Crown Gall Disease of Nursery Crops

By L.W. Moore, Bacteriologist and Plant Pathologist, OSU.

Crown gall has been a major problem for the nursery industry. It can affect over 391 plant genera including many species and cultivars within each group. The disease has been called crown gall, gall, crown knot, root knot, and root gall. The pathogens involved include Agrobacterium tumefaciens, A. rubi, and A. vitis, all of which 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 pathogenic species of Agrobacterium. Agrobacterium is a bacterial genus 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, insects, 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^oF. Latent infections typically develop into galls in a later growing season. The gall provides a nutrient-rich environment for further bacterial growth. Pathogenic bacteria escape from the gall into the surrounding soil or water where they colonize or infect new plant tissues.

Host Range

Types of plants affected include shrubs, ornamental flowering trees, fruit trees (temperate to tropical) tubers, grapevines, tobacco, annuals, and members of the coniferae. The table on this page gives examples of host plants infected by Agrobacterium species and the relative frequency of infection. The frequency of crown gall on plants at any given location varies because the host range of Agrobacterium is strain-dependent. Some strains infect a wide range of hosts, others a narrow range.¹ Bradbury⁴ lists 391 susceptible plant genera, many of which have many susceptible species. However, crown gall disease has been observed on only a few of these species in their natural habitat. Even the root systems of nonhost plants such as weeds, grasses, and cereals can harbor the pathogen and serve as a reservoir of inoculum.

Symptoms and Damage

The disease is called crown gall because the galls typically are on the plant's crown at or below the soil line along the main root, often at the point that the main root was pruned off before transplanting. Galls also are on lateral roots and on above-ground stems, canes, and vines. Galls can be on pruning wounds. Galls above ground are often close to the soil surface, are rounded, and are either smooth or fissured. On woody perennial plants, galls become more woody and fissured with age, sometimes reaching a diameter of 4 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.

Plants infected the first year they are planted out are more severely damaged. 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^{11, 35} to debilitating to death-dealing.^{12, 16, 23, 24, 39}

Symptoms become evident 2 to 4 weeks after infection if temperatures are at or above 68^oF, 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^oF and stops below 50^oF. Infection is inhibited above 92 to 95^oF. Latent infections²² 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.¹²

Some problems can look like crown gall but are not pathogenic. Aerial burrknot on apple tree trunks and branches is a cushion-like assemblage of adventitious roots; it is considered to be caused by genetic factors rather than an infectious agent.³⁸ Tissue proliferation is another tumor-like problem, on Rhododendron, that is caused by factors other than Agrobacterium. Vascular tissue differentiation in tissue proliferation distinguishes it from wound callus and crown gall.

Small galls require careful diagnosis because they may be confused with excessive wound callus or with galls induced by nematodes, fungi, or insects.^{15, 34} Thus, pathogenic strains of Agrobacterium must be isolated to confirm a crown gall diagnosis.²⁷ 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 nonpathogens can constitute over 99% of the Agrobacterium population. Pathogenic strains of Agrobacterium were isolated from blueberry plants displaying crown gall-like symptoms.⁶ DNA probe technology was crucial for recognition of pathogenic isolates among the general Agrobacterium population.²⁰

Disease Management

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 sanitation² and cultural practices are important deterrents to crown gall. At harvest, discard all nursery stock showing symptoms to avoid contaminating healthy plants and storage facilities. While digging at harvest, leave noticeably galled plants in the field for later pickup and destruction. If possible, choose a rootstock that is less susceptible^{10, 13, 17, 18, 19, 28, 30 46}, avoid planting sites with heavy infestations of root-attacking insects and nematodes^{9, 40, 45}, disinfect pruning equipment between trees, and adopt management practices that minimize wounding.⁷ Avoid planting into heavy, wet soil. Don't plant trees deeper than they were grown in the nursery.¹² If possible, incubate dormant seedling roots at 73 to 76^oF for 10 to 14 days to heal wounds and reduce susceptibility to A. tumefaciens before planting them in wet soil.²⁶ Use irrigation water from wells, if possible. Avoid planting where galled plants grew in the last 4 to 5 years;⁴⁰ choose fields that were planted recently to vegetables or grain. In summary, think prevention - avoid exposing plants to pathogenic Agrobacterium at any stage of plant production.

