Kylee Peterson
Plant Galls:  Amazing Manipulations

Thesis:
Plant galls are one type of defensive response to invasions by many different pathogens and symbiotes, which manipulate their hosts to create an advantage for themselves.  Galls affect other parts of the ecosystem as well, particularly humans who have an interest in the host plants.

I.  General information on galls
  A.  Location and appearance
  B.  Definition
    1.  Abnormal cell multiplication and growth
    2.  Initiated by pathogen
    3.  Characteristic of plant/pathogen combination
    4.  Non-hyperplase definition
  C.  Type terminology

II.  Galling agents
  A.  Insects
    1.  Forms
      a.  Wasps:  closed galls
      b.  Flies:  closed galls
      c.  Aphids:  pouch galls
    2.  Controlled galls
    3.  Dependent differentiation
    4.  Sample gall formation technique:  Mikiola fagi
    5.  Sample life cycle: Adelges cooleyi
  C.  Fungi
    1.  Plant parasites and symbiotes
    2.  Crop pathogens
    3.  Sample life cycle:  Gymnosporangium juniperi-virginianae
    3.  Sample gall type:  Puccinia monoica
  D.  Bacteria
    1.  Excellent pathogens
    2.  Sample life cycle:  Agrobacterium
  E.  Nematodes
    1.  Types
    2.  Sample gall type:  Meloidogyne
  F.  Mites
  G.  Parasitic plants

III.  Mechanisms
  A.  Hormone injection:  sawflies
  B.  DNA transfer:  Agrobacterium
  C.  Bacterial symbiosis

IV.  Plant responses
  A.  Faster healing
  B.  Additional toxins
  C.  Parasitoids

V.  Effects on ecosystem
  A.  Predator coevolution:  Mordellistena convicta
  B.  Plant viability

VI.  Effects on humans
  A.  Damage
    1.  Crops
    2.  Wild plants:  chestnut blight
    3.  Garden plants
    4.  Amelioration
      a.  Resistant varieties
      b.  Nonvirulent strains
      c.  Crop rotation
      d.  Companion planting
      e.  Predators
  B.  Benefits:  Rhizobium
  C.  Uses
    1.  Tannins
    2.  Genetic engineering

Many plant pathogens and symbiotes manipulate their hosts to create an advantage for themselves.  Plant galls are not only a defensive response to invasion, but an engineered shelter and feeding site for galling agents, which thrive thanks to their sophisticated ability to alter the plant's responses.  Galls also affect any other organism which has an interest in the gall agent or the plant.  Humans are often concerned with the host plants, whether as ornamental plantings, important parts of a wilderness ecosystem, or food crops.

Most people have seen a plant gall, whether or not they recognized it for what it was.  Galls are usually visible as an obviously inappropriate-looking growth on some part of the plant.  They usually appear on the root, leaf, flower, or fruit, because those parts of the plant are growing when the gall agent attacks, rather than the stem (Abrahamson 931).  The defining characteristic of a gall is that it be an abnormal, tumorous growth, which is to say that it is not a leaf, a shoot, or anything the plant could normally be expected to produce.  Misplaced leaves or flower parts appear fairly commonly on most plants, and these do not qualify as galls.  A gall grows because the cells constituting it are dividing, not just growing larger, in a form of excess replication called hyperplase (Boothroyd et al.).  Gall growth is always initiated and controlled by a galling agent, which is adapted to exploit the host plant for food and usually for shelter.  An agent can be any of a wide variety of organisms, from insects to bacteria.  For a gall to be classifiable, it must be characteristic of the interaction of agent and host, which is generally the case because gall production requires specialized tools on the part of the agent.  Some members of the British Plant Gall Society are more liberal in their definition of galls, allowing dwarfing and other kinds of altered shoot development to be included, provided the conditions regarding the galling agent are met. (Introduction)  

