title: QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions.
abstract: The allocation of carbon and nitrogen resources to the synthesis of plant proteins, carbohydrates, and lipids is complex and under the control of many genes; much remains to be understood about this process. QQS (Qua-Quine Starch; At3g30720), an orphan gene unique to Arabidopsis thaliana, regulates metabolic processes affecting carbon and nitrogen partitioning among proteins and carbohydrates, modulating leaf and seed composition in Arabidopsis and soybean. Here the universality of QQS function in modulating carbon and nitrogen allocation is exemplified by a series of transgenic experiments. We show that ectopic expression of QQS increases soybean protein independent of the genetic background and original protein content of the cultivar. Furthermore, transgenic QQS expression increases the protein content of maize, a C4 species (a species that uses 4-carbon photosynthesis), and rice, a protein-poor agronomic crop, both highly divergent from Arabidopsis. We determine that QQS protein binds to the transcriptional regulator AtNF-YC4 (Arabidopsis nuclear factor Y, subunit C4). Overexpression of AtNF-YC4 in Arabidopsis mimics the QQS-overexpression phenotype, increasing protein and decreasing starch levels. NF-YC, a component of the NF-Y complex, is conserved across eukaryotes. The NF-YC4 homologs of soybean, rice, and maize also bind to QQS, which provides an explanation of how QQS can act in species where it does not occur endogenously. These findings are, to our knowledge, the first insight into the mechanism of action of QQS in modulating carbon and nitrogen allocation across species. They have major implications for the emergence and function of orphan genes, and identify a nontransgenic strategy for modulating protein levels in crop species, a trait of great agronomic significance.
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011; Center for Metabolic Biology, Iowa State University, Ames, IA 50011; liling@iastate.edu mash@iastate.edu.
authors.forename: Ling
authors.initials: L
authors.lastname: Li
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011; Center for Metabolic Biology, Iowa State University, Ames, IA 50011;
authors.forename: Wenguang
authors.initials: W
authors.lastname: Zheng
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Yanbing
authors.initials: Y
authors.lastname: Zhu
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Huaxun
authors.initials: H
authors.lastname: Ye
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Buyun
authors.initials: B
authors.lastname: Tang
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Zebulun W
authors.initials: ZW
authors.lastname: Arendsee
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Dallas
authors.initials: D
authors.lastname: Jones
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Ruoran
authors.initials: R
authors.lastname: Li
authors.affiliation: Department of Agronomy, Iowa State University, Ames, IA 50011;
authors.forename: Diego
authors.initials: D
authors.lastname: Ortiz
authors.affiliation: Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA 50011;
authors.forename: Xuefeng
authors.initials: X
authors.lastname: Zhao
authors.affiliation: Department of Statistics, Iowa State University, Ames, IA 50011;
authors.forename: Chuanlong
authors.initials: C
authors.lastname: Du
authors.affiliation: Department of Statistics, Iowa State University, Ames, IA 50011;
authors.forename: Dan
authors.initials: D
authors.lastname: Nettleton
authors.affiliation: Department of Agronomy, Iowa State University, Ames, IA 50011; Corn Insects and Crop Genetics Research Unit, Agricultural Research Service, US Department of Agriculture, Ames, IA 50011.
authors.forename: M Paul
authors.initials: MP
authors.lastname: Scott
authors.affiliation: Department of Agronomy, Iowa State University, Ames, IA 50011;
authors.forename: Maria G
authors.initials: MG
authors.lastname: Salas-Fernandez
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011;
authors.forename: Yanhai
authors.initials: Y
authors.lastname: Yin
authors.affiliation: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA 50011; Center for Metabolic Biology, Iowa State University, Ames, IA 50011; liling@iastate.edu mash@iastate.edu.
authors.forename: Eve Syrkin
authors.initials: ES
authors.lastname: Wurtele
mesh_terms: D017360:Arabidopsis / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002244:Carbon / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D008954:Models, Biological; D009154:Mutation; D009584:Nitrogen / Q000378:metabolism*; D012275:Oryza / Q000235:genetics; D010641:Phenotype; D010788:Photosynthesis; D010802:Phylogeny; D018515:Plant Leaves / Q000502:physiology; D030821:Plants, Genetically Modified; D011485:Protein Binding; D017434:Protein Structure, Tertiary; D013025:Glycine max / Q000235:genetics / Q000254:growth & development; D013045:Species Specificity; D014157:Transcription Factors / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; C000605821:NF-YC4 protein, Arabidopsis; C000601590:QQS protein, Arabidopsis; D014157:Transcription Factors; D002244:Carbon; D009584:Nitrogen
keywords: NF-YC4; QQS; carbon allocation; nitrogen allocation; orphan