Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis

Clark, Natalie M; Nolan, Trevor M.; Wang, Ping; Song, Gaoyuan; Montes, Christian; Valentine, Conner T.; Guo, Hongqing; Sozzani, Rosangela; Yin, Yanhai; Walley, Justin W.

doi:10.1038/s41467-021-26165-3

Cited by 53 publications

(66 citation statements)

References 86 publications

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“…In order to infer regulatory relationships between auxin responsive root transcription factors (TFs) and their targets we generated a gene regulatory network (GRN). To reconstruct the predictive GRN we implemented our network inference pipeline, SC-ION, which is an extension of RTP-STAR and has been shown previously to successfully identify novel TF roles in response to hormone treatment (Clark et al, 2019; Broeck et al, 2021; Clark et al, 2021). The resulting GRN consisted of 15,856 nodes (genes) with a total of 86,461 directed edges (Figure 4 and Supplemental Table 3).…”

Section: Resultsmentioning

confidence: 99%

“…Transcription factor (TF)-centered gene regulatory networks (GRNs) were generated using SC-ION version 2.1 (Clark et al, 2021) and annotated maize TFs from Grassius (Yilmaz et al, 2009). We first clustered the transcript data by root region (MZ, EZ, C, or S) using Independent Component Analysis (ICA) (Nascimento et al, 2017) implemented in SC-ION.…”

Section: Methodsmentioning

confidence: 99%

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Temporal and spatial auxin responsive networks in maize primary roots

McReynolds

Dash

Montes

et al. 2022

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Auxin is a key regulator of root morphogenesis across angiosperms. To better understand auxin regulated networks underlying maize root development we have characterized auxin responsive transcription across two time points (30 and 120 minutes) and four regions of the primary root: the meristematic zone, elongation zone, cortex, and stele. Hundreds of auxin-regulated genes involved in diverse biological processes were quantified in these different root regions. In general, most auxin regulated genes are region unique and are predominantly observed in differentiated tissues compared to the root meristem. Auxin gene regulatory networks (GRNs) were reconstructed with these data to identify key transcription factors that may underlie auxin responses in maize roots. Additionally, Auxin Response Factor (ARF) subnetworks were generated to identify target genes which exhibit tissue or temporal specificity in response to auxin. These networks describe novel molecular connections underlying maize root development and provide a foundation for functional genomic studies in a key crop.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Temporal and spatial auxin responsive networks in maize primary roots

McReynolds

Dash

Montes

et al. 2022

Preprint

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“…transcriptomic, proteomic, and phosphoproteomic data) can increase the predictive power of Gene Regulatory Network (GRN) inference (Walley et al, 2016). With this in mind, we also inferred two separate transcription factor (TF)-centered GRNs, for each of our mutants ( bin2D, bin2T , and raptor1b ), using the SC-ION pipeline (Figure 5) (Clark et al, 2021). In the first network, called “abundance GRN”, TF protein abundance (when quantified) or TF transcript abundance (when cognate protein was not quantified) was used as the “regulator” value to infer their “target” transcript abundance.…”

Section: Resultsmentioning

confidence: 99%

“…Protein kinases were identified using a modified version of the pipeline described by (Walley et al, 2013;Clark et al, 2021). Briefly, all 35,386 protein sequences available in the TAIR10 annotation (https://www.arabidopsis.org/download_files/Proteins/TAIR10_protein_lists/TAIR10_pep _20101214) were searched for kinase domain using The National Center for Biotechnology Information batch conserved domain search tool (Lu et al, 2020).…”

Section: Kinase Activation Loop Predictionmentioning

confidence: 99%

Integration of multi-omics data reveals interplay between brassinosteroid and TORC signaling in Arabidopsis

Montes

Wang

Liao

et al. 2022

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Brassinosteroids (BR) and Target of Rapamycin Complex (TORC) are two major actors coordinating plant growth and stress responses. BRs function through a signaling pathway to extensively regulate gene expression and TORC is known to regulate translation and autophagy. Recent studies revealed that these two pathways crosstalk, but a system-wide view of their interplay is still missing. Thus, we quantified the level of 23,975 transcripts, 11,183 proteins, and 27,887 phosphorylation sites in wild-type Arabidopsis and in mutants with altered levels of either BRASSINOSTEROID INSENSITIVE 2 (BIN2) or REGULATORY ASSOCIATED PROTEIN OF TOR 1B (RAPTOR1B), two key players in BR and TORC signaling, respectively. We found that perturbation of BIN2 or RAPTOR1B levels affects a common set of gene-products involved in growth and stress responses. Furthermore, we used the multi-omic data to reconstruct an integrated signaling network. We screened 41 candidate genes identified from the reconstructed network and found that loss of function mutants of many of these proteins led to an altered BR response and/or modulated autophagy activity. Altogether, these results establish a predictive network that defines different layers of molecular interactions between BR- or TORC-regulated growth and autophagy.

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“…BIN2 may regulate TOR substrate recruitment efficiency or substrate selectivity through direct phosphorylation at the RAPTOR1B Ser916 site. Analysis of a recently published BL time-series dataset 47 indicated that Ser916 phosphorylation status varies in response to different BL treatment times. Consistent with our observations in Figure S2, Ser916 phosphorylation rapidly increased in the beginning of BL treatment and decreased at the later time points.…”

Section: Discussionmentioning

confidence: 99%

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

Liao

Nolan

et al. 2022

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Macroautophagy/autophagy is a conserved recycling process that maintains cellular homeostasis during environmental stress. Autophagy is negatively regulated by TARGET OF RAPAMYCIN (TOR), a nutrient-regulated protein kinase that in plants is activated by several phytohormones, leading to increased growth. However, the detailed molecular mechanisms by which TOR integrates autophagy and hormone-signaling are poorly understood. Here, we show that TOR modulates brassinosteroid (BR)-regulated plant growth and stress-response pathways. Active TOR was required for full BR-induced growth in Arabidopsis thaliana. Autophagy was constitutively up-regulated upon blocking BR biosynthesis or signaling, and down-regulated by increasing the activity of the BR pathway. BRASSINOSTEROID-INSENSITIVE 2 (BIN2) kinase, a GSK3-like kinase functioning as a negative regulator in BR signaling, directly phosphorylated Regulatory-Associated Protein of TOR 1B (RAPTOR1B), a substrate-recruiting subunit in the TOR complex, at a conserved serine residue within a typical BIN2 phosphorylation motif. Mutation of RAPTOR1B serine 916 to alanine, to block phosphorylation by BIN2, repressed autophagy and increased phosphorylation of the TOR substrate autophagy-related protein 13a (ATG13a). By contrast, this mutation had only a limited effect on growth. We present a model in which RAPTOR1B is phosphorylated and inhibited by BIN2 when BRs are absent, activating the autophagy pathway. When BRs signal and inhibit BIN2, RAPTOR1B is thus less inhibited by BIN2 phosphorylation. This leads to increased TOR activity and ATG13a phosphorylation, and decreased autophagy activity. Our studies define a new mechanism by which coordination between BR and TOR signaling pathways helps to maintain the balance between plant growth and stress responses.

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Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis

Cited by 53 publications

References 86 publications

Temporal and spatial auxin responsive networks in maize primary roots

Temporal and spatial auxin responsive networks in maize primary roots

Integration of multi-omics data reveals interplay between brassinosteroid and TORC signaling in Arabidopsis

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

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