Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells

Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Molecular Genetics, Ghent University, 9052 Ghent, Belgium

Contributed by Marc Van Montagu, December 3, 2007 (received for review September 27, 2007)

Abstract

Jasmonates (JAs) are plant-specific signaling molecules that steer a diverse set of physiological and developmental processes. Pathogen attack and wounding inflicted by herbivores induce the biosynthesis of these hormones, triggering defense responses both locally and systemically. We report on alterations in the transcriptome of a fast-dividing cell culture of the model plant Arabidopsis thaliana after exogenous application of methyl JA (MeJA). Early MeJA response genes encoded the JA biosynthesis pathway proteins and key regulators of MeJA responses, including most JA ZIM domain proteins and MYC2, together with transcriptional regulators with potential, but yet unknown, functions in MeJA signaling. In a second transcriptional wave, MeJA reprogrammed cellular metabolism and cell cycle progression. Up-regulation of the monolignol biosynthesis gene set resulted in an increased production of monolignols and oligolignols, the building blocks of lignin. Simultaneously, MeJA repressed activation of M-phase genes, arresting the cell cycle in G₂. MeJA-responsive transcription factors were screened for their involvement in early signaling events, in particular the regulation of JA biosynthesis. Parallel screens based on yeast one-hybrid and transient transactivation assays identified both positive (MYC2 and the AP2/ERF factor ORA47) and negative (the C2H2 Zn finger proteins STZ/ZAT10 and AZF2) regulators, revealing a complex control of the JA autoregulatory loop and possibly other MeJA-mediated downstream processes.

Footnotes

*To whom correspondence may be addressed. E-mail: mamon{at}psb.ugent.be or alain.goossens{at}psb.ugent.be
Author contributions: M.V.M., W.B., D.I., and A.G. designed research; L.P., K.M., E.D.W., and F.L. performed research; L.P., W.B., and A.G. analyzed data; and L.P., W.B., D.I., and A.G. wrote the paper.
The authors declare no conflict of interest.
Data deposition: The microarray data have been submitted to the ArrayExpress database, www.ebi.ac.uk/arrayexpress (accession no. E-ATMX-13).
This article contains supporting information online at www.pnas.org/cgi/content/full/0711203105/DC1.