A combined RAD-Seq and WGS approach reveals the genomic basis of yellow color variation in bumble bee Bombus terrestris

AbstractBackgroundIn the model bumble bee species B. terrestris, both males and females exhibit black coloration on the third thoracic and first metasomal segments. We discovered a fortuitous lab-generated mutant in which this typical black coloration is replaced by yellow. As this same color variant is found in several sister lineages to B. terrestris within the Bombus s.s. subgenus, this could be a result of ancestral allele sorting.ResultsUtilizing a combination of RAD-Seq and whole-genome re-sequencing approaches, we localized the color-generating variant to a single SNP in the protein-coding sequence of a homeobox transcription factor, cut. Sanger sequencing confirmed fixation of this SNP between wildtype and yellow mutants. Protein domain analysis revealed this SNP to generate an amino acid change (Ala38Pro) that modifies the conformation of coiled-coil structural elements which lie outside the characteristic DNA binding domains. We found all Hymenopterans including B. terrestris sister lineages possess the non-mutant allele, indicating different mechanism(s) are involved in the same black to yellow transition in nature.ConclusionsCut is a highly pleiotropic gene important for multiple facets of development, yet this mutation generated no noticeable external phenotypic effects outside of setal characteristics. Reproductive capacity was observed to be reduced, however, with queens being less likely to mate and produce female offspring, in a manner similar to workers. Our research implicates a novel developmental player in pigmentation, and potentially caste as well, thus contributing to a better understanding of the evolution of diversity in both of these processes.

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A combined RAD-Seq and WGS approach reveals the genomic basis of yellow color variation in bumble bee Bombus terrestris

Scientific Reports ◽

10.1038/s41598-021-87194-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Sarthok Rasique Rahman ◽

Jonathan Cnaani ◽

Lisa N. Kinch ◽

Nick V. Grishin ◽

Heather M. Hines

Keyword(s):

Bombus Terrestris ◽

Coiled Coil ◽

Female Offspring ◽

Color Variation ◽

Reproductive Capacity ◽

Bumble Bee ◽

Protein Coding ◽

Dna Binding Domains ◽

Binding Domains ◽

Body Coloration

AbstractBumble bees exhibit exceptional diversity in their segmental body coloration largely as a result of mimicry. In this study we sought to discover genes involved in this variation through studying a lab-generated mutant in bumble bee Bombus terrestris, in which the typical black coloration of the pleuron, scutellum, and first metasomal tergite is replaced by yellow, a color variant also found in sister lineages to B. terrestris. Utilizing a combination of RAD-Seq and whole-genome re-sequencing, we localized the color-generating variant to a single SNP in the protein-coding sequence of transcription factor cut. This mutation generates an amino acid change that modifies the conformation of a coiled-coil structure outside DNA-binding domains. We found that all sequenced Hymenoptera, including sister lineages, possess the non-mutant allele, indicating different mechanisms are involved in the same color transition in nature. Cut is important for multiple facets of development, yet this mutation generated no noticeable external phenotypic effects outside of setal characteristics. Reproductive capacity was reduced, however, as queens were less likely to mate and produce female offspring, exhibiting behavior similar to that of workers. Our research implicates a novel developmental player in pigmentation, and potentially caste, thus contributing to a better understanding of the evolution of diversity in both of these processes.

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Recurrent evolution of vertebrate transcription factors by transposase capture

Science ◽

10.1126/science.abc6405 ◽

2021 ◽

Vol 371 (6531) ◽

pp. eabc6405 ◽

Cited By ~ 1

Author(s):

Rachel L. Cosby ◽

Julius Judd ◽

Ruiling Zhang ◽

Alan Zhong ◽

Nathaniel Garry ◽

...

Keyword(s):

Fusion Proteins ◽

Regulatory Elements ◽

Exon Shuffling ◽

Cellular Functions ◽

Protein Coding ◽

Regulatory Domains ◽

Dna Binding Domains ◽

Binding Domains ◽

Genome Wide ◽

Tetrapod Evolution

Genes with novel cellular functions may evolve through exon shuffling, which can assemble novel protein architectures. Here, we show that DNA transposons provide a recurrent supply of materials to assemble protein-coding genes through exon shuffling. We find that transposase domains have been captured—primarily via alternative splicing—to form fusion proteins at least 94 times independently over the course of ~350 million years of tetrapod evolution. We find an excess of transposase DNA binding domains fused to host regulatory domains, especially the Krüppel-associated box (KRAB) domain, and identify four independently evolved KRAB-transposase fusion proteins repressing gene expression in a sequence-specific fashion. The bat-specific KRABINER fusion protein binds its cognate transposons genome-wide and controls a network of genes and cis-regulatory elements. These results illustrate how a transcription factor and its binding sites can emerge.

