Evolution of Chlorophyll Biosynthesis—The Challenge to Survive Photooxidation

The capability to perform protochlorophyllide reduction under aerobic conditions and thereby to avoid the danger of photooxidation was certainly a landmark in the evolution of porphyrin biosynthesis. Such a scenario, however, rests on the assumption that POR already occurred at the roots of all plant organisms. In fact, por-related gene sequences have been shown to occur in cyanobacteria (Suzuki and Bauer 1995xSuzuki, J.Y and Bauer, C.E. Proc. Natl. Acad. Sci. USA. 1995; 92: 3749–3753Crossref | PubMedSee all ReferencesSuzuki and Bauer 1995) and thus can be traced back to the presumed endosymbiotic origin of chloroplasts.In ancestral cyanobacteria and presumably also in early forms of vascular plants, such as the rhyniophytes, both types of protochlorophyllide-reducing enzymes, BCHLNB and POR, were likely to coexist. However, during the evolution of angiosperms, bchL, bchB, and bchN were lost.Molecular evidence based on the analysis of chloroplast DNA structure and organization of the major extant lineages of vascular land plants suggests that presumably as a result of a DNA inversion in a particular 30-kb region, the chlB, chlL, and chlN genes, which are the counterparts of bchB, bchL, and bchN of Rhodobacter and chlB, chlL, and chlN of extant cyanobacteria, were lost at the divergence point between gymnosperms and angiosperms (Raubeson and Jansen 1992xRaubeson, L.A and Jansen, R.K. Science. 1992; 255: 1697–1699Crossref | PubMedSee all ReferencesRaubeson and Jansen 1992). By contrast, the gene encoding POR was preserved and relocated to the nucleus, where it duplicated and diverged into two distinct por genes, termed porA and porB (3xArmstrong, G.A, Runge, S, Frick, G, Sperling, U, and Apel, K. Plant Physiol. 1995; 108: 1505–1517Crossref | PubMedSee all References, 7xHoltorf, H, Reinbothe, S, Reinbothe, C, Bereza, B, and Apel, K. Proc. Natl. Acad. Sci. USA. 1995; 92: 3254–3258Crossref | PubMedSee all References). This diversification is likely to have occurred even before speciation of gymnosperms and angiosperms.Reasons that evolution invented and maintained two POR enzymes may be deduced from our studies of the expression patterns of the PORA and PORB polypeptides (3xArmstrong, G.A, Runge, S, Frick, G, Sperling, U, and Apel, K. Plant Physiol. 1995; 108: 1505–1517Crossref | PubMedSee all References, 7xHoltorf, H, Reinbothe, S, Reinbothe, C, Bereza, B, and Apel, K. Proc. Natl. Acad. Sci. USA. 1995; 92: 3254–3258Crossref | PubMedSee all References). In both gymnosperms and angiosperms, PORA and possibly PORB are active during the transitory stage from dark to light growth (Lebedev et al. 1995xLebedev, N, van Cleve, B, Armstrong, G.A, and Apel, K. Plant Cell. 1995; 7: 2081–2090PubMedSee all ReferencesLebedev et al. 1995) when protochlorophyllide and chlorin must be shielded from interacting with O2 in the atmosphere. PORB is present also in light-adapted plants, where it may serve housekeeping functions in chlorophyll synthesis (3xArmstrong, G.A, Runge, S, Frick, G, Sperling, U, and Apel, K. Plant Physiol. 1995; 108: 1505–1517Crossref | PubMedSee all References, 7xHoltorf, H, Reinbothe, S, Reinbothe, C, Bereza, B, and Apel, K. Proc. Natl. Acad. Sci. USA. 1995; 92: 3254–3258Crossref | PubMedSee all References). Due to the operation of PORA and PORB, the risk is kept very low that porphyrins, such as protochlorophyllide and chlorin, will cause photooxidative damage to cellular and subcellular structures during the entire plant life cycle.The proposed rooting of POR is based on the hidden assumption that the last common ancestor of all photosynthetic eubacteria contained bacteriochlorophyll, not chlorophyll, in its reaction center. In such a “bacteriochlorophyll-first” scenario, chlorophyll-based photosynthesis would be a late invention unique to the cyanobacteria/chloroplast lineage. In the alternative, “chlorophyll-first” scenario, however, extant bacteriochlorophyll-containing purple bacteria would represent “deposed monarchs,” waiting, in specialized environments such as thermoclines of lakes, until “aerobic republicans” have gone out of fashion (Allen 1995xAllen, J.F. Nature. 1995; 376: 26CrossrefSee all ReferencesAllen 1995). The lower number of steps required for chlorophyll biosynthesis, as compared to bacteriochlorophyll synthesis, would be consistent with such a model. However, the “chlorophyll-first” hypothesis does not account for the fact that primitive cyanobacteria, by analogy to those existing today, already contained both, the oxygen-insensitive POR and the bchLNB-encoded protochlorophyllide reductase. We therefore prefer the “bacteriochlorophyll-first” hypothesis, which could explain why anoxygenic purple bacteria, which synthesize a photosystem only under anaerobic conditions, contain only a light-independent form and why cyanobacteria, which produce oxygen as a consequence of photosynthesis, have evolved an additional protochlorophyllide-reducing enzyme. Presumably the need to cope with the problem of photooxidation in the O2-rich atmosphere led to the evolution of POR.