Crown gall continues to be a major problem for the nursery industry, both in woody and herbaceous plants. The pathogen traditionally known to cause crown gall in the most plants is Agrobacterium tumefaciens (Rhizobium radiobacter). The pathogen name has been under dispute for decades, and A. tumefaciens is known to be a species complex, consisting of at least 11 different genomospecies. Here we will refer to the bacteria that cause crown gall as tumorigenic agrobacteria. Other species of Agrobacterium can also cause galls: A. rubi is much less common; named for the host in which it was first found (Rubus spp.), it has since been found in galls on rose, and will likely be found in other plants with time. Agrobacterium vitis (=Allorhizobium vitis) causes galls on grapevines. A. larrymoorei causes galling of Ficus benjamina, and has recently been found in rose galls. A novel gall-forming species, also isolated from rose, was recently described and named A. rosae. It is likely that additional species will be named in coming years, as bacteria associated with galls are examined more closely using modern molecular techniques. All of these species have a similar biology. This discussion covers the biology, host range, symptoms, and management of the disease.
Biology
Crown gall is a tumor-forming disease of plants caused by tumorigenic agrobacteria, many of which are thought to be present in most agricultural soils. The pathogens, in soil or on infested plants, are disseminated by splashing rain, irrigation water, heeling-in galled plants with healthy plants, farm machinery, pruning tools, wind, and plant parts used for propagation. Wounds are required for the pathogen to infect a plant. Wounds are made by pruning and cultivation, emergence of lateral roots, frost injury, and insect and nematode feeding. The pathogen colonizes the wound, attaches firmly to injured plant cells, and transfers part of its DNA into the DNA of the plant. Galls appear in a matter of weeks at temperatures above 70°F on herbaceous plants; woody plants such as roses may not show galls until months or years after exposure. Latent infections typically develop into galls in a later growing season. Pathogenic bacteria can be shed from the gall into the surrounding soil or water where they colonize or infect new plant tissues.
Host Range
Although commonly reported to have a host range of hundreds, this information is based on artificial inoculations often of just a single isolate. On a practical basis, far fewer plants are naturally susceptible. (Examples of host plants infected by Agrobacterium are listed in Table 3.) However, the root systems of non-host plants such as weeds, grasses, and cereals can harbor the pathogen and serve as a reservoir of inoculum in natural settings.
Symptoms and Damage
The disease is called crown gall, but galling may be found at the base of cuttings, on roots, crowns, or on stems, canes, vines, or leaves. Leaf galls are usually found on herbaceous plants that have a systemic infection. (Herbaceous ornamental plants susceptible to crown gall are shown in Table 1.) Galls often occur at pruning wounds. Galls are usually rounded and may be smooth or textured like a cauliflower head. On woody perennial plants, galls become more woody and fissured with age, sometimes reaching a diameter of 6 inches, and girdling the stem. Galls on grapevines, blueberry, and bramble fruit are usually elongate, erumpent ridges of tissue bursting through the outer stem tissues.
Woody plants infected the first year they are planted out are more severely damaged. (Woody plants susceptible to crown gall are shown in Table 2.) Severely galled young plants are weakened, stunted, and unproductive and occasionally die due to an inferior root system. Literature reports of crown gall damage are contradictory; they range from benign to debilitating to deadly.
Symptoms become evident 2 to 4 weeks after infection if temperatures are at or above 68°F, usually coinciding with warmer soil temperatures in May or June. Initially, the galls look like callus outgrowths but then increase rapidly in size and number. Symptom development slows greatly below 58°F and stops below 50°F. Infection is inhibited above 92°F to 95°F. Latent infections are symptomless and usually occur when soils are cool. Gall symptoms typically develop at the infected wound the following season; on rare occasions galls don’t appear until the third growing season.
Some problems can look like crown gall but are not pathogenic. Aerial burr knot on apple tree trunks and branches is a cushion-like assemblage of adventitious roots; its cause is thought to be genetic rather than an infectious agent.
