Neofunctionalization in an ancestral insect desaturase lineage led to rare Δ6 pheromone signals in the Chinese tussah silkworm.
The Chinese tussah silkworm, Antheraea pernyi (Lepidoptera: Saturniidae) produces a rare dienoic sex pheromone composed of (E,Z)-6,11-hexadecadienal, (E,Z)-6,11-hexadecadienyl acetate and (E,Z)-4,9-tetradecadienyl acetate, and for which the biosynthetic routes are yet unresolved. By means of gland composition analyses and in vivo labeling we evidenced that pheromone biosynthesis towards the immediate dienoic gland precursor, the (E,Z)-6,11-hexadecadienoic acid, involves desaturation steps with Δ(6) and Δ(11) regioselectivity. cDNA cloning of pheromone gland desaturases and heterologous expression in yeast demonstrated that the 6,11-dienoic pheromone is generated from two biosynthetic routes implicating a Δ(6) and Δ(11) desaturase duo albeit with an inverted reaction order. The two desaturases first catalyze the formation of the (E)-6-hexadecenoic acid or (Z)-11-hexadecenoic acid, key mono-unsaturated biosynthetic intermediates. Subsequently, each enzyme is able to produce the (E,Z)-6,11-hexadecadienoic acid by accommodating its non-respective mono-unsaturated product. Besides elucidating an unusually flexible pheromone biosynthetic pathway, our data provide the first identification of a biosynthetic Δ(6) desaturase involved in insect mate communication. The occurrence of this novel Δ(6) desaturase function is consistent with an evolutionary scenario involving neo-functionalization of an ancestral desaturase belonging to a gene lineage different from the Δ(11) desaturases commonly involved in moth pheromone biosynthesis.
Wang
Hong-Lei
HL
Chemical Ecology and Ecotoxicology, Department of Biology, Lund University, SE-223 62 Lund, Sweden.
Liénard
Marjorie A
MA
Zhao
Cheng-Hua
CH
Wang
Chen-Zhu
CZ
Löfstedt
Christer
C
D000818:Animals; D012831:Bombyx / Q000737:chemistry / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D044943:Fatty Acid Desaturases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D019476:Insect Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D007313:Insecta / Q000737:chemistry / Q000145:classification / Q000201:enzymology* / Q000235:genetics; D008969:Molecular Sequence Data; D010675:Pheromones / Q000096:biosynthesis* / Q000737:chemistry; D010802:Phylogeny; D013379:Substrate Specificity
D019476:Insect Proteins; D010675:Pheromones; D044943:Fatty Acid Desaturases