PIF4 and HOOKLESS1 Impinge on Common Transcriptome and Isoform Regulation in Thermomorphogenesis

Abstract

High temperature activates the transcription factor PHYTOCHROME-INTERACTING FACTOR4 (PIF4) to stimulate auxin signaling, which causes hypocotyl elongation and leaf hyponasty (thermomorphogenesis). HOOKLESS1 (HLS1) is a recently reported positive regulator of thermomorphogenesis, but the molecular mechanisms by which HLS1 regulates thermomorphogenesis remain unknown. In this study, we initially compared PIF4- and/or HLS1-dependent differential gene expression (DEG) upon high-temperature treatment. We found that a large number of genes are coregulated by PIF4 and HLS1, especially genes involved in plant growth or defense responses. Moreover, we found that HLS1 interacts with PIF4 to form a regulatory module and that, among the HLS1-PIF4-coregulated genes, 27.7% are direct targets of PIF4. We also identified 870 differentially alternatively spliced genes (DASGs) in wild-type plants under high temperature. Interestingly, more than half of these DASG events (52.4%) are dependent on both HLS1 and PIF4, and the spliceosome-defective mutant plantsexhibit a hyposensitive response to high temperature, indicating that DASGs are required for thermomorphogenesis. Further comparative analyses showed that the HLS1/PIF4-coregulated DEGs and DASGs exhibit almost no overlap, suggesting that high temperature triggers two distinct strategies to control plant responses and thermomorphogenesis. Taken together, these results demonstrate that the HLS1-PIF4 module precisely controls both transcriptional and posttranscriptional regulation during plant thermomorphogenesis.

PIF4 and PIF4-Interacting Proteins: At the Nexus of Plant Light, Temperature and Hormone Signal Integrations

“…Moreover, HLS1 interacts with PIF4 to collectively regulate thermomorphogenesis partially through their co-regulations on differentially alternative splicing events and differentially expressed genes [ 19 ]. PIF4 and HLS1 co-regulate a large number of common target genes.…”

“…PIF4 and HLS1 co-regulate a large number of common target genes. Moreover, 27.7% of them are direct targets of PIF4 [ 19 ]. Thus, HLS1-PIF4 module controls both transcriptional and posttranscriptional regulations during plant thermomorphogenesis ( Figure 5 A) [ 19 ].…”

“…Moreover, 27.7% of them are direct targets of PIF4 [19]. Thus, HLS1-PIF4 module controls both transcriptional and posttranscriptional regulations during plant thermomorphogenesis (Figure 5A) [19]. At high temperature, HEC2 interacts with PIF4 and inhibits PIF4 DNA-binding activity and represses hypocotyl elongation.…”

Plant AFC2 kinase desensitizes thermomorphogenesis through modulation of alternative splicing

“…In addition to causing differential gene expression, high ambient temperatures also trigger a number of alternative splicing events ( Lee et al., 2013 ; Pose et al., 2013 ; Sureshkumar et al., 2016 ; Jin et al., 2020 ; Neumann et al., 2020 ). Alternative splicing either produces distinct mature mRNAs that are then translated into different protein isoforms with different functions ( Lee et al., 2013 ; Pose et al., 2013 ) or transcribes aberrant mRNAs and causes mRNA decay normally through the nonsense-mediated mRNA decay (NMD) pathway ( Chaudhary et al., 2019 ; Neumann et al., 2020 ; Lin and Zhu, 2021 ).…”

Overexpression of BBX18 Promotes Thermomorphogenesis Through the PRR5-PIF4 Pathway

“…PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) is a bHLH transcription factor that mediates high temperature-dependent gene expression and alternative splicing events to trigger thermomorphogenesis ( Franklin et al, 2011 ; Sun et al, 2012 ; Jin et al, 2020 ). Over the last decade, significant progress has been made in understanding how PIF4 activity and cellular levels are regulated by temperature.…”