Orthogonal regulation of phytochrome B abundance by stress-specific plastidial retrograde signaling metabolite

Abstract

Plant survival necessitates constant monitoring of fluctuating light and balancing growth demands with adaptive responses, tasks mediated via interconnected sensing and signaling networks. Photoreceptor phytochrome B (phyB) and plastidial retrograde signaling metabolite methylerythritol cyclodiphosphate (MEcPP) are evolutionarily conserved sensing and signaling components eliciting responses through unknown connection(s). Here, via a suppressor screen, we identify two phyB mutant alleles that revert the dwarf and high salicylic acid phenotypes of the high MEcPP containing mutant ceh1 . Biochemical analyses show high phyB protein levels in MEcPP-accumulating plants resulting from reduced expression of phyB antagonists and decreased auxin levels. We show that auxin treatment negatively regulates phyB abundance. Additional studies identify CAMTA3, a MEcPP-activated calcium-dependent transcriptional regulator, as critical for maintaining phyB abundance. These studies provide insights into biological organization fundamentals whereby a signal from a single plastidial metabolite is transduced into an ensemble of regulatory networks controlling the abundance of phyB, positioning plastids at the information apex directing adaptive responses.

Retrograde induction of phyB orchestrates ethylene-auxin hierarchy to regulate growth

“…S1 D ), immunoblot analyses show notable increase in phyB protein abundance in the ceh1 mutant compared to the WT seedlings (Fig. S1 E & S1 F ), verifying the earlier report using white light grown seedlings (Jiang et al, 2019).…”

“…The degradation of phyB is established to be through intermolecular transaction of this photoreceptor with PIF transcription factors (Ni et al, 2013), thereby supporting the prospect of significantly reduced PIF4 and 5 transcript levels as the likely cause of enhanced phyB protein abundance in ceh1 seedlings grown in Rc. Furthermore, reversion of ceh1 stunted hypocotyls in ceh1/phyB-9 confirms the key role of enhanced phyB protein abundance in growth retardation of the mutant, confirming the earlier finding using white light grown seedlings (Jiang et al, 2019)…”

“…Collectively, these results support involvement of cryptochrome as well and phyB in ceh1 hypocotyl growth, albeit at different degrees. However, the more drastic effect of phyB in regulating hypocotyl growth of Rc grown high MEcPP accumulating seedlings in conjunction with the supporting evidence from the earlier data using white light grown ceh1 seedlings (Jiang et al, 2019), led us to primarily focus on the role of phyB.…”

“…Quantification of SA, JA,ABA and IAA was carried out by gas chromatography-mass spectrometry (GC-MS), using dihydro-JA and deuterated SA and ABA, and IAA as internal standard, as previously described (Savchenko et al, 2010). MEcPP extraction and quantification was performed as previously described (Jiang et al, 2019).…”

Retrograde Induction of phyB Orchestrates Ethylene-Auxin Hierarchy to Regulate Growth

“…Collectively, these results support the involvement of cryptochromes as well as phyB in ceh1 hypocotyl growth, albeit to different degrees. However, the more drastic effect of phyB in regulating hypocotyl growth of Rc-grown, high MEcPP-accumulating seedlings, in conjunction with the supporting evidence from earlier data using white light-grown ceh1 seedlings (Jiang et al, 2019), led us to primarily focus on the role of phyB.…”