Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development

Plant Physiol. 2009 May;150(1):388-401. doi: 10.1104/pp.109.136648. Epub 2009 Mar 18.

Abstract

The virescent3 (v3) and stripe1 (st1) mutants in rice (Oryza sativa) produce chlorotic leaves in a growth stage-dependent manner under field conditions. They are temperature-conditional mutants that produce bleached leaves at a constant 20 degrees C or 30 degrees C but almost green leaves under diurnal 30 degrees C/20 degrees C conditions. Here, we show V3 and St1, which encode the large and small subunits of ribonucleotide reductase (RNR), RNRL1, and RNRS1, respectively. RNR regulates the rate of deoxyribonucleotide production for DNA synthesis and repair. RNRL1 and RNRS1 are highly expressed in the shoot base and in young leaves, and the expression of the genes that function in plastid transcription/translation and in photosynthesis is altered in v3 and st1 mutants, indicating that a threshold activity of RNR is required for chloroplast biogenesis in developing leaves. There are additional RNR homologs in rice, RNRL2 and RNRS2, and eukaryotic RNRs comprise alpha(2)beta(2) heterodimers. In yeast, RNRL1 interacts with RNRS1 (RNRL1:RNRS1) and RNRL2:RNRS2, but no interaction occurs between other combinations of the large and small subunits. The interacting activities are RNRL1:RNRS1 > RNRL1:rnrs1(st1) > rnrl1(v3):RNRS1 > rnrl1(v3):rnrs1(st1), which correlate with the degree of chlorosis for each genotype. This suggests that missense mutations in rnrl1(v3) and rnrs1(st1) attenuate the first alphabeta dimerization. Moreover, wild-type plants exposed to a low concentration of an RNR inhibitor, hydroxyurea, produce chlorotic leaves without growth retardation, reminiscent of v3 and st1 mutants. We thus propose that upon insufficient activity of RNR, plastid DNA synthesis is preferentially arrested to allow nuclear genome replication in developing leaves, leading to continuous plant growth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Division
  • Chloroplasts / drug effects
  • Chloroplasts / metabolism*
  • Chromosome Mapping
  • Chromosomes, Plant
  • Cloning, Molecular
  • Gene Expression Profiling
  • Genetic Complementation Test
  • Hydroxyurea / pharmacology
  • Mutation
  • Oryza / drug effects
  • Oryza / genetics
  • Oryza / growth & development*
  • Oryza / metabolism
  • Phenotype
  • Plant Leaves / drug effects
  • Plant Leaves / genetics
  • Plant Leaves / growth & development
  • Plant Leaves / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Proteins / physiology*
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Protein Subunits / physiology
  • Ribonucleotide Reductases / genetics
  • Ribonucleotide Reductases / metabolism
  • Ribonucleotide Reductases / physiology*

Substances

  • Plant Proteins
  • Protein Subunits
  • Ribonucleotide Reductases
  • Hydroxyurea