Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods

Abstract

The synthesis of tetrapyrroles is regulated in anticipation of rhythmic changes in environmental conditions such as light intensity and temperature. To assess the control of the rate-limiting steps of the metabolic¯ow as well as the distribution of precursors for chlorophyll and heme synthesis, RNA steady-state levels and activities of enzymes involved in tetrapyrrole biosynthesis were analysed from 4-week-old tobacco (Nicotiana tobacum L.) plants grown under photoperiodically changing conditions. The kinetics of RNA levels and the enzyme activities were compared with those from plants which grew subsequent to the light/ dark cycles for 48 h under constant light or dark conditions. The analysis revealed that the two peak activities for 5-aminolevulinic acid synthesis and of magnesium-protoporphyrin IX chelatase (Mg-chelatase) corresponded with the highest accumulation of the transcripts encoding glutamyl-tRNA reductase and CHL H, a subunit of Mg-chelatase, in the ®rst half of the light period during a light/dark cycle. The activity of ferrochelatase (Fe-chelatase) and the level of its RNA showed a maximum just at the transition from light to dark and oscillated with a phase approximately opposite to that of Mg-chelatase activity. The control of 5-aminolevulinic acid synthesis and of the allocation of protoporphyrin IX to Mg-or Fe-chelatase probably re¯ect the functional coordination of tetrapyrrole biosynthesis in response to daily¯uctuations in tetrapyrrole requirements. It is suggested that the coordination of expression and enzyme activities allows, in the light phase, an extensive¯ow of substrates into the chlorophyll-synthesizing branch of the metabolic pathway and, after the transition from light to dark, a channeling into the heme biosynthetic pathway. Implications for feedback control in the pathway are discussed.

Molecular Interactions between the Specialist HerbivoreManduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. I. Large-Scale Changes in the Accumulation of Growth- and Defense-Related Plant mRNAs

“…1; Table I). Consistent with the literature, dramatic diurnal effects were seen in the accumulation of transcripts of lhb C1 and chl H, but not of rbc S (Kloppstech, 1985;Gibson et al, 1996;Papenbrock et al, 1999). The diurnal effects were superimposed on the herbivore-induced responses (Fig.…”

Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms

“…11). Nevertheless, a significant rate of ALA formation is observed, which is suggested to provide precursors for the synthesis of heme in darkness (Papenbrock et al, 1999;Richter et al, 2010;Czarnecki et al, 2011). Heme is an essential cofactor of several enzymes, including those that act in the mitochondrial electron transport chain even when light is limiting.…”

“…Heme is an essential cofactor of several enzymes, including those that act in the mitochondrial electron transport chain even when light is limiting. Then it is questionable how the differential allocation of the tetrapyrrole precursor Proto into the heme and Chl branch of TBS is regulated in darkness and how the dominating MgCh activity is decelerated (Papenbrock et al, 1999).…”

Tetrapyrrole Synthesis of Photosynthetic Chromerids Is Likely Homologous to the Unusual Pathway of Apicomplexan Parasites

“…The remaining steps are catalyzed by the same enzymes as in heterotrophs, but the entire pathway is localized in the plastid, and most of the involved enzymes originate from its cyanobacterial ancestor (Oborník and Green, 2005) (Figure 3B). This compartmentalization reflects the major need for the tetrapyrroles in the plastid, where chlorophyll and most of the synthesized heme are required for photosynthetic functions (Papenbrock et al, 1999;Castelfranco and Jones, 1975).…”