Brassinosteroids modulate autophagy through phosphorylation of RAPTOR1B by the GSK3-like kinase BIN2 in Arabidopsis

Liao, Ching‐Yi; Pu, Yunting; Nolan, Trevor M.; Montes, Christian; Guo, Hongqing; Walley, Justin W.; Yin, Yanhai; Bassham, Diane C.

doi:10.1080/15548627.2022.2124501

Cited by 15 publications

(8 citation statements)

References 97 publications

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“…These observations are consistent with Tre6P acting via inhibition of SnRK1 to repress ABA signaling. Other known downstream phosphorylation targets of TOR (Scarpin et al, 2020; Meng et al ., 2022; Liao et al, 2022) were also found in the G1 iTPS response, including several initiation and elongation factors (Supplemental Figure S4E). Overall, our data point to a synergy between post-translational regulation of ribosome assembly, translation and other processes like ABA signaling by TOR, and transcriptional regulation of these processes by Tre6P-mediated signaling.…”

Section: Resultsmentioning

confidence: 94%

“…The emerging evidence for links between sugar- and BR-signaling (Zhang et al, 2016; 2021; Liao et al, 2022) prompted us to inspect the iTPS response of genes assigned to BR synthesis and signaling (Supplemental Figure 17 and Supplemental text). iTPS repressed genes in the biosynthesis pathway, probably via indirect effects, but elevated Tre6P had a direct impact on signaling components like BRASSINOSTEROID INSENSITIVE 2 ( BIN2 ), BRASSINOSTEROID ENHANCED EXPRESSION1 ( BEE1 ) and BEE2 .…”

Section: Resultsmentioning

confidence: 99%

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Direct and indirect responses of the Arabidopsis transcriptome to an induced increase in trehalose 6-phosphate

Avidan,

Martins,

Feil

et al. 2023

Preprint

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Trehalose 6-phosphate (Tre6P) is an essential signal metabolite that reports and regulates the level of sucrose, linking growth and development to the metabolic status. We hypothesized that Tre6P plays a role in mediating the regulation of gene expression by sucrose. To test this, we performed transcriptomic profiling on Arabidopsis plants that expressed a bacterial trehalose-6-phosphate synthase (TPS) under the control of an ethanol-inducible promoter. Induction led to a 4-fold rise in Tre6P levels, a concomitant decrease in sucrose, and significant changes of over 13,000 transcripts and two-fold or larger changes of over 5000 transcripts. Comparison with nine published responses to sugar availability allowed some of these changes to be linked to the rise in Tre6P, while others were probably due to lower sucrose or other indirect effects. Changes linked to Tre6P included repression of photosynthesis and induction of many growth-related processes including ribosome biogenesis. About 500 starvation-related genes are known to be induced by SUCROSE-NON-FERMENTING-1-RELATED KINASE 1 (SnRK1). They were largely repressed by Tre6P in a manner consistent with Tre6P acting to inhibit SnRK1. SnRK1 also represses many genes that are involved in biosynthesis and growth. These responded to Tre6P in a more complex manner, pointing to Tre6P also interacting with further C-signaling pathways. In addition, elevated Tre6P modified expression of genes encoding regulatory subunits of the SnRK1 complex and TPS class II and FLZ proteins that are thought to modulate SnRK1 function, and genes involved in the circadian clock and in TOR, light, abscisic acid and other hormone signaling.

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Section: Resultsmentioning

confidence: 94%

Section: Resultsmentioning

confidence: 99%

Direct and indirect responses of the Arabidopsis transcriptome to an induced increase in trehalose 6-phosphate

Avidan,

Martins,

Feil

et al. 2023

Preprint

View full text Add to dashboard Cite

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“…Hence, additional signals driven by the normalized TOR activity are responsible for restoring growth in plants deficient in CYTc. The potential benefits of enhanced nitrogen uptake and utilization (Lutt & Brunkard, 2022), optimized metabolism (Ingargiola et al, 2023), and hormonal pathways (Liao et al, 2023) are among the possible explanations that we pursue to evaluate in future work. ATP and/or other unknown potential signals related to mitochondrial function (?)…”

