CAREER: De novo emergence of novel regulatory mechanisms that determine carbon and nitrogen resource allocations in plants

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The bulk molecular composition of biological systems is determined by complex metabolic networks that mediate the allocation of primarily carbon (C) and nitrogen (N) to the assembly of macromolecules such as proteins, oils, and carbohydrates. This metabolic allocation is of major importance in determining the nutritional quality of plant seeds, which fundamentally affects the ability of the seed to act as the propagule and is also of major importance to agricultural production of food, feed and bio-based feedstocks. The Arabidopsis QQS (Qua-Quine Starch, At3g30720) gene has the potential of being a universal novel regulator of C and N allocation to the assembly of proteins and carbohydrates. QQS is archetypal of a class of “orphan” genes that shares no sequence homology in any other species and is exemplary of the “dark-genome”. When QQS is expressed in crops, it increases protein and decreases starch content. QQS physically interacts with the C4 subunit of the trimeric Nuclear Factor Y (NF-Y) that regulates eukaryotic transcription. The broader impacts of the project include the intrinsic nature of the research, which could provide a major breakthrough in our ability to systematically direct metabolism towards the production of food and feed, and biorenewable resources. In addition, the project will provide excellent projects for postdoctoral researchers, graduate, undergraduate and high/middle/elementary school students and education of plant biotechnology in Mississippi, accessible inter-disciplinary training to increase student exposure to biology early, and to increase the number of early career researchers who may spur innovation in STEM research. The overall research goal is to identify and expand the novel regulatory network that enables QQS to control protein and carbohydrate composition in plants. The overarching hypothesis is that protein-coding orphan genes, which have evolutionarily only recently emerged (e.g., QQS), can be selected and maintained in evolution by acting on existing metabolic networks to mediate responses that confer selective advantages. This research proposes to elucidate the regulatory network that QQS disrupts, which impacts the metabolic network determining protein and carbohydrate content. This research will provide a paradigm for understanding how an orphan gene can be integrated into established genetic and biochemical networks and spur the rapid acquisition of novel traits. Specifically, the QQS protein interacts with NF-YC4 regulatory complex, affecting the C and N partitioning between starch and protein reserves. This attribute is transgenically transferable across species barriers and has the potential to regulate plant reserves to the benefit of human consumption. Moreover, the QQS gene offers unique opportunities to fundamentally understand the intersection between genetic and metabolic networks regulating one of the most important traits in agriculture: seed composition determinants.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.