Small galls require careful diagnosis because they may be confused with excessive wound callus. Detection using molecular methods specific to plasmid gene regions involved with virulence, or isolation of bacteria later identified as pathogenic is necessary to confirm a crown gall diagnosis. Nonpathogenic Agrobacterium cells are often prevalent in these same tissues and can reach high populations. That makes diagnosis difficult, especially in galls on apple, blueberry, and grapevines where non-pathogens can constitute over 99% of the Agrobacterium population.
Disease Management – Woody Nursery Stock
Pathogen-free plants grown in uninfested soil will not develop crown gall. This emphasizes the importance of planting clean propagating material in clean soil. Good sanitation and cultural practices are important deterrents to crown gall. Discard all nursery stock showing symptoms to avoid contaminating healthy plants and storage facilities. At harvest, leave noticeably galled plants in the field for later pickup and destruction. If possible, choose a rootstock that is less susceptible, avoid planting sites heavily infested by root-attacking insects and nematodes, disinfect pruning equipment between trees, and adopt management practices that minimize wounding. Avoid planting into heavy, wet soil. Don’t plant trees deeper than they grew in the nursery. If possible, incubate dormant seedling roots at 73°F to 76°F for 10 to 14 days to heal wounds and reduce susceptibility to tumorigenic agrobacteria before planting them in wet soil. Use irrigation water from wells, if possible. Avoid planting where galled plants grew in the last 4 to 5 years; choose fields that were planted recently to vegetables or grain. In summary, think prevention—avoid exposing plants to tumorigenic agrobacteria at any stage of plant production.
Planting Site
Crown gall is generally much more prevalent in heavy soils or in soil where water stands for a day or so. In New York, crown gall incidence was highest on a heavy clay knoll (15 ft elevation) from which water drained toward flat, loamy portions of the field. In Oregon, gall incidence on an Old Home x Farmingdale pear rootstock selection was severe (495 of 500 trees infected) in a heavy, wet soil, but in the same field only 1 of 500 trees was galled outside the wet area.
Cropping history can influence crown gall incidence. Budded apple trees became badly galled in fields where a previous nursery crop such as grape, peach, raspberry, and rose had been heavily infected. This situation isn’t repeated at every site, but we still recommend avoiding fields with a recent history of crown gall.
Natural Resistance
Reports of resistance in plants normally susceptible to crown gall are limited and depend on the strains of bacteria present in a given location. There are no reliable lists of cultivars with resistance that hold up in all geographic locations. It is better to select plants that are not susceptible in the first place if crown gall is a chronic problem in a particular field.
Biological Control
Using A. radiobacter K84, a biological control agent, has been very effective against crown gall on a number of hosts, but exceptions exist. Strain K84 produces a toxin against some tumorigenic strains of agrobacteria. This biological control is solely preventive, not curative; application timing is critical to properly protect plant wounds caused at harvest or by pruning. Htay and Kerr recommend seed and root treatment with K84 for best results. Not all strains of tumorigenic agrobacteria are sensitive to K84. For example, most agrobacteria isolated from grape tumors are A. vitis, which are insensitive to K84. If K84 has been used properly and galling persists, its use should be discontinued since it is likely the bacteria present are not sensitive to the product.
An improved, genetically engineered strain of K84 called K1026 is available. Its use is preferable, since the K1026 bacteria are not capable of transferring to other bacteria the genes that produce the toxin.
Biological control is compatible with a few pesticides such as metalaxy (Ridomil), thiram and thiophanate-methyl (Topsin) but not with captan, etridiazole alone (Truban), etridiazole plus thiophanate-methyl (Banrot or Zyban), mancozeb, PCNB or streptomycin. It is also not compatible with chlorinated water.
Chemical Treatments
No registered chemicals that effectively control crown gall are currently available in the United States. In general, chemical preplant dips or soil drenches have been ineffective.
