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Plant senescence is an integrated program of plant development that aims to remobilize nutrients and energy from senescing tissues to developing organs under developmental and stress-induced conditions. Upstream in the regulatory network, a small family of single-stranded DNA/RNA-binding proteins known as WHIRLYs occupy a central node, acting at multiple regulatory levels and via trans-localization between the nucleus and organelles. In this review, we summarize the current progress on the role of WHIRLY members in plant development and stress-induced senescence. WHIRLY proteins can be traced back in evolution to green algae. WHIRLY proteins trade off the balance of plant developmental senescence and stress-induced senescence through maintaining organelle genome stability via R-loop homeostasis, repressing the transcription at a configuration condition, recruiting RNA to impact organelle RNA editing and splicing, as evidenced in several species, WHIRLY proteins also act as retrograde signal transducers between organelles and the nucleus through protein modification and stromule or vesicle trafficking. In addition, WHIRLY proteins interact with hormones, ROS and environmental signals to orchestrate cell fate in an age-dependent manner. Finally, prospects for further research and promotion to improve crop production under environmental constraints are highlighted.

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Mitochondria are the only organelles regulated by two genomes. The coordinated translation of nuclear DNA (nDNA) and mitochondrial DNA (mtDNA), which together co-encode the subunits of the oxidative phosphorylation (OXPHOS) complex, is critical for determining the metabolic plasticity of tumor cells. RNA-binding protein (RBP) is a post-transcriptional regulatory factor that plays a pivotal role in determining the fate of mRNA. RBP rapidly and effectively reshapes the mitochondrial proteome in response to intracellular and extracellular stressors, mediating the cytoplasmic and mitochondrial translation balance to adjust mitochondrial respiratory capacity and provide energy for tumor cells to adapt to different environmental pressures and growth needs. This review highlights the ability of RBPs to use liquid-liquid phase separation (LLPS) as a platform for translation regulation, integrating nuclear-mitochondrial positive and retrograde signals to coordinate cross-department translation, reshape mitochondrial energy metabolism, and promote the development and survival of tumor cells.

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Communication from plastids to the nucleus via retrograde signal cascades is essential to modulate nuclear gene expression, impacting plant development and environmental responses. Recently, a new class of plastid retrograde signals has emerged, consisting of acyclic and cyclic carotenoids and/or their degradation products, apocarotenoids. Although the biochemical identity of many of the apocarotenoid signals is still under current investigation, the examples described herein demonstrate the central roles that these carotenoid-derived signals play in ensuring plant development and survival. We present recent advances in the discovery of apocarotenoid signals and their role in various plant developmental transitions and environmental stress responses. Moreover, we highlight the emerging data exposing the highly complex signal transduction pathways underlying plastid to nucleus apocarotenoid retrograde signaling cascades. Altogether, this review summarizes the central role of the carotenoid pathway as a major source of retrograde signals in plants.

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The red phytochrome and blue cryptochrome plant photoreceptors play essential roles in promoting genome-wide changes in nuclear and chloroplastic gene expression for photomorphogenesis, plastid development, and greening. While their importance in anterograde signalling has been long recognized, the molecular mechanisms involved remain under active investigation. More recently, the intertwining of the light signalling cascades with the retrograde signals for the optimization of chloroplast functions has been acknowledged. Advances in the field support the participation of phytochromes, cryptochromes, and key light-modulated transcription factors, including HY5 and the PIFs, in the regulation of chloroplastic biochemical pathways that produce retrograde signals, including the tetrapyrroles and the chloroplastic MEP-isoprenoids. Interestingly, in a feedback loop, the photoreceptors and their signalling components are targets themselves of these retrograde signals, aimed at optimizing photomorphogenesis to the status of the chloroplasts, with GUN proteins functioning at the convergence points. High light and shade are also conditions where the photoreceptors tune growth responses to chloroplast functions. Interestingly, photoreceptors and retrograde signals also converge in the modulation of dual-localized proteins (chloroplastic/nuclear) including WHIRLY and HEMERA/pTAC12, whose functions are required for the optimization of photosynthetic activities in changing environments and are proposed to act themselves as retrograde signals.

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Chloroplasts and mitochondria evolved from free-living prokaryotic organisms that entered the eukaryotic cell through endosymbiosis. The gradual conversion from endosymbiont to organelle during the course of evolution was accompanied by the development of a communication system between the host and the endosymbiont, referred to as retrograde signaling or organelle-to-nucleus signaling. In higher plants, plastid-to-nucleus signaling involves multiple signaling pathways necessary to coordinate plastid function and cellular responses to developmental and environmental stimuli. Phylogenetic reconstructions using sequence information from evolutionarily diverse photosynthetic eukaryotes have begun to provide information about how retrograde signaling pathways were adopted and modified in different lineages over time. A tight communication system was likely a major facilitator of plants conquest of the land because it would have enabled the algal ancestors of land plants to better allocate their cellular resources in response to high light and desiccation, the major stressor for streptophyte algae in a terrestrial habitat. In this review, we aim to give an evolutionary perspective on plastid-to-nucleus signaling.

