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Metabolic enzyme involved in seedling establishment provides clues about photosynthetic transition

Mingjie Chen

Mingjie Chen

Columbia, Mo. — The first few days of growth, when a plant switches from growing on reserves to harvesting its own energy, are a make-or-break time for crops. Scientists call this the transition from heterotrophy, a dependence on external sources of energy, to autotrophy, the ability to synthesize energy. In a new study published in The Plant Cell, researchers at the University of Missouri provide significant new information about the metabolic changes that occur during this important turning point in a seed plant's life, which could lead to more targeted plant improvement.

Jay Thelen, MU associate professor of biochemistry, and his team worked with Arabidopsis thaliana, a relative of the canola crop plant that is often used in laboratory studies. Arabidopsis seedlings with mutations in a gene that controls expression of the triose phosphate isomerase (TPI) enzyme show severe growth defects, including shortened roots, pale-green cotyledons (first leaves), and stunted growth, and die before reaching reproductive maturity. Electron microscopy also revealed alterations in the appearance of the chloroplasts, the sites of photosynthesis, in the seedlings.

"There are multiple cellular forms of TPI that are known to be involved in several metabolic pathways," said senior author Mingjie Chen, a postdoctoral research fellow in the Department of Biochemistry and the Christopher S. Bond Life Sciences Center. "Until now, however, the physiological role of the plastid TPI form in planta has been unclear." Metabolic analyses conducted by the researchers found higher levels of four metabolites - glycerol, glycerol phosphate, dihydroxyacetone phosphate and methylglyoxal - in seedlings with the mutations in TPI.

"At these elevated levels, these compounds essentially act as toxins," Chen said. Exogenous applications of the four compounds to normal Arabidopsis seedlings confirmed the toxic effect. "When applied to wildtype seedlings, the substances had a similar deleterious effect on root growth and biosynthesis," Chen said.

The researchers suggest that TPI plays a pivotal role in several metabolic pathways during the transition from seed to seedling. "When the amount of TPI is reduced, these metabolites accumulate in the plastid and, at these high levels, disrupt plastid membrane lipid biosynthesis," Chen said. Lipid composition was also shown to be altered in the mutant plant.

"These metabolic changes would explain the defects in the chloroplast as well as the stunted and chlorotic phenotype," Chen said.

Mutations in TPI have been linked to neurodegenerative diseases in both humans and fruit flies.

Chen, who is also a member of MU's Interdisciplinary Plant Group, sees potential applications of the research to future crop improvement. "Once we have a better understanding of a gene's function at a system level, we will be more capable of predicting the outcome when we try to tinker with the expression of this and other metabolic activities to produce genetically modified plants with desirable traits," he said.

Sjef Smeekens, of Utrecht University, praised the study on the Faculty of 1000 Biology website for illustrating "the importance of metabolic regulation for proper plant functioning" and demonstrating "the power of metabolomics."

The researchers were invited to expand on the implications of the study in an addendum, "The Essential Role of Plastidial Triose Phosphate Isomerase in the Integration of Seed Reserve Mobilization and Seedling Establishment," that appeared in the March online issue of Plant Signaling & Behavior.

Funding for the study was provided by a Plant Genome Program grant from the National Science Foundation and a Life Sciences Postdoctoral Fellowship from MU.