Finding the missing honey bee genes: lessons learned from a genome upgrade

Elsik, Christine G.; Worley, Kim C.; Bennett, Anna; Beye, Martin; Câmara, Francisco; Childers, Christopher P.; Graaf, Dirk C. de; Debyser, Griet; Deng, Jixin; Devreese, Bart; Elhaik, Eran; Evans, Jay D.; Foster, Leonard J.; Graur, Dan; Guigó, Roderic; Hoff, Katharina J.; Holder, Michael; Hudson, Matthew E.; Hunt, Greg J.; Jiang, Huaiyang; Joshi, Vandita; Khetani, Radhika S.; Kosarev, Peter; Kovar, Christie; Ma, Jian; Maleszka, Ryszard; Moritz, Robin F. A.; Muñoz-Torres, Monica; Murphy, Terence; Muzny, Donna M.; Newsham, Irene; Reese, Justin; Robertson, Hugh M.; Robinson, Gene E.; Rueppell, Olav; Solovyev, Victor; Stanke, Mario; Stolle, Eckart; Tsuruda, Jennifer M.; Vaerenbergh, Matthias Van; Waterhouse, Robert M.; Weaver, Daniel; Whitfield, Charles W.; Wu, Yuanqing; Zdobnov, Evgeny M.; Zhang, Lan; Zhu, Dianhui; Gibbs, Richard A.

doi:10.1186/1471-2164-15-86

Cited by 394 publications

(400 citation statements)

References 105 publications

(164 reference statements)

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“…Thus, I annotated the data using the current official gene set from beebase (Elsik et al, 2014). The majority of DMRs was either intergenic (i.e.…”

Section: Resultsmentioning

confidence: 99%

“…Following this, reads were aligned to the honey bee genome assembly 4.5 from beebase (http://hymenopteragenome.org/beebase/; Elsik et al (2014)) using BWA .…”

Section: Methodsmentioning

confidence: 99%

“…Especially since the publication of the honey bee genome in 2006 (Honeybee Genome Sequencing Consortium, 2006), and its updated version in 2014 (Elsik et al, 2014), we gained much information about the molecular mechanisms underlying memory. One advantage of honey bees in this field of research is that they are wild animals.…”

Section: Molecular Mechanisms Of Honey Bee Memory Formationmentioning

confidence: 99%

“…The honey bee genome is rather GC poor (Honeybee Genome Sequencing Consortium, 2006;Elsik et al, 2014). The CpG (i.e.…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 99%

“…Since the honey bee genome was sequenced in 2006 (Honeybee Genome Sequencing Consortium, 2006), and updated by Elsik et al (2014), our knowledge about the molecular landscape of bees continuously expands. The honey bee genome has an estimated size of 250 Mb and 15314 protein coding genes are annotated.…”

Section: Introductionmentioning

confidence: 99%

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DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

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Memory formation is a crucial task of the brain. It allows animals to dynamically respond to a changing environment by combining information about current and previous experiences. Thus, it promotes complex behaviours such as living in social groups and elaborate foraging tactics. The ability to form memories is present across the animal kingdom in a variety of forms. The honeybee -an eusocial insect -is capable of both 'simple' associative and complex rule learning. Despite decades of research into the mechanisms of memory formation, however, much remains unknown.One little-understood aspect is the regulation of molecular mechanisms during memory formation.Understanding regulation of transcription is particularly important in this context, as transcription is a requirement for any stable memory. Epigenetic mechanisms regulate transcription by directly interacting with chromatin. Importantly, epigenetic mechanisms are conserved across species as distinct as humans and honeybees. This thesis aims to investigate one particular epigenetic mechanism -DNA methylation -and its role in honey bee memory formation by using behavioural, physiological and molecular assays.First, I studied the role of DNA methyltransferases (Dnmts), which catalyse DNA methylation, after olfactory reward learning. Bees were trained to associate an odour with a sugar reward. Dnmts were then blocked after conditioning using a pharmacological inhibitor. 24 hours later, bees were tested for memory retention and generalisation. Dnmt inhibition increased the generalisation to an odour that was not present during the training, thus impairing stimulus-specific memory. This effect was learning-dependent, as bees' response to odours or sugar water alone did not change after treatment. Furthermore, this effect was robust against alterations in the training paradigm, but the directionality depended on the number of training trials. Next, I used Ca2+ -imaging of the bees' primary olfactory centre (i.e. antennal lobe, AL) to investigate whether Dnmts affect changes in AL processing established during memory formation. The AL is involved in odour discrimination and olfactory learning; both processes are also crucial for stimulus-specific memory formation. If Dnmts were inhibited after olfactory reward learning, the AL response to a new odour changed 48 hours later. This effect potentially serves as a functional explanation for the behavioural phenotype observed after Dnmt inhibition. Furthermore, this study provides the first in vivo evidence for Dnmt-mediated regulation of neuronal networks during memory formation.As DNA methylation regulates transcription, I next investigated the effect of Dnmt inhibition on gene expression. Using qPCR I studied 30 memory-associated genes. In response to Dnmt inhibition, 9 genes were upregulated after conditioning. For some of these genes I then investigated their i methylation patterns using a bisulfite conversion based Mass spectrometry approach. Memory formation changed the methylation pattern compared to both...