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Iron (Fe) is an essential micronutrient for plants and is present abundantly in the Earth's crust. However, Fe bioavailability in alkaline soils is low due to the decreased solubility of the ferric ions. Previously, we have demonstrated the relationship between the PAP/SAL1 retrograde signaling pathway, the activity of Strategy I Fe uptake genes (FIT, FRO2, IRT1), and ethylene signaling. In this work, we have characterized mutant lines that are deficient in this retrograde signaling pathway and their ability to grow in alkaline soils. This adverse growth condition caused less impact on mutant plants, which showed less reduced rosette area, and higher carotenoid, chlorophyll and Fe content than wild-type plants. Several genes involved in the biosynthesis and excretion of secondary metabolites derived from the phenylpropanoid pathway, which improve Fe uptake, were elevated in mutant plants. Finally, we observed an increase in excreted fluorescent phenolic compounds in mutant lines compared to wild-type plants. In this way, PAP/SAL1 mutants showed alterations in the biosynthesis of metabolites that mobilize Fe, which ultimately improved these plants ability to grow in alkaline soils. Results agree with the existence of a link between the PAP/SAL1 retrograde signaling pathway and the regulation of Fe deficiency responses in Arabidopsis.

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The transition from an engulfed autonomous unicellular photosynthetic bacterium to a semiautonomous endosymbiont plastid was accompanied by the transfer of genetic material from the endosymbiont to the nuclear genome of the host, followed by the establishment of plastid-to-nucleus (retrograde) signaling. The retrograde coordinated activities of the two subcellular genomes ensure chloroplast biogenesis and function as the photosynthetic hub and sensing and signaling center that tailors growth-regulating and adaptive processes. This review specifically focuses on the current knowledge of selected stress-induced retrograde signals, genomes uncoupled 1 (GUN1), methylerythritol cyclodiphosphate (MEcPP), apocarotenoid and ß-cyclocitral, and 3'-phosphoadenosine 5'-phosphate (PAP), which evolved to establish the photoautotrophic lifestyle and are instrumental in the integration of light and hormonal signaling networks to ultimately fashion adaptive responses in an ever-changing environment.

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Plants have a high level of developmental plasticity that allows them to respond and adapt to changes in the environment. Among the environmental cues, light controls almost every aspect of A. thaliana's life cycle, including seed maturation, seed germination, seedling de-etiolation and flowering time. Light signals induce massive reprogramming of gene expression, producing changes in RNA polymerase II transcription, alternative splicing, and chromatin state. Since splicing reactions occur mainly while transcription takes place, the regulation of RNAPII transcription has repercussions in the splicing outcomes. This cotranscriptional nature allows a functional coupling between transcription and splicing, in which properties of the splicing reactions are affected by the transcriptional process. Chromatin landscapes influence both transcription and splicing. In this review, we highlight, summarize and discuss recent progress in the field to gain a comprehensive insight on the cross-regulation between chromatin state, RNAPII transcription and splicing decisions in plants, with a special focus on light-triggered responses. We also introduce several examples of transcription and splicing factors that could be acting as coupling factors in plants. Unravelling how these connected regulatory networks operate, can help in the design of better crops with higher productivity and tolerance.

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Increased temperatures caused by global warming threaten agricultural production, as warmer conditions can inhibit plant growth and development or even destroy crops in extreme circumstances. Extensive research over the past several decades has revealed that chloroplasts, the photosynthetic organelles of plants, are highly sensitive to heat stress, which affects a variety of photosynthetic processes including chlorophyll biosynthesis, photochemical reactions, electron transport, and CO2 assimilation. Important mechanisms by which plant cells respond to heat stress to protect these photosynthetic organelles have been identified and analyzed. More recent studies have made it clear that chloroplasts play an important role in inducing the expression of nuclear heat-response genes during the heat stress response. In this review, we summarize these important advances in plant-based research and discuss how the sensitivity, responses, and signaling roles of chloroplasts contribute to plant heat sensitivity and tolerance.

