scholarly journals Dual-targeted transcription factors are required for optimal photosynthesis and stress responses in Arabidopsis thaliana

2019 ◽  
Author(s):  
Piotr Gawroński ◽  
Paweł Burdiak ◽  
Lars B. Scharff ◽  
Jakub Mielecki ◽  
Magdalena Zaborowska ◽  
...  

SummaryChloroplast to nucleus retrograde signaling is essential for cell function, acclimation to fluctuating environmental conditions, plant growth and development. The vast majority of chloroplast proteins are nuclear-encoded and must be imported into the organelle after synthesis in the cytoplasm. This import is essential for the development of fully functional chloroplasts. On the other hand, functional chloroplasts act as sensors of environmental changes and can trigger acclimatory responses that influence nuclear gene expression. Signaling via mobile transcription factors (TFs) has been recently recognized as a way of communication between organelles and the nucleus. In this study, we performed a targeted reverse genetic screen to identify novel dual-localized TFs involved in chloroplast retrograde signaling during stress responses. We found that CHLOROPLAST IMPORT APPARATUS 2 (CIA2), a TF with putative plastid transit peptide can be detected in chloroplasts and the nucleus. Further, we found that CIA2, along with its homolog CIA2-like (CIL) act in an unequally redundant manner and are involved in the regulation of Arabidopsis responses to UV-AB, high light, and heat shock. Finally, our results suggest that both CIA2 and CIL are crucial for chloroplast translation. Our results contribute to a deeper understanding of signaling events in the chloroplast-nucleus cross-talk.SignificanceWe found that a transcription factor CIA2 can be located in chloroplasts and nucleus. CIA2 and is close homolog CIL are involved in protein translation and abiotic stress responses, and we suggest that they play an essential role in retrograde signaling between these organelles.

2021 ◽  
Author(s):  
Ky Young Park ◽  
So Yeon Seo

Chloroplasts play a pivotal role in biotic and abiotic stress responses, accompanying changes in the cell reduction/oxidation (redox) state. Chloroplasts are an endosymbiotic organelle that sends retrograde signals to the nucleus to integrate with environmental changes. This study showed that salt stress causes the rapid accumulation of the nonexpressor of pathogenesis-related genes 1 (NPR1) protein, a redox-sensitive transcription coactivator that elicits many tolerance responses in chloroplasts and the nucleus. The transiently accumulated chloroplast NPR1 protein was translocated to the nucleus in a redox-dependent manner under salinity stress. In addition, immunoblotting and fluorescence image analysis showed that chloroplast-targeted NPR1-GFP fused with cTP (chloroplast transit peptide from RbcS) was localized in the nucleus during the responses to salt stress. Chloroplast functionality was essential for retrograde translocation, in which the stomules and cytoplasmic vesicles participated. Treatments with H2O2 and an ethylene precursor enhanced this retrograde translocation. Compared to each wild-type plant, retrograde signaling-related gene expression was severely impaired in the npr1-1 mutant in Arabidopsis, but enhanced transiently in the NPR1-Ox transgenic tobacco line. Therefore, NPR1 might be a retrograde signaling hub that improves a plant's adaptability to changing environments.


2020 ◽  
Vol 0 (0) ◽  
Author(s):  
Daniel Wittmann ◽  
Neha Sinha ◽  
Bernhard Grimm

AbstractPlastids are specialized organelles found in plants, which are endowed with their own genomes, and differ in many respects from the intracellular compartments of organisms belonging to other kingdoms of life. They differentiate into diverse, plant organ-specific variants, and are perhaps the most versatile organelles known. Chloroplasts are the green plastids in the leaves and stems of plants, whose primary function is photosynthesis. In response to environmental changes, chloroplasts use several mechanisms to coordinate their photosynthetic activities with nuclear gene expression and other metabolic pathways. Here, we focus on a redox-based regulatory network composed of thioredoxins (TRX) and TRX-like proteins. Among multiple redox-controlled metabolic activities in chloroplasts, tetrapyrrole biosynthesis is particularly rich in TRX-dependent enzymes. This review summarizes the effects of plastid-localized reductants on several enzymes of this pathway, which have been shown to undergo dithiol-disulfide transitions. We describe the impact of TRX-dependent control on the activity, stability and interactions of these enzymes, and assess its contribution to the provision of adequate supplies of metabolic intermediates in the face of diurnal and more rapid and transient changes in light levels and other environmental factors.


2016 ◽  
Vol 2 (1) ◽  
Author(s):  
Manti Guha ◽  
Satish Srinivasan ◽  
Kip Guja ◽  
Edison Mejia ◽  
Miguel Garcia-Diaz ◽  
...  