Planting Site

Site conditions play an important part in the incidence of crown gall. Crown gall is generally much more prevalent in heavy soils or in soil where water stands for a day or so.⁴¹ 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.¹² 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.^{12, 25} This situation isn't repeated at every site, but we still recommend avoiding fields with a recent history of crown gall.

Vectors

Nematodes, grubs and other chewing insects have been implicated as passive carriers of A. tumefaciens that subsequently infect the feeding wounds.²⁵ Crown gall incidence on raspberry increased significantly in the presence of root-lesion nematodes, Pratylenchus penetrans.^{40, 45}

Natural Resistance

Reports of plant resistance to crown gall are limited, and findings are varied. In Britain, apple rootstock Malling Jewel was considerably more resistant than Malling Delight. McIntosh apple trees in Oklahoma, but not in Oregon, were very susceptible to A. tumefanciens. In Italy and the Pacific Northwest, Malling 7 is considered the most susceptible apple rootstock to A. tumefaciens³ followed by Malling 9 and 26. M9, however, is reportedly the most susceptible rootstock in Switzerland.⁴⁴ Interestingly, the new rootstock Mark, a selection from Malling 9, was much more susceptible to A. tumefaciens than Malling 7 (Moore and Canfield, unpublished). This variability is likely because strains of the pathogen are better adapted to one nursery site than to another.

Over the past 25 years, we've encountered numerous other examples of variability in our studies of crown gall. They include differences in plant host susceptibility, in symptom development, in disease conduciveness of planting sites, in ratios of nonpathogenic to pathogenic agrobacteria in soil, on roots, and in galls, even from the same location, and in pathogen sensitivity to the biocontrol agent K84. Failure to recognize Agrobacterium diversity leads to studies comprising only a few isolates, which can lead to unwarranted assumptions and generalizations about the biology of Agrobacterium under natural conditions.

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.⁴² This biological control is solely preventative, not curative; hence, application timing is important to properly protect plant wounds caused at harvest or by pruning. Htay and Kerr¹⁶ recommend seed and root treatment with K84 for best results. Not all pathogenic strains of Agrobacterium are sensitive to K84. For example, most pathogenic agrobacteria isolated from grape tumors are A. vitis which are insensitive to K84. Even so, K84 has been effective against several insensitive Agrobacterium pathogens in field tests.⁴³ K84 is compatible with etridiazole alone (Truban), etridiazole plus thiophanate-methyl (Banrot or Zyban), benomyl (Benlate), and Captan - fungicides that have been used to protect dormant trees in cold storage (Moore, unpublished).

A new, genetically engineered strain of K84 called K1026 has been patented in the United States. K1026 was developed with a view to the possibility that K84's effectiveness as a biological control of crown gall might break down.³⁷ K1026 gives the same biological control as K84 and is being used commercially in Australia and Spain.⁴³ BioCare, Ltd. (Australia) has submitted a registration packet to the U.S. Environmental Protection Agency for approval to market K1026 in this country.

Chemical Treatments

No registered chemicals that effectively control crown gall are currently available in the United States. Field tests in Oregon and Washington with the antibiotic Terramycin and a discontinued copper product, Copac E (11), consistently gave best results in reducing tumor incidence on apple rootstocks,⁵ but they are not at present registered for public or commercial use. In general, chemical preplant dips or soil drenches have been ineffective.²¹

Soil Fumigation

Fumigation to rid soil of Agrobacterium generally has been ineffective,^{36, 42} and in some cases growers have reported higher amounts of disease following fumigation.⁸ However, when methyl isothiocyanate (Vorlex, a product that has been discontinued) was applied to soil 2 months before planting indexed grapevines, soil populations of A. vitis were reduced, and the incidence of galled grapevines dropped from 100 to 16%.³² In contrast, Dhanvantari et al.⁹ reported no significant reduction in galled peach plants after a similar fumigation.

