Phytochrome and Ethylene Signaling Integration in Arabidopsis Occurs via the Transcriptional Regulation of Genes Co-targeted by PIFs and EIN3

Abstract

Plant seedlings germinating under the soil are challenged by rough soil grains that can induce physical damage and sudden exposure to light, which can induce photobleaching. Seedlings overcome these challenges by developing apical hooks and by suppressing chlorophyll precursor biosynthesis. These adaptive responses are, respectively, regulated by the phytochrome and ethylene signaling pathways via the PHYTOCHROME-INTERACTING FACTORs (PIFs) and the ETHYLENE INSENSITIVE 3 (EIN3)/EIN3-LIKE transcription factors. Although many processes downstream of phytochrome and ethylene signaling are similar, it remains unclear if and where these pathways converge. Here, we show PIFs and EIN3 induce similar changes in the transcriptome without robustly regulating each other’s signaling pathways. PIFs and EIN3 target highly overlapped gene promoters and activate subsets of the co-target genes either interdependently or additively to induce plant responses. For chlorophyll biosynthesis, PIFs and EIN3 target and interdependently activate the expression of HOOKLESS1. HOOKLESS1, in turn, represses chlorophyll synthesis genes to prevent photobleaching. Thus, our results indicate an integration of the phytochrome and ethylene signaling pathways at the level of transcriptional gene regulation by two core groups of transcription factors, PIFs and EIN3.

Transcriptome analysis of shade avoidance and shade tolerance in conifers

“…Shade reduces phyB activity and, consequently, increases the mRNA levels of the bHLH transcription factors such as phytochrome interacting factors (PIF) (Lorrain et al 2008). PIFs regulate a large number of genes encoding metabolic enzymes and genes in the phytohormones signalling pathway such as auxin (AUX/IAA) (Hersch et al 2014), ethylene (Jeong et al 2016), brassinosteroids (BRs) (Oh et al 2012), and gibberellins (Schwechheimer 2011), which control low R:FRinduced shade avoidance responses.…”

Genome-wide regulation of light-controlled seedling morphogenesis by three families of transcription factors

“…EIN3 proteins are highly accumulated in buried seedlings through both mechanical stress-evoked ethylene production and darkness (19,21,22). Previous studies suggest that EIN3 and PIFs regulate the expressions of their common target genes in either an additive or interdependent way (30). Recently, EIN3/EIL1 have been shown to promote seedling soil emergence by exaggerating apical hook formation (22), inhibiting cotyledon opening and expansion (19), and repressing chloroplast development (6).…”

On hormonal regulation of the dynamic apical hook development

“…This transcriptional coupling integratively mediates the effects of multiple hormones, such as ethylene, gibberellin and jasmonate, and environmental factors, such as light and mechanical pressure, on apical hook development ( Fig. 1) (Gallego-Bartolome et al, 2011;An et al, 2012;Zhang et al, 2014Zhang et al, , 2018Jeong et al, 2016;Shen et al, 2016;Shi et al, 2018).…”