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“…Thus, I annotated the data using the current official gene set from beebase (Elsik et al, 2014). The majority of DMRs was either intergenic (i.e.…”

Section: Resultsmentioning

confidence: 99%

“…Following this, reads were aligned to the honey bee genome assembly 4.5 from beebase (http://hymenopteragenome.org/beebase/; Elsik et al (2014)) using BWA .…”

Section: Methodsmentioning

confidence: 99%

Section: Molecular Mechanisms Of Honey Bee Memory Formationmentioning

confidence: 99%

“…The honey bee genome is rather GC poor (Honeybee Genome Sequencing Consortium, 2006;Elsik et al, 2014). The CpG (i.e.…”

Section: Dna Methylation and Demethylation In Honey Beesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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DNA methylation and the regulation of stimulus-specific memory formation

Biergans¹

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An Introduction to Genome Annotation

Campbell

Yandell

2015

CP in Bioinformatics

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Genome projects have evolved from large international undertakings to tractable endeavors for a single lab. Accurate genome annotation is critical for successful genomic, genetic, and molecular biology experiments. These annotations can be generated using a number of approaches and available software tools. This unit describes methods for genome annotation and a number of software tools commonly used in gene annotation. © 2015 by John Wiley & Sons, Inc.

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Differential expression of a fructose receptor gene in honey bee workers according to age and behavioral role

Takada

Sasaki

Satō

et al. 2017

Arch Insect Biochem Physiol

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Honey bee (Apis mellifera) workers contribute to the maintenance of colonies in various ways. The primary functions of workers are divided into two types depending on age: young workers (nurses) primarily engage in such behaviors as cleaning and food handling within the hive, whereas older workers (foragers) acquire floral nutrients beyond the colony. Concomitant with this age-dependent change in activity, physiological changes occur in the tissues and organs of workers. Nurses supply younger larvae with honey containing high levels of glucose and supply older larvae with honey containing high levels of fructose. Given that nurses must determine both the concentration and type of sugar used in honey, gustatory receptors (Gr) expressed in the chemosensory organs likely play a role in distinguishing between sugars. Glucose is recognized by Gr1 in honey bees (AmGr1); however, it remains unclear which Gr are responsible for fructose recognition. This study aimed to identify fructose receptors in honey bees and reported that AmGr3, when transiently expressed in Xenopus oocytes, responded only to fructose, and to no other sugars. We analyzed expression levels of AmGr3 to identify which tissues and organs of workers are involved in fructose recognition and determined that expression of AmGr3 was particularly high in the antennae and legs of nurses. Our results suggest that nurses use their antennae and legs to recognize fructose, and that AmGr3 functions as an accurate nutrient sensor used to maintain food quality in honey bee hives.

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Finding the missing honey bee genes: lessons learned from a genome upgrade

Cited by 394 publications

References 105 publications

DNA methylation and the regulation of stimulus-specific memory formation

DNA methylation and the regulation of stimulus-specific memory formation

An Introduction to Genome Annotation

Differential expression of a fructose receptor gene in honey bee workers according to age and behavioral role

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