Greening Disease Threat to Texas Citrus...

Other Diseases

Disease Management

Diseases of citrus that affect the entire tree can be classified into two general categories:
• Biotic diseases, which are caused by living entities such as fungi, bacteria, viruses/viroids (a viroid is like a virus but does not have a protein coat), mycoplasmas/spiroplasmas and nematodes. Some biotic agents are restricted to certain parts of the plant, such as the root, trunk or fruit; others may affect several or all parts of the plant.
• Abiotic diseases, which are physiological disorders caused by excesses or deficiencies of certain nutrients or by unfavorable environmental conditions. Some of the most common abiotic diseases of citrus in Texas are iron chlorosis, micronutrient mottle leaf, salt injury and water table injury. In addition to the economic losses, these physiological disorders often predispose the tree to attack by disease-causing organisms.

The diseases discussed below are those present in or potentially devastating to the Texas citrus industry. For chemical control measures, see the Texas A&M University–Kingsville Citrus Center's Pest Control Guide. For organic measures, refer to the Texas Department of Agriculture's Organic Certification Program.

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  1. Melanose
  2. Greasy Spot
  3. Phytophthora
  4. Viral Diseases

Fungal Diseases

1. Melanose

Melanose is a fungal disease of citrus caused by Diaporthe citri Wolf (also known as Phomopsis citri Fawc). It produces pustules (small bumps) of various sizes on the fruit. A light infection on small to relatively large fruit produces small, discrete pustules. In a heavy infestation, the pustules are larger and may coalesce, often causing the tissue to crack and produce a stage called mudcake melanose.

Melanose disease is directly associated with the presence of dead twigs, especially recently killed ones. Dead twigs often harbor the fungus, which produces several dark, egg-shaped structures called pycnidia that contain many spores.

The spores are released from these structures when they become wet. Rainwater washes the spores onto the young fruit, leaves and twigs. The spores that land on young tissue initiate the infection process.

Grapefruit is most sensitive to melanose infection. Although infected fruit become less marketable as fresh fruit, the internal quality is unaffected.

Some growers are confused by melanose and rust mite symptoms. The following tips may help you identify melanose symptoms:

The melanose fungus can also cause a serious post-harvest disease called Phomopsis stem end rot. Both orange and grapefruit cultivars are susceptible to this disease, in which the infected tissue at the stem end part of the fruit shrinks.

A prominent feature of Phomopsis stem end rot is a clear demarcation line visible between the infected and the noninfected part of the fruit. In contrast, another type of postharvest stem end rot caused by the fungus Diplodia develops a characteristic finger-like projection of diseased tissue.

If the citrus tree is exposed to hours of below-freezing temperatures, the fungus could cause leaf drop, twig die back and, in a few cases, tree death.

The most important strategy for both melanose and stem end rot disease control is good cultural practice. Remove dead twigs from the tree by pruning, hedging or topping. Timely application of fungicides in the orchard can also reduce melanose infection.

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2. Greasy Spot

Greasy spot (GS) is an important disease of citrus caused by the fungus Mycosphaerella citri Whiteside. It is becoming more severe in the LRGV – within the past 3 years, trees in many orchards have been heavily defoliated. Many growers have had greasy spot-infected fruit.

GS reduces tree vigor and thereby fruit size. GS-infected fruit also tend to regreen; such fruit are culled for fresh-market fruit.

To be able to manage the disease, growers need to understand the three stages of the GS life cycle: the epiphytic, the saprophytic and the parasitic stages.

In the epiphytic stage, the GS fungus grows on the lower surface of leaves for a long period before it enters the stomata (air pores) to begin infection. In this stage, which can last for several weeks, asexual spores or conidia are produced. The hyphal tips (threadlike parts) growing on the undersurface of the leaves can function as a germ tube and begin the infection process.

The most important factor involved in the fungal spread of GS is the ascospores, which are the sexual spores developed in special fruiting bodies called perithecia. Perithecia are developed in decaying infected leaves on the ground. The ideal conditions for ascospore germination and epiphytic (surrounding the leaf surface) growth of the fungus include the presence of water or relative humidity near 100 percent and temperatures between 77 to 86 degrees F. The saprophytic stage of the fungus is the period when the perithecia develop and mature in decaying fallen leaves. Water from rain or irrigation enhances the release of ascospores into the air, and air currents carry the spores to the young growth flushes.

The major factors influencing greasy spot infection and disease severity are the number of infected leaves on the ground, the relative humidity, temperature, insect exudations (discharges), the amount of epiphytic growth and the physiological condition of the trees.

Stem-end rot disease showing tear staining and caused by Colletotrichum sp.

In the parasitic stage, the fungal filaments growing on the leaf surface enter the stomatal openings. The fungal growth causes the underside of the leaf surface to swell. This swelling is the first visible symptom of a new GS infection. The next sign is yellow spots, which develop into dark brown blisters resembling oil spots.

The most effective control material is citrus spray oil. Oil may help the cells resist the fungus. Fungicides will destroy the epiphytic growth of the fungus on the leaf surface. They provide protection for several weeks, which prevents the fungus from recolonizing.

The major source of ascospores for the new cycle of infection is infected leaf litter on the ground. If defoliation is severe, the leaf litter must be destroyed.

