TY - JOUR
T1 - Complex Sexual Deception in an Orchid Is Achieved by Co-opting Two Independent Biosynthetic Pathways for Pollinator Attraction
AU - Xu, Haiyang
AU - Bohman, Björn
AU - Wong, Darren C.J.
AU - Rodriguez-Delgado, Claudia
AU - Scaffidi, Adrian
AU - Flematti, Gavin R.
AU - Phillips, Ryan D.
AU - Pichersky, Eran
AU - Peakall, Rod
N1 - Publisher Copyright:
© 2017 Elsevier Ltd
PY - 2017/7/10
Y1 - 2017/7/10
N2 - Sexually deceptive orchids lure their specific male pollinators using volatile semiochemicals that mimic female sex pheromones. To date, the semiochemicals known to be involved consist of blends of chemically and biosynthetically related compounds. In contrast, we report that (S)-β-citronellol and 2-hydroxy-6-methylacetophenone, two biosynthetically distinct compounds, are the active semiochemicals in Caladenia plicata, which is pollinated by male Zeleboria sp. thynnine wasps. They are also sex pheromone components of the female Zeleboria. A 1:4 blend elicits a high rate of attempted copulation (∼70%) in bioassays, equivalent to rates observed at orchid flowers. Whereas β-citronellol is well known, 2-hydroxy-6-methylacetophenone appears to be previously unknown as a floral volatile. Production of the two compounds is restricted to glandular sepal tips; thus, differential expression analysis of contrasting floral tissue transcriptomes was employed to illuminate the biosynthesis. As expected, production of (S)-β-citronellol commences with the terpene synthase GES1 catalyzing the irreversible conversion of geranyl diphosphate (GPP) to geraniol. Contrary to prediction, biosynthesis subsequently proceeds in three steps, commencing with the oxidation of geraniol to geranial by alcohol dehydrogenase ADH3, followed by the enantioselective reduction of a double bond in geranial by geranial reductase GER1 to give (S)-β-citronellal. Finally, ADH3-catalyzed reduction of (S)-β-citronellal results in (S)-β-citronellol. In line with previous work on insects showing that 2-hydroxy-6-methylacetophenone is derived from a polyketide pathway, we report a differentially expressed polyketide synthase (PKS) gene candidate. Thus, in this unique example of sexual deception, pollination is achieved by co-opting and regulating two independent biosynthetic pathways of floral volatile compounds.
AB - Sexually deceptive orchids lure their specific male pollinators using volatile semiochemicals that mimic female sex pheromones. To date, the semiochemicals known to be involved consist of blends of chemically and biosynthetically related compounds. In contrast, we report that (S)-β-citronellol and 2-hydroxy-6-methylacetophenone, two biosynthetically distinct compounds, are the active semiochemicals in Caladenia plicata, which is pollinated by male Zeleboria sp. thynnine wasps. They are also sex pheromone components of the female Zeleboria. A 1:4 blend elicits a high rate of attempted copulation (∼70%) in bioassays, equivalent to rates observed at orchid flowers. Whereas β-citronellol is well known, 2-hydroxy-6-methylacetophenone appears to be previously unknown as a floral volatile. Production of the two compounds is restricted to glandular sepal tips; thus, differential expression analysis of contrasting floral tissue transcriptomes was employed to illuminate the biosynthesis. As expected, production of (S)-β-citronellol commences with the terpene synthase GES1 catalyzing the irreversible conversion of geranyl diphosphate (GPP) to geraniol. Contrary to prediction, biosynthesis subsequently proceeds in three steps, commencing with the oxidation of geraniol to geranial by alcohol dehydrogenase ADH3, followed by the enantioselective reduction of a double bond in geranial by geranial reductase GER1 to give (S)-β-citronellal. Finally, ADH3-catalyzed reduction of (S)-β-citronellal results in (S)-β-citronellol. In line with previous work on insects showing that 2-hydroxy-6-methylacetophenone is derived from a polyketide pathway, we report a differentially expressed polyketide synthase (PKS) gene candidate. Thus, in this unique example of sexual deception, pollination is achieved by co-opting and regulating two independent biosynthetic pathways of floral volatile compounds.
KW - (S)-β-citronellol
KW - 2-hydroxy-6-methylacetophenone
KW - Caladenia
KW - double-bond reduction
KW - floral volatile
KW - pollination
KW - semiochemical
KW - sex pheromone
KW - sexual deception
KW - terpene biosynthesis
UR - http://www.scopus.com/inward/record.url?scp=85020803003&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2017.05.065
DO - 10.1016/j.cub.2017.05.065
M3 - Article
SN - 0960-9822
VL - 27
SP - 1867-1877.e5
JO - Current Biology
JF - Current Biology
IS - 13
ER -