Yellow-Leaf 1 encodes a magnesium-protoporphyrin IX monomethyl ester cyclase, involved in chlorophyll biosynthesis in rice (Oryza sativa L.)

Magnesium-protoporphyrin IX monomethyl ester cyclase (MPEC) catalyzes the conversion of MPME to divinyl protochlorophyllide (DVpchlide). This is an essential enzyme during chlorophyll (Chl) biosynthesis but details of its function in rice are still lacking. Here, we identified a novel rice mutant yellow-leaf 1 (yl-1), which showed decreased Chl accumulation, abnormal chloroplast ultrastructure and attenuated photosynthetic activity. Map-based cloning and over-expression analysis suggested that YL-1 encodes a subunit of MPEC. The YL-1 protein localizes in chloroplasts, and it is mainly expressed in green tissues, with greatest abundance in leaves and young panicles. Results of qRT-PCR showed that Chl biosynthesis upstream genes were highly expressed in the yl-1 mutant, while downstream genes were compromised, indicating that YL-1 plays a pivotal role in the Chl biosynthesis. Furthermore, the expression levels of photosynthesis and chloroplast development genes were also affected. RNA-seq results futher proved that numerous membrane-associated genes, including many plastid membrane-associated genes, have altered expression pattern in the yl-1 mutant, implying that YL-1 is required for plastid membrane stability. Thus, our study confirms a putative MPME cyclase as a novel key enzyme essential for Chl biosynthesis and chloroplast membrane stability in rice.

[1]  D. Klessig,et al.  DAMPs, MAMPs, and NAMPs in plant innate immunity , 2016, BMC Plant Biology.

[2]  H. Zhai,et al.  The catalytic subunit of magnesium-protoporphyrin IX monomethyl ester cyclase forms a chloroplast complex to regulate chlorophyll biosynthesis in rice , 2016, Plant Molecular Biology.

[3]  Y. Ling,et al.  Map-based cloning and functional analysis of YGL8, which controls leaf colour in rice (Oryza sativa) , 2016, BMC Plant Biology.

[4]  H. Lütken,et al.  Towards development of new ornamental plants: status and progress in wide hybridization , 2016, Planta.

[5]  G. Johnsen,et al.  Divinyl chlorophyll a in the marine eukaryotic protist Alexandrium ostenfeldii (Dinophyceae). , 2016, Environmental microbiology.

[6]  Q. Qian,et al.  PGL, encoding chlorophyllide a oxygenase 1, impacts leaf senescence and indirectly affects grain yield and quality in rice , 2015, Journal of experimental botany.

[7]  Fuqing Wu,et al.  Young Seedling Stripe1 encodes a chloroplast nucleoid-associated protein required for chloroplast development in rice seedlings , 2016, Planta.

[8]  M. Hansson,et al.  The Ycf54 protein is part of the membrane component of Mg‐protoporphyrin IX monomethyl ester cyclase from barley (Hordeum vulgareL.) , 2014, The FEBS journal.

[9]  Li-hong Xie,et al.  The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions , 2014, Plant Molecular Biology.

[10]  Guixue Wang,et al.  Mutation of OsDET1 increases chlorophyll content in rice. , 2013, Plant science : an international journal of experimental plant biology.

[11]  Koji Watanabe,et al.  Spectral properties of a divinyl chlorophyll a harboring mutant of Synechocystis sp. PCC6803 , 2013, Photosynthesis Research.

[12]  N. Su,et al.  A Rice Virescent-Yellow Leaf Mutant Reveals New Insights into the Role and Assembly of Plastid Caseinolytic Protease in Higher Plants1[W][OPEN] , 2013, Plant Physiology.

[13]  Wenming Wang,et al.  One Divinyl Reductase Reduces the 8-Vinyl Groups in Various Intermediates of Chlorophyll Biosynthesis in a Given Higher Plant Species, But the Isozyme Differs between Species1[W][OA] , 2012, Plant Physiology.

[14]  Meizhong Luo,et al.  C‐terminal residues of Oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis , 2012, FEBS letters.

[15]  S. Bischof,et al.  FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++‐branch of this pathway , 2012, FEBS letters.

[16]  Hisashi Ito,et al.  Evolution of a divinyl chlorophyll-based photosystem in Prochlorococcus , 2011, Proceedings of the National Academy of Sciences.

