The aim of our research is to dissect and elucidate the signalling pathways between the chloroplast and the nucleus that regulate the expression of nuclear genes encoding photosynthetic proteins. We use an integrative approach with a combination of genetics, molecular biology and biochemistry to identify components of these signalling pathways.

 

The function of the eukaryotic cell depends on the regulated and reciprocal interaction between its different compartments. This includes not only the exchange of energy equivalents but also information. The presence of genes encoding organellar proteins in different cellular compartments necessitates a tight coordination of expression by the different genomes. Most information exchange flows from the nucleus to the organelles because the large majority of genes encoding proteins with organellar function are encoded in the nucleus. Nevertheless, there is evidence that expression of these genes is regulated by signals originating in the organelles.

 

The photosynthetic apparatus in the plant cell is composed of proteins encoded by genes from both the nucleus and the chloroplast. Communication between plastids and the nucleus is necessary for the initiation of chloroplast development in the light, and also for the ability of the plant cell to respond correctly to fluctuations in the environment. It is clear that several different plastid processes produce signals influencing nuclear photosynthetic gene expression, and to date at least three different signals have been identified that originate in the plastid (Fig. 1). In Arabidopsis, two plastid-to-nucleus signalling pathways, the GUN1 and GUN2-5 pathways, have been identified and the chloroplastic source of the signal in the GUN2-5 pathway has recently been shown to be the tetrapyrrole intermediate Mg-ProtoIX (Strand et al., ). The redox responsive signal(s) is not related to the GUN signalling pathways and represents a different pathway(s).

 

Expression levels of one of the nuclear genes regulated by the GUN-pathways and the redox-pathway(s), LHCB1, can be used as a marker for plastid-to-nucleus communication. LHCB1 encodes one of the chlorophyll a/b binding proteins associated with PSII. To facilitate the detection of LHCB1 expression we use a transgenic line containing a LHCB1::Luciferase promoter reporter construct. By taking advantage of the activity of the Luciferase reporter gene, transcriptional activity of the LHCB1 promoter can easily be monitored (Fig. 2). We are currently performing screens for novel mutants in the plastid-to-nucleus signalling pathways and for suppressors of existing mutants.

 

Strand, Å., Asami, T., Alonzo, J., Ecker, J., and Chory, J. () Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421: 79-83.

 

Strand, Å., Foyer, C., Gustafsson, P., Gardeström, P. and Hurry, V. () Increased expression of sucrose-phosphate-synthase increases freezing tolerance and photosynthetic performance at low temperature in transgenic Arabidopsis thaliana. Plant Cell Environ. In press

 

Hurry, V., Druart, N., Cavaco, A., Gardeström, P. and Strand, Å. () Photosynthesis at low temperatures: a case study with Arabidopsis. In Plant Cold Hardiness: gene regulation and genetic engineering. (P.H. Li & E.T. Palva, eds). Kluwer Academic Press, New York.

 

Strand, Å., Zrenner. R., Trevanion. S., Stitt. M., Gustafsson, P. and Gardeström, P. () Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose-phosphate-synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J. 23: 759-770.

 

Hurry, V., Strand, Å., Henkes, S., Furbank, R. and Stitt, M. () The role of inorganic phosphate in the development of freezing tolerance and acclimation of photosynthetic carbon metabolism to low growth temperature is revealed by studies of pho mutants of Arabidopsis thaliana. Plant J. 24: 383-396.

 

Strand, Å., Hurry, V., Henkes, S., Huner, N., Gustafsson, P., Gardeström, P. and Stitt, M. () Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol, 119: .

 

Strand, Å., Hurry, V., Gustafsson, P. and Gardeström, P. () Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J., 12: 605-614.