ABOVE: Plant cells form a graft union between cells. Plastids are labeled red throughout the graft and nuclei and cytosol are labeled in blue on one side of the graft (bottom). Plastid genome exchange is indicated by arrowheads.
HERTLE ET AL., SCIENCE ADVANCES, 2021
Past genetic experiments have shown that, when plants are grafted together, entire genomes can move between the host and the graft, but it was not clear how the genetic material was traveling. In a study published January 1 in Science Advances, researchers demonstrated that entire organelles can move between plant cells, bringing their genomes along for the ride.
In the studies before this one, “there was no way to rationally explain how a whole genome got over, other than it went into an organelle. Otherwise, you would have seen genetic recombination between an incoming genome and the resident genome,” says Pal Maliga, a plant biologist at Rutgers University who did not participate in the work. The nucleus, mitochondria, and plastids—the group of small organelles that includes chloroplasts—all contain genetic material. Researchers therefore made the inference that the genomes were moving via organelles, he explains, “but this paper is beautifully showing what the details are. I was very happy to see that the assumptions that were there to explain the biology are actually real.”
A team led by Ralph Bock of the Max Planck Institute of Molecular Plant Physiology showed in a study published in 2009 that grafted tobacco plants could share entire genomes. Horizontal gene transfer—when genetic material passes between individuals via some method other than fertilization—has been shown to influence plant evolution at various levels, including sharing of beneficial genes, but the movement of entire genomes is much less common and understood. While the initial and subsequent studies hinted that the transferred DNA was likely coming from the genomes contained in moving organelles, researchers couldn’t be sure that naked DNA wasn’t being shared in large chunks.
Enter Alexander Hertle, a postdoc at the institute with extensive microscopy experience. He and Bock came together to combine the Bock lab’s years of genetic evidence in support of organelle movement and Hertle’s imaging expertise. “I was interested in seeing if that is really true, what [Bock’s] showing in his papers,” Hertle says.
In the current study, the researchers used tobacco plants that contained an antibiotic resistance gene and a fluorescent reporter in the nuclear genome and another strain with a different antibiotic resistance gene and fluorescent reporter in the chloroplast genome. When they grafted the plants together, resulting plants grew on growth medium containing both antibiotics and produced both fluorescent reporters. These findings were consistent with earlier studies, but still did not allow the scientists to distinguish between transfer of genomic information via organelles or naked DNA.
To make this distinction, the authors dissected the tissue at the graft junction and imaged the cells, both live and after fixing. This revealed plastids near pores in the cell walls and spots where the cytoplasm of one cell protruded into another. The researchers also found plastids that were smaller than resident plastids—small enough to move through the pores between cells. During live imaging, these mini plastids moved in an ameboid way from one cell to another. The team also showed that these traveling organelles contained DNA, confirming that they could be a source of the genomic transfer the researchers had observed genetically.
While they cannot entirely rule out that naked DNA is moving between cells, “what we saw live . . . was that the organelles can go from one cell into the other,” Hertle says.
The “outstanding question is, why is this actually happening?” says Charles Melnyk, a plant biologist at the Swedish University of Agricultural Sciences who did not participate in the study. The authors have looked at this in the context of grafting, which is precipitated by wounding the plants, he adds. “As soon as a plant cell gets damaged, it seems like it’s changing its cell wall properties, and then these changes are then allowing these type of transfer events to occur.”
“Maybe plant cells do this, even without the graft, but somebody has to look,” Maliga says.
A.P. Hertle et al., “Horizontal genome transfer by cell-to-cell travel of whole organelles,” Science Advances, doi:10.1126/sciadv.abd8215, 2021.
Clarification (January 9): We updated the structure of a sentence so the description of plastids is more clear. The Scientist regrets any confusion.
