Nitric oxide sensing in plants is mediated by proteolytic control of Group VII ERF transcription factors

[EN] Nitric oxide (NO) is an important signaling compound in prokaryotes and eukaryotes. In plants, NO regulates critical developmental transitions and stress responses. Here, we identify a mechanism for NO sensing that coordinates responses throughout development based on targeted degradation of plant-specific transcriptional regulators, the group VII ethylene response factors (ERFs). We show that the N-end rule pathway of targeted proteolysis targets these proteins for destruction in the presence of NO, and we establish them as critical regulators of diverse NO-regulated processes, including seed germination, stomatal closure, and hypocotyl elongation. Furthermore, we define the molecular mechanism for NO control of germination and crosstalk with abscisic acid (ABA) signaling through ERF-regulated expression of ABSCISIC ACID INSENSITIVE5 (ABI5). Our work demonstrates how NO sensing is integrated across multiple physiological processes by direct modulation of transcription factor stability and identifies group VII ERFs as central hubs for the perception of gaseous signals in plants.M.J.H., S.P.P., D.J.G., G.M.M., J.V.C., and C.S.C. were supported by UK Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/G02488X/1, BB/G010595/1, BB/F006934/1, and BB/K000144/1 (including financial support from SAB Miller plc); J.E.G. was supported by BB/K000063/1; N.M.I. by a MARA PhD fellowship from the Malaysian government; S.B. by a University of Nottingham PhD fellowship; and M.M. by a University of Sheffield Faculty of Science Studentship. D.J.G. was supported by a Nottingham Advanced Research Fellowship for part of this work. J.L.-J., A.C., and J.L. were supported by grants CSD2007-00057 and BIO2011-27526 from the Spanish government. G.W.B. was supported by a Marie Curie IIF Fellowship. The work of A.B. was supported by the Austrian Science foundation FWF (grants P21215 and P25488). Rothamsted Research receives grant-aided support from the BBSRC. D.F.A.T. and J.B. were funded by BBSRC grant BB/G015066/1. N.M.-d.I.R. and D.A. were supported by grants from the Spanish Ministry of Science and Innovation (BIO2010-15071). We thank Susan Liddell (Sutton Bonington Proteomics Facility) and Pauline Roubira for technical assistance.Gibbs, DJ.; Isa, NMD.; Movahedi, M.; Lozano Juste, J.; Mendiondo, GM.; Berckhan, S.; Marín-De La Rosa, NA.... (2014). Nitric oxide sensing in plants is mediated by proteolytic control of Group VII ERF transcription factors. Molecular Cell. 53(3):369-379. https://doi.org/10.1016/j.molcel.2013.12.020S36937953