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Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast.

Estavillo GM, Chan KX, Phua SY, Pogson BJ - Front Plant Sci (2013)

Bottom Line: Many signals of different chemical nature have been described in the past decades, including chlorophyll intermediates, reactive oxygen species (ROS), and adenosine derivatives.While the effects of retrograde signaling on gene expression are well understood, the initiation and transport of the signals and their mode of action have either not been resolved, or are a matter of speculation.Here we summarize current plastid retrograde signaling models in plants, with a focus on new signaling pathways, SAL1-PAP, methylerythritol cyclodiphosphate (MEcPP), and β-cyclocitral (β-CC), and outline missing links or future areas of research that we believe need to be addressed to have a better understanding of plant intracellular signaling networks.

View Article: PubMed Central - PubMed

Affiliation: ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University Canberra, ACT, Australia.

ABSTRACT
Plant organelles produce retrograde signals to alter nuclear gene expression in order to coordinate their biogenesis, maintain homeostasis, or optimize their performance under adverse conditions. Many signals of different chemical nature have been described in the past decades, including chlorophyll intermediates, reactive oxygen species (ROS), and adenosine derivatives. While the effects of retrograde signaling on gene expression are well understood, the initiation and transport of the signals and their mode of action have either not been resolved, or are a matter of speculation. Moreover, retrograde signaling should be considered as part of a broader cellular network, instead of as separate pathways, required to adjust to changing physiologically relevant conditions. Here we summarize current plastid retrograde signaling models in plants, with a focus on new signaling pathways, SAL1-PAP, methylerythritol cyclodiphosphate (MEcPP), and β-cyclocitral (β-CC), and outline missing links or future areas of research that we believe need to be addressed to have a better understanding of plant intracellular signaling networks.

No MeSH data available.


Related in: MedlinePlus

New metabolic retrograde signaling pathways. The different components of recently discovered plant retrograde signaling pathways are shown. (A) β-CC is most likely produced by oxidation of carotenes by 1O2 in the chloroplast and could diffuse through the membrane into the cytosol. Feeding β-CC results in the up-regulation of genes involved in stress responses, particularly those triggered by 1O2. It is speculated that the electrophilic carbonyl group could react with electron donors, such as sulfhydryl groups; however, the actual targets and mode of action are unknown. (B) MEcPP, an intermediary of isoprenoid precursors, is produced by MDS in the plastidic MEP pathway. MEcPP over accumulating mutants present high levels of SA and are resistant to biotrophic pathogens. MEcPP regulates the expression of the HPL and ICS1 gene, with concomitant production of SA. Although the transport and action mechanism are unknown, MEcPP could promote chromatin reorganization and induction of transcription of target genes. (C) PAP levels are catabolically regulated by SAL1 in the chloroplast and PAP transport is probably mediated by PAPST1. Cytosolic PAP could diffuse to the nucleus via the pores (cylinder) where it inhibits nuclear XRNs and affects gene regulation of stress inducible genes (i.e., APX2 and ELIP2). This mechanism is thought to play a role during drought, as PAP levels increase 30-fold. Other potential PAP targets (Nucleotide diphosphate kinase, NDK, and poly (ADP-ribose) polymerase, PARP, proteins) may mediate other aspects of signaling. The control mechanism of gene regulation by the XRNs proteins is a matter of investigation. Red lines, inhibition; black arrows, induction or activation; proteins involved in the signaling are indicated as ovals. Unknown components, processes or targets are indicated with red “?” or with dashed arrows. β-CC, β-cyclocitral; MEP, Methylerythritol phosphate pathway; MEcPP, methylerythritol cyclodiphosphate; MDS, MEcPP synthase; IPP, isopentenyl diphosphate; G3P, glyceraldehyde 3-phosphate; SA, salicylic acid; HL, high light. Figure adapted from Xiao et al. (2012) and Estavillo et al. (2011).
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Figure 1: New metabolic retrograde signaling pathways. The different components of recently discovered plant retrograde signaling pathways are shown. (A) β-CC is most likely produced by oxidation of carotenes by 1O2 in the chloroplast and could diffuse through the membrane into the cytosol. Feeding β-CC results in the up-regulation of genes involved in stress responses, particularly those triggered by 1O2. It is speculated that the electrophilic carbonyl group could react with electron donors, such as sulfhydryl groups; however, the actual targets and mode of action are unknown. (B) MEcPP, an intermediary of isoprenoid precursors, is produced by MDS in the plastidic MEP pathway. MEcPP over accumulating mutants present high levels of SA and are resistant to biotrophic pathogens. MEcPP regulates the expression of the HPL and ICS1 gene, with concomitant production of SA. Although the transport and action mechanism are unknown, MEcPP could promote chromatin reorganization and induction of transcription of target genes. (C) PAP levels are catabolically regulated by SAL1 in the chloroplast and PAP transport is probably mediated by PAPST1. Cytosolic PAP could diffuse to the nucleus via the pores (cylinder) where it inhibits nuclear XRNs and affects gene regulation of stress inducible genes (i.e., APX2 and ELIP2). This mechanism is thought to play a role during drought, as PAP levels increase 30-fold. Other potential PAP targets (Nucleotide diphosphate kinase, NDK, and poly (ADP-ribose) polymerase, PARP, proteins) may mediate other aspects of signaling. The control mechanism of gene regulation by the XRNs proteins is a matter of investigation. Red lines, inhibition; black arrows, induction or activation; proteins involved in the signaling are indicated as ovals. Unknown components, processes or targets are indicated with red “?” or with dashed arrows. β-CC, β-cyclocitral; MEP, Methylerythritol phosphate pathway; MEcPP, methylerythritol cyclodiphosphate; MDS, MEcPP synthase; IPP, isopentenyl diphosphate; G3P, glyceraldehyde 3-phosphate; SA, salicylic acid; HL, high light. Figure adapted from Xiao et al. (2012) and Estavillo et al. (2011).

