EIN3 and PIF3 Form an Interdependent Module That Represses Chloroplast Development in Buried Seedlings

Abstract

In buried seedlings, chloroplasts are arrested at the etioplast stage, but they rapidly mature upon emergence of the seedling. Etioplast-chloroplast differentiation is halted through the integration of soil-induced signals, including pressure and the absence of light, although the details on how this information converges to regulate cellular decisions remain unclear. Here, we identify an interdependent transcription module that integrates the mechanical pressure and darkness signals to control chloroplast development in Mutations of ETHYLENE-INSENSITIVE3 (EIN3), the primary transcription factor in the ethylene signaling pathway that is activated in response to mechanical pressure, cause early development of etioplasts in the dark and severe photobleaching upon light exposure. Genetic studies demonstrate that repression of etioplast differentiation by EIN3 requires PHYTOCHROME INTERACTING FACTOR3 (PIF3), a darkness-stabilized bHLH transcription factor. EIN3 and PIF3 directly interact and form an interdependent module to repress the expression of most () genes; overexpressing even one could cause premature development of etioplasts. The EIN3-PIF3 transcription module synergistically halts chloroplast development by interdependently co-occupying the promoters of genes. Thus, our results define a transcriptional regulatory module and provide mechanistic insight on the concerted regulation of chloroplast development by multiple soil-induced signals.

Life’s a Gas under Pressure: Ethylene and Etioplast Maintenance in Germinating Seedlings

“…Overexpression of PIF3 (in ein3 eil1) or EIN3 (in pif3) does not rescue full prolamellar body formation and the pif3 ein3 eil1 triple mutant shows the same extent of prothylakoid membranes as the pif3 single and ein3 eil1 double mutants. Both of these results underscore the true synergy between PIF3 and EIN3 (Liu et al, 2017).…”

“…As seedlings grow closer to the surface, soil pressure lessens, ethylene production decreases, and EIN3 protein degradation accelerates (Shi et al, 2016). Now, new results by Liu et al (2017) show how PIF3 and EIN3 cooperate at the molecular and transcriptional level to suppress the maturation of etioplasts into chloroplasts until seedlings emerge from underneath the soil.…”

“…Apparently, not much: Overexpression of individual members of the LHCB family results in extensive unraveling of the prolamellar body in etioplasts (Liu et al, 2017). These lines still accumulate protochlorophyllid, but the absence of the prolamellar body for sequestration of the chlorophyll precursor now renders seedlings highly sensitive to photooxidation when exposed to light (see figure), just like in pif3 and ein3 eil1 mutants.…”

“…Seedling greening was obvious only in Col-0 from chlorophyll autofluorescence, while ein3 eil1 and Lhcb2.1 ox lines showed extensive reactive oxygen species accumulation due to loss of prolamellar body (as shown in etioplast transmission electron microscopy). (Adapted from Liu et al [2017], Figures 2,7,and 8. ) OPEN Articles can be viewed without a subscription.…”

A role for two‐component signaling elements in the Arabidopsis growth recovery response to ethylene

“…As noted above, both pathways contribute to varying extents in the control of different ethylene responses. A potential mechanism that would facilitate such control is combinatorial regulation between the EIN3/EIL and type‐B ARR transcription factors, EIN3 and ARR having each individually been found to coregulate gene expression in conjunction with other transcription factors (Feng et al., ; Liu et al., ; Marin‐de la Rosa et al., ).…”