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Chloroplast signaling within, between and beyond cells.

Bobik K, Burch-Smith TM - Front Plant Sci (2015)

Bottom Line: Another important role of the plastid we will discuss is the involvement of plastid signaling in biotic and abiotic stress that, in addition to influencing retrograde signaling, has direct effects on several cellular compartments including the cell wall.Thus, accumulating evidence highlights that chloroplasts, with their complex signaling pathways, provide a mechanism for exquisite regulation of plant development, metabolism and responses to the environment.As chloroplast processes are targeted for engineering for improved productivity the effect of such modifications on chloroplast signaling will have to be carefully considered in order to avoid unintended consequences on plant growth and development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville TN, USA.

ABSTRACT
The most conspicuous function of plastids is the oxygenic photosynthesis of chloroplasts, yet plastids are super-factories that produce a plethora of compounds that are indispensable for proper plant physiology and development. Given their origins as free-living prokaryotes, it is not surprising that plastids possess their own genomes whose expression is essential to plastid function. This semi-autonomous character of plastids requires the existence of sophisticated regulatory mechanisms that provide reliable communication between them and other cellular compartments. Such intracellular signaling is necessary for coordinating whole-cell responses to constantly varying environmental cues and cellular metabolic needs. This is achieved by plastids acting as receivers and transmitters of specific signals that coordinate expression of the nuclear and plastid genomes according to particular needs. In this review we will consider the so-called retrograde signaling occurring between plastids and nuclei, and between plastids and other organelles. Another important role of the plastid we will discuss is the involvement of plastid signaling in biotic and abiotic stress that, in addition to influencing retrograde signaling, has direct effects on several cellular compartments including the cell wall. We will also review recent evidence pointing to an intriguing function of chloroplasts in regulating intercellular symplasmic transport. Finally, we consider an intriguing yet less widely known aspect of plant biology, chloroplast signaling from the perspective of the entire plant. Thus, accumulating evidence highlights that chloroplasts, with their complex signaling pathways, provide a mechanism for exquisite regulation of plant development, metabolism and responses to the environment. As chloroplast processes are targeted for engineering for improved productivity the effect of such modifications on chloroplast signaling will have to be carefully considered in order to avoid unintended consequences on plant growth and development.

No MeSH data available.


Related in: MedlinePlus

Chloroplast behavior during defense. (A) Stromules (arrows) are observed intermittently from chloroplasts in the epidermis of Nicotiana benthamiana leaves. (B) Upon infection with Tobacco mosaic virus, chloroplasts cluster around the nucleus (asterisk), and stromule formation is induced (arrow). The chloroplasts shown are expressing NRIP1-CFP (Caplan et al., 2008, 2015). Note the NRIP1-CFP signal detected in the nucleus in TMV-infected chloroplasts, indicative of the translocation of NRIP1 from the chloroplasts to the nucleus. Images were collected on a Zeiss LSM 710 confocal laser scanning microscope and single focal plane images are shown. Scale bar is 10 μm.
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Figure 5: Chloroplast behavior during defense. (A) Stromules (arrows) are observed intermittently from chloroplasts in the epidermis of Nicotiana benthamiana leaves. (B) Upon infection with Tobacco mosaic virus, chloroplasts cluster around the nucleus (asterisk), and stromule formation is induced (arrow). The chloroplasts shown are expressing NRIP1-CFP (Caplan et al., 2008, 2015). Note the NRIP1-CFP signal detected in the nucleus in TMV-infected chloroplasts, indicative of the translocation of NRIP1 from the chloroplasts to the nucleus. Images were collected on a Zeiss LSM 710 confocal laser scanning microscope and single focal plane images are shown. Scale bar is 10 μm.

