Genome-wide expression and network analyses of mutants in key brassinosteroid signaling genes

Abstract

Background Brassinosteroid (BR) signaling regulates plant growth and development in concert with other signaling pathways. Although many genes have been identified that play a role in BR signaling, the biological and functional consequences of disrupting those key BR genes still require detailed investigation. Results Here we performed phenotypic and transcriptomic comparisons of A. thaliana lines carrying a loss-of-function mutation in BRI1 gene, bri1–5, that exhibits a dwarf phenotype and its three activation-tag suppressor lines that were able to partially revert the bri1–5 mutant phenotype to a WS2 phenotype, namely bri1–5/bri1–1D, bri1–5/brs1–1D, and bri1–5/bak1–1D. From the three investigated bri1–5 suppressors, bri1–5/bak1–1D was the most effective suppressor at the transcriptional level. All three bri1–5 suppressors showed altered expression of the genes in the abscisic acid (ABA signaling) pathway, indicating that ABA likely contributes to the partial recovery of the wild-type phenotype in these bri1–5 suppressors. Network analysis revealed crosstalk between BR and other phytohormone signaling pathways, suggesting that interference with one hormone signaling pathway affects other hormone signaling pathways. In addition, differential expression analysis suggested the existence of a strong negative feedback from BR signaling on BR biosynthesis and also predicted that BRS1, rather than being directly involved in signaling, might be responsible for providing an optimal environment for the interaction between BRI1 and its ligand. Conclusions Our study provides insights into the molecular mechanisms and functions of key brassinosteroid (BR) signaling genes, especially BRS1.

Brassinosteroid gene regulatory networks at cellular resolution in the Arabidopsis root

“…Previous studies have inferred global ( 19 , 20 , 22 , 23 ) or temporally resolved GRNs ( 21 ) for brassinosteroid response, but they have lacked cell type and developmental stage specificity. To infer GRN configurations across our brassinosteroid time series, we used CellOracle (materials and methods), focusing on BL DEGs and associated transcription factors.…”

“…Brassinosteroids are sensed at the plasma membrane by BRASSINOSTEROID INSENSITIVE 1 (BRI1) family receptors (13)(14)(15)(16), initiating signal transduction events that activate BES1 and BZR1 fam-ily transcription factors to control thousands of genes (17)(18)(19)(20). The brassinosteroid GRN is typically represented singularly without consideration of cell specificity (20)(21)(22)(23), even though brassinosteroids lead to different responses depending on the developmental context (24)(25)(26)(27)(28).…”

Brassinosteroid gene regulatory networks at cellular resolution

“…Furthermore, HAT7 and GTL1 are direct targets of BES1 and BZR1 (Oh et al, 2014;Sun et al, 2010;Yu et al, 2011), suggesting that they may be part of the BR-directed GRN activated as cells progress from proliferation to elongation. Previous studies have inferred global (Guo et al, 2013;Seyed Rahmani et al, 2021;Sun et al, 2010;Xie et al, 2019a;Yu et al, 2011) or temporally resolved GRNs (Clark et al, 2021) for BR response, but they lack cell type and developmentalstage specificity. To infer GRN configurations across our BR time series we used CellOracle (see methods; Data S8) focusing on BL DEGs and associated transcription factors.…”

“…BES1 and BZR1 direct BR-responsive GRNs by interacting with other transcription factors to control thousands of genes (Clark et al, 2021;Nolan et al, 2017Nolan et al, , 2020Sun et al, 2010;Yu et al, 2011). This downstream GRN is typically represented singularly without consideration of cell specificity (Clark et al, 2021;Guo et al, 2013;Seyed Rahmani et al, 2021;Yu et al, 2011), but BRs lead to different responses depending on cell type and developmental stage, suggesting that multiple BR GRN configurations exist (Ackerman-Lavert et al, 2021;Fridman et al, 2014;Vilarrasa-Blasi et al, 2014). The Arabidopsis root is well suited to investigate spatiotemporal BR responses (Jaillais and Vert, 2016).…”

Excavation of Genes Responsive to Brassinosteroids by Transcriptome Sequencing in Adiantum flabellulatum Gametophytes

“…Additionally, plants have the regulatory mechanisms for maintaining BR homeostasis [ 18 ]. For example, the expressions of BR synthase genes ( CYP90B1 ( DWF4 ), CYP90C1 ( ROT3 ), CYP90D1 , CPD , BR6ox1, and BR6ox2 ) are negatively regulated by BRs in A. thaliana [ 19 , 20 ]. Although many BR synthase genes are present in ferns [ 12 ], it is still unknown whether their expressions are negatively regulated by BRs.…”