Evolution of plant sulfur metabolism
We are interested in the variations in organisation and regulation of sulfate assimilation between lower plants and algae and higher plants and in understanding the origin and evolution of the genes involved in sulfate reduction.
Sulfate assimilation in lower plants and algae
Sulfate assimilation is relatively well understood in flowering plants, but very little information exists on sulfate assimilation in lower plants and algae. Since the finding of a putative 3’-phosphoadenosine 5’-phosphosulfate (PAPS) reductase in Physcomitrella patens, an enigmatic enzyme thought to exist in fungi and some bacteria only, it has been evident that sulfur metabolism in lower plants may substantially differ from seed plant models. The genomic sequencing of two basal plant species, the Bryophyte Physcomitrella patens, and the Lycophyte Selaginella moellendorffii, and of several algal species including Chlamydomonas reinhardtii, Thalassiosira pseudonana, Phaeodactylum tricornutum, or Emiliania huxleyi opens up the possibility to search for differences between lower and higher plants and algae at the genomic level. The genomes of these species contain a surprising number of new enzyme variants and fusion. Also the complexity of several gene families involved in sulfate assimilation is substantially different in the various genomes. We are analysing some of these novel enzyme variants in vitro to understand the biochemistry of sulfate activation and reduction and to identify genes that can be used to improve sulfur use efficiency in higher plants. In addition, in collaboration with University of Freiburg, we are searching for novel alternative enzymes of sulfur metabolism by analysis of targeted knock-out mutants of Physcomitrella patens. In fact, recently we found that the putative PAPS reductase represents a new variant of APS reductase, lacking an iron sulfur cofactor, which has been named APR-B. Both forms of APS reductase on their own possess sufficient reducing capacity, but are not efficient enough during conditions of increased demand for reduced sulfur, i.e. the knock-out lines are Cd sensitive. However, in vitro, catalytic efficiency of the FeS containing APR is much higher than that of APR-B (Kopriva et al., 2007b).
Relevant publications:
Hermsen C., Matthewman C., Wesenberg D., Krauss G.-J., Kopriva S. (2010) Regulation of sulfate assimilation in Physcomitrella patens - mosses are different! Planta 232, 461-470
Wiedemann G., Hermsen C., Melzer M., Büttner-Mainik A., Rennenberg H., Reski R., Kopriva S. (2010) Linking sulfate assimilation with moss development: Targeted knock-out of sulfite reductase in Physcomitrella patens prevents spore maturation. FEBS Lett., 584, 2271-2278
Kopriva S., Wiedemann G., Reski R. (2007a) Sulfate assimilation in basal land plants – what does genomic sequencing tell us? Plant Biol. 9, 556-564
Kopriva S., Fritzemeier K., Wiedemann G., Reski R. (2007b) The putative moss 3’phosphoadenosine 5’phosphosulfate reductase is a novel form of adenosine 5’phosphosulfate reductase without iron sulfur cluster. J. Biol. Chem. 282, 22930-22938
Wiedemann G., Koprivova A., Schneider M., Herschbach C., Reski R., Kopriva S. (2007) The role of the novel adenosine 5'-phosphosulfate reductase in regulation of sulfate assimilation of Physcomitrella patens. Plant Mol. Biol. 65, 667-676
Koprivova A., Meyer A., Schween G., Herschbach C., Reski R., Kopriva S. (2002) Functional knockout of the adenosine 5´phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation. J. Biol. Chem. 277: 32195-32201
Phylogenetic analysis of sulfate assimilation and cysteine biosynthesis in phototrophic organisms
Assimilatory sulfate reduction occurs in various chemotrophic bacteria and fungi and in photosynthetic organisms, but is missing in animals and most prokaryotic and eukaryotic obligate parasites. We have made use of the vast amount of available sequence data to perform a phylogenetic analysis of sulfate assimilation genes from a range of lineages of photosynthetic organisms including photosynthetic bacteria, eukaryotes with primary symbionts such as plants, green and red algae and various eukaryotes with secondary and tertiary symbionts. The analysis revealed very complicated relations between the different lineages and different evolutionary histories of the individual genes of the pathway. Whereas, for example, plant sulfite reductase is clearly of a cyanobacterial origin, the other genes in the pathway are not of cyanobacterial origin despite the proteins being targeted to the plastid. The clear separation between APS- and PAPS-reducing organisms seen in previous analyses has been lost with the inclusion of genes from diatom and cryptomonad secondary symbiont algae, because they possess genes related to the moss APR-B in genomes of various marine microalgae (Patron et al. 2008).
Fig.2. Neighbor joining tree of APS and PAPS reductase sequences. PAPS reductases are marked in blue, the new form of APR, APR-B, in lower plants is marked in green.
Relevant publications
Patron N., Durnford D., Kopriva S. (2008) Sulfate assimilation in Eukaryotes: Evolutionary origins and subcellular localisation. BMC Evol. Biol. 8, 39
Kopriva S., Patron N., Leustek T., Keeling P. (2008) Phylogenetic analysis of sulfate assimilation and cysteine biosynthesis in phototrophic organisms. In: Advances in Photosynthesis and Respiration Vol. 27 - Sulfur metabolism in phototrophic organisms. Hell R., Leustek T., Dahl C., Knaff D. eds. Springer, Dordrecht, pp. 33-60
Kopriva S., Koprivova A. (2004) Plant adenosine 5'phosphosulfate reductase - the past, the present, and the future. J. Exp. Bot. 55: 1775-1783
Kopriva S., Büchert T., Fritz G., Suter M., Benda R., Schünemann V., Koprivova A., Schürmann P., Trautwein A.X., Kroneck P.M.H., Brunold C. (2002) The presence of an iron-sulfur cluster in adenosine 5'-phosphosulfate reductase separates organisms utilizing adenosine 5'-phosphosulfate and phosphoadenosine 5'-phosphosulfate for sulfate assimilation. J. Biol. Chem. 277: 21786-21791