Mechanisms of C4 Photosynthetic Evolution

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C4 photosynthesis enhances productivity and resource-use efficiency in higher plants by inhibiting the wasteful process of photorespiration. Despite its advantages, few major food and fiber crops use the C4 pathway, relying instead on the C3 pathway which can suffer from high rates of photorespiration. To meet growing demands for food, fiber and fuel, there is much interest in further exploiting C4 photosynthesis, either through the engineering of the C4 pathway into C3 crops, improving existing C4 crops, or domesticating wild C4 species. The Sage lab at the University of Toronto is a recognized leader in C4 plant biology, with expertise at the interfaces between molecular mechanisms, genomics, whole plant physiology, photosynthetic evolution, systematics, and ecology/biodiversity. Through our efforts, we have shown that C4 photosynthesis evolved at least 65 times, indicating it is relatively easy to evolve in nature and for humanity to engineer into our C3 crops, such as wheat and rice. By studying how C4 plants evolved, we should be able to learn how to engineer the C4 pathway into C3 plants, and to improve existing C4 crops. In this proposal, funds are requested to support research that will elucidate the physiological, developmental, and molecular mechanisms governing the evolution of C4 photosynthesis. To support this work, we have acquired the world's largest collection of related C3, C4 and C3-C4 intermediate species from 34 independent origins of C4 photosynthesis, including a diverse set of C3-C4 intermediate species from nine C4 evolutionary lineages. This diversity will enable us to use a comparative approach to examine the physiological, developmental and molecular mechanisms by which C4 photosynthesis evolved. In the comparative studies, we will characterize C4 trait acquisition along an evolutionary gradient in genera such as Blepharis and Flaveria, which contain multiple species with intermediate C3- C4 traits. Trait acquisition will then be compared with the species' transcriptomes to identify corresponding shifts in gene expression. We have also generated fertile hybrids of C3 and C4 species of Atriplex which exhibit segregation of C4 traits. Using a combined analysis of parental gene assortment in the transcriptomes of the hybrids, along with measurement of leaf physiology, cell biology and development, we will be able to link genetic controls with the expression of specific C4 traits. Together, the comparative approach and the hybrid analysis will provide us with an unprecedented ability to discover critical controls over C4 trait expression, and to address when during the evolutionary process they were engaged. Through our work, novel gene candidates will be funneled to the C4 Rice effort, contributing to the success of a program that could improve the efficiency of major crops such as rice and wheat by 50% or more, thus eliminating world hunger for the foreseeable future.