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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 proteins as retrograde signals. A few chloroplast proteins have been implicated in directly modulating nuclear gene expression by their nuclear localization. These proteins may transit the cytoplasm by an unknown mechanism. Alternatively, it has also been proposed that they may move through stromules to enter the nucleus. High light, lincomycin or norflurazon treatments induce a serine protease-dependent (blue dot) proteolytic-cleavage of the PTM, a chloroplast envelope-bound plant homeodomain (PHD) transcription factor. The cleavage product is found in the nucleus where it binds to promoter region of the ABI4 transcription factor. ABI4 in turn associates with the regulatory sequences of the Lhcb genes and prevents their transcription. The chloroplast protein Whirly1 also localizes to the nucleus and this is correlated with increased expression of PATHOGENESIS RELATED GENE 1 and 2 (PR1/2). Upon TMV infection the chloroplast-localized NRIP1 is also detected in the nucleus where it interacts with the helicase domain of the TMV replicase (p50). Finally a trimeric complex of p50, NRIP1 and the N protein is localized to nucleus to provide resistance against the virus. It is suggested that NRIP1 may use stromules to translocate from the chloroplast to the nucleus.
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Figure 3: Chloroplast proteins as retrograde signals. A few chloroplast proteins have been implicated in directly modulating nuclear gene expression by their nuclear localization. These proteins may transit the cytoplasm by an unknown mechanism. Alternatively, it has also been proposed that they may move through stromules to enter the nucleus. High light, lincomycin or norflurazon treatments induce a serine protease-dependent (blue dot) proteolytic-cleavage of the PTM, a chloroplast envelope-bound plant homeodomain (PHD) transcription factor. The cleavage product is found in the nucleus where it binds to promoter region of the ABI4 transcription factor. ABI4 in turn associates with the regulatory sequences of the Lhcb genes and prevents their transcription. The chloroplast protein Whirly1 also localizes to the nucleus and this is correlated with increased expression of PATHOGENESIS RELATED GENE 1 and 2 (PR1/2). Upon TMV infection the chloroplast-localized NRIP1 is also detected in the nucleus where it interacts with the helicase domain of the TMV replicase (p50). Finally a trimeric complex of p50, NRIP1 and the N protein is localized to nucleus to provide resistance against the virus. It is suggested that NRIP1 may use stromules to translocate from the chloroplast to the nucleus.

Mentions: One such protein, PTM (PHD type transcription factor with transmembrane domains) was shown to provide a physical link in signaling between chloroplasts and nucleus to regulate gene expression (Sun et al., 2011). This membrane-bound transcription factor (MTF) is localized to chloroplast outer envelope by four transmembrane domains at its C-terminus (Figure 3). The N-terminus of PTM contains a DNA-binding homeodomain box, a different transcription factors (DDT) domain and a plant homeodomain (PHD). Interestingly, a shorter variant of this protein, lacking the transmembrane domains, was detected in nuclear fractions. Notably, increased amounts of the shorter PTM variant were detected upon treatment with either norflurazon or lincomycin, and on exposure to high light. Through the application of protease inhibitors, it was demonstrated that the shorter form of PTM was the result of serine protease activity (Sun et al., 2011; Adam, 2015). According to the proposed model, chloroplast signals induce the intramembrane proteolytic cleavage of full length PTM, producing a soluble shorter variant (∼58 kDa) that is released to the cytoplasm and finally transclocates to the nucleus where it binds, through its PHD domain, to the ABI4 promoter to induce ABI4 expression. ABI4, in turn binds to the Lhcb promoter, close to the CUF1 element and precludes binding of G-box-binding factors required for the expression of Lhcb and other PhANGs. This model explains the gun phenotype observed in ptm and abi4 mutants. Moreover, the amount of processed PTM declined in the gun1 mutant, suggesting a complex regulatory network.


Chloroplast signaling within, between and beyond cells.

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

Chloroplast proteins as retrograde signals. A few chloroplast proteins have been implicated in directly modulating nuclear gene expression by their nuclear localization. These proteins may transit the cytoplasm by an unknown mechanism. Alternatively, it has also been proposed that they may move through stromules to enter the nucleus. High light, lincomycin or norflurazon treatments induce a serine protease-dependent (blue dot) proteolytic-cleavage of the PTM, a chloroplast envelope-bound plant homeodomain (PHD) transcription factor. The cleavage product is found in the nucleus where it binds to promoter region of the ABI4 transcription factor. ABI4 in turn associates with the regulatory sequences of the Lhcb genes and prevents their transcription. The chloroplast protein Whirly1 also localizes to the nucleus and this is correlated with increased expression of PATHOGENESIS RELATED GENE 1 and 2 (PR1/2). Upon TMV infection the chloroplast-localized NRIP1 is also detected in the nucleus where it interacts with the helicase domain of the TMV replicase (p50). Finally a trimeric complex of p50, NRIP1 and the N protein is localized to nucleus to provide resistance against the virus. It is suggested that NRIP1 may use stromules to translocate from the chloroplast to the nucleus.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4593955&req=5

Figure 3: Chloroplast proteins as retrograde signals. A few chloroplast proteins have been implicated in directly modulating nuclear gene expression by their nuclear localization. These proteins may transit the cytoplasm by an unknown mechanism. Alternatively, it has also been proposed that they may move through stromules to enter the nucleus. High light, lincomycin or norflurazon treatments induce a serine protease-dependent (blue dot) proteolytic-cleavage of the PTM, a chloroplast envelope-bound plant homeodomain (PHD) transcription factor. The cleavage product is found in the nucleus where it binds to promoter region of the ABI4 transcription factor. ABI4 in turn associates with the regulatory sequences of the Lhcb genes and prevents their transcription. The chloroplast protein Whirly1 also localizes to the nucleus and this is correlated with increased expression of PATHOGENESIS RELATED GENE 1 and 2 (PR1/2). Upon TMV infection the chloroplast-localized NRIP1 is also detected in the nucleus where it interacts with the helicase domain of the TMV replicase (p50). Finally a trimeric complex of p50, NRIP1 and the N protein is localized to nucleus to provide resistance against the virus. It is suggested that NRIP1 may use stromules to translocate from the chloroplast to the nucleus.
Mentions: One such protein, PTM (PHD type transcription factor with transmembrane domains) was shown to provide a physical link in signaling between chloroplasts and nucleus to regulate gene expression (Sun et al., 2011). This membrane-bound transcription factor (MTF) is localized to chloroplast outer envelope by four transmembrane domains at its C-terminus (Figure 3). The N-terminus of PTM contains a DNA-binding homeodomain box, a different transcription factors (DDT) domain and a plant homeodomain (PHD). Interestingly, a shorter variant of this protein, lacking the transmembrane domains, was detected in nuclear fractions. Notably, increased amounts of the shorter PTM variant were detected upon treatment with either norflurazon or lincomycin, and on exposure to high light. Through the application of protease inhibitors, it was demonstrated that the shorter form of PTM was the result of serine protease activity (Sun et al., 2011; Adam, 2015). According to the proposed model, chloroplast signals induce the intramembrane proteolytic cleavage of full length PTM, producing a soluble shorter variant (∼58 kDa) that is released to the cytoplasm and finally transclocates to the nucleus where it binds, through its PHD domain, to the ABI4 promoter to induce ABI4 expression. ABI4, in turn binds to the Lhcb promoter, close to the CUF1 element and precludes binding of G-box-binding factors required for the expression of Lhcb and other PhANGs. This model explains the gun phenotype observed in ptm and abi4 mutants. Moreover, the amount of processed PTM declined in the gun1 mutant, suggesting a complex regulatory network.

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