Ubiquitin-Proteasome Dependent Regulation of the GOLDEN2-LIKE 1 Transcription Factor in Response to Plastid Signals

Tokumaru, Mitsuaki; Adachi, Fumi; Toda, Makoto; Ito‐Inaba, Yasuko; Yazu, Fumiko; Hirosawa, Yoshihiro; Sakakibara, Yoichi; Suiko, Masahito; Kakizaki, Tomohiro; Inaba, Tomoki

doi:10.1104/pp.16.01546

Cited by 82 publications

(89 citation statements)

References 37 publications

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“…In turn GLKs, under GUN1-mediated retrograde signalling (Tokumaru, Adachi et al, 2017) (Porra, Thompson et al, 1989). PAP8 and ∆cTP or XhoI-to-PmlI fragments for ∆NLS and ∆cTP/∆NLS after PCR fragment cloning using oPAP8ΔNLS_PmlI.…”

Section: Introductionmentioning

confidence: 99%

Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

Liebers

Gillet

Israel

et al. 2020

Preprint

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The initial greening of angiosperm occurs upon light-activation of photoreceptors that trigger photomorphogenesis followed with the development of chloroplasts. In these semiautonomous organelles, the construction of the photosynthetic apparatus depends on the coordination of nuclear and plastid gene expression. Here we show that PAP8, as an essential subunit of the plastid-encoded RNA polymerase, is under the control of a regulatory element recognized by the photomorphogenic factor HY5. PAP8 is localized and active in both plastids and the nucleus and particularly essential for the formation of late photobodies.In the albino pap8 mutant, phytochrome-mediated signalling is altered, PIFs are maintained, HY5 is not stabilized, and GLK1 expression is impaired. PAP8 translocates into plastids losing its pre-sequence, interacts with the PEP, and using an unknown route or a retrograde transport, reaches the nucleus where it has the ability to interact with pTAC12/HMR/PAP5.

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Section: Introductionmentioning

confidence: 99%

Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

Liebers

Gillet

Israel

et al. 2020

Preprint

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“…It is not known why GLK1 is so highly upregulated in this mutant. It is well established, however, that GLK1 gene transcription and protein accumulation is regulated by plastid retrograde signals (Martin et al, 2016; Tokumaru et al, 2017) and it is possible to consider that endogenous CK levels may have an effect on this signalling. Nevertheless, this result further underscores the requirement of RGO in CK response.…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis geneRGOmediates cytokinin responses and increases seed yield

Murmu

Allard

Chabot

et al. 2020

Preprint

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17One-sentence summary: RGO, a novel gene from Arabidopsis, is essential for plant development, 18 mediates CK signaling and increases seed yield in Arabidopsis and rapeseed when overexpressed. Abstract 1 A novel gene, At1g77960, from Arabidopsis thaliana was characterized. At1g77960 transcripts 2 accumulate to very high levels in plants ectopically overexpressing the Golden2-like1 (GLK1) 3 transcription factor and is designated as a Response to GLK1 Overexpression (RGO) gene. RGO 4 encodes a protein with domains of tandem QH and QN repeats. Transcripts and promoter GUS 5 reporter analyses indicated that RGO is expressed in roots, leaves, stems, floral and siliques tissues 6 but not in seeds. Expression of the RGO:YFP fusion protein demonstrated that RGO is localized 7 to the endoplasmic reticulum. MicroRNA mediated silencing of RGO resulted in severe reductions 8 in vegetative and root growth, delayed flowering and reduced seed yield and viability, suggesting 9 that RGO is essential for plant development. Conversely, ectopic overexpression of RGO resulted 10 in enhanced vegetative growth including increased axillary bud formation and a 20% higher seed 11 yield. Stable overexpression of RGO in Brassica napus also produced a similar increase in seed 12 yield. Cytokinin (CK) response assays including root growth, green calli formation from excised 13 hypocotyls and chlorophyll retention during dark-induced senescence suggest that one role of RGO 14 is to mediate CK responses in plant development. These results suggest that RGO could be a target 15 gene for increasing crop seed yields. 16 Keywords 17 Arabidopsis thaliana, At1g77960, GLK1 overexpression, cytokinin response, seed yield 18 19 [Type text] [Type text] 4 1A direct link between GLKs and CK signalling however, is lacking. There is evidence to suggest 2 that type B ARRs coordinate the expression of HY5 (elongated hypocotyl 5), which is required by 3 GLK2 for maximal (although not essential) greening in roots (Kobayashi et al., 2012).

