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Comparative Genomic Study Underscores Distinct Properties of Specialized Metabolites in Plants

NEW YORK (GenomeWeb) – Plant genes encoding specialized metabolic functions such as ones that allow plants to fend off predators have spread throughout plants and appear in clusters in their genomes, according to a study published today in Science from researchers at the Carnegie Institute for Science in California.

Using a computational approach, researchers led by Carnegie's Seung Rhee teased out the metabolic networks of some 16 plant species, ranging from algae to angiosperms, as well as the genes involved in those networks.

"We found that, relative to their primary metabolic counterparts, genes coding for specialized metabolic functions have proliferated to a much greater degree and by different mechanisms and display lineage-specific patterns of physical clustering within the genome and co-expression," Rhee and her colleagues said.

Plants produce specialized metabolites to stave off being eaten or infected by a virus, and a number of these compounds have also found a place in human medicine. The researchers noted that more than a third of drugs could be traced to a product synthesized by plants.

To investigate how specialized metabolism has evolved, Rhee and her colleagues compared 16 plant species, including six chlorophyte algae, two early diverging land plants, three grasses, and five eudicots.

They annotated the enzymes encoded in those plants' genomes with four-part Enzyme Commission numbers, and uncovered nearly 1,300 enzymes in Ostreocuccus and more than 12,100 in soybeans. Using these annotated enzymes, the researchers could reconstruct bi-directional, reaction-based metabolic networks. Those networks fell into 13 classes, including primary metabolism-related categories like amino acid, nucleotide, and energy metabolism, in addition to specialized metabolism.

The researchers examined how the networks differed in both their structure and content to tease out how the various metabolic networks diverged.

While the size and density of the networks were similar across the species, the researchers noted that land plants had higher numbers of reaction nodes than, say, did algae. This, they added, suggests that land plants have a more complex set of networks.

Grouping the plants according to their network content reflected species phylogeny, suggesting to Rhee and her colleagues that the evolution of plant metabolic networks followed a decent with modification pattern?, with closely related species sharing similar metabolic reaction sets.

They noted, though, that reconstructing such events across a deep phylogeny like this is "challenged by the paucity of high-quality genome sequence data across the plant kingdom."

Still, the grouping of enzymatic reactions within the plant lineages hints at how metabolic functions changed as the lineages diverged. For instance, the researchers noted that algae were enriched with hormone-related reactions while early land plants were enriched with carbohydrate metabolic reactions.

Many of the metabolic reactions unique to angiosperms were secondary metabolic processes. This, the researchers said, indicates that primary metabolism was likely established earlier in the evolutionary history of plants and that the evolution of specialized metabolism occurred mainly after the rise of vascular plants.

Rhee and her colleagues noted, though, that the "extent of specialized metabolism evolution in basal plant lineages is difficult to ascertain, as much of our knowledge of plant specialized metabolism derives from angiosperms."

The researchers also found that primary and specialized metabolism processes are under differing selective pressures — selective pressures on specialized metabolism seem to be driving the expansion of gene families that code for specific processes, a process that appears to be driven by local duplication events.

Specialized metabolic genes were enriched for local duplication events in Arabidopsis, soybean, and sorghum, according to the researchers. But soybean and sorghum also exhibited significant depletions of whole-genome duplication-derived specialized metabolic genes, they noted.

Rhee and her colleagues also noted that the functional impact of those local duplications were different. For example, they noted a local duplication of sinapate ester production-related genes in Arabidopsis and a local duplication of terpenoid genes linked to phytoalexins in sorghum.

Metabolic genes also appeared to cluster within plant genomes, the researchers reported. About a third of metabolic genes in Arabidopsis, soybean, and sorghum and slightly more than 22 percent of metabolic genes in rice were in clusters.

Arabidopsis and soybean clusters were enriched for specialized metabolism genes, but sorghum and rice clusters were not.

These clustering patterns further varied across species and the classes of metabolic compounds.

In Arabidopsis, phenylpropanoid and terpenoid metabolism-related genes are located in clusters, while nitrogen-containing specialized compound metabolism genes are found in unclustered regions.

But in soybean, by contrast, clustered genes were enriched for nitrogen-containing compounds. And in sorghum, gene clusters were enriched for terpenoid metabolism genes, but phenylpropanoid metabolism genes were not in clusters. Rice had no enrichment patterns.

"The differing results among the four species suggest that specialized metabolic gene clusters are a product of independent, lineage-specific metabolic evolution, rather than a broad mechanism underlying specialized metabolism evolution," Rhee and colleagues said.

Drawing on a large microarray dataset, the researchers found that clusters containing these specialized metabolic genes are more likely to be co-expressed than nonspecialized ones.

"Given that genes in the same metabolic pathway tend to co-express with each other, newly identified clusters exhibiting high degrees of gene co-expression may represent novel metabolic pathways," the researchers said.

They additionally noted that the unusual properties of specialized metabolic genes — differences in how they evolved, tendency to clustering, and their penchant toward co-expression — could form a sort of signature to detect other specialized metabolic genes.

"We hope that our findings will enable researchers to use these signatures as a tool to discover previously unknown specialized metabolites, to investigate how they benefit the plant, and to determine how they might benefit us," Rhee said in a statement.