Abstract Reduced mitochondrial DNA copy number, mitochondrial DNA mutations or disruption of electron transfer chain complexes induce mitochondria-to-nucleus retrograde signaling, which induces global change in nuclear gene expression ultimately contributing to various human pathologies including cancer. Recent studies suggest that these mitochondrial changes cause transcriptional reprogramming of nuclear genes although the mechanism of this cross talk remains unclear. Here, we provide evidence that mitochondria-to-nucleus retrograde signaling regulates chromatin acetylation and alters nuclear gene expression through the heterogeneous ribonucleoprotein A2 (hnRNAP2). These processes are reversed when mitochondrial DNA content is restored to near normal cell levels. We show that the mitochondrial stress-induced transcription coactivator hnRNAP2 acetylates Lys 8 of H4 through an intrinsic histone lysine acetyltransferase (KAT) activity with Arg 48 and Arg 50 of hnRNAP2 being essential for acetyl-CoA binding and acetyltransferase activity. H4K8 acetylation at the mitochondrial stress-responsive promoters by hnRNAP2 is essential for transcriptional activation. We found that the previously described mitochondria-to-nucleus retrograde signaling-mediated transformation of C2C12 cells caused an increased expression of genes involved in various oncogenic processes, which is retarded in hnRNAP2 silenced or hnRNAP2 KAT mutant cells. Taken together, these data show that altered gene expression by mitochondria-to-nucleus retrograde signaling involves a novel hnRNAP2-dependent epigenetic mechanism that may have a role in cancer and other pathologies.


2015 ◽  
Vol 47 (8) ◽  
pp. 299-307 ◽  
Author(s):  
Alessandra Castegna ◽  
Vito Iacobazzi ◽  
Vittoria Infantino

The bidirectional cross talk between nuclear and mitochondrial DNA is essential for cellular homeostasis and proper functioning. Mitochondria depend on nuclear contribution for much of their functionality, but their activities have been recently recognized to control nuclear gene expression as well as cell function in many different ways. Epigenetic mechanisms, which tune gene expression in response to environmental stimuli, are key regulatory events at the interplay between mitochondrial and nuclear interactions. Emerging findings indicate that epigenetic factors can be targets or instruments of mitochondrial-nuclear cross talk. Additionally, the growing interest into mtDNA epigenetic modifications opens new avenues into the interaction mechanisms between mitochondria and nucleus. In this review we summarize the points of mitochondrial and nuclear reciprocal control involving epigenetic factors, focusing on the role of mitochondrial genome and metabolism in shaping epigenetic modulation of gene expression. The relevance of the new findings on the methylation of mtDNA is also highlighted as a new frontier in the complex scenario of mitochondrial-nuclear communication.


2020 ◽  
Vol 117 (12) ◽  
pp. 6918-6927 ◽  
Author(s):  
Liangsheng Wang ◽  
Dario Leister ◽  
Li Guan ◽  
Yi Zheng ◽  
Katja Schneider ◽  
...  

Singlet oxygen (1O2), the major reactive oxygen species (ROS) produced in chloroplasts, has been demonstrated recently to be a highly versatile signal that induces various stress responses. In thefluorescent(flu) mutant, its release causes seedling lethality and inhibits mature plant growth. However, these drastic phenotypes are suppressed when EXECUTER1 (EX1) is absent in theflu ex1double mutant. We identified SAFEGUARD1 (SAFE1) in a screen of ethyl methanesulfonate (EMS) mutagenizedflu ex1plants for suppressor mutants with aflu-like phenotype. Influ ex1 safe1, all1O2-induced responses, including transcriptional rewiring of nuclear gene expression, return to levels, such as, or even higher than, those influ. Without SAFE1, grana margins (GMs) of chloroplast thylakoids (Thys) are specifically damaged upon1O2generation and associate with plastoglobules (PGs). SAFE1 is localized in the chloroplast stroma, and release of1O2induces SAFE1 degradation via chloroplast-originated vesicles. Our paper demonstrates thatflu-produced1O2triggers an EX1-independent signaling pathway and proves that SAFE1 suppresses this signaling pathway by protecting GMs.


2018 ◽  
Author(s):  
Alexey Shapiguzov ◽  
Julia P. Vainonen ◽  
Kerri Hunter ◽  
Helena Tossavainen ◽  
Arjun Tiwari ◽  
...  

AbstractSignaling from chloroplasts and mitochondria, both dependent on reactive oxygen species (ROS), merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). ROS produced in the chloroplasts affect the abundance, thiol redox state and oligomerization of RCD1. RCD1 directly interacts in vivo with ANAC013 and ANAC017 transcription factors, which are the mediators of the ROS-related mitochondrial complex III retrograde signa and suppresses activity of ANAC013 and ANAC017. Inactivation of RCD1 leads to increased expression of ANAC013 and ANAC017-regulated genes belonging to the mitochondrial dysfunction stimulon (MDS), including genes for mitochondrial alternative oxidases (AOXs). Accumulating AOXs and other MDS gene products alter electron transfer pathways in the chloroplasts, leading to diminished production of chloroplastic ROS and increased protection of photosynthetic apparatus from ROS damage. RCD1-dependent regulation affects chloroplastic and mitochondrial retrograde signaling including chloroplast signaling by 3’-phosphoadenosine 5’-phosphate (PAP). Sensitivity of RCD1 to organellar ROS provides feedback control of nuclear gene expression.