[17]  Fantao Zhang,et al.  Divinyl Chlorophyll(ide) a Can Be Converted to Monovinyl Chlorophyll(ide) a by a Divinyl Reductase in Rice1[W] , 2010, Plant Physiology.

[18]  Jiedao Zhang,et al.  Tissue-specific expression of the PNZIP promoter is mediated by combinatorial interaction of different cis-elements and a novel transcriptional factor , 2009, Nucleic acids research.

[19]  O. Matsuda,et al.  Contribution of chloroplast biogenesis to carbon–nitrogen balance during early leaf development in rice , 2009, Journal of Plant Research.

[20]  T. Masuda,et al.  Regulation and evolution of chlorophyll metabolism , 2008, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[21]  Young Sim Son,et al.  Role of Arabidopsis CHL27 protein for photosynthesis, chloroplast development and gene expression profiling. , 2008, Plant & cell physiology.

[22]  Young Sim Son,et al.  Role of Arabidopsis CHL 27 Protein for Photosynthesis , Chloroplast Development and Gene Expression Profiling , 2008 .

[23]  M. Yano,et al.  The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. , 2007, The Plant journal : for cell and molecular biology.

[24]  Ya-ping Fu,et al.  Identification and fine mapping of a thermo-sensitive chlorophyll deficient mutant in rice (Oryza sativa L.) , 2007, Planta.

[25]  Ning Su,et al.  A Chlorophyll-Deficient Rice Mutant with Impaired Chlorophyllide Esterification in Chlorophyll Biosynthesis1[W][OA] , 2007, Plant Physiology.

[26]  P. L. Mitchell,et al.  Supercharging rice photosynthesis to increase yield. , 2006, The New phytologist.

[27]  Kenji Umemura,et al.  A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. , 2006, Molecular plant pathology.

[28]  H. Seo,et al.  Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development , 2006, Plant Molecular Biology.

[29]  S. Merchant,et al.  Xantha-l encodes a membrane subunit of the aerobic Mg-protoporphyrin IX monomethyl ester cyclase involved in chlorophyll biosynthesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. An,et al.  Differential regulation of chlorophyll a oxygenase genes in rice , 2005, Plant Molecular Biology.

[31]  B. Grimm,et al.  Recent advances in chlorophyll biosynthesis and breakdown in higher plants , 2004, Plant Molecular Biology.

[32]  J. Brusslan,et al.  Chlorophyllide a Oxygenase mRNA and Protein Levels Correlate with the Chlorophyll a/b Ratio in Arabidopsis thaliana , 2004, Photosynthesis Research.

[33]  B. M. Lange,et al.  Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism , 2003, Plant Molecular Biology.

[34]  S. Merchant,et al.  Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  P. Fromme,et al.  Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems , 2003, FEBS letters.

[36]  K. Jung,et al.  Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. , 2003, Plant & cell physiology.

[37]  J. Ecker,et al.  GUN4, a Regulator of Chlorophyll Synthesis and Intracellular Signaling , 2003, Science.

[38]  S. Merchant,et al.  Reciprocal Expression of Two Candidate Di-Iron Enzymes Affecting Photosystem I and Light-Harvesting Complex Accumulation , 2002, The Plant Cell Online.

[39]  M. Picaud,et al.  Rubrivivax gelatinosus acsF (Previously orf358) Codes for a Conserved, Putative Binuclear-Iron-Cluster-Containing Protein Involved in Aerobic Oxidative Cyclization of Mg-Protoporphyrin IX Monomethylester , 2002, Journal of bacteriology.

[40]  S. Merchant,et al.  The Crd1 gene encodes a putative di‐iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii , 2000, The EMBO journal.

[41]  J. Brusslan,et al.  The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Kuroiwa,et al.  Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles , 1998, Planta.

[43]  T. Kuroiwa,et al.  Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles. Investigations of tissues and cells by fluorescence microscopy. , 1998, Planta.

[44]  C. Zheng,et al.  PNZIP is a novel mesophyll-specific cDNA that is regulated by phytochrome and the circadian rhythm and encodes a protein with a leucine zipper motif. , 1998, Plant physiology.

[45]  Takanori Hirano,et al.  Engineered GFP as a vital reporter in plants , 1996, Current Biology.

[46]  M. Maroof,et al.  Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. , 1994, Proceedings of the National Academy of Sciences of the United States of America.