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Scientists See Extensive Transcript Swaps Between Parasitic Plant and Hosts

NEW YORK (GenomeWeb) – A parasitic strangleweed plant called dodder routinely swaps protein-coding transcripts with its host plants, according to a study published online today in Science.

Researchers from Virginia Tech and Pennsylvania State University used transcriptome sequencing to track interactions between the dodder (Cuscuta pentagona) and two different host plants — tomato or Arabidopsis thaliana.

Their results revealed extensive messenger RNA transfer back and forth between the nutrient- and water-sucking parasite and its hosts. This bidirectional movement involved mobile transcripts corresponding to hundreds or thousands of genes, depending on the host species involved.

"We were surprised to see that the transcripts [detected] represent a broad cross-section of the transcriptome in the parasitized tissue," senior author James Westwood, a plant pathology, physiology, and weed science researcher at Virginia Tech, told GenomeWeb Daily News.

The dodder plant saps resources from other plants by wrapping itself around and piercing the host's stem to tap into the existing plant vasculature. In this manner, the parasite draws on not only on material consumed by its host, but also host plant products such as mRNA.

Exchanges of some mRNA, viral particles, and other molecules have been documented in the past. But the team decided to take a closer look at the extent of transcript exchange between C. pentagona and its hosts for the current study, as well as the directionality of these molecular swaps.

After growing the parasitic plant on Arabidopsis and tomato hosts — plants with sequenced genomes — the researchers harvested tissue samples from each host-parasite pair before doing RNA sequencing on the samples using Illumina GAIIx or HiSeq 2000 instruments.

"We [sampled] the region of connection and then we took host and parasite stem samples adjacent to that region, so that we would have pure host and pure parasite tissue," Westwood explained.

He and his colleagues then sorted through the sequences to group together reads originating in the parasitic plant, Arabidopsis, or tomato plant.

Transcripts from genes that are too highly conserved to be assigned to one plant or another got tossed before the team mapped the remaining reads to the tomato, Arabidopsis, or newly formed Cuscuta transcriptome assemblies.

In each of the host-parasite pairs, the researchers saw signs of bidirectional mRNA exchange between plants — a phenomenon they further verified by reverse transcription PCR.

Transcript movement was more pronounced between the dodder and Arabidopsis plants than it was between the parasite and tomato, they noted, though the same general patterns occurred in each host-parasite system.

Nearly half of the transcripts produced by Arabidopsis plants turned up in the Cuscuta parasite, for example. On the other hand, the team found just a few hundred tomato transcripts roaming in the parasite, representing roughly 1.6 percent of genes expressed by tomato.

The apparent disparity in transcript exchange accomplished by each host plant may be partly due to differences in sequencing depth used for the experiment, the study's authors noted, though at least some of the effect is believed to be due to features of the host at hand.

"We learned that we need really deep sequencing to get the best data, but that doesn't fully explain the Arabidopsis-tomato differences," Westwood said. "I think there's a real biological difference there."

He noted that the connections dodder makes with each different host may have different properties, though it remains to be seen whether these interactions vary as a result of host anatomy, physiology, or other factors.

Preliminary evidence from the team's follow-up experiments hint that Arabidopsis is especially prone to giving up and taking in mRNAs via interactions with the parasitic dodder plant, he explained, while other plants tested seem to show mobile transcript patterns that are more similar to those detected in tomato.

When they looked at the number and nature of the dodder plant transcripts that had made their way into host plants, meanwhile, researchers once again saw signs of more extensive exchange with Arabidopsis — a host plant that took up transcripts representing almost one-quarter of the 35,614 Cuscuta genes considered.

Again, movement in tomato was more modest. There, the team tracked down transcripts coinciding with fewer than 300 Cuscuta genes.

To get a better sense of the transcript types most prone to mobility, the researchers went on to consider clusters of comparable mobile and non-mobile transcripts from all three plants.

While there appeared to be some relationship between a gene's functional role and the movement of its corresponding transcript, more work is needed to untangle the still murky biological processes involved.

Further research will also be required to understand how wandering transcripts contribute to parasite control over their hosts, if at all, and to assess potential contributions that parasitic plants such as dodder make to horizontal gene transfer between plants.

"It would be very fun to know if a dodder [plant] bridging two hosts could convey RNA or DNA between them or somehow serve as a medium for gene transfer," Westwood said.

In the nearer term, he and his team plan to investigate transcript exchanges between dodder and other host plants. They also hope to figure out whether transcripts that move out of the host are actually translated in the parasite and vice versa.