Salk Institute for Biological Studies


Joseph P. Noel

Joseph P. Noel

Professor and Director, Jack H. Skirball Center for Chemical Biology and Proteomics
Howard Hughes Medical Institute Investigator
Arthur and Julie Woodrow Chair




Mechanistic and Structural Basis for Plant Metabolic Evolution

What shapes natural selection of specialized enzymes and metabolic pathways underlying the emergence and expansion of chemical diversity in living systems remains a fundamental yet largely unanswered question in evolutionary biology. For sessile organisms possessing the developmental and ecological complexity of plants, this adaptive process is especially critical to their survival. The chemical output of these metabolic pathways serve as key mediators of intra- and interspecies interactions resulting in speciation, survival and ecological homeostasis. Specifically, we seek to understand and infer as best as possible the adaptive molecular changes that have occurred in plant specialized metabolism as these enzyme systems emerged and subsequently evolved from their ancestral roots in primary metabolism at the dawn of terrestrial plants nearly 500 millions ago.

Early land plants arose from freshwater ecological niches. Their success on land, driven by evolutionary adaptations such as their ability to screen out damaging UV radiation, their adeptness at resisting desiccation and their mastery of self-support and fluid conduction, had far-reaching consequences for the complexity of terrestrial ecosystems that followed this defining event on the terrestrial earth. Land plant early success and the ongoing diversification of the green plant lineage was then and is to this day due in large part to their ability to biosynthesize specialized or so-called secondary metabolites.

Through photosynthesis, early land plants provided major nutritional stores that precipitated the dawn and development of almost all the early terrestrial life forms, including tetrapods, insects, fungi and even microorganisms. In turn, the rise of land plants profoundly impacted the global climate. For example, carbon fixation by early land plants is considered one of the major factors that led to the significant drop of atmospheric CO2 levels and a corresponding increase of O2 levels during the late Palaeozoic era. These changes in atmospheric composition, in turn, precipitated more physiological innovations, e. g. the evolution of aerial locomotion in insects and the origin of megaphyll leaves in plants.

Given the momentous contribution of plant specialized metabolism to the biodiversity of the terrestrial earth, specialized metabolic pathways and their "chemical output" present us with a rich evolutionary record of where biosynthetic pathways, natural chemicals and biosynthetic enzymes have been (vestigial biochemical traits), what adaptive advantages these complex enzymatic systems hold in the present (emergent function), and ultimately where these pathways may be heading in the future (functional plasticity).

Our decade-long study of these metabolic pathways has coalesced around four fundamental questions regarding the origin of specialized metabolism during land plant evolution. (i) Can one discern the phylogenetic routes through which plant secondary metabolic enzymes evolved from their primary metabolic ancestors? (ii) What are the biophysical features inherited by these enzymes that give rise to evolvability and/or restrain such evolutionary processes? (iii) How was the evolutionary directionality maintained if at all before the emergence of the defining activities that provided obvious selective advantages? (iv) What role did catalytic promiscuity play in shaping the evolvability of these biosynthetic systems? Answering these questions not only will extend our understanding of the biochemical strategies that early land plants adopted in their adaptation to a myriad of terrestrial environments, but will also better shape our appreciation of mutability and the origins of new enzyme function in general. Our work examines the evolution, biology, biochemistry and chemistry underlying the biosynthesis of plant natural products including isoprenoids, phenylpropanoids, polyketides and associated flavonoids and fatty acid-derived metabolites.

"Nature has been perfecting enzymes for at least three billion years because they carry out the hundreds of thousands of chemical reactions in all organisms, and these reactions are needed by us all to survive and prosper. We could learn a lot by understanding that three-billion-year-old experiment."

Noel's laboratory explores how specialized enzymes and metabolic pathways allowed plants to adapt and spread across the planet and what these mechanisms can tell us about improving modern-day agriculture. His team discovered a family of plant proteins that plays a role in the production of seed oils, substances important for animal and human nutrition, biorenewable chemicals and biofuels.

Plant oils are composed primarily of triglycerides, formed by linking together three fatty acid molecules, and are stored mostly in seeds, where they are used for energy during germination. Seeds are crucial sources of oils for nutrition, flavoring and industrial applications, such as the production of soap, cosmetics and biofuels. With growing concerns about global climate change and petroleum security, producing biofuels for use in transportation and energy generation is a burgeoning industry.

Scoring a rare scientific hat trick, Noel's lab identified three related proteins in thale cress plants (Arabidopsis thaliana) that regulate the metabolism of fatty acids, chemical components of all cell membranes and vegetable oils. They dubbed these fatty acid– binding proteins FAP1, FAP2 and FAP3. They found that the proteins bind fatty acids, including the major plant omega-3 fatty acid, an important nutritional component found in certain seeds.

This work has major implications for modulating the fatty acid profiles of plants, which is important to sustainable production of food, biorenewable chemicals and fuels. Because very high-energy molecules such as fatty acids are created in the plant by solar energy, these types of molecules may ultimately provide the most efficient sources for biorenewable products.

The findings of Noel's lab may lead to the development of improved crops yielding higher qualities and quantities of oils, helping to address growing demands for food and fuel and the consequent environmental pressures on the world's ecosystems. The discovery may also help bioengineers focused on creating new enzymes for industrial uses by revealing how nature evolves proteins into chemical machines known as enzymes.

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