ABSTRACT
Triterpene saponins (TS) are a structurally diverse group of metabolites that are widely distributed in plants. They primarily serve as defense compounds and their production is often triggered by biotic stresses through signaling cascades that are modulated by phytohormones such as the jasmonates (JA). Two JA-modulated basic helix-loop-helix (bHLH) transcription factors (TFs), TRITERPENE SAPONIN BIOSYNTHESIS ACTIVATING REGULATOR 1 (TSAR1) and TSAR2, have been previously identified as direct activators of TS biosynthesis in the model legume Medicago truncatula. Here, we report on the involvement of the core endoplasmic reticulum (ER) stress basic leucine zipper (bZIP) TFs bZIP17 and bZIP60 in the regulation of TS biosynthesis. Expression and processing of M. truncatula bZIP17 and bZIP60 proteins was altered in roots with perturbed TS biosynthesis or treated with JA. Accordingly, such roots displayed an altered ER network structure. M. truncatula bZIP17 and bZIP60 proteins were shown to be capable of interfering with the TSAR-mediated transactivation of TS biosynthesis genes, particularly under ER stress conditions, when they translocate from the ER to the nucleus. Furthermore, the inhibitory role of ER stress bZIP TFs in the regulation of JA-dependent terpene biosynthetic pathways appears to be widespread in the plant kingdom, as we demonstrate that it also occurs in the regulation of monoterpene indole alkaloid biosynthesis in the medicinal plant Catharanthus roseus. We postulate that activation of ER stress bZIP TFs provides the plant with a mechanism to balance metabolic activities and thereby adequately govern modulation of growth, development and defense processes in defined stress situations.
One sentence summary ER stress bZIP transcription factors can interfere with the activity of jasmonate-inducible bHLH transcription factors to modulate the elicitation of plant specialized metabolism in stress conditions.
Footnotes
1 This work was supported by the Research Foundation Flanders by research project grants to A.G. (G004515N and G005915N), the Program Ciências Sem Fronteiras for a predoctoral fellowship to B.R. (Grant 201135/2014-0), the Special Research Fund from Ghent University (project O1J14813), the Swiss National Science Foundation for a postdoctoral fellowship to M.C. (P300PA_177831) and the BEC.AR program for overseas training of Argentine professionals in the fields of science, technology and productive innovation for a scholarship to M.P.
↵5 Author for contact: alain.goossens{at}psb.vib-ugent.be.
↵6 Senior author.
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: Alain Goossens (alain.goossens{at}psb.vib-ugent.be). [OPEN] Articles can be viewed without a subscription.
A.G. conceived the project, original screening and research plans; S.L. and A.G. supervised the experiments; B.R., M.E., M. C., C. W., E.L., R.D.C., R.V.B., D.M. and M.P. performed the experiments; B.R., M.E., M. C., C. W., E.L., R.D.C., R.V.B., S.L. and A.G. designed the experiments and analyzed the data; B.R., M.E., and A.G. wrote the article with contributions of all the authors; A.G. agrees to serve as the author responsible for contact and ensures communication.
All scientists who have contributed substantially to the conception, design or execution of the work described in the manuscript are included as authors, in accordance with the guidelines from the Committee on Publication Ethics (COPE) (http://publicationethics.org/resources/guidelines). All authors agree to the list of authors and the identified contributions.