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Msn2/4 transcription factors positively regulate expression of Atg39 ER-phagy receptor.

ABSTRACT: Selective autophagy requires the autophagy receptor specifically localizing to the target for degradation. In the budding yeast, Atg39 and Atg40 function as an autophagy receptor for the endoplasmic reticulum (ER)-selective autophagy, referred to as ER-phagy. The expression level of the ATG39 gene is increased in response to ER stress and nitrogen starvation. Under unstressed conditions, ATG39 transcription is repressed by Mig1/2 repressors. ER stress activates Snf1 AMP-activated protein kinase (AMPK), which negatively regulates Mig1/2 and consequently derepresses ATG39 transcription. However, ATG39 expression is still induced by ER stress and nitrogen starvation in the absence of Snf1, suggesting that additional molecules are involved in regulation of ATG39 expression. Here, we identify Msn2/4 transcription factors as an activator of ATG39 transcription. Not only ATG39 promoter activity but also ER-phagy are downregulated by loss of Msn2/4 and disruption of Msn2/4-binding consensus sequences located in the ATG39 promoter. We also find that the cAMP-dependent protein kinase pathway is involved in Msn2/4-mediated transcriptional regulation of ATG39. Our results suggest that yeast ER-phagy is appropriately controlled through modulation of the expression level of the ER-phagy receptor involving multiple signaling pathways and transcription factors.

SUBMITTER: Mizuno T

PROVIDER: S-EPMC8184937 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:KEY MESSAGE:Subgroup IVc basic helix-loop-helix transcription factors OsbHLH058 and OsbHLH059 positively regulate major iron deficiency responses in rice in a similar but distinct manner, putatively under partial control by OsHRZs. Under low iron availability, plants transcriptionally induce the expression of genes involved in iron uptake and translocation. OsHRZ1 and OsHRZ2 ubiquitin ligases negatively regulate this iron deficiency response in rice. The basic helix-loop-helix (bHLH) transcription factor OsbHLH060 interacts with OsHRZ1, and positively regulates iron deficiency-inducible genes. However, the functions of three other subgroup IVc bHLH transcription factors in rice, OsbHLH057, OsbHLH058, and OsbHLH059, have not yet been characterized. In the present study, we investigated the functions of OsbHLH058 and OsbHLH059 related to iron deficiency response. OsbHLH058 expression was repressed under iron deficiency, whereas the expression of OsbHLH057 and OsbHLH060 was moderately induced. Yeast two-hybrid analysis indicated that OsbHLH058 interacts with OsHRZ1 and OsHRZ2 more strongly than OsbHLH060, whereas OsbHLH059 showed no interaction. An in vitro ubiquitination assay detected no OsbHLH058 and OsbHLH060 ubiquitination by OsHRZ1 and OsHRZ2. Transgenic rice lines overexpressing OsbHLH058 showed tolerance for iron deficiency and higher iron concentration in seeds. These lines also showed enhanced expression of many iron deficiency-inducible genes involved in iron uptake and translocation under iron-sufficient conditions. Conversely, OsbHLH058 knockdown lines showed susceptibility to iron deficiency and reduced expression of many iron deficiency-inducible genes. OsbHLH059 knockdown lines were also susceptible to iron deficiency, and formed characteristic brownish regions in iron-deficient new leaves. OsbHLH059 knockdown lines also showed reduced expression of many iron deficiency-inducible genes. These results indicate that OsbHLH058 and OsbHLH059 positively regulate major iron deficiency responses in a similar but distinct manner, and that this function may be partially controlled by OsHRZs.

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Msn2/4 transcription factors positively regulate expression of Atg39 ER-phagy receptor.

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