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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.


Mechanisms of chloroplast-to-nucleus signaling. (A) Retrograde signaling by PAP. High light or drought stress inhibits SAL1 phosphatase and leads to the accumulation of PAP. PAP likely inhibits specific exoribonucleases (XRNs) to modify nuclear genes expression. APX2 and ELIP2 stand for ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2 genes, respectively. (B) Retrograde signaling by MEcPP. High light or wounding inhibits 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS), leading to the subsequent accumulation of MEcPP. MEcPP affects nuclear gene expression via a mechanism proposed to involve chromatin remodeling by destabilizing DNA-histone interactions. HPL and ICS1 stand for HYDROPEROXIDE LYASE and ISOCHORISMATE SYNTHASE 1genes, respectively. (C) Carotenoid-derivative β-cyclocitral mediates retrograde signaling. The ROS singlet oxygen induces formation of β-cyclocitral during high light treatment. β-cyclocitral’s action on selected nuclear genes is proposed to involve proteins containing sulphydryl groups. The genes depicted are GLUTATHIONE-S-TRANSPHERASE (GST) and UDP-glycosyltransferase.(D) An unidentified apocarotenoid affects expression of nuclear genes. It is proposed that the putative signaling apocarotenoid accumulates in chloroplasts due to compromised ζ-carotene desaturase activity that results in accumulation of phytofluene and ζ-carotene, putative substrates for the carotenoid cleavage deoxygenase 4 (CCD4) enzyme that is prerequisite for the putative apocarotenoid synthesis. CHLH, Lhcb1.3, rbcs and PC stand for genes encoding the subunit H of the Mg-chelatase complex, light-harvesting complex 1.3 isoform, the Rubisco small subunit and plastocyanin, respectively.
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Figure 2: Mechanisms of chloroplast-to-nucleus signaling. (A) Retrograde signaling by PAP. High light or drought stress inhibits SAL1 phosphatase and leads to the accumulation of PAP. PAP likely inhibits specific exoribonucleases (XRNs) to modify nuclear genes expression. APX2 and ELIP2 stand for ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2 genes, respectively. (B) Retrograde signaling by MEcPP. High light or wounding inhibits 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS), leading to the subsequent accumulation of MEcPP. MEcPP affects nuclear gene expression via a mechanism proposed to involve chromatin remodeling by destabilizing DNA-histone interactions. HPL and ICS1 stand for HYDROPEROXIDE LYASE and ISOCHORISMATE SYNTHASE 1genes, respectively. (C) Carotenoid-derivative β-cyclocitral mediates retrograde signaling. The ROS singlet oxygen induces formation of β-cyclocitral during high light treatment. β-cyclocitral’s action on selected nuclear genes is proposed to involve proteins containing sulphydryl groups. The genes depicted are GLUTATHIONE-S-TRANSPHERASE (GST) and UDP-glycosyltransferase.(D) An unidentified apocarotenoid affects expression of nuclear genes. It is proposed that the putative signaling apocarotenoid accumulates in chloroplasts due to compromised ζ-carotene desaturase activity that results in accumulation of phytofluene and ζ-carotene, putative substrates for the carotenoid cleavage deoxygenase 4 (CCD4) enzyme that is prerequisite for the putative apocarotenoid synthesis. CHLH, Lhcb1.3, rbcs and PC stand for genes encoding the subunit H of the Mg-chelatase complex, light-harvesting complex 1.3 isoform, the Rubisco small subunit and plastocyanin, respectively.

Mentions: The detailed analysis of sal1, an Arabidopsis phosphonucleotidase mutant, has identified a known second messenger as acting in chloroplast-to-nucleus signaling. Estavillo et al. (2011) have demonstrated that the chloroplast and mitochondria-localized SAL1 phosphatase regulates the steady-state level of 3′-phosphoadenosine 5′-phosphate (PAP) by dephosphorylating it to an adenosine monophosphate (AMP). In the sal1 mutant, or in response to drought stress or high light intensity, PAP levels increased, inducing expression of ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2, two nuclear genes whose expression is induced by high light stress (Harari-Steinberg et al., 2001; Caverzan et al., 2012). It has been proposed that PAP travels from chloroplasts to the nucleus where it regulates nuclear gene expression. Nucleus-localized exoribonucleases (XRNs) are likely targets of PAP, and by repressing their activity PAP may stimulate expression of high light and drought-responsive genes, leading to increased tolerance (Estavillo et al., 2011; Figure 2A).


Chloroplast signaling within, between and beyond cells.

