The Nature and The Functional Complexity of Retrograde Signals. Retrograde signaling refers to the fact that chloroplasts and mitochondria utilize specific signaling molecules to convey information on their developmental and physiological states to the nucleus and modulate the expression of nuclear genes accordingly.
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Plant organelles produce retrograde signals to alter nuclear gene expression in order
to
Coordinate their biogenesis
Maintain homeostasis
Optimize their performance under adverse conditions
Estavillo et al., 2013 I Frontiers in Plant Science
The term retrograde signaling refers to the fact that chloroplasts and
mitochondria utilize specific signaling molecules to convey
information on their developmental and physiological states to the
nucleus and modulate the expression of nuclear genes accordingly.
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Signals emanating from plastids have been associated with two
main networks:
Biogenic Signals - Active during early stages of chloroplast
development.
Operational Signals - Control functions in response to
environmental fluctuations such as excessive light, drought, or
heat.
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Summary
Intracellular signaling network
Nature of retrograde signals - Different routes of communication and outcomes
Master initiators of interorganellar communication - Ca2+ and ROS
Functional Complexity - Retrograde signaling during chloroplast biogenesis
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Hernández-Verdeja, T. and Strand, A, 2018. Retrograde signals navigate the path to
chloroplast development. Plant physiology, 176(2), pp.967-976.
De Souza, A., Wang, J.Z. and Dehesh, K., 2017. Retrograde signals: integrators of
interorganellar communication and orchestrators of plant development. Annual review
of plant biology, 68, pp.85-108.
Rea, G., Antonacci, A., Lambreva, M.D. and Mattoo, A.K., 2018. Features of cues and
processes during chloroplast-mediated retrograde signaling in the alga
Chlamydomonas.Plant science.
Kacprzak, S.M., Mochizuki, N., Naranjo, B., Xu, D., Leister, D., Kleine, T., Okamoto, H. and
Terry, M.J., 2019. Plastid-to-nucleus retrograde signalling during chloroplast biogenesis
does not require ABI4. Plant physiology, 179(1), pp.18-23.
References
Hinweis der Redaktion
Fig. 1. Schematic illustration of plant intracellular communication networks. Imbalance of plastid homeostasis induced by either environmental or intrinsic cues determines which signaling molecules will be synthesized or called upon to transmit information to the nucleus. As a consequence, remodeling of gene expression patterns, and activation of posttranscriptional and posttranslational processes takes place. Anterograde signaling (nucleus to organelle) is represented by orange arrows; retrograde signaling (organelle to nucleus) by blue arrows, and intra-organellar communication by yellow dashed arrows.
Ca2+ and ROS as the master initiators of interorganellar communications. Shown here are both confirmed and proposed connections between Ca2+ and ROS signals and the transducing regulatory components of stress-responsive genes. Selected proteins involved in signal transduction are shown, including RBOH, RAO1, ANAC013 and ANAC017, ABI4, and the transcription factors WRKY40 and WRKY63. Abbreviations: ABI4, ABSCISIC ACID INSENSITIVE 4; ANAC013/017, NO APICAL MERISTEM/
ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON
013/017; RAO1, REGULATOR OF ALTERNATIVE OXIDASE 1; RBOH, respiratory burst oxidase
homolog; ROS, reactive oxygen species.
AZA, azelaic acid; β-cyc, β-cyclocitral; ER, endoplasmic reticulum; FA, fatty acid; FFA, free fatty acid; JA, jasmonic acid; JA-Ile, jasmonoyl-L-isoleucine; MEcPP, 2-C-methyl-D-erythritol 2,4-cyclodiphosphate; MEP, methylerythritol phosphate; Mg-protoIX, Mg–protoporphyrin IX; MOD FA, modified fatty acid;
1O2, singlet oxygen; ORN, oligoribonuclease; PAP, 3-phosphoadenosine 5-phosphate; PhANG, photosynthesis-associated nuclear gene; PTM, PLANT HOMEODOMAIN–TYPE TRANSCRIPTION FACTOR WITH TRANSMEMBRANE DOMAINS; PUB4, U-BOX DOMAIN–CONTAINING PROTEIN 4; ROS, reactive oxygen species; SP1, SUPPRESSOR OF PPI1 LOCUS 1; TOC, translocon at the outer envelope membrane of chloroplasts; UPR, unfolded protein response; UPS, ubiquitin-proteasome system; XRN, 5-3 exoribonuclease.
Chloroplast biogenesis and development in dicotyledonous seedlings alongside germination. Here illustrating epigaeic seedlings.
Fig. 2. Chloroplast biogenesis and development in monocotyledonous seedlings. Example shown for a maize plant. P: proplastid; m: mesophyll cell; bs: bundle sheath cell (TEM pictures generously provided by Klaas vanWijk).
This technology enabled analyses of adhesion between organelles and demonstrated the light-dependent adhesion between peroxisomes,
chloroplasts, and mitochondria as a mechanism for ensuring efficient metabolite flow during photorespiration (83). The physical connection, together with biochemical evidence during photorespiration, demonstrates the central role of organellar homeostasis in responses to metabolic perturbation (136). Thus, there must exist a tightly regulated communication avenue to align proximity and the optimal interdependent functional status of organelles.
Figure 1. Model of retrograde signaling during chloroplast biogenesis. Chloroplasts develop from etioplasts or proplastids in response to light. In the dark and in the etioplasts/proplastids, the plastid-encoded genes are mainly transcribed by NEP, and PET and TBP are not functional (dashed line boxes). During the greening process, activation of PEP plays a major role. PEP activity requires the rpo core components, SIGMA factors (SIG), PEP-associated proteins (PAPs, like pTAC12), and other proteins located in the nucleoid, like PRIN2. PRIN2 is involved in the light regulation of PEPactivity. The disruption of PET, TBP, or PGE generates a signal that is transduced by GUN1. It is to date unknown if the retrograde signal is of a positive nature that is interrupted in the case
of chloroplast disruption (for example, by GUN1) or if the disrupted chloroplasts emit a negative signal (that can be mediated by GUN1). In response to chloroplast signals, PTM is cleaved, and the N-PTM form is translocated to the nucleus where it activates ABI4 expression, inhibiting LHCB expression and promoting the expression of COP1 and genes involved in hypocotyl elongation. In the dark, HY5 is degraded by COP1, which also degrades ABI4. The PIFs repress a set of PhANGs, the GLKs, and genes encoding the nuclear-encoded PEP components. In the light, the light perception by the photoreceptors CRY1 and PHYs causes exclusion of COP1 from the nucleus and degradation of the PIFs. The chloroplast-localized pTAC12 is an essential part of the PEP
complex, but also is processed and translocated to the nucleus. The nuclear pTAC12 interacts with the active form of PHYs (Pfr)
and contributes to PIF degradation. The exclusion of COP1 allows for accumulation of HY5. Degradation of PIFs releases the transcription of the GLKs and other sets of genes, like the genes encoding the PEP component. HY5 and GLKs induce PhANG LHCBs and genes coding TBPenzymes, among others) expression, and repress COP1 and the elongation-related genes. Figure by Daria Chrobok.