Heat Therapy

Heat therapy promoted healing of pruning wounds and reduced crown gall incidence in Maheleb and Mazzard cherry and Myrobalan plum seedlings. Seedlings were inoculated with pathogenic agrobacteria after incubation in an insulated box for 3 weeks at 73 to 76^oF. Crown gall incidence in the heated seedlings was 6% or less compared to 100% in nonheated controls.²⁶

Hot water treatments of dormant grape cuttings at 122^oF for 30 minutes dramatically reduced populations of A vitis in grape scions 'Chardonnay' and 'Zante Currant' and the rootstock cultivars Ramsey and K51-40. Hot-water-treated grafted vines planted in the field had a tumor incidence of 2% compared to 60% for the control vines.²⁹ We found that 122^oF did not completely kill the pathogen and therefore used 129^oF for eradication (White, Canfield, and Moore, unpublished).

Soil Solarization of Soil

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. A. tumefaciens populations could not be detected in a solarized sandy loam soil, but solarization did not work in the heavier silty-loam.³³ Mazzard cherry seedlings planted later in solarized and in nonsolarized control plots developed crown gall only in the nonsolarized plots.

Below 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 at harvest 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 equipment between plants.

• Plant only disease-free stock. (Plant resistant varieties if available.)

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 Cascades.

• Rotate susceptible crops with small grains.

• Plant when soil is below 50^oF.

• 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 agents K84 or K1026. Apply to seed, bare roots, and above-ground grafts. Heat therapy.

Grape Cultivars

Heat therapy on grape cuttings. Biocontrol agent HLB-2 has been used with spotted results. Some cultivars are more resistant than others.

Table 1. Frequency of Agrobacterium infection in certain host plants.

High Frequency

Almond, apricot cherry, peach, plum (Prunus), Apple (Malus), Euonymous spp., Grape (Vitis), Poplar (Populus), Raspberry (Rubus), Rose (Rosa), Rubus spp., Walnut (Juglans), and Willow (Salix).

Low Frequency

Chrysanthemum spp., Citrus spp., Clematis spp., Ficus sp., Gypsophila sp., Lilac (Syringae), Macadamia, Marigold (Tagetes), Olive (Olea), Pear (Pyrus), Quince (Chaenomeles), Ribes spp., Wild Blackberry (Rubus), and Wisteria.

Occasional/Rare

Aster, Birch (Betula), Blueberry (Vaccinium), Cactus, Dahlia spp., Gossypium, Hydrangea, Impatiens, Incense-Cedar (Calocedrus), Maple (Acer), Rhododendron spp., Sequoia, and Spruce (Picea).

Crown gall of verigated Euonymus. The normal size of this infected stem can be seen on the top left side of the gall.

References:

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2 Aubert, B., A. Faivre Amiot, and J. Luisetti. 1982. Phytosanitary selection work in Reunion on some fruit trees with a low chilling requirement. Fruits 37:87-96.

3 Bassi, C. 1983. Biological control of crown gall in Italy. In: Proceedings of the International Workshop on Crown Gall., ed. R. Grimm, pp. 1-15.

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6 Canfield, M.L., M.L. Putnam, T. White, et al. 1995. Isolation of Agrobacterium tumefaciens from blueberry (Vaccinium corymbosum). Phytopathology :1194 (abst.).

7 Cazelles, O., S. Epard, and J.L. Simon. 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, dÆArboriculture et dÆHorticulture 23:285-288.

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Article last updated on January 1, 2009