pest, disease and physiological disorders management

SOIL-BORNE DISEASES

Brent Holtz, Beth L. Teviotdale, and Lynn Epstein

here are three soil-borne diseases known to the branch or tree ensues with the first warm Tafflict pistachio trees in California. All are weather because the pathogen causes blockage caused by fungi and occur in most pistachio- of vital water-conducting tissues, and the tree growing regions of the state. Of these, demands more water than the root system can Verticillium wilt has killed many trees and as a provide. The classic symptom of Verticillium result growers have suffered severe economic wilt is rapid desiccation and death of one or losses in early planted orchards with more scaffolds or the entire tree, usually in late susceptible rootstocks. Pistachios are relatively spring or early summer. resistant to crown gall, a serious bacterial In another manifestation of Verticillium disease of other perennial crops; crown gall has wilt, called "thin leaf decline," symptoms not been reported on pistachio. The relative develop slowly over several years before the importance of soil-borne diseases varies with tree becomes economically unproductive or changes in choice of rootstocks. As new succumbs to the disease. Thin leaf decline is rootstocks are developed and introduced into characterized by slow loss of vigor and pistachio culture, the array of root diseases may reduction in growth and yield. A gradual differ. thinning of the canopy until most of the remaining leaves are clustered in tufts at the VERTICILLIUM WILT ends of branches and shoots may also be seen Historically, the most destructive disease of (Plate 26B). Why Verticillium causes some pistachio in California is Verticillium wilt, trees to collapse suddenly and others to decline caused by the fungus Verticillium dahliae Kleb. slowly has not been explained. An overall lack Trees of any age are subject to attack and of vigor may be the most common symptom of hundreds die each year (Plate 26A). Verticillium wilt. Verticillium also attacks cotton, tomato, melon, V. dahliae invades and colonizes the plant's stone fruit, and olive in addition to pistachio in vascular system. The water-conducting tissue, the southern San Joaquin Valley. Non- the xylem, is composed of small vertical tubes cultivated plants, both indigenous and weed that together form a cylinder just inside the species, also serve as hosts, and these enable cambium. Only the young xylem, that which is the pathogen to become established in non- formed in the current year, is able to transport cultivated land. Verticillium wilt of pistachio water. Xylem elements infected by Verticillium is more common in the southern half of the San become clogged by substances elaborated by Joaquin Valley than in other areas of the state, the fungus and the tree. These substances are and the disease has been most destructive darkly pigmented, and a cross-section of an where pistachio trees were grown in fields infected root, trunk, or branch reveals the previously planted to other susceptible crops. pattern of Verticillium infection in the new The disease occasionally is found in the xylem: scattered black speckles or a more or Sacramento Valley. less discontinuous black ring, depending upon how many vessels are infected (Plate 26C). Symptoms The uniform discoloration of the innermost The first symptoms of Verticillium wilt are wood is a consequence of the natural aging interveinal patches of yellowing or scorching process. The discolored xylem elements are of the leaves on affected branches. Collapse of non-functional and cannot transport water to

