Abstract
APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) gene clusters regulate the biosynthesis of diverse specialized metabolites, including steroidal glycoalkaloids in tomato (Solanum lycopersicum) and potato (Solanum tuberosum), nicotine in tobacco (Nicotiana tabacum), and pharmaceutically valuable terpenoid indole alkaloids in Madagascar periwinkle (Catharanthus roseus). However, the regulatory relationships between individual AP2/ERF genes within the cluster remain unexplored. We uncovered intracluster regulation of the C. roseus AP2/ERF regulatory circuit, which consists of ORCA3, ORCA4, and ORCA5. ORCA3 and ORCA5 activate ORCA4 by directly binding to a GC-rich motif in the ORCA4 promoter. ORCA5 regulates its own expression through a positive autoregulatory loop and indirectly activates ORCA3. In determining the functional conservation of AP2/ERF clusters in other plant species, we found that GC-rich motifs are present in the promoters of analogous AP2/ERF clusters in tobacco, tomato, and potato. Intracluster regulation is evident within the tobacco NICOTINE2 (NIC2) ERF cluster. Moreover, overexpression of ORCA5 in tobacco and of NIC2 ERF189 in C. roseus hairy roots activates nicotine and terpenoid indole alkaloid pathway genes, respectively, suggesting that the AP2/ERFs are functionally equivalent and are likely to be interchangeable. Elucidation of the intracluster and mutual regulation of transcription factor gene clusters advances our understanding of the underlying molecular mechanism governing regulatory gene clusters in plants.
| Original language | English |
|---|---|
| Pages (from-to) | 840-856 |
| Number of pages | 17 |
| Journal | Plant Physiology |
| Volume | 182 |
| Issue number | 2 |
| DOIs | |
| State | Published - Feb 2020 |
Bibliographical note
Funding Information:1This work was supported by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation under co-operative agreement 1355438 to L.Y. 2These authors contributed equally to the article. 3Senior authors. 4Author for contact: lyuan3@uky.edu. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ling Yuan (lyuan3@uky.edu). L.Y. and S.P. designed the research; P.P., S.K.S., B.P., X.L., and S.P. performed experiments; P.P., S.K.S., and S.P. analyzed data; P.P., S.K.S., S.P., and L.Y. wrote the article. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.19.00772
Funding Information:
1This work was supported by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation under cooperative agreement 1355438 to L.Y. We thank John May (Department of Civil Engineering and Environmental Research Training Laboratories, University of Kentucky) for assistance on liquid chromatography-tandem mass spectrometry and Huihua Ji (Kentucky Tobacco Research and Development Center, University of Kentucky) for assistance on nicotine measurement.
Publisher Copyright:
© 2020 American Society of Plant Biologists. All Rights Reserved.
ASJC Scopus subject areas
- Physiology
- Genetics
- Plant Science