Soil Fumigation
Fumigation to rid soil of Agrobacterium generally has been ineffective, and in some cases, growers reported more disease after fumigation.
Heat Therapy
Heat therapy has been tried in cherry and plum seedlings, and in dormant grape cuttings. Although these measures can reduce the incidence of disease, there will still be a small percentage of plants that remain infected. Time and temperatures needed for effective heat therapy has not been determined for many plants, and injury to the plant material can occur when temperatures are too high. Although promising, heat therapy is not commonly used due to these difficulties.
Soil Solarization
In solarization, a thin plastic film is stretched over moist soil to capture energy from the sun and heat the soil to temperatures that kill pathogenic microbes. Populations of tumorigenic agrobacteria could not be detected in a solarized sandy loam soil, but solarization did not work in the heavier silty-loam. Mazzard cherry seedlings planted later in solarized and in nonsolarized control plots developed crown gall only in the nonsolarized plots.
Following is a summary of the best practices for managing crown gall. They include experimental results and grower observations. Understandably, physical and economic constraints occasionally may impede applying all these practices. But for best results, follow or adapt the procedures as closely as possible to fit your management plan.
Best Practices for Managing Crown Gall
Cultural Practices
- Discard diseased plants as soon as noticed to avoid cross-contaminating other plants, equipment, or storage facilities.
- Don’t heel-in galled plants with healthy plants.
- Use good sanitation in handling planting stock.
- Minimize wounding; disinfect pruning tools between plants.
- Plant only disease-free stock.
Planting Site
- Plant in clean soil.
- Avoid fields with a recent history of high crown gall infestation.
- Avoid fields with heavy infestations of root-attacking insects and nematodes.
- Select well-drained soils; tile heavy soils.
- Field-fallowing is helpful but may be impractical west of the Cascade Range.
- Rotate susceptible crops with small grains.
- Plant when soil is below 50°F.
- Solarize lighter soils.
Cultural Conditions
- Avoid mechanical injury from tillage, hoeing.
- Irrigate with deep-well water or sanitized pond water.
- Keep grafts and buds above soil line.
- Avoid high nitrogen and irrigation late in the growing season.
The following are specific procedures for commonly grown plants that can be used in addition to the above general procedures.
Stone Fruit, Nut Crops, Roses: Dip or spray with the biocontrol agent K84 or K1026. Apply to seed, bare roots, and aboveground grafts.
References
Anderson, A.R., and Moore, L.W. 1979. Host specificity in the genus Agrobacterium. Phytopathology 69:320-323.
Aubert, B., Faivre Amiot, A., and Luisetti, J. 1982. Phytosanitary selection work in Reunion on some fruit trees with a low chilling requirement. Fruits 37:87-96.
Bazzi, C. 1983. Biological control of crown gall in Italy. In: Proceedings of the International Workshop on Crown Gall, Wadensville, Switzerland, R. Grimm (ed.) Wadensville, Switzerland: Swiss Federal Research Station for Fruit-growing, Viticulture, and Horticulture.
Bradbury, J.F. 1986. Guide to Plant Pathogenic Bacteria. Slough, United Kingdom: C.A.B International Press.
Canfield, M.L., and Moore, L.W. 1992. Control of crown gall in apple (Malus) rootstocks using Copac E and Terramycin. Phytopathology 82:1153 (Abst.).
Canfield, M.L., Putnam, M.L.,White, T.J., and Moore, L. W. 1995. Isolation of Agrobacterium tumefaciens from blueberry (Vaccinium corymbosum). Phytopathology 85:1194 (abst.).
Cazelles, O., and Epard, S. et al. 1991. The effect of disinfection with oxyquinoline sulfate of the Berl. x Rip. 5C rootstock on the expression of crown gall in grape propagation. Revue Suisse de Viticulture, d’Arboriculture et d’Horticulture 23:285-288.
Deep, I.W., and McNeilan, R.A. et al. 1968. Soil fumigants tested for control of crown gall. Plant Disease Reporter 52:102-105.
