title: The Rice E3-Ubiquitin Ligase HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 Modulates the Expression of ROOT MEANDER CURLING, a Gene Involved in Root Mechanosensing, through the Interaction with Two ETHYLENE-RESPONSE FACTOR Transcription Factors.
abstract: Plant roots can sense and respond to a wide diversity of mechanical stimuli, including touch and gravity. However, little is known about the signal transduction pathways involved in mechanical stimuli responses in rice (Oryza sativa). This work shows that rice root responses to mechanical stimuli involve the E3-ubiquitin ligase rice HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 (OsHOS1), which mediates protein degradation through the proteasome complex. The morphological analysis of the roots in transgenic RNA interference::OsHOS1 and wild-type plants, exposed to a mechanical barrier, revealed that the OsHOS1 silencing plants keep a straight root in contrast to wild-type plants that exhibit root curling. Moreover, it was observed that the absence of root curling in response to touch can be reverted by jasmonic acid. The straight root phenotype of the RNA interference::OsHOS1 plants was correlated with a higher expression rice ROOT MEANDER CURLING (OsRMC), which encodes a receptor-like kinase characterized as a negative regulator of rice root curling mediated by jasmonic acid. Using the yeast two-hybrid system and bimolecular fluorescence complementation assays, we showed that OsHOS1 interacts with two ETHYLENE-RESPONSE FACTOR transcription factors, rice ETHYLENE-RESPONSIVE ELEMENT BINDING PROTEIN1 (OsEREBP1) and rice OsEREBP2, known to regulate OsRMC gene expression. In addition, we showed that OsHOS1 affects the stability of both transcription factors in a proteasome-dependent way, suggesting that this E3-ubiquitin ligase targets OsEREBP1 and OsEREBP2 for degradation. Our results highlight the function of the proteasome in rice response to mechanical stimuli and in the integration of these signals, through hormonal regulation, into plant growth and developmental programs.
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.).
authors.forename: Tiago F
authors.identifier: http://orcid.org/0000-0001-5085-861X
authors.initials: TF
authors.lastname: Lourenço
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.).
authors.forename: Tânia S
authors.identifier: http://orcid.org/0000-0002-4900-2897
authors.initials: TS
authors.lastname: Serra
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.).
authors.forename: André M
authors.initials: AM
authors.lastname: Cordeiro
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.).
authors.forename: Sarah J
authors.initials: SJ
authors.lastname: Swanson
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.).
authors.forename: Simon
authors.initials: S
authors.lastname: Gilroy
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.) saibo@itqb.unl.pt mmolive@itqb.unl.pt.
authors.forename: Nelson J M
authors.identifier: http://orcid.org/0000-0002-6679-3811
authors.initials: NJ
authors.lastname: Saibo
authors.affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); and Genomics of Plant Stress Unit, iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, 2780-901 Oeiras, Portugal (T.F.L., T.S.S., A.M.C., N.J.M.S., M.M.O.); andDepartment of Botany, University of Wisconsin, Madison, Wisconsin 53706 (S.J.S., S.G.) saibo@itqb.unl.pt mmolive@itqb.unl.pt.
authors.forename: M Margarida
authors.identifier: http://orcid.org/0000-0002-0095-1952
authors.initials: MM
authors.lastname: Oliveira
mesh_terms: D003517:Cyclopentanes / Q000378:metabolism; D005030:Ethylenes / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D040542:Mechanotransduction, Cellular; D012275:Oryza / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D009995:Osmosis; D054883:Oxylipins / Q000378:metabolism; D010937:Plant Growth Regulators / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000201:enzymology / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D046988:Proteasome Endopeptidase Complex / Q000378:metabolism*; D034622:RNA Interference; D020798:Two-Hybrid System Techniques; D044767:Ubiquitin-Protein Ligases / Q000235:genetics / Q000378:metabolism*; D014452:Ubiquitins / Q000378:metabolism
chemical_list: D003517:Cyclopentanes; D005030:Ethylenes; D054883:Oxylipins; D010937:Plant Growth Regulators; D010940:Plant Proteins; D014452:Ubiquitins; C011006:jasmonic acid; C036216:ethylene; D044767:Ubiquitin-Protein Ligases; D046988:Proteasome Endopeptidase Complex