207 the upper portions of the tree. The branches infections may be needed to involve a large that die are those that are connected to the portion of the water-conducting system. infected root and vascular system and no longer Infections located away from the root tip receive adequate water. The history of usually follow another course of events. The Verticillium infection in older trees is recorded fungus invades a few cortical cells, outside the in the necrosis of each year's ring of xylem vascular tissues, and there forms a new (Plate 26D). Verticillium wilt does not cause microsclerotium which later is returned to the rot of bark or wood and does not invade soil. This 'refreshing' of the microsclerotial through the above-ground parts of the plant. population occurs with non-host as well as host plants and helps the fungus to persist, Disease cycle especially in the absence of susceptible species. Verticillium has only limited saprophytic A few such cortical colonies later establish activity in soil, so it does not readily grow and xylem infections which then proceed as reproduce there. Instead, it either lives on the described above. roots of alternate hosts or it survives in soil in the form of resting structures called Inoculum production microsclerotia. Each microsclerotium is a tiny Production of microsclerotia in infected plant cluster of approximately 30 dark-colored cells parts has been studied in annual crops such as that are extremely hardy. A percentage of the cotton and tomatoes but not in tree crops. In microsclerotia can remain viable in soil for annuals, many thousands of microsclerotia are many years. In a soil that was previously formed in leaves, stems and roots as the plant planted with an alternate host of Verticillium withers and dies. When the dead plant is such as cotton or a solanaceous crop, several incorporated into the soil, the tissues decay, hundred microsclerotia can be present in a freeing the microsclerotia. It is not known cubic inch of soil. Most microsclerotia are whether the incorporation of diseased pistachio found in the upper six inches of soil where leaves and branches into the soil contribute to there is the most biomass from a previous host. the inoculum in the soil. Microsclerotia are The microsclerotium is also the infective formed in infected pistachio roots, which may unit of the fungus. It remains dormant in soil contribute to the inoculum level in the soil. until a plant root grows nearby releasing However, in a pistachio field trial in California substances (nutrients) which stimulate it to in Verticillium–infested soil, and a relatively germinate. These substances can be produced weed-free planting, the number of by the roots of both host and non-host plants, microsclerotia per gram of soil dropped from but only young or wounded roots produce 40 in the first year to four by the fifth year and sufficient quantities of nutrients to cause the stayed at two from the eighth to tenth years. microsclerotium to germinate. Many infections Thus, although a pistachio planting may remain in the outer, cortical tissues of roots and maintain a relatively low population of never invade the xylem. However, entry occurs microsclerotia, pistachios in a weed-free field just behind the root tip where the young cells do not support a high inoculum concentration. are undifferentiated, and the fungus may grow into the new xylem. Inside the xylem element, Conditions that affect disease the fungus produces mycelium and conidia Verticillium wilt is favored by cool (spores). The conidia are carried upward with temperatures. Extended spring weather and water. As conidia become lodged in xylem mild summers often are accompanied by severe cells, they germinate, more mycelium is losses to this disease. The fungus apparently is formed which produces more conidia that again eliminated from above-ground portions of trees move upward with the water flow. In this during hot summer weather. Survival in root manner the fungus spreads from root to shoot, tissue and reinvasion of the upper stock is plugging the xylem vessel along the way. possible but has not been demonstrated. Neighboring xylem vessels apparently are not Instead, repeated attacks of wilt apparently easily infected. Thus, many independent represent new infections each year.

