Plastid cues posttranscriptionally regulate the accumulation of key enzymes of the methylerythritol phosphate pathway in Arabidopsis.
Plastid isoprenoids (including hormones and photosynthetic pigments) are essential for plant growth and development, but relatively little is known of how the production of their metabolic precursors via the recently elucidated methylerythritol phosphate (MEP) pathway is regulated. We have identified an Arabidopsis (Arabidopsis thaliana) mutant that survives an otherwise lethal block of the MEP pathway with fosmidomycin (FSM). In rif10 (resistant to inhibition with FSM 10) plants, the accumulation of flux-controlling enzymes of the pathway is posttranscriptionally up-regulated. Strikingly, this phenotype is linked to a lower accumulation of plastidial isoprenoid pigments such as chlorophylls and carotenoids, resulting in mutant plants that are paler and smaller than the wild type. The rif10 mutant is impaired in plastid RNA processing due to a T-DNA insertion in the coding region of the At3g03710 gene encoding the chloroplast-targeted exoribonuclease polyribonucleotide phosphorylase. FSM resistance and other rif10-like phenotypes were also observed in wild-type Arabidopsis, tomato (Lycopersicon esculentum), and rice (Oryza sativa) seedlings grown in the presence of sublethal concentrations of chloramphenicol (an inhibitor of protein synthesis in plastids). By contrast, treatment with norflurazon (an inhibitor of carotenoid biosynthesis causing a similar pale cotyledon phenotype) did not result in FSM resistance. Together, the results support that plastome-encoded proteins are involved in negatively regulating the posttranscriptional accumulation of specific nuclear-encoded MEP pathway enzymes in chloroplasts. Regulation of the MEP pathway by a mechanism dependent on plastid cues might function under physiological conditions to finely adjust plastidial isoprenoid biosynthesis to the metabolic capabilities or requirements of plastids.
Sauret-Güeto
Susanna
S
Departament de Bioquímica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona, 08028 Barcelona, Spain.
Botella-Pavía
Patricia
P
Flores-Pérez
Ursula
U
Martínez-García
Jaime F
JF
San Román
Carolina
C
León
Patricia
P
Boronat
Albert
A
Rodríguez-Concepción
Manuel
M
D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D005578:Fosfomycin / Q000031:analogs & derivatives / Q000494:pharmacology; D018506:Gene Expression Regulation, Plant; D006540:Herbicides / Q000494:pharmacology; D008954:Models, Biological; D009154:Mutation; D010641:Phenotype; D018087:Plastids / Q000378:metabolism*; D011106:Polyisoprenyl Phosphates / Q000378:metabolism; D011724:Pyridazines / Q000494:pharmacology; D018749:RNA, Plant / Q000378:metabolism; D036226:Seedlings / Q000201:enzymology* / Q000235:genetics* / Q000254:growth & development; D015398:Signal Transduction; D013729:Terpenes / Q000378:metabolism*; D014166:Transferases / Q000235:genetics / Q000378:metabolism; D014994:Xylose / Q000031:analogs & derivatives / Q000235:genetics / Q000378:metabolism
D029681:Arabidopsis Proteins; D006540:Herbicides; D011106:Polyisoprenyl Phosphates; D011724:Pyridazines; D018749:RNA, Plant; D013729:Terpenes; C492551:deoxyxylulose phosphate; D005578:Fosfomycin; C024640:fosmidomycin; D014994:Xylose; D014166:Transferases; C109461:deoxyxylulose-5-phosphate synthase; C008677:norflurazone