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

Mechanisms of chloroplast-to-nucleus signaling. (A) Retrograde signaling by PAP. High light or drought stress inhibits SAL1 phosphatase and leads to the accumulation of PAP. PAP likely inhibits specific exoribonucleases (XRNs) to modify nuclear genes expression. APX2 and ELIP2 stand for ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2 genes, respectively. (B) Retrograde signaling by MEcPP. High light or wounding inhibits 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS), leading to the subsequent accumulation of MEcPP. MEcPP affects nuclear gene expression via a mechanism proposed to involve chromatin remodeling by destabilizing DNA-histone interactions. HPL and ICS1 stand for HYDROPEROXIDE LYASE and ISOCHORISMATE SYNTHASE 1genes, respectively. (C) Carotenoid-derivative β-cyclocitral mediates retrograde signaling. The ROS singlet oxygen induces formation of β-cyclocitral during high light treatment. β-cyclocitral’s action on selected nuclear genes is proposed to involve proteins containing sulphydryl groups. The genes depicted are GLUTATHIONE-S-TRANSPHERASE (GST) and UDP-glycosyltransferase.(D) An unidentified apocarotenoid affects expression of nuclear genes. It is proposed that the putative signaling apocarotenoid accumulates in chloroplasts due to compromised ζ-carotene desaturase activity that results in accumulation of phytofluene and ζ-carotene, putative substrates for the carotenoid cleavage deoxygenase 4 (CCD4) enzyme that is prerequisite for the putative apocarotenoid synthesis. CHLH, Lhcb1.3, rbcs and PC stand for genes encoding the subunit H of the Mg-chelatase complex, light-harvesting complex 1.3 isoform, the Rubisco small subunit and plastocyanin, respectively.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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Figure 2: Mechanisms of chloroplast-to-nucleus signaling. (A) Retrograde signaling by PAP. High light or drought stress inhibits SAL1 phosphatase and leads to the accumulation of PAP. PAP likely inhibits specific exoribonucleases (XRNs) to modify nuclear genes expression. APX2 and ELIP2 stand for ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2 genes, respectively. (B) Retrograde signaling by MEcPP. High light or wounding inhibits 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS), leading to the subsequent accumulation of MEcPP. MEcPP affects nuclear gene expression via a mechanism proposed to involve chromatin remodeling by destabilizing DNA-histone interactions. HPL and ICS1 stand for HYDROPEROXIDE LYASE and ISOCHORISMATE SYNTHASE 1genes, respectively. (C) Carotenoid-derivative β-cyclocitral mediates retrograde signaling. The ROS singlet oxygen induces formation of β-cyclocitral during high light treatment. β-cyclocitral’s action on selected nuclear genes is proposed to involve proteins containing sulphydryl groups. The genes depicted are GLUTATHIONE-S-TRANSPHERASE (GST) and UDP-glycosyltransferase.(D) An unidentified apocarotenoid affects expression of nuclear genes. It is proposed that the putative signaling apocarotenoid accumulates in chloroplasts due to compromised ζ-carotene desaturase activity that results in accumulation of phytofluene and ζ-carotene, putative substrates for the carotenoid cleavage deoxygenase 4 (CCD4) enzyme that is prerequisite for the putative apocarotenoid synthesis. CHLH, Lhcb1.3, rbcs and PC stand for genes encoding the subunit H of the Mg-chelatase complex, light-harvesting complex 1.3 isoform, the Rubisco small subunit and plastocyanin, respectively.
Mentions: The detailed analysis of sal1, an Arabidopsis phosphonucleotidase mutant, has identified a known second messenger as acting in chloroplast-to-nucleus signaling. Estavillo et al. (2011) have demonstrated that the chloroplast and mitochondria-localized SAL1 phosphatase regulates the steady-state level of 3′-phosphoadenosine 5′-phosphate (PAP) by dephosphorylating it to an adenosine monophosphate (AMP). In the sal1 mutant, or in response to drought stress or high light intensity, PAP levels increased, inducing expression of ASCORBATE PEROXIDASE 2 and EARLY LIGHT INDUCIBLE PROTEIN 2, two nuclear genes whose expression is induced by high light stress (Harari-Steinberg et al., 2001; Caverzan et al., 2012). It has been proposed that PAP travels from chloroplasts to the nucleus where it regulates nuclear gene expression. Nucleus-localized exoribonucleases (XRNs) are likely targets of PAP, and by repressing their activity PAP may stimulate expression of high light and drought-responsive genes, leading to increased tolerance (Estavillo et al., 2011; Figure 2A).

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.