Limits...
Dual targeting and retrograde translocation: regulators of plant nuclear gene expression can be sequestered by plastids.

Krause K, Oetke S, Krupinska K - Int J Mol Sci (2012)

Bottom Line: Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids.Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated.Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

View Article: PubMed Central - PubMed

Affiliation: Department of Arctic and Marine Biology, University of Tromsø, Tromsø 9037, Norway; E-Mail: kirsten.krause@uit.no.

ABSTRACT
Changes in the developmental or metabolic state of plastids can trigger profound changes in the transcript profiles of nuclear genes. Many nuclear transcription factors were shown to be controlled by signals generated in the organelles. In addition to the many different compounds for which an involvement in retrograde signaling is discussed, accumulating evidence suggests a role for proteins in plastid-to-nucleus communication. These proteins might be sequestered in the plastids before they act as transcriptional regulators in the nucleus. Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids. Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated. Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

Show MeSH

Related in: MedlinePlus

Chloroplasts are involved in the perception of intrinsic triggers controlling plant development and external cues and stresses from the abiotic and the biotic environment. A novel signaling pathway involving chloroplast located proteins that might be translocated to the nucleus in response to the diverse stimuli perceived by chloroplasts (see text) is depicted here. Whirly1 is the only protein for which a bona fide export has been shown to date (arrow with continuous line). This protein is involved in pathogen responses [35,52], but might also play a role in other situations. The NRIP1 protein appears to be released from plastids in response to infection to tobacco with the tobacco mosaic virus [45] but direct evidence for an export is yet missing (arrow with large dotted line). The transcription factor NAC102 is an intriguing candidate for the perception of oxidative stress in chloroplasts [47], but the possibility of its release remains to be investigated (arrow with small dotted line).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC3472732&req=5

f1-ijms-13-11085: Chloroplasts are involved in the perception of intrinsic triggers controlling plant development and external cues and stresses from the abiotic and the biotic environment. A novel signaling pathway involving chloroplast located proteins that might be translocated to the nucleus in response to the diverse stimuli perceived by chloroplasts (see text) is depicted here. Whirly1 is the only protein for which a bona fide export has been shown to date (arrow with continuous line). This protein is involved in pathogen responses [35,52], but might also play a role in other situations. The NRIP1 protein appears to be released from plastids in response to infection to tobacco with the tobacco mosaic virus [45] but direct evidence for an export is yet missing (arrow with large dotted line). The transcription factor NAC102 is an intriguing candidate for the perception of oxidative stress in chloroplasts [47], but the possibility of its release remains to be investigated (arrow with small dotted line).

Mentions: A subset of the dually targeted proteins described above and listed in Table 1 is involved in the reaction to biotic and abiotic factors, including pathogen defense, fitting with the notion that the plastids play a role as sensory organelles for environmental changes [1]. It is, therefore, logical to speculate that such proteins play a vital role in plastid-to-nucleus retrograde signaling. In contrast to other components involved in retrograde signaling (such as intermediates of plastid metabolic pathways, for example) proteins involved in gene regulation could be direct mediators of gene expression changes. The storage and release of proteins from plastids and their subsequent translocation to the nucleus could allow a fast response to changes in plastid-localized processes upon certain triggers (Figure 1). WHIRLY1 was first described as a transcriptional activator of the PR10a gene of potato in the nucleus [35]. Its binding to promoters of target genes was shown to most likely depend on a posttranslational activation by salicylic acid [35], assuming that WHIRLY1 is already present in an inactive state. This pool of WHIRLY1 inactive in binding to PR gene promoters is presumably the pool that is located in the chloroplast. Another example for a chloroplast protein involved in pathogen defense is NRIP1. Infection of plants by tobacco mosaic virus was shown to induce its accumulation in the cytoplasm and nucleus [45]. The involvement of chloroplasts in pathogen response reactions has received more attention after it became apparent that many pathogens attempt to intercept signaling from chloroplasts by deploying effectors that target the chloroplasts in order to dampen the release of retrograde stress signals [50]. Secreted effector proteins of the pathogenic bacterium Pseudomonas syringae, for example, have N-terminal sequences (PTP) that are predicted to allow their import into the chloroplasts of infected cells [9]. It is noteworthy that one protein, Hop U1, targets several chloroplast-localized RNA-binding proteins and thus suppresses plant innate immunity [51]. It is possible that such proteins secreted by pathogens are plastid-targeted in order to interfere with the retrograde signaling from plastids either by preventing the production of defense related second messengers or by inhibiting the release of sequestered nuclear regulators, thus preventing the cascade of events that would otherwise lead to defense reactions.


