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Title: The QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions

item LING, LI - Iowa State University
item ZHENG, WENGUANG - Iowa State University
item ZHU, YANBING - Iowa State University
item YE, HUAXUN - Iowa State University
item TANG, BUYUN - Iowa State University
item ARENDSEE, ZEBULUN - Iowa State University
item JONES, DALLAS - Iowa State University
item LI, RUORAN - Iowa State University
item ORTIZ, DIEGO - Iowa State University
item Scott, Marvin
item SALAS FERNANDEZ, MARIA - Iowa State University
item YIN, YANHAI - Iowa State University
item WURTELE, EVE - Iowa State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2015
Publication Date: 11/9/2015
Citation: Ling, L., Zheng, W., Zhu, Y., Ye, H., Tang, B., Arendsee, Z., Jones, D., Li, R., Ortiz, D., Scott, M.P., Salas Fernandez, M.G., Yin, Y., Wurtele, E.S. 2015. QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions. Proceedings of the National Academy of Sciences. 112(47):14734-14739. doi:10.1073/pnas.1514670112.

Interpretive Summary: Grain composition determines the value of grain for specific end uses, but little is known about how grain composition is determined in plants. A gene named QQS was identified in the plant Arabidopsis thaliana that plays a role in determining grain composition. In this manuscript we did experiments to determine how QQS functions to regulate grain composition. We show that the molecular pathway involved is present and can be manipulated to alter grain composition in the important crop species rice, corn and soybean. This work will facilitate the development of crops with altered grain composition in many crops. Increasing the protein content of staple food crops will have a global impact on food production, alleviating malnutrition for millions of people.

Technical 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/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 the original protein content of the cultivar. Furthermore, transgenic QQS-expression increases the protein content of maize, a C4 species, and rice, a protein-poor agronomic crop, both highly divergent from Arabidopsis. We determine that QQS protein binds to the transcriptional regulator, AtNF-YC4 (Nuclear Factor YC4). 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 provide the first insight into the mechanism of action of QQS in modulating carbon and nitrogen allocation across species. They have major implications about the emergence and function of orphan genes and identify a new strategy for modulating protein levels in crop species, a trait of great agronomic significance.