Botanist Wayne P. Armstrong writes that galls "resemble everything from marbles and ping-pong balls to dunce caps, saucers and sea urchins." (#intro)  They may be attractive feathery tufts, like the bedeguar rose gall; as lumpy as a spoonful of cottage cheese, like cedar-hawthorn rust; bowls with overhanging rims, like the oak saucer gall; or amorphous blobs attached at one small point, like the oak apple gall (Weiss 10-17).  Many kinds of gall are common enough to be named as groups.  A pouch gall is hollow, round, and small, with a small opening on one side of a leaf or its stalk, and the rest bulging out like a coin purse as shelter for the small pests that induced it, which are usually aphids or mites.  In contrast, leaf roll and leaf curl are not technically galls, because, though the leaf's edges are rolled under, it is still a normally sized leaf.  When a gall is created by the implantation of a wasp egg, it is called a closed gall, because the hole left by the female wasp's ovipositor is healed by the plant.  Such galls provide excellent shelter for the insect larva until it eats its way out.  (BPGS Beginners)  Fasciated stems, which look like a slightly curled fan growing from a normal plant shoot, can form due to the influence of galling organisms as well, though the benefit to the agent is not clear (Armstrong, #fasciated).

The great majority of the world's plant galls are caused by insects.  The BPGS cites 833 species of gall-forming insects, far more than the number of galling species in any other classification.  According to Armstrong, most insects responsible for galls are flies, wasps, and aphids, while most host plants belong to the oak, rose, sunflower, juniper, and willow families.  Cynipid wasps are by far the most common gall-forming insect, and half of all known American galls are on trees in the oak genus, Quercus (#insects).  Wasps create closed galls by laying eggs inside the host plant's stem, leaf, or ovary.  The wasp larva produces chemicals which cause cells to multiply and nutrients to be diverted to the gall location, then tunnels out of the gall, usually when it reaches adulthood.  Fly galls are usually similar, housing a larva in a closed or mostly closed gall (Abrahamson 930).  On the other hand, aphids feed on the surface of plants, and have a minimal larval stage, so their galls provide adult insects with access to the outer surface of the plant, like the pouch galls described earlier.

The galls produced by insects continue to grow only under constant stimulation.  If the larva is removed from a typical insect gall, the gall stops growing unless the larva's characteristic chemical exudates are injected manually (Schultz 458).  Because of this trait, insects galls are referred to as controlled galls.  Every insect gall will grow into a size, shape, and color matching those of any other gall from the same agent and host, because the methods used to induce the gall are the same.  Such precision makes it very clear that pathogenic insects are closely adapted to their host plants.

Intricate structures within insect galls give them their characteristic appearances [seems slightly awkward, not sure why].  Plant pathologists Armin C. Braun and Ross B. Pringle, writing for the American Phytopathological Society, say that a gall-forming insect larva applies stimuli which cause the plant cells nearby to lose their differentiation.  Leaf, flower, or fruit cells lose their special abilities and revert to parenchyma cells, the building blocks of plant tissue.  Then the larva orchestrates the formation of layers and regions of gall-specific tissue, causing the gall to develop as determinately as a leaf or fruit, with one key difference:  the pathogen controls its growth.  Gall morphology is so distinctive that, for some closely related species of insects, identification  is more reliable when based on the appearance of the larval gall than when based on examining the adult insect (95-96).

Galls generally form due to chemicals applied to the host plant by the galling agent in some fashion, and those chemicals will be discussed in more detail later.  In the berrylike leaf galls of the tiny fly Mikiola fagi, however, chemical action is not the only technique used.  Braun and Pringle write that, though there are chemicals at work to induce growth in the plant cells, the hyperplase is given its shape by rapid movements of the larva within the gall.  It appears that the larva's motion places a nonspecific growth hormone in certain places, which gives each gall its characteristic shape (96).  Many insects have more complex galls, with differentiated tissue for feeding, but Mikiola fagi uses the tools available to it to make itself a very successful gall.

Most galling insects have simple life cycles:  an egg hatches in a host plant, the larva produces a gall and grows to maturity, an adult emerges and mates.  Some life cycles are more interesting, often including more than one host species.  One insect with a more complex life cycle is the pineapple spruce gall insect, Adelges cooleyi.  This aphidlike insect emerges from a larval gall, which somewhat resembles a pineapple or a spruce cone, on a spruce tree in summer.  The females then lay eggs on Douglas-fir needles, which hatch into a generation with woolly coats that reproduce parthenogenetically,  producing identical daughters, while feeding on the Douglas-fir.  At the beginning of winter, some woolly insects remain on their host tree, and some grow wings for travel to a spruce shoot, where they lay eggs that create the next round of galls.