Mentions: Despite a paucity of discovery of retrograde signals in the last decade, several signaling pathways have been recently proposed in the past 12 months. These novel signals include products of secondary metabolism (Estavillo et al., 2011; Xiao et al., 2012), oxidation products of carotenoids (Ramel et al., 2012), and dual localized proteins (Sun et al., 2011; Isemer et al., 2012) (Figure 1). These findings indicate that many metabolic pathways can act as potential sources of chloroplastic signals during different developmental stages of the plant or upon different stress responses. More importantly, unlike the previously discovered signals during artificial conditions, these new signals were identified during physiologically relevant stress responses like drought or HL. These new discoveries further support the concept that chloroplasts can indeed act as environmental sensors.


Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast.

Estavillo GM, Chan KX, Phua SY, Pogson BJ - Front Plant Sci (2013)

New metabolic retrograde signaling pathways. The different components of recently discovered plant retrograde signaling pathways are shown. (A) β-CC is most likely produced by oxidation of carotenes by 1O2 in the chloroplast and could diffuse through the membrane into the cytosol. Feeding β-CC results in the up-regulation of genes involved in stress responses, particularly those triggered by 1O2. It is speculated that the electrophilic carbonyl group could react with electron donors, such as sulfhydryl groups; however, the actual targets and mode of action are unknown. (B) MEcPP, an intermediary of isoprenoid precursors, is produced by MDS in the plastidic MEP pathway. MEcPP over accumulating mutants present high levels of SA and are resistant to biotrophic pathogens. MEcPP regulates the expression of the HPL and ICS1 gene, with concomitant production of SA. Although the transport and action mechanism are unknown, MEcPP could promote chromatin reorganization and induction of transcription of target genes. (C) PAP levels are catabolically regulated by SAL1 in the chloroplast and PAP transport is probably mediated by PAPST1. Cytosolic PAP could diffuse to the nucleus via the pores (cylinder) where it inhibits nuclear XRNs and affects gene regulation of stress inducible genes (i.e., APX2 and ELIP2). This mechanism is thought to play a role during drought, as PAP levels increase 30-fold. Other potential PAP targets (Nucleotide diphosphate kinase, NDK, and poly (ADP-ribose) polymerase, PARP, proteins) may mediate other aspects of signaling. The control mechanism of gene regulation by the XRNs proteins is a matter of investigation. Red lines, inhibition; black arrows, induction or activation; proteins involved in the signaling are indicated as ovals. Unknown components, processes or targets are indicated with red “?” or with dashed arrows. β-CC, β-cyclocitral; MEP, Methylerythritol phosphate pathway; MEcPP, methylerythritol cyclodiphosphate; MDS, MEcPP synthase; IPP, isopentenyl diphosphate; G3P, glyceraldehyde 3-phosphate; SA, salicylic acid; HL, high light. Figure adapted from Xiao et al. (2012) and Estavillo et al. (2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 1: New metabolic retrograde signaling pathways. The different components of recently discovered plant retrograde signaling pathways are shown. (A) β-CC is most likely produced by oxidation of carotenes by 1O2 in the chloroplast and could diffuse through the membrane into the cytosol. Feeding β-CC results in the up-regulation of genes involved in stress responses, particularly those triggered by 1O2. It is speculated that the electrophilic carbonyl group could react with electron donors, such as sulfhydryl groups; however, the actual targets and mode of action are unknown. (B) MEcPP, an intermediary of isoprenoid precursors, is produced by MDS in the plastidic MEP pathway. MEcPP over accumulating mutants present high levels of SA and are resistant to biotrophic pathogens. MEcPP regulates the expression of the HPL and ICS1 gene, with concomitant production of SA. Although the transport and action mechanism are unknown, MEcPP could promote chromatin