Mentions: The question of why stromule induction and chloroplast-nucleus associations occur during plant–pathogen interactions has recently been addressed. Nicotiana N RECEPTOR INTERACTING PROTEIN (NRIP)1 is a chloroplast rhodanese sulphurtransferase that is required for effector triggered immunity (ETI) against TMV mediated by the N innate immune receptor (Caplan et al., 2008). In the presence of the viral p50 helicase effector NRIP1 was recruited to the cytoplasm and nucleus where it formed a protein complex with the TIR domain of the N immune receptor (Figure 3). The interaction with N in the nucleus and cytoplasm is necessary for ETI. These results raised the intriguing questions of whether NRIP1was remobilized from the chloroplast and how this could be accomplished. Recent data suggest that stromules may provide a route for NRIP to traffic from the chloroplast to the nucleus. Co-expression of N and p50 induced formation of stroumles during HR-PCD associated with this interaction (Caplan et al., 2015; Figure 5). Similarly, stromule induction was observed during ETI initiated in response to bacterial pathogens, and on treatment with the defense-related signaling molecules SA and the ROS H2O2. Through correlative EM-fluorescence microscopy, the authors provide convincing evidence that stromules contact the nucleus during N-mediated defense. In elegant experiments that fuse a nuclear exclusion sequence (NES) to NRIP, the authors provide quantitative evidence that NRIP1 is indeed trafficked from the chloroplast to the nucleus. H2O2 also traffics to the nucleus via stromules. In plants overexpressing chloroplast outer membrane protein CHLOROPLAST UNUSUAL POSITIONING 1 (CHUP1) stromule formation is abolished, suggesting that this membrane plays a role in stromule formation. This was confirmed in chup mutants and knockdown plants, where constitutive stromule formation was observed. The importance of stromules to HR-PCD and the defense response was underscored by the accelerated HR-PCD observed in those plants. These results are suggestive of a role for stromules in intracellular trafficking and possibly signaling during plant–pathogen interactions, and these possibilities warrant further examination. It will be exciting to test whether plastids and/or stromules are able to create hemifusion membranes with the nuclear membrane and whether other signaling molecules or metabolites use this route for chloroplast signaling.


Chloroplast signaling within, between and beyond cells.

Bobik K, Burch-Smith TM - Front Plant Sci (2015)

Chloroplast behavior during defense. (A) Stromules (arrows) are observed intermittently from chloroplasts in the epidermis of Nicotiana benthamiana leaves. (B) Upon infection with Tobacco mosaic virus, chloroplasts cluster around the nucleus (asterisk), and stromule formation is induced (arrow). The chloroplasts shown are expressing NRIP1-CFP (Caplan et al., 2008, 2015). Note the NRIP1-CFP signal detected in the nucleus in TMV-infected chloroplasts, indicative of the translocation of NRIP1 from the chloroplasts to the nucleus. Images were collected on a Zeiss LSM 710 confocal laser scanning microscope and single focal plane images are shown. Scale bar is 10 μm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4593955&req=5

