Interorganellar crosstalk: new perspectives on signaling from the chloroplast to the nucleus
© BioMed Central Ltd 2001
Published: 30 July 2001
Chlorophyll precursors, photosynthetic electron transport, and sugars have all been shown to be involved in signaling from the chloroplast to the nucleus, suggesting the presence of multiple signaling pathways of coordination between these two cellular compartments.
The endosymbiotic theory of chloroplast evolution proposes that a photosynthetic prokaryote was engulfed by a eukaryotic host to produce the eukaryotic plant cell. The ensuing endosymbiosis resulted in gene transfer from the chloroplast genome to the nuclear genome, and thus the chloroplast contains both nucleus-encoded and chloroplast-encoded components. The development of a fully functional chloroplast therefore depends on the coordinate expression of nuclear and chloroplast genes in response to both developmental and environmental signals. Chloroplast function requires the import of both nucleus-encoded photosynthetic proteins and cytoplasmic factors that regulate the expression of chloroplast genes. The plastid also plays a role in nuclear gene expression, with signals that originate in the chloroplast acting to regulate transcription of nucleus-encoded photosynthetic genes. In the last ten years, many studies have revealed the nature of nucleus-derived molecules that affect chloroplast gene expression at all levels (reviewed in [1,2,3]). Although it has been known for many years that the expression of a subset of nuclear genes, whose products are involved in photosynthesis, depends on the presence in the cell of functional plastids , little progress has been made in elucidating the signaling molecules or mechanisms involved in this retrograde signaling. Several recent discoveries have made inroads into this complex mechanism [5,6,7,8] and have begun to shed light on the black box of signaling from the chloroplast to the nucleus.
Chlorophyll precursors signal from the chloroplast
It has long been suspected that chlorophyll precursors play a role in signaling to the nucleus. Indirect evidence came from reports of the repression of nuclear photosynthetic genes in Chlamydomonas reinhardtii by the addition of a specific inhibitor of chlorophyll biosynthesis that results in chlorophyll-precursor accumulation [9,10]. The same chlorophyll precursors have also been reported to act as inducers of nucleus-encoded cytosolic and chloroplast-localized heat-shock proteins [11,12].
Two recent papers, by Mochizuki et al.  and Møller et al. , have identified proteins involved in chlorophyll biosynthesis as regulators of light-stimulated expression of nucleus-encoded photosynthetic genes such as those encoding the light-harvesting chlorophyll a/b binding protein (Lhcb), Rubisco small subunit (RbcS), chalcone synthase (Chs) and ferredoxin-NADP reductase (Fnr).
Møller et al. isolated Arabidopsis long after far red (laf) mutants displaying reduced hypocotyl-growth inhibition in response to far-red light. These mutants also have an inability to become green following treatment with far-red light, and they have reduced expression of the light-regulated genes Lhcb, Chs, and Fnr in far-red light. LAF6 was cloned and shown to encode a novel plant member of the small soluble ATP-binding-cassette transporter family (atABC1); members of this family are usually involved in the import of catabolites across membranes. AtABC1 has a functional amino-terminal chloroplast-transit peptide and localizes to the periphery of chloroplasts, consistent with having a position at the inner envelope. The pale-green phenotype of laf6 seedlings suggested a deficiency in chlorophyll biosynthesis. Subsequent analysis confirmed that laf6 mutants accumulate twice as much protoporphyrin IX (proto IX; see Figure 1) and 40% less chlorophyll than wild-type seedlings.
Plastid redox state and sugars are involved in signaling from the chloroplast
The expression of nucleus-encoded photosynthetic genes, such as Lhcb, has been shown to be repressed in the presence of high levels of sugar (reviewed in ). It has also been proposed that photosynthetic electron transport is required to activate Lhcb transcription . Oswald et al.  investigated whether these two effects operate through a common signaling pathway. They showed that photosynthetic electron transport is essential for the generation of a chloroplast signal that activates transcription of Lhcb and RbcS. This transcriptional activation did not depend on sugar status, implying that it is an independent event. Sucrose feeding repressed the transcription of Lhcb and RbcS, however, suggesting that the two pathways may interact in controlling the expression of these nuclear genes.
