Author response: Expansion of the fatty acyl reductase gene family shaped pheromone communication in Hymenoptera

AbstractThe conserved fatty acyl reductase (FAR) family is involved in biosynthesis of fatty alcohols that serve a range of biological roles. In moths, butterflies (Lepidoptera), and bees (Hymenoptera), FARs biosynthesize fatty alcohol pheromones participating in mate-finding strategies. Using a combination of next-generation sequencing, analysis of transposable elements (TE) in the genomic environment of FAR genes, and functional characterization of FARs from Bombus lucorum, B. lapidarius, and B. terrestris, we uncovered a massive expansion of the FAR gene family in Hymenoptera, presumably facilitated by TEs. Expansion occurred in the common ancestor of bumblebees (Bombini) and stingless bees (Meliponini) after their divergence from the honeybee lineage. We found that FARs from the expanded FAR-A orthology group contributed to the species-specific male marking pheromone composition. Our results indicate that TE-mediated expansion and functional diversification of the FAR gene family played a key role in the evolution of pheromone communication in the crown group of Hymenoptera.AbbreviationsMMP: male marking pheromone, FA: fatty acid, FAME: fatty acid methyl ester, FAR: fatty acyl reductase, LG: labial gland, FB: fat body, TE: transposable element.

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Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1000823107 ◽

2010 ◽

Vol 107 (24) ◽

pp. 10955-10960 ◽

Cited By ~ 59

Author(s):

M. A. Lienard ◽

A. K. Hagstrom ◽

J.-M. Lassance ◽

C. Lofstedt

Keyword(s):

Fatty Acyl ◽

Reductase Gene ◽

Fatty Acyl Reductase ◽

Multicomponent Pheromone

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Tissue-specific expression of the pheromone gland-specific fatty acyl reductase gene inOstrinia scapulalis

Entomologia Experimentalis et Applicata ◽

10.1111/eea.12106 ◽

2013 ◽

Vol 149 (1) ◽

pp. 94-98 ◽

Cited By ~ 3

Author(s):

Binu Antony ◽

Yukio Ishikawa

Keyword(s):

Fatty Acyl ◽

Pheromone Gland ◽

Specific Expression ◽

Tissue Specific ◽

Tissue Specific Expression ◽

Reductase Gene ◽

Fatty Acyl Reductase

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Expansion of the fatty acyl reductase gene family shaped pheromone communication in Hymenoptera

eLife ◽

10.7554/elife.39231 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 8

Author(s):

Michal Tupec ◽

Aleš Buček ◽

Václav Janoušek ◽

Heiko Vogel ◽

Darina Prchalová ◽

...

Keyword(s):

Gene Family ◽

Functional Characterization ◽

Gene Tree ◽

Biological Significance ◽

Fatty Acyl ◽

Pheromone Biosynthesis ◽

Bumble Bee ◽

Pheromone Communication ◽

Genomic Environment ◽

Species Specific

Fatty acyl reductases (FARs) are involved in the biosynthesis of fatty alcohols that serve a range of biological roles. Insects typically harbor numerous FAR gene family members. While some FARs are involved in pheromone biosynthesis, the biological significance of the large number of FARs in insect genomes remains unclear.Using bumble bee (Bombini) FAR expression analysis and functional characterization, hymenopteran FAR gene tree reconstruction, and inspection of transposable elements (TEs) in the genomic environment of FARs, we uncovered a massive expansion of the FAR gene family in Hymenoptera, presumably facilitated by TEs. The expansion occurred in the common ancestor of bumble bees and stingless bees (Meliponini). We found that bumble bee FARs from the expanded FAR-A ortholog group contribute to the species-specific pheromone composition. Our results indicate that expansion and functional diversification of the FAR gene family played a key role in the evolution of pheromone communication in Hymenoptera.

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Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones

Nature ◽

10.1038/nature09058 ◽

2010 ◽

Vol 466 (7305) ◽

pp. 486-489 ◽

Cited By ~ 134

Author(s):

Jean-Marc Lassance ◽

Astrid T. Groot ◽

Marjorie A. Liénard ◽

Binu Antony ◽

Christin Borgwardt ◽

...

Keyword(s):

Sex Pheromones ◽

Allelic Variation ◽

Fatty Acyl ◽

Reductase Gene ◽

Fatty Acyl Reductase

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Evolution of the codling moth pheromone via an ancient gene duplication

BMC Biology ◽

10.1186/s12915-021-01001-8 ◽

2021 ◽

Vol 19 (1) ◽

Author(s):

Jean-Marc Lassance ◽

Bao-Jian Ding ◽

Christer Löfstedt

Keyword(s):

Gene Family ◽

Developmental Stages ◽

Cydia Pomonella ◽

Fatty Acid Desaturase ◽

Codling Moth ◽

Fatty Acyl ◽

Integrative Approach ◽

Heterologous Expression Systems ◽

Genetic Novelty ◽

Ancient Gene

AbstractBackgroundDefining the origin of genetic novelty is central to our understanding of the evolution of novel traits. Diversification among fatty acid desaturase (FAD) genes has played a fundamental role in the introduction of structural variation in fatty acyl derivatives. Because of its central role in generating diversity in insect semiochemicals, the FAD gene family has become a model to study how gene family expansions can contribute to the evolution of lineage-specific innovations. Here we used the codling moth (Cydia pomonella) as a study system to decipher the proximate mechanism underlying the production of the ∆8∆10 signature structure of olethreutine moths. Biosynthesis of the codling moth sex pheromone, (E8,E10)-dodecadienol (codlemone), involves two consecutive desaturation steps, the first of which is unusual in that it generates anE9 unsaturation. The second step is also atypical: it generates a conjugated diene system from theE9 monoene C12intermediate via 1,4-desaturation.ResultsHere we describe the characterization of the FAD gene acting in codlemone biosynthesis. We identify 27 FAD genes corresponding to the various functional classes identified in insects and Lepidoptera. These genes are distributed across theC. pomonellagenome in tandem arrays or isolated genes, indicating that the FAD repertoire consists of both ancient and recent duplications and expansions. Using transcriptomics, we show large divergence in expression domains: some genes appear ubiquitously expressed across tissue and developmental stages; others appear more restricted in their expression pattern. Functional assays using heterologous expression systems reveal that one gene, Cpo_CPRQ, which is prominently and exclusively expressed in the female pheromone gland, encodes an FAD that possesses bothE9 and ∆8∆10 desaturation activities. Phylogenetically, Cpo_CPRQ clusters within the Lepidoptera-specific ∆10/∆11 clade of FADs, a classic reservoir of unusual desaturase activities in moths.ConclusionsOur integrative approach shows that the evolution of the signature pheromone structure of olethreutine moths relied on a gene belonging to an ancient gene expansion. Members of other expanded FAD subfamilies do not appear to play a role in chemical communication. This advises for caution when postulating the consequences of lineage-specific expansions based on genomics alone.

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