Switching roles: Flipped pathway in tomato "hairs" gives rise to new plant traits, biology approaches

  • Jan 14, 2018
  • agricultural pests, evolution, postdoctoral researchers, Plant science
  • Homepage News, Faculty & Staff, Research, Biochemistry, College of Natural Science, Plant Biology

A collaborative study led by Michigan State University researchers has documented a metabolic pathway event that happened during the past 3 million years, leading to the production of a new set of defensive acyl sugars (a class of compounds that play a critical role in allowing wild tomatoes to fend off bugs) in the hair-like protrusions of tomatoes known as trichomes.

The research, published recently in the journal Nature Communications, demonstrates how small numbers of amino acid changes in multiple pathway enzymes can lead to diversification of specialized metabolites in plants.

Image of Pengxiang Fan preparing biochemical assays of tomato enzymes in his lab.

Pengxiang Fan, a research associate in Barnett Rosenberg Professor Robert Lats's lab (above), sets up biochemical assays to test enzymatic functions in the tomato enzymes he is studying. Photo courtesy Robert Last lab.

“I think the importance of this is reflected in two key ways,” said Pengxiang Fan, a research associate in the laboratory of Robert Last, Barnett Rosenberg Professor in the Departments of Biochemistry and Molecular Biology (BMB) and Plant Biology in the MSU College of Natural Science, and lead author of the study.  

“First, these results are an elegant example of how simple changes in multiple genes can lead to the evolution of a new trait,” Fan explained. “These mutations altered their enzymatic functions and finally led to the switch of their roles in the modern pathway – so-called ‘flipped pathway’ – giving rise to the new acyl sugar types.

“Second, elucidation of the molecular basis for acylsugar chemical diversity combined with the ability to modify the acylsugar types in the plant provides opportunities for synthetic biology approaches to exploit the beneficial properties of these compounds as natural pesticides.”

For example, Fan said the key amino acid residues that shaped the acylsugar biosynthetic pathway could be used as metabolic engineering targets to facilitate breeding of desired acylsugar chemotypes in crops, which could ultimately reduce pesticides use in the field.

“The evolutionary milestone for the production of the new acylsugar chemotype is the result of accumulated mutations in two biosynthetic enzymes of a more ancient pathway,” Fan added.

The project focused on an area not previously well exploited in plants—evolutionary biochemistry—and required knowledge from different fields to complete many pieces of the puzzle. These included plant transformation, enzyme assay, compound purification, chemical identification by nuclear magnetic resonance (NMR), and building phylogenetic trees for evolutionary analysis.

While Fan conceived the project and saw it through to manuscript publication, collaboration was key, he said, as various techniques would be impossible for one person to master.

MSU BMB Professor Dan Jones’ lab led identification of the chemical structures for the key enzymatic products, which set the basis for the hypotheses in the early stage of the study. Evolutionary biologist Gaurav Moghe, who previously worked in Last’s lab and is now an assistant professor at Cornell University, and Shin-Han Shiu, professor of plant biology at MSU, also provided insights that helped build rigorous interpretations of the evolutionary relationships of the two pathways.

The project also influenced then-undergraduate student Abigail Miller, who received the American Society of Plant Biologists Summer Undergraduate Research Fellowship award under Fan’s mentoring. Miller is now a Ph.D. student working in the Department of Molecular Biology and Genetics at Cornell University.

“This study, along with recently published work from Cornelius Barry’s group in the MSU Department of Horticulture and the Jones labs in BMB and chemistry, reveals how metabolic evolution creates novel traits from seemingly simple changes in biosynthetic enzymes,” said Last, senior author of the paper. “Ultimately, this work should lead to a deep understanding of how plant natural defenses evolved, and these insights will suggest new ways to breed or engineer crops that thrive with less insecticide treatments.” 

 

Banner image: The structure of F-type acylsugars found in cultivated tomato trichomes (background image) is in contrast with P-type found in wild tomatoes, demonstrating how metabolic evolution creates novel traits from seemingly simple changes in biosynthetic enzymes. Photo courtesy of the Rob Last laboratory.