Lindsey L Bechen1,2, Matthew G Johnson3,4, Geoffrey T Broadhead5,6, Rachel A Levin7, Rick P Overson3,8, Tania Jogesh3, Jeremie B Fant3,9, Robert A Raguso5, Krissa A Skogen3,9, Norman J Wickett10,11. 1. Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL, 60022, USA. lindseybechen@gmail.com. 2. Department of Biology, Amherst College, 25 East Drive, Amherst, MA, 01002, USA. lindseybechen@gmail.com. 3. Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL, 60022, USA. 4. Texas Tech University, Box 43131, Lubbock, TX, 79409, USA. 5. Cornell University, 215 Tower Rd, Ithaca, NY, 14853, USA. 6. University of Florida, 1881 Natural Area Drive, Gainesville, FL, 32608, USA. 7. Department of Biology, Amherst College, 25 East Drive, Amherst, MA, 01002, USA. 8. Arizona State University, PO Box 875502, Tempe, AZ, 85287, USA. 9. Northwestern University, 2205 Tech Drive, Evanston, IL, 60208, USA. 10. Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL, 60022, USA. nwickett@chicagobotanic.org. 11. Northwestern University, 2205 Tech Drive, Evanston, IL, 60208, USA. nwickett@chicagobotanic.org.
Abstract
BACKGROUND: Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(-)-linalool; some plants emit (R)-(-)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(-)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants. RESULTS: Three clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(-)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(-)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants. CONCLUSIONS: By using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(-)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.
BACKGROUND: Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(-)-linalool; some plants emit (R)-(-)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(-)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants. RESULTS: Three clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(-)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(-)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants. CONCLUSIONS: By using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(-)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.
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