin proteins ( Figure 1A) (Mermall et al. 1998); the neck domain possesses one or more IQ motifs, which directly interact with calmodulin or calmodulin-related myosin light chains (Coluccio 1997;Barylko et al. 2000), and the tail domains are divided into short and long types. Short tails contain a single tail homology 1 (TH1) domain, which is rich in basic residues and thought to interact with plasma membranes (Coluccio 1997;Barylko...

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The Monarch Butterfly Genome Yields Insights into Long-Distance Migration

Cited by 504 publications

References 124 publications

A heterozygous moth genome provides insights into herbivory and detoxification

A heterozygous moth genome provides insights into herbivory and detoxification

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

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