Section: Discussionmentioning

confidence: 99%

“…It also controls cell proliferation in the root and shoot apical meristems (Li et al ., 2017). Autophagy is also regulated by TOR and depends on soluble sugars and brassinosteroid levels (Dobrenel et al ., 2016; Liao et al ., 2023). The signaling pathway mediated by TOR responds to changes in nutrient concentrations and amino acid levels that impact respiratory and energetic metabolism (Caldana et al ., 2013; Cao et al ., 2019; O'Leary et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions

Canal,

Mansilla,

Gras

et al. 2024

New Phytologist

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Summary Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood. We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain component cytochrome c (CYTc) in Arabidopsis, to understand how mitochondria communicate their status to coordinate metabolism and growth. Plants with CYTc deficiency show decreased mitochondrial membrane potential and lower ATP content, even when carbon sources are present. They also exhibit higher free amino acid content, induced autophagy, and increased resistance to nutritional stress caused by prolonged darkness, similar to plants with triggered starvation signals. CYTc deficiency affects target of rapamycin (TOR)‐pathway activation, reducing S6 kinase (S6K) and RPS6A phosphorylation, as well as total S6K protein levels due to increased protein degradation via proteasome and autophagy. TOR overexpression restores growth and other parameters affected in cytc‐1 mutants, even if mitochondrial membrane potential and ATP levels remain low. We propose that CYTc‐deficient plants coordinate their metabolism and energy availability by reducing TOR‐pathway activation as a preventive signal to adjust growth in anticipation of energy exhaustion, thus providing a mechanism by which changes in mitochondrial activity are transduced to the rest of the cell.

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“…Moreover, C availability leads to the stabilization of BRASSINAZOLE-RESISTANT 1 (BZR1) mediated by the TOR-brassinosteroid signaling axis, preventing BZR1 degradation by autophagy during hypocotyl elongation (Zhang et al, 2016). BRASSINOSTEROID-INSENSITIVE 2 (BIN2) directly phosphorylates RAPTOR1B, inhibiting TORdependent ATG13 phosphorylation and thereby activating autophagy (Liao et al, 2022). This crosstalk between nutrient availability and hormones ensures a supply and demand trade-off for plant growth.…”

Section: The Emerging Role Of Snrk1-nin-like Proteins In N Signalingmentioning

confidence: 99%

Sensing and regulation of C and N metabolism – novel features and mechanisms of the TOR and SnRK1 signaling pathways

Artins,

Martins,

Meyer

et al. 2024

The Plant Journal

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SUMMARYCarbon (C) and nitrogen (N) metabolisms are tightly integrated to allow proper plant growth and development. Photosynthesis is dependent on N invested in chlorophylls, enzymes, and structural components of the photosynthetic machinery, while N uptake and assimilation rely on ATP, reducing equivalents, and C‐skeletons provided by photosynthesis. The direct connection between N availability and photosynthetic efficiency allows the synthesis of precursors for all metabolites and building blocks in plants. Thus, the capacity to sense and respond to sudden changes in C and N availability is crucial for plant survival and is mediated by complex yet efficient signaling pathways such as TARGET OF RAPAMYCIN (TOR) and SUCROSE‐NON‐FERMENTING‐1‐RELATED PROTEIN KINASE 1 (SnRK1). In this review, we present recent advances in mechanisms involved in sensing C and N status as well as identifying current gaps in our understanding. We finally attempt to provide new perspectives and hypotheses on the interconnection of diverse signaling pathways that will allow us to understand the integration and orchestration of the major players governing the regulation of the CN balance.

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Brassinosteroids modulate autophagy through phosphorylation of RAPTOR1B by the GSK3-like kinase BIN2 in Arabidopsis

Cited by 15 publications

References 97 publications

Direct and indirect responses of the Arabidopsis transcriptome to an induced increase in trehalose 6-phosphate

Direct and indirect responses of the Arabidopsis transcriptome to an induced increase in trehalose 6-phosphate

Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions

Sensing and regulation of C and N metabolism – novel features and mechanisms of the TOR and SnRK1 signaling pathways

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