Another common source of plant galls is the fungal kingdom.  The BPGS knows of 300 species of fungi that induce galls (Introduction).  Many of them have exotic life cycles with multiple hosts and impressively complex galls.  Fungi are well adapted to dissolving plant cells, living or dead, so many have evolved a parasitic or symbiotic existence.  In fact, plants grow poorly in conditions that completely lack fungi, because they are unable to form the common partnership which allows them to barter photosynthesized sugars for extra nutrients that fungi can draw from organic matter in the soil.  The feeding sites involved in that partnership are not galls because the roots form no hyperplase, though fungal hyphae may enter and even fill root cells.  

Root galls do form as a result of fungi, though, as well as many other types of gall.  Perhaps the mutually helpful partnership between fungus and plant never worked out [evolved?] in these cases, or perhaps it went astray, but some of the most economically significant gall pathogens are root-gall fungi.  The agent of club-root in brassicas, including cabbage, cauliflower, and broccoli, is Plasmodiophora brassicae (Grabowski).  Polymyxa betae in combination with a virus causes rhizomania in sugar beets, and other plasmodiophorids cause many other gall-type ailments as well (Braselton).

Galling fungi often alternate hosts as part of their life cycle, as with the cedar-apple fungus, Gymnosporangium juniperi-virginianae.  Common in dry areas, cedar apples appear in junipers or related cypress trees as swollen reddish balls which grow fingerlike spikes in spring.  The basidiospores from the juniper stage infect the flowers of trees in the rose family, particularly apples and crabapples, and cause defoliation.  Infected apple trees suffer from loss of leaves, and their fruit may be damaged as well.  Spores from the apple-tree stage of the fungus infect junipers again, forming a gall over the next eighteen months and eventually releasing more apple-attacking spores (Christensen and Steinegger).

As fascinating as the cedar-apple fungus is, some rust fungi of the genus Puccinia surpass it completely in their manipulation of their hosts.  The galls formed by Puccinia monoica on some species of rock-cress in the genus Arabis look for all the world like exotic flowers, and have nectar and scent to match (Roy).  Puccinia causes a leafy stalk to grow, then induces the host plant to produce a brightly colored cluster of leaves with nectaries to attract would-be pollinators.  When the insects arrive at the pseudoflower, they pick up fungal sex cells along with their sugar reward and spread them to their next stops, which are very likely pseudoflowers as well.  Puccinia has hijacked its host's reproductive mechanism and gained the benefits of insect-mediated sex for itself.

Plant pathogenic bacteria spread by water or insect vectors and enter host plants through wounds or natural openings (Boothroyd et al.).  The BPGS lists only nineteen types of bacterial gall-makers (Introduction), but several of them are well known, such as Rhizobium, the agent of root nodules in legumes, and Xanthomonas, the economically important citrus canker bacterium (Boothroyd et al.).  Horticulturists routinely breed plants for resistance against bacterial diseases, but the short generations of bacteria make staying ahead of adaptation a struggle.  Bacteria's evolutionary speed also means that they can produce plant proteins more readily than most other organisms, so they are very well suited to pathogenicity.

The crown gall bacterium, Agrobacterium, enters plants only through wounds. According to Braun and Pringle, Agrobacterium transforms healthy plant cells into non-self-limiting tumor cells over a period of 72 hours after the injury (96-7).  The bacteria spread and reproduce within the plant, causing nearby cells to multiply and form a bulging, hypertrophied gall.  Gall growth is limited only by the amount of nutrition the plant is able to provide to its parasite.  Mature galls shed bacteria from their surfaces back into the soil, where the bacteria can survive the winter before infecting other plants (Boothroyd et al.).

