Monday, 3 April 2017

Plant leaves - hijacked as insect and bacterial nurseries

Figure 1: Large, red growths on tree leaves. What are they?
Several months ago we were hiking in Washington state and saw some bizarre red growths on the leaves of many of the trees in the area (Fig. 1). We hadn't seen anything like these gross bulbous growths before. What are they? Cancer? Blisters? Aliens?!? Let's explore the answer to this question.

Burls and cankers are two types of plant outgrowths - Burls, bark-covered growths that look like warts, often form around wounds or insect infestations. Burls most frequently occur underground on the roots of the plant, but also occur above ground (Figure 2A). In these structures, the cell pattern that makes up the grain of the wood is chaotic - forming whirls and other complex designs that are very beautiful (Figure 2B). For this reason, wood from burls is highly prized, and has unfortunately led to burl poaching in some U.S. national parks [1]. Cankers, a broad class of plant diseases caused by microorganisms and viruses, can also cause visual physical deformities on the plant, which can vary from discolored bark to bulbous growths. Canker-causers are usually species-specific, meaning that each disease spreader affects only one particular species. Cankers vary greatly in the amount of harm they cause to the plant: some are not very harmful, and some are deadly.

Galls are outgrowths induced by parasites - Galls, unlike the large masses of disorganized cells characteristic of the burls and cankers, are highly organized abnormal growths that are induced by a parasite, often a fungus, bacteria, insect, or mite. These parasites inject specialized chemicals into regions of the plant that are undergoing rapid growth. The rapidly growing cells then quickly develop into structures that shelter and feed the parasite!

Figure 2: Burl outgrowths. One type of outgrowth plants can develop is called a burl. These form around wounds and infestations and have a wart-like appearance (A). Inside, burls have beautiful grain patterns that make them prized for woodworking (B).
Gall-inducers can modify plant defense chemistry - In some cases, the gall-inducing organisms are able to modify the plant in amazing ways. As an example, let's look at the chestnut oak, Quercus prinus, and the gall wasp, Andricus petiolicolus. When the wasp lays its eggs on the oak leaves, leaf-altering substances from the wasp are injected into the leaf, causing the leaf to grow a protective casing (a gall) around the eggs, which protects them from the elements as they develop into larvae and begin to consume the leaf for sustenance. These galls look similar to those we observed in Washington (Figure 1). Usually when something eats the leaves of the oak tree, the tree quickly fills its leaves with polyphenols - distasteful and toxic chemicals designed to repel the predator. Amazingly, when the wasp reprograms the leaf to form the gall around its young, it also modifies the polyphenol defense program. Instead of being present throughout the leaf, the polyphenols leave the area of the leaf inside the gall, leaving behind a tender, nutritious tissue for the larvae to eat [2]. The polyphenols instead congregate in the shell of the gall, protecting the larvae from insects that may otherwise eat the leaf, gall and all. Devious!

Agrobacterium modifies plants by injecting DNA - Another amazing gall-inducing organism is Agrobacterium. This bacteria senses chemicals that are unique to plants and moves towards them. When the bacteria get on the surface of the plant, usually underground, they synthesize small fibers, anchor themselves to the plant, and form a small colony. Then the bacterial cells synthesize specialized tunnels between themselves and the adjacent plant cells. Through these tunnels the bacteria pump small pieces of their DNA into the plant cells. The injected DNA fragments, once inside the plant, make the plant synthesize a large gall to protect the bacterial colonies. The bacterial DNA also forces the plant to combine some of its most crucial metabolic resources, amino acids and keto acids, to form new molecules called opines, a special food that only the Agrobacterium can eat [3].

Figure 3: Galls induced by Agrobacterium. Agrobacterium infect the roots of many different plants and inject bacterial DNA into the root cells. This DNA causes the plant to produce these large shelters (galls) for the bacteria (A). The plant is also forced to use its own keto acids and amino acids to produce special food for the bacteria called opine (B).
More than just Agrobacteria infect others with their DNA - DNA is a tightly controlled and protected component of living cells - it contains instructions that influence each and every process that makes the cell work. For this reason scientists were astonished to find that Agrobactiera play fast and loose with this important biomolecule: not only do they infect others with fragments of their DNA, but Agrobacteria can also transfer DNA directly to one another and take in pieces of DNA lying around in the soil [4]. The ability of these bacteria to transfer and uptake DNA has made them a major subject of scientific investigation, the results of which actually suggest that there are many species of bacteria that inject small pieces of DNA into other organisms - apparently this process is more common than our intuition tells us!

Nature's genetic engineers - Due to the shocking effects that gall-inducing insects have on the internal chemistry of plants, they have been studied in substantial detail, resulting in a remarkable discovery: bacteria that transfer DNA between organisms, and the use of such transfers to manipulate the internal chemistry of plants. I'm not sure about you, but the next time I see little bumps on the leaves of oaks near my house, I won't be so quick to move on to my next thought... inside are nature's own genetic engineers, hijacking plant leaves to create nurseries for their young.

[1] National Park Service:
[2] Allison, Steven D., and Jack C. Schultz. "Biochemical responses of chestnut oak to a galling cynipid." Journal of chemical ecology 31.1 (2005): 151-166.
[3] Zupan, John, et al. "The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights." The Plant Journal 23.1 (2000): 11-28.
[4] Demanèche, Sandrine, et al. "Natural transformation of Pseudomonas fluorescens and Agrobacterium tumefaciens in soil." Applied and environmental microbiology 67.6 (2001): 2617-2621.