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Transcriptome Study IDs Organ-Specific Plant Pathogen, Host Interactions

By Andrea Anderson

NEW YORK (GenomeWeb News) – An American and German research team has garnered evidence of organ-specific gene expression patterns for a plant pathogen and its host.

The researchers used microarrays to gauge gene expression in the parasitic fungus Ustilago maydis and its maize host, looking at a range of infected maize tissues. Their results suggest fungal gene expression varies depending on where the infection occurs in the corn plant. Similarly, infection by the fungus altered the expression of distinct plant genes in different corn organs. The research appears online today in Science.

"Ustilago expresses different genes depending where it is in the plant," senior author Virginia Walbot, a Stanford University biologist, told GenomeWeb Daily News. "Presumably the fungus is able to detect the key characteristics of the different [maize] organs."

While researchers once assumed that pathogens used all available weapons to attack their hosts, she explained, the new research suggests some pathogens can tweak their gene expression to fine-tune their exploitation of the host.

U. maydis is a fungus that infects maize and its wild ancestor teosinte, causing a condition called corn smut that is characterized by excessive cell division and tumor formation in plant leaves, stem, and flowers (collectively known as "aerial organs").

The pathogen's genome sequence, published in Nature in 2006, revealed a dozen gene clusters coding for proteins that are secreted when the fungus infects plants. Of these, at least five gene clusters seem to contribute to the formation of tumors in corn.

While U. maydis is not a major economic pest, Walbot said, it is a useful model system for studying a range of biological processes — from meiosis to plant-pathogen interactions. Consequently, she added, clues from the current study may help inform studies of other plant and animal parasites and their hosts.

For the current study, Walbot and her team used custom, duel organism Agilent arrays to simultaneously assess the expression of about 6,700 U. maydis genes and 36,800 maize genes in several infected corn tissues.

They found that the sets of corn genes that were differentially expressed during the fungal infection varied by tissue. Fewer than 250 common transcripts were up-regulated or turned on in all of the infected tissues, and just 135 were down-regulated in all of these tissues.

"Host responses were primarily organ-specific in both the up- and down-regulated classes," the researchers wrote.

Likewise, U. maydis gene expression patterns shifted depending on the pathogen's location in the plant. For example, the team reported that at least 118 of the transcripts coding for U. maydis secretory proteins were differentially expressed depending on the maize organ tested.

The team confirmed the organ-specific interactions between the fungus and plant through a set of experiments involving corn plants with mutations in specific gene pathways.

"Collectively, the gene expression and genetic findings demonstrate organ-specific expression of U. maydis effectors, showing essential roles in tumorigenesis," the researchers explained. "These secretome proteins, which likely constitute the majority of effector molecules eliciting host responses, indicate deployment of different 'weapons' tuned to host organ properties."

More research is needed to understand whether pathogens infecting other plants and animals show similar fine-tuning of gene expression based on their location in the host, Walbot noted. But, she said, if human pathogens show such characteristics, it's possible that future treatments could be more carefully targeted based on where pathogens are most active in the body.

The findings may also have implications for plant-breeding programs aimed at developing resistance to more economically important plant pathogens.

For their part, Walbot and her team plan to exploit the wide range of compounds secreted by U. maydis during infection to study various aspects of plant biology. For example, the group plans to collaborate with researchers from a neighboring lab to implant miniature cameras inside corn flowers treated with fungal proteins to visually track the cellular effects.

"We now have hundreds of potential disruptive drugs," Walbot said. "It's very exciting."

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