Most soil nematodes are beneficial scavengers, similar to the better-known annelid earthworm, but some nematodes eat living plants, and a subset of those induce plant galls when feeding.  Ectoparasitic nematodes remain in the soil when feeding on a plant.  They puncture the wall of a single cell using a sharp, hollow mouthpart called a stylet, inject digestive enzymes, and use their muscular esophagus to extract the cell contents as food.  Semi-sedentary ectoparasites create limited galling at the feeding site (Boothroyd et al.), but that feeding style is relatively uncommon.  Cyst nematodes burrow partially into plant roots and create nodules, intercepting the flow of water and nutrients in the root and creating a globe joined to the root by an isthmus of flesh.  Anguina, the seed gall nematode, replaces grain seeds with dense, dark masses of nematodes, which stay viable even after being dried and infect new fields when planted with true seed.  Stem and bulb galls, caused by Ditylenchus, cause swelling and fibrous masses called "narcissus wool" to appear near the soil line in some vegetable crops (Boothroyd et al.).

Root-knot nematodes create round root galls, which completely enclose the endoparasites.  These Meloidogyne nematodes attack most kinds of plant, creating "elaborate feeding sites" in which the host plant's cells become syncytia, or giant cells, which have thicker walls, denser cytoplasm than normal, and multiple enlarged nuclei.  The nematode induces the host plant to divert nutrients to the syncytia, where they are available for easy consumption (Boothroyd et al.).

Mites also cause a large number of plant galls, usually as shelter for external feeding, like aphids.  The mites are usually minuscule, in the range of 0.1 millimeter, but their galls are frequently quite noticeable as pouches or pockets on leaves (BPGS Notes).  Mite galls often house large numbers of the tiny arthropods.

Parasitic plants do not normally cause gall formation, and deformations that appear are largely due to physical pressure.  The rootlike penetrating organs of the parasite, called haustoria, can leave swollen marks on a host plant.  Some old oaks have grown very large tumors in response to mistletoe haustoria, as Armstrong notes, and mistletoes can also produce "witches' brooms," hyperplases with a thickly branching habit.  Some tropical relatives of mistletoe cause pressure marks with ripply fan shapes, which are called wood roses and often incorporated into carved sculpture (#mistletoe), but wood roses cannot truly be called galls.

The production of galls can be very different from one agent species to another, and much remains unknown.  Hormone introduction can cause cell hypertrophy, which is usually the case with insect-produced galls.  Jack C. Schultz lists several cases in which insects have been found to use plant growth hormones in gall induction, and adds that some metabolically important insect proteins are very similar to plant hormones.  Such a similarity positions insects very well for a manipulative, gall-making attack on host plants.  Tenthridinid galling sawflies stimulate gall growth with the contents of an accessory gland, which holds plant growth hormones called cytokinins and similar molecules, to initiate gall development when injected with the egg and to continue it when the same substances are produced by the larva (458).

Professor Emeritus of Plant Pathology Alan Kerr has mentioned that Agrobacterium, the crown gall pathogen examined previously, accomplishes its tumorigenic activity by way of DNA transfer.  Viruses are a well-known example of this type of pathogenicity, in which the pathogen injects DNA plasmids into the host cell and causes the cell to duplicate them at its own expense.  Viruses generally exploit the cell until it explodes, but Agrobacterium changes the cell instead, into an unboundedly growing tumor cell much like a cancer.  It uses plant auxins, which cause nutrient concentrations to rise, and cytokinins, which cause hyperplase.  The gall cells produce different substances than healthy plant cells, which are not useful to the plant but are preferred by the pathogen.

In a combination of the previous two methods, herbivorous insects sometimes host bacteria with the ability to produce plant hormones.  Schultz lists tephritid flies' endosymbiosis with a bacterium formerly called Erwinia, which makes plant auxins and cytokinins, and aphids with Buchnera bacteria inside them producing the auxin precursor tryptophan.  Bacterial genes can pass into other organisms, too, probably in a process similar to Agrobacterium's genetic alterations; caterpillars and some nematodes can produce bacterially derived proteins that aid them in eating plants (459).

