Distinct Light-Mediated Pathways Regulate the Biosynthesis and Exchange of Isoprenoid Precursors during Arabidopsis Seedling Development

Abstract

Plants synthesize an astonishing diversity of isoprenoids, some of which play essential roles in photosynthesis, respiration, and the regulation of growth and development. Two independent pathways for the biosynthesis of isoprenoid precursors coexist within the plant cell: the cytosolic mevalonic acid (MVA) pathway and the plastidial methylerythritol phosphate (MEP) pathway. In at least some plants (including Arabidopsis), common precursors are exchanged between the cytosol and the plastid. However, little is known about the signals that coordinate their biosynthesis and exchange. To identify such signals, we arrested seedling development by specifically blocking the MVA pathway with mevinolin (MEV) or the MEP pathway with fosmidomycin (FSM) and searched for MEV-resistant Arabidopsis mutants that also could survive in the presence of FSM. Here, we show that one such mutant, rim1 , is a new phyB allele ( phyB-m1 ). Although the MEV-resistant phenotype of mutant seedlings is caused by the upregulation of MVA synthesis, its resistance to FSM most likely is the result of an enhanced intake of MVA-derived isoprenoid precursors by the plastid. The analysis of other light-hyposensitive mutants showed that distinct light perception and signal transduction pathways regulate these two differential mechanisms for resistance, providing evidence for a coordinated regulation of the activity of the MVA pathway and the crosstalk between cell compartments for isoprenoid biosynthesis during the first stages of seedling development.

Disruption of the 1-deoxy-D-xylulose-5-phosphate reductoisomerase (DXR) gene results in albino, dwarf and defects in trichome initiation and stomata closure in Arabidopsis

“…One is posttranscriptional regulation of DXR, such as translational modulation [19,53]. In Arabidopsis, HMGR, a critical enzyme involved in the MVA pathway, has even more complicated regulation mechanisms [26,[54][55][56][57]. The other possibility is that DXR might not be a determinant enzyme in the MEP pathway.…”

“…The transcript pattern of DXR covers almost all plant organs, with the highest level in inflorescence tissue [19,22]. Blocking of DXR activity using the specific inhibitor fosmidomycin (FSM) led to the accumulation of DXR protein, the bleach phenotype, and the failure of seedling establishment [19,20,[23][24][25][26]. An insertion mutant of DXR was found to be an albino, and down-regulation of DXR transcript level resulted in abnormal chloroplast development [20,27].…”

Synergistic Substrate Inhibition of ent-Copalyl Diphosphate Synthase: A Potential Feed-Forward Inhibition Mechanism Limiting Gibberellin Metabolism

“…Whereas CPS is preferentially expressed in nonphotosynthetic cell types (Silverstone et al, 1997) and its activity is associated with proplastids and seems to be essentially absent from chloroplasts (Aach et al, 1995), indicating transcriptional and posttranscriptional regulation during chloroplast development, we hypothesize that the kinetic properties of CPS reported here represent an additional regulatory mechanism limiting GA metabolism, at least in deetiolation, although potentially also more broadly in chloroplast development. Specifically, it has been demonstrated that light induces an increase in Mg 21 levels in plastids (Ishijima et al, 2003), along with up-regulation of the 2-Cmethyl-D-erythritol-4-P pathway that provides isoprenoid precursors for the production of GGPP in plastids (Carretero-Paulet et al, 2002;Rodriguez-Concepcion et al, 2004). Whereas the previously noted GGPPdependent substrate inhibition of CPS has been suggested to regulate GA metabolism (Kawaide et al, 2000), any increase in GGPP levels remains hypothetical given the difficulties inherent in measuring the physiological concentration of this labile metabolite.…”

Plastid Cues Posttranscriptionally Regulate the Accumulation of Key Enzymes of the Methylerythritol Phosphate Pathway in Arabidopsis

“…MEP production can be blocked by fosmidomycin (FSM), a strong inhibitor of DXR (Steinbacher et al, 2003). FSM causes a bleached phenotype and a block in the production of true leaves by the shoot apical meristem, eventually resulting in a seedling-lethal phenotype (Laule et al, 2003;Rodríguez-Concepció n et al, 2004). After conversion of MEP into methylerythritol 2,4-cyclodiphosphate in three enzymatic steps, a reduction catalyzed by hydroxymethylbutenyl diphosphate (HMBPP) synthase (HDS) produces HMBPP, which is finally converted by the enzyme HMBPP reductase (HDR) into IPP and DMAPP (Fig.…”