Two fatty acyl reductases involved in moth pheromone biosynthesis

Abstract

Fatty acyl reductases (FARs) constitute an evolutionarily conserved gene family found in all kingdoms of life. Members of the FAR gene family play diverse roles, including seed oil synthesis, insect pheromone biosynthesis, and mammalian wax biosynthesis. In insects, FAR genes dedicated to sex pheromone biosynthesis (pheromone-gland-specific fatty acyl reductase, pgFAR) form a unique clade that exhibits substantial modifications in gene structure and possesses unique specificity and selectivity for fatty acyl substrates. Highly selective and semi-selective 'single pgFARs' produce single and multicomponent pheromone signals in bombycid, pyralid, yponomeutid and noctuid moths. An intriguing question is how a 'single reductase' can direct the synthesis of several fatty alcohols of various chain lengths and isomeric forms. Here, we report two active pgFARs in the pheromone gland of Spodoptera, namely a semi-selective, C14:acyl-specific pgFAR and a highly selective, C16:acyl-specific pgFAR, and demonstrate that these pgFARs play a pivotal role in the formation of species-specific signals, a finding that is strongly supported by functional gene expression data. The study envisages a new area of research for disclosing evolutionary changes associated with C 14 -and C 16 -specific FARs in moth pheromone biosynthesis.Insects use sophisticated chemical communication systems, including behavior-modifying pheromones, and these systems reinforce intra-and interspecific reproductive isolation and thus play pivotal roles in the evolutionary process. The insect order Lepidoptera (moth and butterflies) contains the second largest number of species (approximately 180,000 species described to date), and their richness and diversity are linked to pheromone-based communication and sophisticated chemosensory systems [1][2][3] . In moths, chemical communication is the major factor in the premating isolation mechanism, and sex pheromone differences inhibit successful mating and disfavor reproductive success 4 . The female signal and male response are highly species specific, but the mechanism regulating concomitant changes in signals and responses has not been established. These changes must occur at the gene level, and it is important to identify and characterize the genes responsible for pheromone production and to thus provide conclusive proof regarding pheromone-driven evolution in Lepidoptera 5,6 . The pheromone race is generally described in moths, and the variability in chemical mating signals and responses is genetically determined and under stabilizing selection [7][8][9] . Studies over the last two decades have pinpointed that the epigenetic effect of pheromone-driven adaptive evolution is one of the major factors driving the successful diversification of Lepidopteran insects 10 . In moths, a few substitutions in critical amino acids in the key pheromone biosynthetic enzymes are sufficient to create a novel pheromone component 11,12 . Few studies have reported the genetic basis of pheromone divergence in insects due to a lack ...

Characterization and functional assay of a fatty acyl‐CoA reductase gene in the scale insect, Ericerus pela Chavannes (Hemiptera: Coccoidae)

“…Later studies reported the roles of these enzymes in the production of sex pheromones. Subsequently, FAR s were reported in many other lepidopteran species (Antony, Ding, Moto, Aldosari, & Aldawood, ; Hagström, Liénard, Groot, Hedenström, & Löfstedt, ; Lassance et al., ; Lassance et al., ). Some pheromone‐gland‐specific FAR s ( pgFAR s) reduce a broad range of saturated or unsaturated fatty acids to corresponding fatty alcohols in sex‐pheromone biosynthesis.…”

“…Some pheromone‐gland‐specific FAR s ( pgFAR s) reduce a broad range of saturated or unsaturated fatty acids to corresponding fatty alcohols in sex‐pheromone biosynthesis. Some pgFAR s show a wide range of functional flexibility (Antony et al., ; Liénard & Löfstedt, ). The honey bee AmFAR1 and Drosophila waterproof are similarly flexible.…”

Biotechnological potential of insect fatty acid-modifying enzymes

“…The majority of the findings available to date suggest that the FARs in general exhibit diverse substrate specificities with respect to the fatty acyl chain length and unsaturation state of the substrate. The pool of fatty acyls available for reduction in the host organism can also influence the apparent FAR specificity [111][112][113].…”

“…In silk moth (Bombyx mori), researchers discovered a pheromone gland-specific FAR [118] that is able to convert E10,Z12-16:2 FA precursor to the corresponding alcohol bombykol, the main component of the female sex pheromone. Since then, a range of moth pheromone-biosynthetic FARs have been isolated and functionally characterized [89,111,[119][120][121][122][123] (Table 2). Although moth FARs usually exhibit a broad substrate preference [77,89,111,120,122,123], some of them display specificity to unsaturated substrates with a double bond in either the E or Z configuration [119], a particular chain length and double bond position [120], or a system of conjugated double bonds [118].…”

“…Since then, a range of moth pheromone-biosynthetic FARs have been isolated and functionally characterized [89,111,[119][120][121][122][123] (Table 2). Although moth FARs usually exhibit a broad substrate preference [77,89,111,120,122,123], some of them display specificity to unsaturated substrates with a double bond in either the E or Z configuration [119], a particular chain length and double bond position [120], or a system of conjugated double bonds [118]. Given the multiple FAR paralogs generally present in insect genomes [13,14,16,17,111,124] and limited knowledge of their properties, there is a demand to perform functional characterization of these biologically and biotechnologically relevant enzymes.…”