Plants are not merely systems to be manipulated, however.  While they may be vulnerable to the induction of galls that only help their pathogens, they can nonetheless bring to bear a few resources of their own.  Studies show that plants under attack by insects can accelerate their healing responses, which would lessen the time spent vulnerable to bacteria and allow the plant to regain any lost biomass more quickly.  Oak galls are often very high in tannins, the pesticides that make acorns bitter, which shows that plants can increase the toxicity of attacked tissue.  Schultz has even found that tannins increase in oak leaves in response to one particular insect prostaglandin, not merely to general damage.  He also lists an amazing reaction in which caterpillar regurgitant causes the attacked plant not only to raise its defenses but to emanate volatile substances into the air, which attract parasitoids to eat the caterpillar (459).  The plant-parasite arms race is in no way one-sided.

Plant parasites affect the ecosystem in more subtle ways than a simple herbivore's grazing.  Predators on gall insects find it more difficult to catch their prey when it lives inside a cozy plant-made shelter, and some alter their hunting methods to suit.  Warren G. Abrahamson et al. write that Mordellistena convicta, an omnivorous beetle, has adapted to bore into plant galls and eat the fly larvae inside, but not yet to preying on the larvae whose parents placed them on a slightly different species of goldenrod (931).  Plants which are not attacked by a gall-forming pathogen may have more resources to devote to their own success, and outcompete afflicted plants.  The likelihood of a plant's extinction due to parasitism is small, because the most successful parasites are those that do not damage their host any more than they require, but the oscillations in a plant's population can certainly have widespread consequences for many other kinds of organism.

Humans have bred crop plants to produce a large, nutritious harvest.  Pathogen resistance is also important for a plant's success, but a human breeder's priority is generally for the best and largest amount of food grown.  For this reason, crop plants may have less resistance to diseases and galling agents than their wild relatives.  Many kinds of gall cause significant damage to commercial crops.  A variety of fungal smuts, related to the cedar-apple fungus, strike maize and other grain crops, causing swollen galls on the kernels which later break open to disperse black spores.  Smuts have been known since ancient times in Europe, and have always represented serious trouble for agriculturists.  Grains are also vulnerable to attack by galling nematodes.  As detailed earlier, plasmodiophorid fungi cause root ailments in many important crops, especially the brassicas, or cruciferous vegetables.  Root galls may cause the host plants to wither and die by obstructing water flow into the stem, and no amount of irrigation can save them.  The stem and bulb galls induced by nematode feeding can have a similar effect.  Citrus and olive galls, caused by bacteria, can damage those crops as well (Boothroyd et al.).

Sometimes, wild plants are also damaged by galls to an extent that worries ecologically or aesthetically conscious humans.  When a new pathogen reaches a population of hosts without previous exposure to it, many of the hosts will probably die in the first infection.  Neither the hosts nor the parasites have adapted to dealing with the other well enough to coëxist.  The impact of chestnut blight [not a gall] on the American population of chestnut trees is well known.  It is now about one hundred years after the accidental introduction of the fungus, and very few native chestnuts survive in the United States.  Gall-forming pathogens can be just as damaging to their hosts when they have not yet evolved to manipulate the new species with enough sophistication.  

Galling pathogens are among the many pests in the ornamental garden as well.  Rose galls annoy gardeners quite often, particularly because they often form in the inviting bud tissues and abort the flowers, and most plants in a garden are vulnerable to pouch galls caused by aphids or mites.  Many people grow fruit trees for attractive spring flowers and summer shade, and find galls on them to be distasteful.  Every gardener has had a plant sicken and die for no apparent reason, a problem which can often be traced to gall-making nematodes.

Reducing the effect of galling agents on a plant is often difficult.  The best long-term solution is to breed varieties of the plant that can resist the effects of the pathogen, whether that means the host can fight off attack or simply survive and grow regardless.  Most commercial growers douse the soil in antibiotics and fungicides at any sign of disease, but overuse of any chemical breeds resistant pathogen strains.  Chemical pest management also kills many beneficial soil inhabitants, making it harder for crops to thrive.  Weakened plants are even more vulnerable to attack by pathogens, many of which can arrive by air.  It is far better to selectively save seed from the plants that do best under pathogen attack, and in time arrive at a variety that can produce well even when forced to divert some of its resources to parasites.