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The Hyperthermophile Protein Sso10a is a Dimer of Winged Helix DNA-binding Domains Linked by an Antiparallel Coiled Coil Rod

Journal of Molecular Biology ◽

10.1016/j.jmb.2004.05.044 ◽

2004 ◽

Vol 341 (1) ◽

pp. 73-91 ◽

Cited By ~ 22

Author(s):

Liqing Chen ◽

Li-Rong Chen ◽

Xiaoyin E. Zhou ◽

Yujun Wang ◽

Mebrahtu A. Kahsai ◽

...

Keyword(s):

Dna Binding ◽

Coiled Coil ◽

Winged Helix ◽

Dna Binding Domains ◽

Binding Domains ◽

Antiparallel Coiled Coil

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Recurrent evolution of vertebrate transcription factors by transposase capture

10.1101/2020.05.07.082677 ◽

2020 ◽

Author(s):

Rachel L. Cosby ◽

Julius Judd ◽

Ruiling Zhang ◽

Alan Zhong ◽

Nathaniel Garry ◽

...

Keyword(s):

Transcription Factors ◽

Fusion Proteins ◽

Fusion Gene ◽

Regulatory Elements ◽

Exon Shuffling ◽

Protein Coding ◽

Regulatory Domains ◽

Dna Binding Domains ◽

Binding Domains ◽

Cellular Genes

AbstractHow genes with novel cellular functions evolve is a central biological question. Exon shuffling is one mechanism to assemble new protein architectures. Here we show that DNA transposons, which are mobile and pervasive in genomes, have provided a recurrent supply of exons and splice sites to assemble protein-coding genes in vertebrates via exon-shuffling. We find that transposase domains have been captured, primarily via alternative splicing, to form new fusion proteins at least 94 times independently over ∼350 million years of tetrapod evolution. Evolution favors fusion of transposase DNA-binding domains to host regulatory domains, especially the Krüppel-associated Box (KRAB), suggesting transposase capture frequently yields new transcriptional repressors. We show that four independently evolved KRAB-transposase fusion proteins repress gene expression in a sequence-specific fashion. Genetic knockout and rescue of the bat-specific KRABINER fusion gene in cells demonstrates that it binds its cognate transposons genome-wide and controls a vast network of genes and cis-regulatory elements. These results illustrate a powerful mechanism by which a transcription factor and its dispersed binding sites emerge at once from a transposon family.One Sentence SummaryHost-transposase fusion generates novel cellular genes, including deeply conserved and lineage specific transcription factors.

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The Chromokinesin Kid Is Required for Maintenance of Proper Metaphase Spindle Size

Molecular Biology of the Cell ◽

10.1091/mbc.e05-03-0244 ◽

2005 ◽

Vol 16 (11) ◽

pp. 5455-5463 ◽

Cited By ~ 57

Author(s):

Noriko Tokai-Nishizumi ◽

Miho Ohsugi ◽

Emiko Suzuki ◽

Tadashi Yamamoto

Keyword(s):

Dna Binding ◽

Coiled Coil ◽

Metaphase Plate ◽

Wild Type ◽

Dna Binding Domains ◽

Binding Domains ◽

Chromosome Alignment ◽

Spindle Microtubules ◽

Similar Domain

The human chromokinesin Kid/kinesin-10, a plus end-directed microtubule (MT)-based motor with both microtubule- and DNA-binding domains, is required for proper chromosome alignment at the metaphase plate. Here, we performed RNA interference experiments to deplete endogenous Kid from HeLa cells and confirmed defects in metaphase chromosome arm alignment in Kid-depleted cells. In addition, we noted a shortening of the spindle length, resulting in a pole-to-pole distance only 80% of wild type. The spindle microtubule-bundles with which Kid normally colocalize became less robust. Rescue of the two Kid deficiency phenotypes—imprecise chromosome alignment at metaphase and shortened spindles— exhibited distinct requirements. Mutants lacking either the DNA-binding domain or the MT motor ATPase failed to rescue the former defect, whereas rescue of the shortened spindle phenotype required neither activity. Kid also exhibits microtubule bundling activity in vitro, and rescue of the shortened spindle phenotype and the bundling activity displayed similar domain requirements, except that rescue required a coiled-coil domain not needed for bundling. These results suggest that distinct from its role in chromosome movement, Kid contributes to spindle morphogenesis by mediating spindle microtubules stabilization.