Dhanvantari, B.N., and Johnson, P.W. et al. 1975. The role of nematodes (Pratylenchus penetrans, Meloidogyne hapla, Meloidogyne incognita) in crown gall infection (Agrobacterium tumefaciens) of peach in southwestern Ontario. Plant Disease Reporter 59:109-112.
Durgapal, J.C. 1977. Evaluation of rootstocks of pome and stone fruits and related wild species for resistance to crown gall. Current Science 46:389-390.
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Table 1. Herbaceous ornamental plants susceptible to crown gall |
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Achillea millefolium |
Yarrow |
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Argyranthemum frutescens |
Marguerite daisy |
|
Aster spp. |
Aster |
|
Begonia spp. |
Begonia |
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Chrysanthemum x morifolium |
Chrysanthemum |
|
Coreopsis sp. |
Tickseed |
|
Cosmos sp. |
Cosmos |
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Dahlia variabilis and hybrids |
Dahlia |
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Dianthus caryophyllus |
Carnation |
|
Gaillardia x grandiflora |
Blanket-flower |
|
Helianthus annuus |
Sunflower |
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Heuchera sanguinea |
Coralbells |
|
Hosta spp. |
Hosta |
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Lamium maculatum |
Dead-nettle |
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Leucanthemum x superbum |
Shasta daisy |
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Lobelia sp. |
Lobelia |
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Osteospermum sp. |
Osteospermum |
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Pentas sp. |
Pentas |
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Perovskia atriplicifolia |
Russian sage |
|
Stachys monieri |
Betony |
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Verbena spp. |
Verbena |
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Note: this is not a complete list, but represents the most commonly infected species. |
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Table 2. Woody plants susceptible to crown gall. |
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Euonymus spp. |
Euonymus |
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Juglans regia |
English walnut |
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Malus spp. and hybrids |
Apple, crabapple |
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Photinia sp. |
Photinia |
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Populus angustifolia |
Willow-leaved poplar |
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Populus spp. |
Cottonwood |
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Populus tremula |
Aspen |
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Populus tremuloides |
Quaking aspen |
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Prunus amygdalus |
Almond |
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Prunus armeniaca |
Apricot |
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Prunus avium |
Cherry |
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Prunus cerasifolia |
Cherry plum |
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Prunus domestica |
Garden plum |
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Prunus x |
Flowering cherry |
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Pyrus communis |
Pear |
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Pyrus ussuriensis |
Manchurian Pear |
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Rosa spp. and hybrids |
Rose |
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Rubus spp. |
Caneberries |
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Salix spp. |
Willow |
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Vaccinium corymbosum |
Blueberry |
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Vitis spp. |
Grape |
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Note: this is not a complete list, but represents commonly infected species. |
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Table 3. Frequency of Agrobacterium Infection in Certain Host Plants |
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High |
Low |
Occasional/Rare |
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almond |
Chrysanthemum spp. |
aster |
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apricot |
Citrus sp. |
birch (Betula) |
|
cherry |
Clematis spp. |
blueberry (Vaccinium) |
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peach |
Ficus sp. |
cactus |
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plum (Prunus) |
Gypsophila sp. |
Dahlia spp. |
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apple (Malus) |
lilac (Syringae) |
gossypium |
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Euonymous spp. |
Macadamia |
hydrangea |
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grape (Vitis) |
marigold (Tagetes) |
impatiens |
|
poplar (Populus) |
olive (Olea) |
incense-cedar (Calocedrus) |
|
raspberry (Rubus) |
pear (Pyrus) |
maple (Acer) |
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rose (Rosa) |
quince (Chaenomeles) |
Rhododendron spp. |
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Rubus spp. |
Ribes spp. |
sequoia |
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walnut (Juglans) |
wild blackberry (Rubus) |
spruce (Picea) |
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willow (Salix) |
wisteria |
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