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Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae)

Lindsey L. Bechen, View ORCID ProfileMatthew G. Johnson, View ORCID ProfileGeoffrey T. Broadhead, Rachel A. Levin, View ORCID ProfileRick P. Overson, View ORCID ProfileTania Jogesh, View ORCID ProfileJeremie B. Fant, View ORCID ProfileRobert A. Raguso, View ORCID ProfileKrissa A. Skogen, View ORCID ProfileNorman J. Wickett
doi: https://doi.org/10.1101/2021.01.12.426409
Lindsey L. Bechen
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
2Amherst College, 25 Merrill Science Drive, Amherst, MA 01002, USA
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  • For correspondence: lindseybechen@gmail.com nwickett@chicagobotanic.org
Matthew G. Johnson
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
3Texas Tech University, Box 43131, Lubbock, TX 79409, USA
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  • ORCID record for Matthew G. Johnson
Geoffrey T. Broadhead
4Cornell University, 215 Tower Rd, Ithaca, NY 14853, USA
5University of Florida, 1881 Natural Area Drive, Gainesville, FL 32608, USA
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Rachel A. Levin
2Amherst College, 25 Merrill Science Drive, Amherst, MA 01002, USA
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Rick P. Overson
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
6Arizona State University, PO Box 875502, Tempe, AZ 85287, USA
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Tania Jogesh
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
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  • ORCID record for Tania Jogesh
Jeremie B. Fant
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
7Northwestern University, 2205 Tech Drive, Evanston, IL 60208, USA
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Robert A. Raguso
4Cornell University, 215 Tower Rd, Ithaca, NY 14853, USA
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  • ORCID record for Robert A. Raguso
Krissa A. Skogen
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
7Northwestern University, 2205 Tech Drive, Evanston, IL 60208, USA
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Norman J. Wickett
1Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Rd, Glencoe, IL 60022, USA
7Northwestern University, 2205 Tech Drive, Evanston, IL 60208, USA
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  • ORCID record for Norman J. Wickett
  • For correspondence: lindseybechen@gmail.com nwickett@chicagobotanic.org
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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 genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool-plants 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.

Competing Interest Statement

The authors have declared no competing interest.

  • List of Abbreviations

    DEG
    Differentially expressed genes
    FDR
    False discovery rate
    GC-MS
    Gas chromatography-mass spectrometry
    GO
    Gene ontology
    LIS
    Linalool synthase
    PC
    Principal component
    TPS
    Terpene synthase
    pHMM
    profile Hidden Markov Model
  • Copyright 
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    Posted January 13, 2021.
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    Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae)
    Lindsey L. Bechen, Matthew G. Johnson, Geoffrey T. Broadhead, Rachel A. Levin, Rick P. Overson, Tania Jogesh, Jeremie B. Fant, Robert A. Raguso, Krissa A. Skogen, Norman J. Wickett
    bioRxiv 2021.01.12.426409; doi: https://doi.org/10.1101/2021.01.12.426409
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    Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae)
    Lindsey L. Bechen, Matthew G. Johnson, Geoffrey T. Broadhead, Rachel A. Levin, Rick P. Overson, Tania Jogesh, Jeremie B. Fant, Robert A. Raguso, Krissa A. Skogen, Norman J. Wickett
    bioRxiv 2021.01.12.426409; doi: https://doi.org/10.1101/2021.01.12.426409

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