One lesson of the American chestnut blight is that, when possible, it is best to keep pathogens out of new areas.  Accidents are inevitable, though, and another fact pointed out by the chestnut blight is that many pathogenic organisms are very closely related to nonvirulent strains.  Fungi and bacteria, especially, can be discouraged from invading a plant if a member of the same species is already present.  In the case of chestnut blight, a non-damaging strain of the fungus was found in European trees.  It competes with the pathogenic strain, reducing the effects of the blight even in trees which are already afflicted (Treadwell).  Maybe the best way to address the problem of alien pathogens is to preemptively isolate a nonvirulent strain in case of accidental infection.

Simple mechanical methods such as crop rotation can also be very effective against pathogens.  Farmers traditionally rotate crops from one field to another in successive years, because it is a very successful method of keeping the soil fertile.  For instance, last year's wheat field might contain turnips this year, beans next year, and lie fallow, meaning unplanted, the year after that.  Planting a field in different kinds of crops each year ensures that no resource in the soil is completely exhausted, because different crops draw on different nutrients and all of the nutrients are naturally replenished over time.  Crop rotation is also helpful with regard to pathogens, because the agent of club root in brassicas might infect turnips but is not adapted to deal with beans, and by the time turnips come around to that field again the fungus will be mostly gone from the soil.  

Companion planting is another traditional method that can help combat pathogens.  Some plants exude chemicals which deter parasites, such as marigolds, which are excellent for repelling nematodes.  The pesticide is not present in injurious amounts immediately, so the parasites have time to leave the area rather than being selected for resistance on a life-or-death basis.  Other preferred companion plants attract pests to themselves and away from less hardy plants.  Garlic is often planted near roses for this reason.  It is also possible for a companion plant to host part of the life cycle of an organism that preys upon pathogens, such as lacewings, assassin bugs, and lady beetles.

Another reason to refrain from using soil antibiotics whenever possible is that some gall-forming bacteria are actually beneficial to plants.  Rhizobium bacteria form root nodules on plants of the pea family, in which they convert atmospheric nitrogen gas into bioavailable forms.  Most plants must absorb nitrogen, which is an essential component of proteins, from decaying organic matter in the soil.  Because of their partnership with nitrifying bacteria, legumes do not depend on rich soil to grow.  They can thrive even in soil that has been depleted, whether by natural causes, excessive irrigation, or overfarming.  This advantage is completely lost if all of the soil bacteria are killed by pesticides.

Galls and galling organisms have other uses to humans.  Oak galls are very high in tannins, which are used for leathermaking, dyeing, and inkmaking -- any application requiring an astringent solution.  Before synthetic alternatives became available, oak galls were widely used in Europe and East Asia, and were so popular that the craft workers could distinguish among galls from different areas.  The most valued galls still had the insect larva inside (Briggs), which probably indicates that the tree was still attempting to kill off its invader by keeping the tannin level high.

The crown gall agent, Agrobacterium, is very useful to humans in the pursuit of genetic engineering.  Its innate ability to transfer DNA into plant cells, which in its natural state causes tumors to grow and produce nutrients for the bacterium, makes it ideal for scientists who want to transfer tailored DNA into plant cells.  As of 1983, genetic engineers are able to edit the DNA plasmid transferred to the host cell by the pathogen, splicing in genes from animals, plants, or other bacteria at will (Kerr), a technique which is still used in many laboratories.  Genetic engineering has many problems and may always be inexact, but Agrobacterium has helped it advance immensely.

Gall-forming pathogens are extremely sophisticated organisms, capable of using hormonal disinformation to win an advantage for themselves at the expense of their host plants.  Parasites from every kingdom of life induce galls to provide themselves with easy food and shelter.  Galls affect not only the host plant but many other organisms, notably humans, who sometimes depend on host plants for food.  There is much more to be learned about these fascinating interspecies manipulations.

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Additional Bibliography
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Todd, Timothy C., and Douglas J. Jardine.  "Nematodes:  Management Guidelines for Kansas Crops."  Plant 
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     <http://nematode.unl.edu/extpubs/nemakan.htm>.
Wood, R.K.S.  "Pathogen factors in the Physiology of Disease -- Pectic Enzymes."  American Phytopathological 
     Society.  Plant pathology, problems and progress, 1908-1958. Madison: University of Wisconsin Press, 1959.