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Review
. 2021 Jan 21;10(2):196.
doi: 10.3390/plants10020196.

The Role of Tetrapyrrole- and GUN1-Dependent Signaling on Chloroplast Biogenesis

Takayuki Shimizu  1 , Tatsuru Masuda  1
Affiliations
Review

The Role of Tetrapyrrole- and GUN1-Dependent Signaling on Chloroplast Biogenesis

Takayuki Shimizu et al. Plants (Basel). .

Abstract

Chloroplast biogenesis requires the coordinated expression of the chloroplast and nuclear genomes, which is achieved by communication between the developing chloroplasts and the nucleus. Signals emitted from the plastids, so-called retrograde signals, control nuclear gene expression depending on plastid development and functionality. Genetic analysis of this pathway identified a set of mutants defective in retrograde signaling and designated genomes uncoupled (gun) mutants. Subsequent research has pointed to a significant role of tetrapyrrole biosynthesis in retrograde signaling. Meanwhile, the molecular functions of GUN1, the proposed integrator of multiple retrograde signals, have not been identified yet. However, based on the interactions of GUN1, some working hypotheses have been proposed. Interestingly, GUN1 contributes to important biological processes, including plastid protein homeostasis, through transcription, translation, and protein import. Furthermore, the interactions of GUN1 with tetrapyrroles and their biosynthetic enzymes have been revealed. This review focuses on our current understanding of the function of tetrapyrrole retrograde signaling on chloroplast biogenesis.

Keywords: chloroplast; gun mutants; heme; plastid; retrograde signaling; tetrapyrrole.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Tetrapyrrole biosynthetic pathway. Enzymes involved in the tetrapyrrole biosynthetic pathway are indicated by red. Important genes described in this article are shown in yellow boxes and genes encoding GUN proteins are indicated by red borders. It is noted that GUN2~GUN6 genes are found at the branch points of Chl and heme biosynthesis. GUN1 interacting proteins are indicated by blue borders.
Figure 2
Figure 2
Schematic overview of genomes uncoupled (GUN)1 interacting proteins involved in plastid protein homeostasis (transcription (brown circles), editing and maturation (red circles), translation (orange circles), and chaperone (green circles)) and tetrapyrrole biosynthesis (blue circles). Yellow arrows indicate GUN1 interactions. It is possible that through the N-terminal intrinsically disordered region (IDR) region or pentatricopeptide repeat (PPR) domain, GUN1 forms a droplet that causes molecular crowding, which enhances entropically favor molecular association events, thereby accelerating molecular reactions. Interactions of GUN1 with indicated proteins were demonstrated by co-immunoprecipitation, bimolecular fluorescence complementation (BiFC), and yeast two-hybrid assays.
Figure 3
Figure 3
A hypothesis of the heme biogenic plastid-to-nucleus retrograde signaling pathway. (a) In plastids (left), the transition of proplastid to chloroplast is indicated from left to right. Blue circles indicate GUN1-dependent droplets and red symbols represent ferrochelatase (FC)1-dependent heme. 1. At the initial phase of proplastid to chloroplast transition, a putative GUN-dependent droplet may form in proplastids, which enhances nuclear-encoded polymerase (NEP)-dependent transcription and translation, import of nuclear-encoded proteins, and heme biosynthesis. Synthesized heme may bind to the GUN1-dependent droplets. 2. During chloroplast biogenesis, GUN1 is degraded by Clp-protease-dependent manner, causing disappearance of the blue circles. 3. FC1-derived hemes bound to GUN1 condensates were released and emitted from plastids via cytosolic or ER-plastid membrane contact sites (MCSs)-dependent pathway (dashed lines) through a plastid-envelop-localized putative transporter (orange circles). In the cytosolic pathway, heme may bind to cytosolic heme carrier proteins (green circles) to reach other organelles. 4. In the nucleus, heme may inactivate PIFs or activate transcription factors, GLK1, and/or HY5. 5. Consequently, PhANG expression is activated. (b) In the wild type, when chloroplasts are rendered dysfunctional by inhibitor treatments, Clp-protease-dependent degradation is protected resulting in the dispersion of the GUN1 droplet (blue circle), as well as retention of heme (red symbols) in plastids. (c) In gun1, when the chloroplasts become dysfunctional, heme can be emitted from plastids because the GUN1-dependent condensates are deficient.
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