WHITE AND LESION-MIMIC LEAF1, encoding a lumazine synthase, affects reactive oxygen species balance and chloroplast development in rice

Plant J. 2021 Dec;108(6):1690-1703. doi: 10.1111/tpj.15537. Epub 2021 Oct 27.

Abstract

The riboflavin derivatives flavin mononucleotide (FMN) and flavin adenine dinucleotide (FAD) are essential cofactors for enzymes in multiple cellular processes. Characterizing mutants with impaired riboflavin metabolism can help clarify the role of riboflavin in plant development. Here, we characterized a rice (Oryza sativa) white and lesion-mimic (wll1) mutant, which displays a lesion-mimic phenotype with white leaves, chlorophyll loss, chloroplast defects, excess reactive oxygen species (ROS) accumulation, decreased photosystem protein levels, changes in expression of chloroplast development and photosynthesis genes, and cell death. Map-based cloning and complementation test revealed that WLL1 encodes lumazine synthase, which participates in riboflavin biosynthesis. Indeed, the wll1 mutant showed riboflavin deficiency, and application of FAD rescued the wll1 phenotype. In addition, transcriptome analysis showed that cytokinin metabolism was significantly affected in wll1 mutant, which had increased cytokinin and δ-aminolevulinic acid contents. Furthermore, WLL1 and riboflavin synthase (RS) formed a complex, and the rs mutant had a similar phenotype to the wll1 mutant. Taken together, our findings revealed that WLL1 and RS play pivotal roles in riboflavin biosynthesis, which is necessary for ROS balance and chloroplast development in rice.

Keywords: WLL1; chloroplast development; reactive oxygen species balance; riboflavin; rice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chlorophyll / genetics
  • Chlorophyll / metabolism
  • Chloroplasts / physiology*
  • Cytokinins / genetics
  • Cytokinins / metabolism
  • DNA Damage
  • Evolution, Molecular
  • Flavin-Adenine Dinucleotide / genetics
  • Flavin-Adenine Dinucleotide / metabolism
  • Gene Expression Regulation, Plant
  • Multienzyme Complexes / genetics
  • Multienzyme Complexes / metabolism*
  • Mutation
  • Oryza / physiology*
  • Phenotype
  • Phylogeny
  • Plant Leaves / cytology
  • Plant Leaves / genetics
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plants, Genetically Modified
  • Reactive Oxygen Species / metabolism*
  • Riboflavin / genetics
  • Riboflavin / metabolism
  • Two-Hybrid System Techniques

Substances

  • Cytokinins
  • Multienzyme Complexes
  • Plant Proteins
  • Reactive Oxygen Species
  • Chlorophyll
  • Flavin-Adenine Dinucleotide
  • 6,7-dimethyl-8-ribityllumazine synthase
  • Riboflavin