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“…In this mechanism, SP1, a RING-type ubiquitin ligase located in the outer chloroplast membrane directly regulates the content of the TOC complex. In addition, ubiquitin-proteasome-dependent post-translational regulation has been also shown to modulate levels of the transcription factor GOLDEN2-LIKE 1 (GLK1), which is known to positively regulate the expression of photosynthesis-related genes during chloroplast biogenesis (Tokumaru et al, 2017). Thus our results, together with previous reports, indicate that ubiquitination and the 26S proteasome are integral parts of retrograde signaling pathways, together with the reprogramming of nuclear transcription, and all are engaged in the maintenance of functional chloroplasts within plant cells.…”

Section: Discussionmentioning

confidence: 99%

GUN1 influences the accumulation of NEP-dependent transcripts and chloroplast protein import in Arabidopsis cotyledons upon perturbation of chloroplast protein homeostasis

Tadini

Peracchio

Trotta

et al. 2019

Preprint

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Correct chloroplast development and function require coordinated expression of chloroplast and nuclear genes. This is achieved through chloroplast signals that modulate nuclear gene expression in accordance with the chloroplast's needs. Genetic evidence indicates that GUN1, a chloroplast-localized pentatricopeptide-repeat (PPR) protein with a C-terminal Small MutS-Related (SMR) domain, is involved in integrating multiple developmental and stress-related signals in both young seedlings and adult leaves. Recently, GUN1 was found to interact physically with factors involved in chloroplast protein homeostasis, and with enzymes of tetrapyrrole biosynthesis in adult leaves that function in various retrograde signaling pathways. Here we show that, following perturbation of chloroplast protein homeostasis i) by growth in lincomycin-containing medium, or ii) in mutants defective in either the FtsH protease complex (ftsh), plastid ribosome activity (prps21-1 and prpl11-1) or plastid protein import and folding (cphsp70-1), GUN1 influences NEP-dependent transcript accumulation during cotyledon greening and also intervenes in chloroplast protein import. import Chloroplast biogenesis is achieved through a cascade of events that include cytosolic synthesis of chloroplasttargeted proteins, followed by their import, assembly and folding, while unfolded/misfolded proteins and damaged or malformed chloroplasts are degraded (Sakamoto et al., 2008; Jarvi and López-Jauez, 2013; Izumi and Nakamura, 2018; Otegui, 2018). Most chloroplast-targeted proteins enter the chloroplasts via the protein complexes TOC ('translocon at outer envelope of chloroplast') and TIC ('translocon at inner envelope of chloroplast'). On the cytosolic side, precursor proteins are directed to the Toc34 and Toc159 receptors through the interaction of their chloroplast-targeting peptides with the chaperone heat shock protein 90 (Hsp90) and the guidance complex formed by Hsp70 and a 14-3-3 protein. Active transport through the chloroplast envelope is then mediated by an ATP-dependent import motor, consisting of Hsp70, Hsp90 and the stromal Hsp93 (ClpC2) proteins (Kessler and Schnell, 2009; Sjuts et al., 2017).On the stromal side, transcription of the plastid-encoded genes in higher plants requires two different RNA polymerases: the nuclear-encoded RNA polymerase (NEP), also termed RpoTp (located specifically in the chloroplasts and encoded by the RPOT3 gene) or RpoTmp (located both in mitochondria and plastids and encoded by the RPOT2 gene) and the plastid-encoded RNA polymerase (PEP) (Yu et al., 2014; Börner et al., 2015). NEP is a monomeric T3-T7 bacteriophage-type RNA polymerase that is mainly responsible for transcribing housekeeping genes, whereas PEP is a bacterial-type multisubunit enzyme largely tasked with transcribing photosynthesis-related genes. Chloroplast development is associated with a shift in the primary RNA polymerase from NEP to PEP. Furthermore, compensatory responses can be observed between the two RNA polymerases, as depletion of PEP activ...

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Ubiquitin-Proteasome Dependent Regulation of the GOLDEN2-LIKE 1 Transcription Factor in Response to Plastid Signals

Cited by 82 publications

References 37 publications

Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

The Arabidopsis geneRGOmediates cytokinin responses and increases seed yield

GUN1 influences the accumulation of NEP-dependent transcripts and chloroplast protein import in Arabidopsis cotyledons upon perturbation of chloroplast protein homeostasis

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