Dual targeting and retrograde translocation: regulators of plant nuclear gene expression can be sequestered by plastids.

Krause K, Oetke S, Krupinska K - Int J Mol Sci (2012)

Chloroplasts are involved in the perception of intrinsic triggers controlling plant development and external cues and stresses from the abiotic and the biotic environment. A novel signaling pathway involving chloroplast located proteins that might be translocated to the nucleus in response to the diverse stimuli perceived by chloroplasts (see text) is depicted here. Whirly1 is the only protein for which a bona fide export has been shown to date (arrow with continuous line). This protein is involved in pathogen responses [35,52], but might also play a role in other situations. The NRIP1 protein appears to be released from plastids in response to infection to tobacco with the tobacco mosaic virus [45] but direct evidence for an export is yet missing (arrow with large dotted line). The transcription factor NAC102 is an intriguing candidate for the perception of oxidative stress in chloroplasts [47], but the possibility of its release remains to be investigated (arrow with small dotted line).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3472732&req=5

f1-ijms-13-11085: Chloroplasts are involved in the perception of intrinsic triggers controlling plant development and external cues and stresses from the abiotic and the biotic environment. A novel signaling pathway involving chloroplast located proteins that might be translocated to the nucleus in response to the diverse stimuli perceived by chloroplasts (see text) is depicted here. Whirly1 is the only protein for which a bona fide export has been shown to date (arrow with continuous line). This protein is involved in pathogen responses [35,52], but might also play a role in other situations. The NRIP1 protein appears to be released from plastids in response to infection to tobacco with the tobacco mosaic virus [45] but direct evidence for an export is yet missing (arrow with large dotted line). The transcription factor NAC102 is an intriguing candidate for the perception of oxidative stress in chloroplasts [47], but the possibility of its release remains to be investigated (arrow with small dotted line).
Mentions: A subset of the dually targeted proteins described above and listed in Table 1 is involved in the reaction to biotic and abiotic factors, including pathogen defense, fitting with the notion that the plastids play a role as sensory organelles for environmental changes [1]. It is, therefore, logical to speculate that such proteins play a vital role in plastid-to-nucleus retrograde signaling. In contrast to other components involved in retrograde signaling (such as intermediates of plastid metabolic pathways, for example) proteins involved in gene regulation could be direct mediators of gene expression changes. The storage and release of proteins from plastids and their subsequent translocation to the nucleus could allow a fast response to changes in plastid-localized processes upon certain triggers (Figure 1). WHIRLY1 was first described as a transcriptional activator of the PR10a gene of potato in the nucleus [35]. Its binding to promoters of target genes was shown to most likely depend on a posttranslational activation by salicylic acid [35], assuming that WHIRLY1 is already present in an inactive state. This pool of WHIRLY1 inactive in binding to PR gene promoters is presumably the pool that is located in the chloroplast. Another example for a chloroplast protein involved in pathogen defense is NRIP1. Infection of plants by tobacco mosaic virus was shown to induce its accumulation in the cytoplasm and nucleus [45]. The involvement of chloroplasts in pathogen response reactions has received more attention after it became apparent that many pathogens attempt to intercept signaling from chloroplasts by deploying effectors that target the chloroplasts in order to dampen the release of retrograde stress signals [50]. Secreted effector proteins of the pathogenic bacterium Pseudomonas syringae, for example, have N-terminal sequences (PTP) that are predicted to allow their import into the chloroplasts of infected cells [9]. It is noteworthy that one protein, Hop U1, targets several chloroplast-localized RNA-binding proteins and thus suppresses plant innate immunity [51]. It is possible that such proteins secreted by pathogens are plastid-targeted in order to interfere with the retrograde signaling from plastids either by preventing the production of defense related second messengers or by inhibiting the release of sequestered nuclear regulators, thus preventing the cascade of events that would otherwise lead to defense reactions.

Bottom Line: Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids.Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated.Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

View Article: PubMed Central - PubMed

Affiliation: Department of Arctic and Marine Biology, University of Tromsø, Tromsø 9037, Norway; E-Mail: kirsten.krause@uit.no.

ABSTRACT
Changes in the developmental or metabolic state of plastids can trigger profound changes in the transcript profiles of nuclear genes. Many nuclear transcription factors were shown to be controlled by signals generated in the organelles. In addition to the many different compounds for which an involvement in retrograde signaling is discussed, accumulating evidence suggests a role for proteins in plastid-to-nucleus communication. These proteins might be sequestered in the plastids before they act as transcriptional regulators in the nucleus. Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids. Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated. Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

Show MeSH
Related in: MedlinePlus