Author(s):  
Piting Li ◽  
Zhe Chai ◽  
Pingping Lin ◽  
Chaohua Huang ◽  
Guoqiang Huang ◽  
...  

Abstract Background: APETALA2/ETHYLENE RESPONSIVE FACTOR (AP2/ERF) transcription factors play important roles in plant growth, development, metabolism, as well as in biotic and abiotic stress responses. However, there are few studies concerning AP2/ERF genes in sugarcane, which is the most critical sugar and energy crop worldwide. Results: A total of 218 AP2/ERF genes were identified in the Saccharum spontaneum genome. Phylogenetic analysis showed that these genes could be divided into four groups, including 43 AP2s, 160 ERFs, and Dehydration-responsive element-binding (DREB) factors, 11 ABI3/VPs (RAV) and 4 Soloist genes. These genes were unevenly distributed on 32 chromosomes. Analysis of the structural of SsAP2/ERF genes showed that 91 SsAP2/ERFs lacked introns. Sugarcane and sorghum have a collinear relationship between 168 SsAP2/ERF genes and sorghum AP2/ERF genes that reflects their similarity. Multiple cis-regulatory elements (CREs) are present in the SsAP2/ERF promoter, and many are related to abiotic stresses, suggesting that SsAP2/ERF activity could contribute to the adaptation of sugarcane crops to environmental changes. The tissue-specific analysis showed spatiotemporal expression of SsAP2/ERF in the stems and leaves of sugarcane at different stages of development. In 10 sugarcane samples, 39 SsAP2/ERFs were not expressed at all, whereas 58 SsAP2/ERFs were expressed in all samples. Quantitative PCR experiments showed that SsERF52 expression was up-regulated under salt stress, but suppressed under drought stress. SsSoloist4 had the most considerable upregulation in response to treatment with the exogenous hormones ABA and GA. Within 3 hours of ABA or PEG6000 treatment, SsSoloist4 expression was up-regulated, indicating that this gene could play a role in ABA and GA-associated drought stress response mechanisms. Analysis of AP2/ERF gene expression patterns under different treatments indicated that SsAP2/ERF genes play an important role in drought and salt stress responses of S. spontaneum. Conclusions: In this study, a total of 218 members of the AP2 / ERF superfamily were identified in sugarcane, and their genetic structure, evolution characteristics, and expression patterns were studied and analyzed. The results of this study provide a foundation for future analyses to elucidate the importance of AP2/ERF transcription factors in the function and molecular breeding of sugarcane.


Plants ◽  
2021 ◽  
Vol 10 (2) ◽  
pp. 196
Author(s):  
Takayuki Shimizu ◽  
Tatsuru Masuda

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.


2017 ◽  
Vol 30 (10) ◽  
pp. 829-841 ◽  
Author(s):  
Yasuhiro Ishiga ◽  
Mutsumi Watanabe ◽  
Takako Ishiga ◽  
Takayuki Tohge ◽  
Takakazu Matsuura ◽  
...  

Chloroplasts have a crucial role in plant immunity against pathogens. Increasing evidence suggests that phytopathogens target chloroplast homeostasis as a pathogenicity mechanism. In order to regulate the performance of chloroplasts under stress conditions, chloroplasts produce retrograde signals to alter nuclear gene expression. Many signals for the chloroplast retrograde pathway have been identified, including chlorophyll intermediates, reactive oxygen species, and metabolic retrograde signals. Although there is a reasonably good understanding of chloroplast retrograde signaling in plant immunity, some signals are not well-understood. In order to understand the role of chloroplast retrograde signaling in plant immunity, we investigated Arabidopsis chloroplast retrograde signaling mutants in response to pathogen inoculation. sal1 mutants (fry1-2 and alx8) responsible for the SAL1-PAP retrograde signaling pathway showed enhanced disease symptoms not only to the hemibiotrophic pathogen Pseudomonas syringae pv. tomato DC3000 but, also, to the necrotrophic pathogen Pectobacterium carotovorum subsp. carotovorum EC1. Glucosinolate profiles demonstrated the reduced accumulation of aliphatic glucosinolates in the fry1-2 and alx8 mutants compared with the wild-type Col-0 in response to DC3000 infection. In addition, quantification of multiple phytohormones and analyses of their gene expression profiles revealed that both the salicylic acid (SA)- and jasmonic acid (JA)-mediated signaling pathways were down-regulated in the fry1-2 and alx8 mutants. These results suggest that the SAL1-PAP chloroplast retrograde pathway is involved in plant immunity by regulating the SA- and JA-mediated signaling pathways.


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