In studies of a mutant of the maize Sucrose export defective (Sxd1) gene, Provencher et al.  reported accumulation of sugars in photosynthetic bundle sheath cells as a result of a defect in sucrose export to the vascular parenchyma cells. The sxd1 mutant did not show repression of the nucleus-encoded photosynthetic genes Lhcb and RbcS, despite accumulation of high sugar levels. This result implies that SXD1 has a role in repression of Lhcb and RbcS in response to high sugar levels. On the basis of this observation and the localization of Sxd1 to the chloroplast, the authors proposed that SXD1 might play a role in the sugar-sensing mechanism involved in chloroplast-to-nucleus signaling.
A model of chloroplast-to-nucleus signaling
Undoubtedly, there is still much to be discovered in this complex field. It will become increasingly difficult to study individual pathways in isolation, as one can envisage an elaborate network of crosstalk between the pathways. As these recent papers have shown, however, the search for retrograde signaling components that pass from the plastid back to the nucleus is gathering momentum.
Work in our laboratory is supported by funds from the US Department of Energy (93ER70116) and the National Institutes of Health (GM54659) to S.P.M.; E.C.B. and A.S. are supported by Skaggs post-doctoral fellowships.
- Somanchi A, Mayfield SP: Nuclear-chloroplast signalling. Curr Opin Plant Biol. 1999, 2: 404-409. 10.1016/S1369-5266(99)00013-8.PubMedView ArticleGoogle Scholar
- Goldschmidt-Clermont M: Coordination of nuclear and chloroplast gene expression in plant cells. Int Rev Cytol. 1998, 177: 115-180.PubMedView ArticleGoogle Scholar
- Barkan A, Goldschmidt-Clermont M: Participation of nuclear genes in chloroplast gene expression. Biochimie. 2000, 82: 559-572. 10.1016/S0300-9084(00)00602-7.PubMedView ArticleGoogle Scholar
- Mayfield SP, Taylor WC: Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur J Biochem. 1984, 144: 79-84.PubMedView ArticleGoogle Scholar
- Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J: Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA. 2001, 98: 2053-2058. 10.1073/pnas.98.4.2053.PubMedPubMed CentralView ArticleGoogle Scholar
- Møller SG, Kunkel T, Chua N-H: A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev. 2001, 15: 90-103. 10.1101/gad.850101.PubMedPubMed CentralView ArticleGoogle Scholar
- Oswald O, Martin T, Dominy PJ, Graham IA: Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA. 2001, 98: 2047-2052. 10.1073/pnas.021449998.PubMedPubMed CentralView ArticleGoogle Scholar
- Provencher LM, Miao L, Sinha N, Lucas WJ: Sucrose export defective 1 encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell. 2001, 13: 1127-1141. 10.1105/tpc.13.5.1127.PubMedPubMed CentralView ArticleGoogle Scholar
- Johanningmeier U, Howell SH: Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. J Biol Chem. 1984, 259: 13541-13549.PubMedGoogle Scholar
- Johanningmeier U: Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem. 1988, 177: 417-424.PubMedView ArticleGoogle Scholar
- Kropat J, Oster U, Rudiger W, Beck CF: Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci USA. 1997, 94: 14168-14172. 10.1073/pnas.94.25.14168.PubMedPubMed CentralView ArticleGoogle Scholar
- Kropat J, Oster U, Rudiger W, Beck CF: Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J. 2000, 24: 523-531. 10.1046/j.1365-313X.2000.00898.x.PubMedView ArticleGoogle Scholar
- Susek R, Ausubel FM, Chory J: Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell. 1993, 74: 787-799.PubMedView ArticleGoogle Scholar
- Jang JC, Sheen J: Sugar sensing in higher plants. Plant Cell. 1994, 6: 1665-1679. 10.1105/tpc.6.11.1665.PubMedPubMed CentralView ArticleGoogle Scholar
- Escoubas J-M, Lomas M, LaRoche J, Falkowski PG: Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA. 1995, 92: 10237-10241.PubMedPubMed CentralView ArticleGoogle Scholar
- Sheen J: Protein phosphatase activity is required for light-inducible gene expression in maize. EMBO J. 1993, 12: 3497-3505.PubMedPubMed CentralGoogle Scholar
- Chandok MR, Sopory SK, Oelmuller R: Cytoplasmic kinase and phosphatase activities can induce PsaF gene expression in the absence of functional plastids: evidence that phosphorylation/dephosphorylation events are involved in interorganellar crosstalk. Mol Gen Genet. 2001, 264: 819-826. 10.1007/s004380000371.PubMedView ArticleGoogle Scholar