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Faculty Opinions recommendation of Excess non-synonymous substitutions suggest that positive selection episodes occurred during the evolution of DNA-binding domains in the Arabidopsis R2R3-MYB gene family.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1015386.196756 ◽

2003 ◽

Author(s):

Elena Alvarez-Buylla

Keyword(s):

Dna Binding ◽

Positive Selection ◽

Gene Family ◽

Synonymous Substitutions ◽

Dna Binding Domains ◽

Binding Domains ◽

Myb Gene ◽

R2r3 Myb

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Juvenile hormone affects the development and strength of circadian rhythms in young bumble bee (Bombus terrestris) workers

Neurobiology of Sleep and Circadian Rhythms ◽

10.1016/j.nbscr.2020.100056 ◽

2020 ◽

Vol 9 ◽

pp. 100056

Author(s):

Atul Pandey ◽

Uzi Motro ◽

Guy Bloch

Keyword(s):

Circadian Rhythms ◽

Juvenile Hormone ◽

Bombus Terrestris ◽

Bumble Bee

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Genome Sequence of the Asian Honeybee in Pakistan Sheds Light on Its Phylogenetic Relationship with Other Honeybees

Insects ◽

10.3390/insects12070652 ◽

2021 ◽

Vol 12 (7) ◽

pp. 652

Author(s):

Hongwei Tan ◽

Muhammad Naeem ◽

Hussain Ali ◽

Muhammad Shakeel ◽

Haiou Kuang ◽

...

Keyword(s):

Phylogenetic Relationship ◽

Genome Sequence ◽

Apis Cerana ◽

Gc Content ◽

Protein Domain ◽

Pollination Services ◽

Protein Coding ◽

Close Relationship ◽

Genome Scale ◽

Asian Honeybee

In Pakistan, Apis cerana, the Asian honeybee, has been used for honey production and pollination services. However, its genomic makeup and phylogenetic relationship with those in other countries are still unknown. We collected A. cerana samples from the main cerana-keeping region in Pakistan and performed whole genome sequencing. A total of 28 Gb of Illumina shotgun reads were generated, which were used to assemble the genome. The obtained genome assembly had a total length of 214 Mb, with a GC content of 32.77%. The assembly had a scaffold N50 of 2.85 Mb and a BUSCO completeness score of 99%, suggesting a remarkably complete genome sequence for A. cerana in Pakistan. A MAKER pipeline was employed to annotate the genome sequence, and a total of 11,864 protein-coding genes were identified. Of them, 6750 genes were assigned at least one GO term, and 8813 genes were annotated with at least one protein domain. Genome-scale phylogeny analysis indicated an unexpectedly close relationship between A. cerana in Pakistan and those in China, suggesting a potential human introduction of the species between the two countries. Our results will facilitate the genetic improvement and conservation of A. cerana in Pakistan.

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Olfactory coding in the antennal lobe of the bumble bee Bombus terrestris

Scientific Reports ◽

10.1038/s41598-021-90400-6 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Marcel Mertes ◽

Julie Carcaud ◽

Jean-Christophe Sandoz

Keyword(s):

Honey Bees ◽

Antennal Lobe ◽

Bombus Terrestris ◽

Bumble Bees ◽

Foraging Strategies ◽

Bumble Bee ◽

Carbon Chain Length ◽

Olfactory Coding ◽

Major Transitions

AbstractSociality is classified as one of the major transitions in evolution, with the largest number of eusocial species found in the insect order Hymenoptera, including the Apini (honey bees) and the Bombini (bumble bees). Bumble bees and honey bees not only differ in their social organization and foraging strategies, but comparative analyses of their genomes demonstrated that bumble bees have a slightly less diverse family of olfactory receptors than honey bees, suggesting that their olfactory abilities have adapted to different social and/or ecological conditions. However, unfortunately, no precise comparison of olfactory coding has been performed so far between honey bees and bumble bees, and little is known about the rules underlying olfactory coding in the bumble bee brain. In this study, we used in vivo calcium imaging to study olfactory coding of a panel of floral odorants in the antennal lobe of the bumble bee Bombus terrestris. Our results show that odorants induce reproducible neuronal activity in the bumble bee antennal lobe. Each odorant evokes a different glomerular activity pattern revealing this molecule’s chemical structure, i.e. its carbon chain length and functional group. In addition, pairwise similarity among odor representations are conserved in bumble bees and honey bees. This study thus suggests that bumble bees, like honey bees, are equipped to respond to odorants according to their chemical features.

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