208 The disease is more prevalent in wet soils, presumably partly because they are cooler than Control dry soils, and irrigation influences the The best defense against Verticillium wilt is the incidence of Verticillium wilt in some annual use of the resistant or tolerant rootstocks, crops. In pistachio, the disease increased more Pioneer Gold (P. integerrima) PG I or UCB I down than across rows in an experiment in a (a P. atlantica x P. integerrima hybrid). UCB I drip irrigated orchard. Roots were more is a relatively new rootstock that may exhibited concentrated down rows and between trees slightly less tolerance to Verticillium wilt when than in the aisle between rows. This suggests compared to PG I, but showed more frost and that the denser root system down rows salt tolerance. P. atlantica and P. terebinthus improved the chances for infection. Also, rootstocks are very susceptible and should be inoculum build-up would increase where more avoided where Verticillium is present. Another infected roots are present. An irrigation system pistachio hybrid, PG II (P. integerrima x P. that would discourage root growth in this area atlantica), is extremely susceptible to might alleviate damage from the disease. In a Verticillium. recent experiment, drip irrigation systems Criteria for site selection for an orchard buried at different depths fostered changes in should include a crop history and an root density. More roots developed deeper in assessment of the inoculum level in the soil. the soil, but no decrease in the microsclerotial The microsclerotial population of the soil can population or incidence of Verticillium was be determined, and this service is available measured. through private laboratories. Pre-plant or Plant vigor affects susceptibility to planting site fumigation can reduce soil Verticillium wilt; stressed trees are more inoculum levels but will not eradicate the vulnerable than non-stressed trees. Inasmuch as fungus or prevent its re-establishment. Plastic the nutritional status contributes to the overall mulches (soil solarization) on fallow soil for health of the tree, nutrition may affect several weeks in summer can lower inoculum susceptibility. However, there is no evidence levels. Application of plastic mulches to that nutrient imbalance enhances disease planted pistachio orchards is limited in development or that improvement in nutritional effectiveness and does not work well in shade. status of trees prevents or alleviates infection Chemical treatments to soil or by tree injection by Verticillium. have not protected trees from Verticillium wilt. The population of V. dahliae is genetically diverse. There are many differences in the ARMILLARIA ROOT ROT pathogenicity and virulence of isolates of the Armillaria root rot, also called oak root fungus, fungus, and several strains and races have been is caused by the soil-borne fungus, Armillaria identified. To date, isolates cultured from mellea (Vahl.) Quel. A. mellea is a pathogen of pistachios are also pathogenic to cotton and can many cultivated and wild plant species, be further separated according to their effects including some species of oak. Orchards on tomato. The significance of this grouping is planted where oak trees once grew often are unclear, but no strong pattern of 'wilt' and severely damaged by the disease, hence the 'decline' isolates has emerged. Nonetheless, name oak root fungus. Plants growing in the variability within the fungus population is an soils of flood plains and along rivers and important factor in breeding and screening streams generally are more at risk than are plant material for resistance. those in other soils on the valley floor. Thus, The nature of resistance to Verticillium the disease is most frequently encountered in wilt by pistachio is not well understood. The orchards planted in the Sacramento Valley and fungus is able to invade roots of both along the eastern side of the San Joaquin susceptible and resistant plants, but once inside Valley. Armillaria root rot limits cultivation of the xylem, movement of the fungus up the several tree crops in California but only vascular tissue is slower in resistant than in occasionally affects pistachios. susceptible plants.

209 Symptoms human activity. Soil or water that does not The first symptoms, which usually begin on contain infected plant parts does not carry the one side of the tree, are reduced growth, early fungus. The spores produced by the yellowing and defoliation. Within a few years mushrooms have not been implicated in natural the entire tree becomes affected and eventually spread of the disease. Often, Armillaria root rot dies. The disease progresses to adjacent trees appears to be naturally restricted to certain leaving areas of dead trees in its wake. Internal areas of an orchard and in such cases does not tissues of bark and outer wood of the upper threaten an entire planting. roots and crown are discolored, and distinctive white, fan-shaped sheets of fungal mycelium, Control called plaques, are located between the bark Control is extremely difficult and usually not and wood (Plate 26E). With the onset of winter successful. Removal of infected roots followed rains, clumps of honey-colored mushrooms by fumigation as pre-plant treatment can slow may develop at the base of infected trees (Plate progress of the disease, but eradication is not 26F). Rhizomorphs, which are flat, root-like likely. Nothing is available for use in structures composed of white mycelium established plantings. Other soil covered by a dark, protective coating, grow microorganisms, chiefly Trichoderma spp., are along the surface of infected roots. antagonistic to A. mellea and provide some Rhizomorphs are not always present or may be measure of biological control. This biocontrol difficult to find and can be confused with small occurs only when the fungus has been roots. The presence of mycelial plaques within, weakened by sublethal doses of fumigant or by or rhizomorphs on infected roots, is sufficient heat or drying. When healthy, Armillaria is not evidence to confirm a diagnosis of Armillaria harmed by Trichoderma. root rot. Resistant rootstocks would offer the best protection against oak root fungus disease. Disease cycle Recent field trials indicate that P. terebinthus A. mellea does not live freely in the soil. It is and UCBI (a P. atlantica x P. integerrima always associated with infected or dead woody hybrid) are tolerant, whereas P. atlantica and tissues, with which it can survive for decades if P. integerrima are susceptible. However, not subjected to desiccation. Deep-rooted pathogenicity and virulence in the natural plants, such as oak, when infected by population of A. mellea ranges from weak to Armillaria, leave a legacy of many potential severe. Thus, disease response may vary with sources of inoculum distributed through the different combinations of host and pathogen. soil. Breeding programs may incorporate some Infection of healthy plants occurs when resistance in future stock. roots grow near dead or diseased roots which harbor the fungus. Close proximity between PHYTOPHTHORA ROOT AND CROWN infected and healthy roots is necessary for ROTAND TRUNK CANKER infection because rhizomorphs are infective Root and crown rot can devastate stone fruit, only for short distances away from their food almond and walnut orchards but is not common source. Rhizomorphs present on such material on pistachio trees in California. Trunk cankers penetrate the nearby root and establish an occur occasionally in sprinkler-irrigated infection. Both the formation of rhizomorphs orchards. These diseases caused by soil-borne and infection are favored by moist soil. The fungi belong to the genus Phytophthora. Most fungus also moves from infected to healthy of our knowledge of Phytophthora disease on individuals through root grafts. The pattern of pistachio is borrowed from research on other disease spread in the orchard -- enlarging crops. circles of affected trees -- reflects these Symptoms methods of transmission. All parts of the root system may be attacked by A. mellea is spread when infected roots are Phytophthora. The term 'root rot' refers to moved. This is accomplished by floods or infection of small roots, including the fine