Figure 5: Chloroplast behavior during defense. (A) Stromules (arrows) are observed intermittently from chloroplasts in the epidermis of Nicotiana benthamiana leaves. (B) Upon infection with Tobacco mosaic virus, chloroplasts cluster around the nucleus (asterisk), and stromule formation is induced (arrow). The chloroplasts shown are expressing NRIP1-CFP (Caplan et al., 2008, 2015). Note the NRIP1-CFP signal detected in the nucleus in TMV-infected chloroplasts, indicative of the translocation of NRIP1 from the chloroplasts to the nucleus. Images were collected on a Zeiss LSM 710 confocal laser scanning microscope and single focal plane images are shown. Scale bar is 10 μm.
Mentions: The question of why stromule induction and chloroplast-nucleus associations occur during plant–pathogen interactions has recently been addressed. Nicotiana N RECEPTOR INTERACTING PROTEIN (NRIP)1 is a chloroplast rhodanese sulphurtransferase that is required for effector triggered immunity (ETI) against TMV mediated by the N innate immune receptor (Caplan et al., 2008). In the presence of the viral p50 helicase effector NRIP1 was recruited to the cytoplasm and nucleus where it formed a protein complex with the TIR domain of the N immune receptor (Figure 3). The interaction with N in the nucleus and cytoplasm is necessary for ETI. These results raised the intriguing questions of whether NRIP1was remobilized from the chloroplast and how this could be accomplished. Recent data suggest that stromules may provide a route for NRIP to traffic from the chloroplast to the nucleus. Co-expression of N and p50 induced formation of stroumles during HR-PCD associated with this interaction (Caplan et al., 2015; Figure 5). Similarly, stromule induction was observed during ETI initiated in response to bacterial pathogens, and on treatment with the defense-related signaling molecules SA and the ROS H2O2. Through correlative EM-fluorescence microscopy, the authors provide convincing evidence that stromules contact the nucleus during N-mediated defense. In elegant experiments that fuse a nuclear exclusion sequence (NES) to NRIP, the authors provide quantitative evidence that NRIP1 is indeed trafficked from the chloroplast to the nucleus. H2O2 also traffics to the nucleus via stromules. In plants overexpressing chloroplast outer membrane protein CHLOROPLAST UNUSUAL POSITIONING 1 (CHUP1) stromule formation is abolished, suggesting that this membrane plays a role in stromule formation. This was confirmed in chup mutants and knockdown plants, where constitutive stromule formation was observed. The importance of stromules to HR-PCD and the defense response was underscored by the accelerated HR-PCD observed in those plants. These results are suggestive of a role for stromules in intracellular trafficking and possibly signaling during plant–pathogen interactions, and these possibilities warrant further examination. It will be exciting to test whether plastids and/or stromules are able to create hemifusion membranes with the nuclear membrane and whether other signaling molecules or metabolites use this route for chloroplast signaling.

Bottom Line: Another important role of the plastid we will discuss is the involvement of plastid signaling in biotic and abiotic stress that, in addition to influencing retrograde signaling, has direct effects on several cellular compartments including the cell wall.Thus, accumulating evidence highlights that chloroplasts, with their complex signaling pathways, provide a mechanism for exquisite regulation of plant development, metabolism and responses to the environment.As chloroplast processes are targeted for engineering for improved productivity the effect of such modifications on chloroplast signaling will have to be carefully considered in order to avoid unintended consequences on plant growth and development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville TN, USA.

ABSTRACT
The most conspicuous function of plastids is the oxygenic photosynthesis of chloroplasts, yet plastids are super-factories that produce a plethora of compounds that are indispensable for proper plant physiology and development. Given their origins as free-living prokaryotes, it is not surprising that plastids possess their own genomes whose expression is essential to plastid function. This semi-autonomous character of plastids requires the existence of sophisticated regulatory mechanisms that provide reliable communication between them and other cellular compartments. Such intracellular signaling is necessary for coordinating whole-cell responses to constantly varying environmental cues and cellular metabolic needs. This is achieved by plastids acting as receivers and transmitters of specific signals that coordinate expression of the nuclear and plastid genomes according to particular needs. In this review we will consider the so-called retrograde signaling occurring between plastids and nuclei, and between plastids and other organelles. Another important role of the plastid we will discuss is the involvement of plastid signaling in biotic and abiotic stress that, in addition to influencing retrograde signaling, has direct effects on several cellular compartments including the cell wall. We will also review recent evidence pointing to an intriguing function of chloroplasts in regulating intercellular symplasmic transport. Finally, we consider an intriguing yet less widely known aspect of plant biology, chloroplast signaling from the perspective of the entire plant. Thus, accumulating evidence highlights that chloroplasts, with their complex signaling pathways, provide a mechanism for exquisite regulation of plant development, metabolism and responses to the environment. As chloroplast processes are targeted for engineering for improved productivity the effect of such modifications on chloroplast signaling will have to be carefully considered in order to avoid unintended consequences on plant growth and development.

No MeSH data available.


Related in: MedlinePlus