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KEY MESSAGE: There is a link between PAP/SAL retrograde pathway, ethylene signaling and Fe metabolism in Arabidopsis. Nuclear gene expression is regulated by a diversity of retrograde signals that travel from organelles to the nucleus in a lineal or classical model. One such signal molecule is 3'-phosphoadenisine-5'-phosphate (PAP) and it's in vivo levels are regulated by SAL1/FRY1, a phosphatase enzyme located in chloroplast and mitochondria. This metabolite inhibits the action of a group of exorribonucleases which participate in post-transcriptional gene expression regulation. Transcriptome analysis of Arabidopsis thaliana mutant plants in PAP-SAL1 pathway revealed that the ferritin genes AtFER1, AtFER3, and AtFER4 are up-regulated. In this work we studied Fe metabolism in three different mutants of the PAP/SAL1 retrograde pathway. Mutant plants showed increased Fe accumulation in roots, shoots and seeds when grown in Fe-sufficient condition, and a constitutive activation of the Strategy I Fe uptake genes. As a consequence, they grew more vigorously than wild type plants in Fe-deficient medium. However, when mutant plants grown in Fe-deficient conditions were sprayed with Fe in their leaves, they were unable to deactivate root Fe uptake. Ethylene synthesis inhibition revert the constitutive Fe uptake phenotype. We propose that there is a link between PAP/SAL pathway, ethylene signaling and Fe metabolism.

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Light is a major environmental factor regulating flowering time, thus ensuring reproductive success of higher plants. In contrast to our detailed understanding of light quality and photoperiod mechanisms involved, the molecular basis underlying high light-promoted flowering remains elusive. Here we show that, in Arabidopsis, a chloroplast-derived signal is critical for high light-regulated flowering mediated by the FLOWERING LOCUS C (FLC). We also demonstrate that PTM, a PHD transcription factor involved in chloroplast retrograde signaling, perceives such a signal and mediates transcriptional repression of FLC through recruitment of FVE, a component of the histone deacetylase complex. Thus, our data suggest that chloroplasts function as essential sensors of high light to regulate flowering and adaptive responses by triggering nuclear transcriptional changes at the chromatin level.

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The general stress response (GSR) is an evolutionarily conserved rapid and transient transcriptional reprograming of genes central for transducing environmental signals into cellular responses, leading to metabolic and physiological readjustments to cope with prevailing conditions. Defining the regulatory components of the GSR will provide crucial insight into the design principles of early stress-response modules and their role in orchestrating master regulators of adaptive responses. Overaccumulation of methylerythritol cyclodiphosphate (MEcPP), a bifunctional chemical entity serving as both a precursor of isoprenoids produced by the plastidial methylerythritol phosphate (MEP) pathway and a stress-specific retrograde signal, in ceh1 (constitutively expressing hydroperoxide lyase1)-mutant plants leads to large-scale transcriptional alterations. Bioinformatic analyses of microarray data in ceh1 plants established the overrepresentation of a stress-responsive cis element and key GSR marker, the rapid stress response element (RSRE), in the promoters of robustly induced genes. ceh1 plants carrying an established 4×RSRE:Luciferase reporter for monitoring the GSR support constitutive activation of the response in this mutant background. Genetics and pharmacological approaches confirmed the specificity of MEcPP in RSRE induction via the transcription factor CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3), in a calcium-dependent manner. Moreover, CAMTA3-dependent activation of IRE1a (inositol-requiring protein-1) and bZIP60 (basic leucine zipper 60), two RSRE containing unfolded protein-response genes, bridges MEcPP-mediated GSR induction to the potentiation of protein-folding homeostasis in the endoplasmic reticulum. These findings introduce the notion of transcriptional regulation by a key plastidial retrograde signaling metabolite that induces nuclear GSR, thereby offering a window into the role of interorgannellar communication in shaping cellular adaptive responses.

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INCREASED SIZE EXCLUSION LIMIT 2 (ISE2) encodes a putative DEVH-box RNA helicase originally identified through a genetic screening for Arabidopsis mutants altered in plasmodesmata (PD) aperture. Depletion of ISE2 also affects chloroplasts activity, decreases accumulation of photosynthetic pigments and alters expression of photosynthetic genes. In this work, we show the chloroplast localization of ISE2 and decipher its role in plastidic RNA processing and, consequently, PD function. Group II intron-containing RNAs from chloroplasts exhibit defective splicing in ise2 mutants and ISE2-silenced plants, compromising plastid viability. Furthermore, RNA immunoprecipitation suggests that ISE2 binds in vivo to several splicing-regulated RNAs. Finally, we show that the chloroplast clpr2 mutant (defective in a subunit of a plastidic Clp protease) also exhibits abnormal PD function during embryogenesis, supporting the idea that chloroplast RNA processing is required to regulate cell-cell communication in plants.

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Changes in the developmental or metabolic state of plastids can trigger profound changes in the transcript profiles of nuclear genes. Many nuclear transcription factors were shown to be controlled by signals generated in the organelles. In addition to the many different compounds for which an involvement in retrograde signaling is discussed, accumulating evidence suggests a role for proteins in plastid-to-nucleus communication. These proteins might be sequestered in the plastids before they act as transcriptional regulators in the nucleus. Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids. Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated. Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

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