Mitochondrial retrograde signaling through UCP1-mediated inhibition of the plant oxygen-sensing pathway

Autor: Pedro Barreto, Charlene Dambire, Gunjan Sharma, Jorge Vicente, Rory Osborne, Juliana Yassitepe, Daniel J. Gibbs, Ivan G. Maia, Michael J. Holdsworth, Paulo Arruda
Přispěvatelé: Universidade Estadual Paulista (UNESP), Loughborough, University of Birmingham, Universidade Estadual de Campinas (UNICAMP)
Jazyk: angličtina
Rok vydání: 2022
Předmět:
Zdroj: Scopus
Repositório Institucional da UNESP
Universidade Estadual Paulista (UNESP)
instacron:UNESP
Popis: Made available in DSpace on 2022-04-29T08:39:52Z (GMT). No. of bitstreams: 0 Previous issue date: 2022-01-01 Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) European Research Council Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) Biotechnology and Biological Sciences Research Council Mitochondrial retrograde signaling is an important component of intracellular stress signaling in eukaryotes. UNCOUPLING PROTEIN (UCP)1 is an abundant plant inner-mitochondrial membrane protein with multiple functions including uncoupled respiration and amino-acid transport1,2 that influences broad abiotic stress responses. Although the mechanism(s) through which this retrograde function acts is unknown, overexpression of UCP1 activates expression of hypoxia (low oxygen)-associated nuclear genes.3,4 Here we show in Arabidopsis thaliana that UCP1 influences nuclear gene expression and physiological response by inhibiting the cytoplasmic PLANT CYSTEINE OXIDASE (PCO) branch of the PROTEOLYSIS (PRT)6 N-degron pathway, a major mechanism of oxygen and nitric oxide (NO) sensing.5 Overexpression of UCP1 (UCP1ox) resulted in the stabilization of an artificial PCO N-degron pathway substrate, and stability of this reporter protein was influenced by pharmacological interventions that control UCP1 activity. Hypoxia and salt-tolerant phenotypes observed in UCP1ox lines resembled those observed for the PRT6 N-recognin E3 ligase mutant prt6-1. Genetic analysis showed that UCP1 regulation of hypoxia responses required the activity of PCO N-degron pathway ETHYLENE RESPONSE FACTOR (ERF)VII substrates. Transcript expression analysis indicated that UCP1 regulation of hypoxia-related gene expression is a normal component of seedling development. Our results show that mitochondrial retrograde signaling represses the PCO N-degron pathway, enhancing substrate function, thus facilitating downstream stress responses. This work reveals a novel mechanism through which mitochondrial retrograde signaling influences nuclear response to hypoxia by inhibition of an ancient cytoplasmic pathway of eukaryotic oxygen sensing. Departamento de Ciências Químicas e Biológicas Instituto de Biociências de Botucatu UNESP, SP School of Biosciences University of Nottingham Loughborough School of Biosciences University of Birmingham Genomics for Climate Change Research Center Universidade Estadual de Campinas, SP Departamento de Genética e Evolução Instituto de Biologia Universidade Estadual de Campinas (UNICAMP), SP Centro de Biologia Molecular e Engenharia Genetica Universidade Estadual de Campinas, SP Departamento de Ciências Químicas e Biológicas Instituto de Biociências de Botucatu UNESP, SP FAPESP: 2014/17634-5 FAPESP: 2015/24881-1 FAPESP: 2016/23218-0 FAPESP: 2017/22745-9 European Research Council: 715441-GasPlaNt CAPES: 88887.572598/2020-00 Biotechnology and Biological Sciences Research Council: BB/R002428/1 Biotechnology and Biological Sciences Research Council: BB/S005293/1
Databáze: OpenAIRE