reorganization and induction of transcription of target genes. (C) PAP levels are catabolically regulated by SAL1 in the chloroplast and PAP transport is probably mediated by PAPST1. Cytosolic PAP could diffuse to the nucleus via the pores (cylinder) where it inhibits nuclear XRNs and affects gene regulation of stress inducible genes (i.e., APX2 and ELIP2). This mechanism is thought to play a role during drought, as PAP levels increase 30-fold. Other potential PAP targets (Nucleotide diphosphate kinase, NDK, and poly (ADP-ribose) polymerase, PARP, proteins) may mediate other aspects of signaling. The control mechanism of gene regulation by the XRNs proteins is a matter of investigation. Red lines, inhibition; black arrows, induction or activation; proteins involved in the signaling are indicated as ovals. Unknown components, processes or targets are indicated with red “?” or with dashed arrows. β-CC, β-cyclocitral; MEP, Methylerythritol phosphate pathway; MEcPP, methylerythritol cyclodiphosphate; MDS, MEcPP synthase; IPP, isopentenyl diphosphate; G3P, glyceraldehyde 3-phosphate; SA, salicylic acid; HL, high light. Figure adapted from Xiao et al. (2012) and Estavillo et al. (2011).
Mentions: Despite a paucity of discovery of retrograde signals in the last decade, several signaling pathways have been recently proposed in the past 12 months. These novel signals include products of secondary metabolism (Estavillo et al., 2011; Xiao et al., 2012), oxidation products of carotenoids (Ramel et al., 2012), and dual localized proteins (Sun et al., 2011; Isemer et al., 2012) (Figure 1). These findings indicate that many metabolic pathways can act as potential sources of chloroplastic signals during different developmental stages of the plant or upon different stress responses. More importantly, unlike the previously discovered signals during artificial conditions, these new signals were identified during physiologically relevant stress responses like drought or HL. These new discoveries further support the concept that chloroplasts can indeed act as environmental sensors.

Bottom Line: Many signals of different chemical nature have been described in the past decades, including chlorophyll intermediates, reactive oxygen species (ROS), and adenosine derivatives.While the effects of retrograde signaling on gene expression are well understood, the initiation and transport of the signals and their mode of action have either not been resolved, or are a matter of speculation.Here we summarize current plastid retrograde signaling models in plants, with a focus on new signaling pathways, SAL1-PAP, methylerythritol cyclodiphosphate (MEcPP), and β-cyclocitral (β-CC), and outline missing links or future areas of research that we believe need to be addressed to have a better understanding of plant intracellular signaling networks.

View Article: PubMed Central - PubMed

Affiliation: ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University Canberra, ACT, Australia.

ABSTRACT
Plant organelles produce retrograde signals to alter nuclear gene expression in order to coordinate their biogenesis, maintain homeostasis, or optimize their performance under adverse conditions. Many signals of different chemical nature have been described in the past decades, including chlorophyll intermediates, reactive oxygen species (ROS), and adenosine derivatives. While the effects of retrograde signaling on gene expression are well understood, the initiation and transport of the signals and their mode of action have either not been resolved, or are a matter of speculation. Moreover, retrograde signaling should be considered as part of a broader cellular network, instead of as separate pathways, required to adjust to changing physiologically relevant conditions. Here we summarize current plastid retrograde signaling models in plants, with a focus on new signaling pathways, SAL1-PAP, methylerythritol cyclodiphosphate (MEcPP), and β-cyclocitral (β-CC), and outline missing links or future areas of research that we believe need to be addressed to have a better understanding of plant intracellular signaling networks.

No MeSH data available.


Related in: MedlinePlus