210 feeder roots, and results in reduced uptake of into fields and orchards irrigated with water water and nutrients. This leads to a weakening from these sources. To date, Phytophthora has and decline of the tree. Above-ground not been found in well water. symptoms of root rot usually develop slowly, P. parasitica has been cultured from rotted and diseased trees show reduced growth, roots and crowns and usually is found in trunk thinned canopy and early defoliation for and canker infections of pistachio trees. P. several years. By contrast, crown rot girdles the cactorum and P. cryptogea also have been tree by destroying the crown and large roots isolated from trunk and scaffold cankers. In that anchor the tree in the soil. Trees with other crops, certain species of Phytophthora are crown rot typically die within a year or two associated with root rot, others with crown rot, after infection; they leaf out in spring then and some may cause both. Species also differ collapse with the first hot weather. The bark in their temperature, moisture, and nutritional and outer wood of infected roots and crowns requirements. Much is known about the are discolored, but the mycelium of interaction of different Phytophthora species Phytophthora in the infected tissues cannot be with various rootstocks and the environment seen by the naked eye. for other crops but not for pistachio. Phytophthora infections on the trunk or scaffolds of trees form cankers in the bark, and Control the tree gums profusely. If the trunk or scaffold Because prolonged periods of high soil is girdled by the infection, the portion of the moisture promote disease, water management tree above the site also dies. is the basis for control of Phytophthora root and crown rot. Cultural practices such as Disease cycle planting on berms, shortening irrigation time, Phytophthora species live independently in the and improving water penetration, all contribute soil and survive long dry periods as oospores, to lessened root and crown rot. Where root or the sexual fruiting bodies of the fungus, or crown rot are of concern, soil should not be wet chlamydospores, which are resistant asexual longer than 24 hours at a time. The relative spores. The infective units of Phytophthora are susceptibility of pistachio rootstocks to called zoospores. These are one-celled Phytophthora species is unknown. No structures that are capable of swimming chemicals are registered for control of this through water present in the soil. In response to disease on pistachios. Sprinklers should be set certain conditions of moisture and temperature, to avoid water hitting the tree or causing the fungus mycelium in the soil produces puddling around the crown. This is especially reproductive structures called sporangia. As important where irrigation water is taken from many as 100 zoospores develop inside each canals or rivers that may be contaminated with sporangium, and when the soil is flooded, the Phytophthora. zoospores are released. They are attracted to root exudates and swim to the root surface. SEEDLING BLIGHT There they attach themselves and invade the Seedling blight was first reported from tissues to establish an infection. Free moisture, California in 1995. In one nursery, over 10,000 i.e. liquid water, is required for both the seedlings, consisting of Pistacia atlantica, P. production and dissemination of the zoospores. integerrima, and P. atlantica×P. integerrima, Consequently, root and crown rots are were lost. The disease has not been observed in associated with heavy soils and prolonged orchard trees. periods of high soil moisture. Alternating Symptoms. Leaves turn brown, wither, and cycles of wet and dry soil are known to cling to the shoots. Brown cortical lesions exacerbate Phytophthora diseases in some develop on roots, which become discolored. crops. Stressed plants often are more Seedlings are stunted, blighted, and die (Plate susceptible to infection. 26G). The rotting tissues decompose and dry, Many Phytophthora spp. are present in forming a sunken area filled with dried plant canal and river water. The fungi are introduced

