Can plants have cancer?
It may seem hard to believe but plants, like humans and many other eukaryotic organisms can develop cancer. However, the process of tumor formation in plants may be a little different from how it develops in humans. In plants, the development and progression of tumorigenesis are evident by the presence of large rough woody tumor-like galls, also referred to as crown galls, on the exterior of plant surfaces. These crown galls can be found not just on trunks and branches but also on roots.
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| Crown Gall tumor |
In most cases, the main causative agent that initiates tumor formation is a very powerful natural genetic engineer, the Agrobacterium tumefaciens microbe. A. tumefaciens is an alphaproteobacterium that belongs from the family of nitrogen-fixing symbionts. What sets A. tumefaciens apart from its close relatives is its pathogenic nature of interaction with plant species. A. tumefaciens commonly infects grape vines, sugar beets, and rhubarb. Thus, plants infested with A. tumefaciens remain a major concern for the agriculture industry as it greatly reduces plant’s productivity and viability. More specifically, galls, in particular, can be extremely detrimental for young growing plants compared to mature plants. Galls can limit the effective flow of nutrients and water within the plant, thereby reducing the plant’s overall vigor and growth capabilities. Additionally, plants with galls are generally more susceptible to stress induced through drought or severe winter conditions. Consequently, reducing the overall viability of plants and their ability to reproduce.
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| Electron microscopic view of A. tumefaciens |
For decades, it was difficult for scientists to uncover the enigma associated with the unique ability of A. tumefaciens to initiate tumorigenesis in plants. Many questions arose as scientists researched and delved deeper into understanding the intricate workings of A. tumefaciens: Why was this bacteria only needed for the initiation step and not for the actual formation of tumors in plants? What advantage did the bacterium confer through this transformation in plants? How did the plant alter it’s physical machinery for tumorigenesis in response to the changes induced by this bacterium?
It wasn’t until the late 1970s when Marc Van Montagu and Jozef Schell at the University of Ghent, Belgium discovered the mechanism under which A. tumefaciens transformed plant cells which later led to tumorigenesis in plants. They discovered the presence of and the transfer of a large circular piece of cytoplasmic chromosome (Ti-plasmid) from the bacterial cell into the host plant cell through the process of conjugation (the exchange of genetic material between bacterial cells). What they found was astounding! A certain sub-section of the Ti-plasmid (T-DNA) was being directly inserted into the plant’s genome. This resulting insertion and transcription of T-DNA genes caused the newly transformed plant cell to produce specific enzymes. These enzymes catalyze plant hormone synthesis needed for tumor formation and the production of amino-acid conjugates termed opines that serve as a carbon and nitrogen source for these species of bacteria specifically.
Thus, this whole natural system of bacteria-mediated transformation of an eukaryotic plant cell revolutionized the field of genetic engineering in plants. Scientists could easily use A. tumefaciens as the indefensible genetic vector in which they could insert/edit the T-DNA region of the Ti-plasmid, and get rid of genes that induced tumorigenesis. Consequently ensuring the viability of transformation by guaranteeing that the inserted genes could be passed onto plant daughter cells and that they would confer desirable traits in plants.
Isn’t it mind boggling to learn that these microbes could function as effective natural genetic engineers? They are not only able to successfully transfer their DNA into the plant genome, but also are able to maintain their dominance in face of competition with other bacterial species. Ma LS et al., from Imperial College London discovered the presence of DNase effectors- enzymatic toxins that have the ability to digest nucleic acids of competing target cells. A. tumefaciens effectively use these toxins as molecular weapons to duel with other species. A. tumefaciens rely on the T6SS secretion system (a molecular machine responsible for transporting molecules to the target cell) to release the DNase toxin. T6SS encodes two DNase toxins (Tde 1 and Tde 2) and their respective innate immunity proteins (Tdi 1 and Tdi 2).
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Graphical abstract from Ma LS et al. |
When A. tumefaciens cells are grown in the presence of just the toxin DNase Tde 1 and Tde 2 (Figure 2) they demonstrate reduced to negligible growth, whereas cells that are grown in presence of both the toxin and the immunity proteins (Figure 2) are able to alleviate growth inhibition. The presence of the innate immunity protein deactivates the DNase toxin. The presence and the subsequent release of the toxin can help A. tumefaciens curb intraspecies competition.
