Abstract
Arabidopsis REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1) represses ethylene hormone responses by promoting ethylene receptor ETHYLENE RESPONSE1 (ETR1) signaling, which negatively regulates ethylene responses. To investigate the regulation of RTE1, we performed a genetic screening for mutations that suppress ethylene insensitivity conferred by RTE1 overexpression in Arabidopsis. We isolated HYPER RECOMBINATION1 (HPR1), which is required for RTE1 overexpressor (RTE1ox) ethylene insensitivity at the seedling but not adult stage. HPR1 is a component of the THO complex, which, with other proteins, forms the TRanscription EXport (TREX) complex. In yeast, Drosophila, and humans, the THO/TREX complex is involved in transcription elongation and nucleocytoplasmic RNA export, but its role in plants is to be fully determined. We investigated how HPR1 is involved in RTE1ox ethylene insensitivity in Arabidopsis. The hpr1-5 mutation may affect nucleocytoplasmic mRNA export, as revealed by in vivo hybridization of fluorescein-labeled oligo(dT)45 with unidentified mRNA in the nucleus. The hpr1-5 mutation reduced the total and nuclear RTE1 transcript levels to a similar extent, and RTE1 transcript reduction rate was not affected by hpr1-5 with cordycepin treatment, which prematurely terminates transcription. The defect in the THO-interacting TEX1 protein of TREX but not the mRNA export factor SAC3B also reduced the total and nuclear RTE1 levels. SERINE-ARGININE-RICH (SR) proteins are involved mRNA splicing, and we found that SR protein SR33 co-localized with HPR1 in nuclear speckles, which agreed with the association of human TREX with the splicing machinery. We reveal a role for HPR1 in RTE1 expression during transcription elongation and less likely during export. Gene expression involved in ethylene signaling suppression was not reduced by the hpr1-5 mutation, which indicates selectivity of HPR1 for RTE1 expression affecting the consequent ethylene response. Thus, components of the THO/TREX complex appear to have specific roles in the transcription or export of selected genes.
Highlights
In Arabidopsis, the gaseous plant hormone ethylene is perceived by a family of five ethylene receptor members that structurally resemble prokaryotic “two-component” histidine kinases (HKs)
We reveal a role for HYPER RECOMBINATION1 (HPR1) [the yeast HYPER RECOMBINATION1 (Hpr1) homolog] in REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1) transcription elongation but not activation or export, which agrees with the role of yeast Hpr1 in transcription elongation
The yeast Sub2 protein is an RNA helicase involved in unwinding the inhibitory structure in the nascent RNA, and SUB2 overexpression suppresses yeast Δhpr1 defects; HPR1 could be involved in expression of selected genes with higher-order structure, where RNA polymerase movement could pause
Summary
In Arabidopsis, the gaseous plant hormone ethylene is perceived by a family of five ethylene receptor members that structurally resemble prokaryotic “two-component” histidine kinases (HKs). Ethylene receptor signaling is not associated with HK activity, and the biochemical nature of the receptor signal remains to be determined [1]. Without biochemical knowledge of the ethylene receptor signal output, ethylene receptor signaling is largely evaluated by ethylene-induced growth inhibition or altered gene expression. The five members of the ethylene receptor family have common and divergent functions and act cooperatively as complexes [4,5,6,7]. The ethylene receptor ETR1 can function largely independently of other family members to suppress the ethylene response to a great extent. ETHYLENE RESPONSE SENSOR1 (ERS1) functions differentially depending on other family members [6, 7]
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