A BIN2-GLK1 Signaling Module Integrates Brassinosteroid and Light Signaling to Repress Chloroplast Development in the Dark

Zhang, Dawei; Tan, Wenrong; Yang, Feng; Han, Qing; Deng, Xing-Guang; Guo, Hongqing; Liu, Baohui; Yin, Yanhai; Lin, Honghui

doi:10.1016/j.devcel.2020.12.001

Cited by 80 publications

(81 citation statements)

References 87 publications

(126 reference statements)

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“…The result showed that the N-terminal region excluding all three domains is sufficient to interact with nuSIB1 (Supplemental Figure 8A and 8B). Since the N-terminal part contains a nuclear localization signal (Zhang et al, 2021a), we ended further defining the minimum length of the N-terminal necessitated for the interaction with nuSIB1. It is likely that SA-induced nuSIB1 competitively interacts with GLK1 and GLK2 through the N-terminal part, which consequently enhances the expression of PhANGs and the 1 O 2 level, thereby activating an EX1-mediated cell death response (Figure 7).…”

Section: Resultsmentioning

confidence: 99%

“…We now showed that LSD1 interacts with GLK1 and GLK2 TFs in the nucleus (Figure 1A). Besides their transcriptional regulation (e.g., by GUN1-mediated RS), multiple proteins post-translationally modulate GLK activity (Tang et al, 2016; Tokumaru et al, 2017; Zhang et al, 2021a). The C-terminal GCT-box drives GLK homo-or hetero-dimerization in maize (Rossini et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

“…The turnip yellow mosaic virus (TYMV) protein P69 binds to the GLK1/2 GCT-box, repressing PhANGs and chloroplast biogenesis in Arabidopsis (Ni et al, 2017). On the contrary, BRASSINOSTEROID INSENSITIVE 2 (BIN2)-dependent GLK phosphorylation promotes chloroplast biogenesis by stabilizing GLK proteins in Arabidopsis (Zhang et al, 2021a). These reports indicate that both DBD and GCT-box in GLK1/2 are involved in protein-protein interaction.…”

Section: Discussionmentioning

confidence: 99%

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Antagonistic modules, SIB1 and LSD1, regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors in Arabidopsis

Lee

Liu

et al. 2020

Preprint

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GOLDEN2-LIKE (GLK) transcription factors drive the expression of photosynthesis-associated nuclear genes (PhANGs), indispensable for chloroplast biogenesis. We previously demonstrated that the salicylic acid (SA)-induced SIGMA FACTOR-BINDING PROTEIN1 (SIB1), a transcription coregulator and positive regulator of SA-primed cell death, interacts with GLKs. The SIB1-GLK interaction raises the level of light-harvesting antenna proteins in the photosystem II, aggravating photoinhibition and singlet oxygen (1O2) burst. 1O2 then contributes to SA-primed cell death via EXECUTER1 (EX1, 1O2 sensor protein)-mediated retrograde signaling upon reaching a critical level. We now reveal that LESION-SIMULATING DISEASE 1 (LSD1), a transcription coregulator and negative regulator of SA-primed cell death, interacts with GLKs to repress their activities. Consistently, the overexpression of LSD1 represses the expression of PhANGs, but the loss of LSD1 increases their expression. The SA-induced SIB1 then counteractively interacts with GLKs, leading to EX1-mediated cell death. Collectively, we provide a working model that mutually exclusive SA-signaling components SIB1 and LSD1 antagonistically regulate GLKs to fine-tune the expression of PhANGs, priming SA-induced cell death, and sustaining 1O2 homeostasis, respectively.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Antagonistic modules, SIB1 and LSD1, regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors in Arabidopsis

Lee

Liu

et al. 2020

Preprint

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“…DET2-OX , bes1-D and det2 used in this study were previously reported (Zhang et al, 2021) and BES1-RNAi (Li et al, 2020). 35S::GFP, 35S::BES1-GFP and proBES1::GUS were introduced into Col-0 by Agrobacterium tumefaciens -mediated floral transformation.…”

Section: Plant Materialsmentioning

confidence: 99%

A Brassinosteroids-BES1 Regulatory Module Manipulate Thermomemory in Arabidopsis thaliana

Yao

Chen

et al. 2022

Preprint

Self Cite

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Heat stress (HS) caused by ambient high temperature pose a threat to plants. In the natural and agricultural environment, plants often encounter repeated and changeable HS. Moderate HS primes plants to establishment of a molecular ‘thermomemory’ that enables plants to withstand a later-and possibly more extreme-HS attack. Recent years, brassinosteroids (BRs) have been implicated in HS response whereas little is known about whether BRs signal transduction modulates thermomemory. Here, we uncover the positive role of BRs signaling in thermomemory of Arabidopsis thaliana. Heat priming induces de novo synthesis and nuclear accumulation of BRI1-EMS-SUPPRESSOR (BES1), the key regulator of BRs signaling. BRs promote the accumulation of dephosphorylated BES1 during memory phase, blocking BRs synthesis impairs dephosphorylation. During HS memory, BES1 is required to maintain sustained induction of HS memory genes and directly targets APX2 and HSFA3 for activation. In summary, our results reveal a BES1-required, BRs-enhanced transcriptional control module of thermomemory in Arabidopsis thaliana.

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“…While the HY5/CRY1-BIN2 interaction stimulates the BIN2-catalyzed BZR1 phosphorylation to regulate hypocotyl elongation, the interaction of BIN2 with PIF4 (Phytochrome Interacting Factor4), which is a key component of the phytochrome signaling pathway [ 101 ], enhances the BIN2-catlyzed PIF4 phosphorylation and reduces PIF4 stability to inhibit the hypocotyl elongation [ 102 ]. A recent study also implicated BIN2 in regulating another key aspect of plant photomorphogenesis, light-stimulated development of mature chloroplasts [ 103 ]. It was discovered that BIN2 phosphorylates GLK1 (GOLDEN2-LIKE1), a transcription factor important for chloroplast development [ 104 ], to increase its protein stability and transcriptional activity, thus promoting chloroplast development.…”

Section: Roles In Plant Growth and Developmentmentioning

confidence: 99%

Versatile Physiological Functions of Plant GSK3-Like Kinases

Mao

Liu

et al. 2021

Genes

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The plant glycogen synthase kinase 3 (GSK3)-like kinases are highly conserved protein serine/threonine kinases that are grouped into four subfamilies. Similar to their mammalian homologs, these kinases are constitutively active under normal growth conditions but become inactivated in response to diverse developmental and environmental signals. Since their initial discoveries in the early 1990s, many biochemical and genetic studies were performed to investigate their physiological functions in various plant species. These studies have demonstrated that the plant GSK3-like kinases are multifunctional kinases involved not only in a wide variety of plant growth and developmental processes but also in diverse plant stress responses. Here we summarize our current understanding of the versatile physiological functions of the plant GSK3-like kinases along with their confirmed and potential substrates.

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A BIN2-GLK1 Signaling Module Integrates Brassinosteroid and Light Signaling to Repress Chloroplast Development in the Dark

Cited by 80 publications

References 87 publications

Antagonistic modules, SIB1 and LSD1, regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors in Arabidopsis

Antagonistic modules, SIB1 and LSD1, regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors in Arabidopsis

A Brassinosteroids-BES1 Regulatory Module Manipulate Thermomemory in Arabidopsis thaliana

Versatile Physiological Functions of Plant GSK3-Like Kinases

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