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| Figure 2: Represents toxin-Immunity Pair Analysis (A and B). The growth cultures of A. tumefaciens wild-type harboring Atu4350, DNase toxin, and its respective putative immunity protein Atu4351 or Atu4349 (A). Atu3640 - DNase toxin and its respective immunity protein Atu3639 (B). The y axis represents the concentration of the A. tumefaciens cells. |
Would we also expect the toxin to be effective during interspecies competition?
Ma LS et al., were also interested in answering this question. What they found was E. coli cells when grown together with wild-type A. tumefaciens with the innate toxin-immunity pair experienced a decline in growth. The presence of the toxin-immunity pair conferred a selective advantage to A. tumefaciens in outcompeting E. coli bacterial cells. They further expanded the in vitro experiment, where they grew Pseudomonas aeruginosa (P. aeruginosa) cells with A. tumefaciens. Within 24 hours, P. aeruginosa, unlike E coli, successfully outcompeted the A. tumefaciens. The release of the DNase toxin by A. tumefaciens initiated P. aeruginosa cells to launch a counter-attack - adopting a tit-for-tat strategy by which P. aeruginosa successfully reduced the number of viable A. tumefaciens cells.
However, there appears to be a plot twist! When the P. aeruginosa cells are grown inside the plant host instead of an in vitro setting. P. aeruginosa cells are completely ineffective in outcompeting the A. tumefaciens. This conflicting observation points to the non-static relationship between P. aeruginosa and A. tumefaciens that appears to vary in the context of the environment. On the other hand, A. tumefaciens cells are unaffected in the presence of P. aeruginosa cells within the plant host and unlike in an in-vitro setting, the release of their DNase toxin reduces the number of P. aeruginosa cells inside the plant host. Somehow the A. tumefaciens, after colonizing the host plant are able to allocate their resources in outcompeting other microbial species.
The A. tumefaciens is indeed a powerful pathogen. It is able to successfully insert its genetic material across the different domain of life and maintain itself as a competitive pathogen, outcompeting other bacterial species from colonizing the plant host. It would be interesting to further explore other evolutionary mechanisms if any, that can further explain the effectiveness of Agrobacterium in outcompeting other microbial species inside the plant host. The variation in the relationship between A. tumefaciens and other microbes such as P. aeruginosa in the context of the environment is an interesting observation that warrants further investigation.
However, there appears to be a plot twist! When the P. aeruginosa cells are grown inside the plant host instead of an in vitro setting. P. aeruginosa cells are completely ineffective in outcompeting the A. tumefaciens. This conflicting observation points to the non-static relationship between P. aeruginosa and A. tumefaciens that appears to vary in the context of the environment. On the other hand, A. tumefaciens cells are unaffected in the presence of P. aeruginosa cells within the plant host and unlike in an in-vitro setting, the release of their DNase toxin reduces the number of P. aeruginosa cells inside the plant host. Somehow the A. tumefaciens, after colonizing the host plant are able to allocate their resources in outcompeting other microbial species.
The A. tumefaciens is indeed a powerful pathogen. It is able to successfully insert its genetic material across the different domain of life and maintain itself as a competitive pathogen, outcompeting other bacterial species from colonizing the plant host. It would be interesting to further explore other evolutionary mechanisms if any, that can further explain the effectiveness of Agrobacterium in outcompeting other microbial species inside the plant host. The variation in the relationship between A. tumefaciens and other microbes such as P. aeruginosa in the context of the environment is an interesting observation that warrants further investigation.
Next time you see a crown gall, just imagine these bacterial cells in action!
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References:
Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe. 2014;16(1):94–104.
Özyiğit, I. I. Agrobacterium tumefaciens and its Use in Plant Biotechnology. Crop Production for Agricultural Improvement, 2012; 317-361. doi:10.1007/978-94-007-4116-4_12
Crown gall. Retrieved from https://extension.umn.edu/plant-diseases/crown-gall
Agrobacterium tumefaciens. (2019, April 08). Retrieved from https://en.wikipedia.org/wiki/Agrobacterium_tumefaciens
About the Authors:
Ammal Abbasi '19
Eeman Abbasi '19
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