211 parts mixed with fungus mycelium and soils and once established remains indefinitely. sclerotia. Disease is usually more severe in soils that are Causal Organism. Rhizoctonia solani moderately wet and when plant growth is slow Kühn is a collective species of several strains due to adverse environmental conditions. R. that are distinguished from each other by solani spreads with rain, irrigation or flood anastomosis between isolates of the same water, equipment, and anything carrying anastomosis group. Isolates causing seedling contaminated soil or infected propagative blight belong to anastomosis group AG-4. R. materials. In greenhouses where pistachio solani exists primarily as a sterile mycelium rootstocks are germinated and initially planted, that is hyaline when young but turns yellowish infested benches can be a source of inoculum. or light brown with age. Branches grow at Optimum temperature for infection is 15-18° C approximate right angles to the main hypha and (59-65°F) but the disease is more common in have a cross wall near the slightly constricted warm areas (75-95°F). Seed transmission has junction. Under certain conditions the fungus not been demonstrated and is unlikely. produces hyphal tufts that form brown to black Control. Wet, poorly drained areas should sclerotia or short, barrel-shaped monilioid cells be avoided and seeds should be planted in that function as chlamydospores. The clean soil on raised beds under conditions that teleomorph, Thanatephorus cucumeris (A. B. encourage rapid growth. Greenhouse benches Frank) Donk has not been produced by should be cleaned, especially if a susceptible pistachio isolates. crop was grown previously. Drenching soil or Disease Cycle and Epidemiology. R. solani planting mix with pentachloronitrobenzene overwinters in soil as mycelium, sclerotia or helps reduce damping off in seed beds and chlamydospores. The fungus is present in most greenhouses.

SUMMARY

DISEASE SYMPTOMS WHEN SYMPTOMS CONTROL APPEAR Verticillium wilt Sudden collapse of branches Spring, early summer Plant resistant rootstocks Poor vigor which may be Growing season over several Plant resistant accompanied by slow thinning years rootstocks of canopy Phytophthora Slow thinning of canopy Growing season over several Plant resistant root rot years rootstocks Reduced growth, early Growing season over several Irrigation senescence years management Crown rot Sudden collapse of entire tree Spring or early summer Irrigation management Trunk canker Branch death, profuse Growing season Keep sprinkler water gumming off trunk Armillaria root rot Reduced growth, early Growing season Preplant fumigation; senescence, rhizomorphs on Plant resistant infected roots rootstocks Seedling Blight Leaves turn brown, wither, and Seedling stage in the nursery Sterile potting soil cling to shoots. Seedlings are greenhouse and clean nursery stunted, blighted, and die benches

212 References Rootstock Seedlings in California. Plant Dis. 1. Epstein, L., R. Beede, S. Kaur and L. 80(11):1303. Ferguson. 2004. Rootstock effects on 3. Holtz, B.A. 2002. Pistachio Seedling blight. pistachio trees grown in Verticillium dahliae- Pages 70-71 In. Compendium of Nut Crop infested soil. Phytopathology 94: 388-395. Diseases in Temperate Zones. B.L. 2. Holtz, B.A., T.J. Michailides, L. Ferguson, J.D. Teviotdale, T.J. Michailides and J.W. Pscheidt Hancock and A.R. Weinhold. 1996. First Report (eds.). American Phytopathological Society of Rhizoctonia solani (AG-4) on Pistachio (APS) Press, St. Paul, MN.

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