Florida citrus trees normally are defoliated more heavily than Texas trees. Florida’s rainy season starts in the summer, whereas our rainy season starts in the fall. Spray chemicals after the rainy season.

The epiphytic stage of trees on a microjet irrigation system may have different timing. In Texas, researchers are studying the epiphytic growth of GS fungus in young leaves of Rio Red grapefruit trees.

To destroy the fallen leaves, you can use a combination of blowing, raking and burning, but it is expensive.

Anthracnose

Anthracnose is a plant disease that causes black blisters or lesions. These lesions are caused by a fungus that produces spores in an acervulus, which is a saucer-shaped fruiting body (plural: acervuli). Anthracnose diseases occur worldwide, but the most severe losses are in the tropics and subtropics.
The major anthracnose diseases are caused by four members of the ascomycetes:

Anthracnose diseases are also caused by three members of the imperfect fungi:

Anthracnose in citrus is normally a postharvest disease of grapefruit, navel oranges and tangerines. It requires ethylene degreening.

The causal organism, Colletotrichum gloeosporioides Penz., is common in LRGV citrus orchards. It grows well and produces many spores in acervuli on deadwood. Rainwater may carry spores onto the fruit surface and often produces tear stains.

Normally, the spores germinate, developing a swollen tip, but they remain inactive at this stage. Ethylene treatment for degreening the fruit breaks the dormancy and stimulates the spores to grow.

Anthracnose does not spread from infected fruit to healthy fruit in the packinghouse or in storage. To prevent anthracnose during degreening, keep the degreening process to the minimum amount of time, limit the ethylene concentration to less than 10 ppm, and store packed fruit at 50 degrees F.

Orchard practices that minimize deadwood of the tree canopy are very important in managing anthracnose. A pre-harvest fungicide spray or a post-harvest treatment with a fungicide are effective chemical controls. In recent years, LRGV citrus growers and packers observed unusual blemishes on grapefruit and navel oranges after degreening. The rind of the affected fruit was firm and silvery gray, and some of the fruit showed tear staining. Eventually, the rind turned brown and developed soft rot.

When examined under a microscope, the fruit surface showed many black spores with swollen tips, especially in the tear-stained areas. The problem was more pronounced in grapefruit than in oranges. Also, the blemish problem was apparently connected to the use of a high concentration of ethylene for degreening.

Researchers isolated the cause of the blemishes to be a fungus, Colletotrichum.

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3. Phytophthora diseases

The commonly known fungus Phytophthora has more than 50 different species; most are plant parasites and some species have seriously affected human and plant populations. An important example of Phytophthora-induced disease and destruction is the European potato famine of the mid-19th century as a result of potato late blight caused by Phytophthora infestans.

In citrus, Phytophthora causes foot rot of the trunk, gummosis, feeder root rot, brown rot of fruit and blight disease of leaves and stem. In Texas, foot rot and root rot diseases are more prevalent than is brown rot.

In the Valley, foot rot and gummosis diseases are common, both in commercial orchards and in dooryard citrus. Although it is not unusual to see citrus trees die of Phytophthora, the percentage of infection and tree mortality can vary with the incidence of Phytophthora distribution and with the conditions that favor growth and establishment of the fungus in citrus trees.

In the field, the most important disease of Phytophthora is foot rot and associated gummosis. Foot rot affects the bark of the main trunk or roots at the ground surface. The fungus Phytophthora is normally present in natural soil, mainly in the form of resting spores, which have characteristic thick walls.

The thick walls allow these resting spores to survive in dry soils for long periods. Researchers have recovered Phytophthora from soil that has been air dried for more than 2 months and also after 3 to 4 months storage at -5 bars.

The resting spores germinate in moist soil, producing germ tubes that may end up in a structure called a sporangium, which is the next level of structural development in the distribution of Phytophthora in the field. The sporangium and its spores (sporangiospores) are less resistant to adverse environmental conditions. However, they can also survive some degree of heat, cold and dryness.

The sporangiospores are distributed in water, especially in flood-irrigated orchards. Each sporangiospore can begin an infection process, especially in young tissue.


Infection occurs through wounds or natural cracks on the bark. The fungus grows in the bark, killing the bark tissue. The infected bark becomes discolored because the tissue has died. Although a symptom of foot rot may be abundant gum exudation, the gum can be washed off in heavy rains.

Affected trees may look “pale” and have yellow veins and leaves. The infection may extend downward into the crown root (the main root) and can completely girdle the tree. Once the bark has been damaged substantially, the tree starts to wilt, sheds leaves and experiences twig die back. The fruit may hang on a dead tree for some time.

Feeder root rot, as the name implies, occurs in the feeder roots where the bark (cortex) sloughs off. In susceptible root­stocks, the initial symptoms are limited to the roots. However, as the disease progresses, the trees show substantial decline and yield loss. The trunk does not show symptoms as in foot rot.

Trees under stress from chemical, water, soil type and other horticultural conditions can weaken the feeder roots and predispose them to the easy access of the fungus that causes feeder root rot.

Brown rot is a fruit disease that starts as a light brown discoloration induced by Phytophthora. Under humid conditions, the fruit may develop a white mycelium on the surface. The disease is initiated on fruit in the branches closer to soil through inoculum introduced via water splashing.

Phytophthora-Diaprepes root weevil complex
In several LRGV citrus orchards, orange trees have declined rapidly and died. The affected trees first showed leaf wilt, yellowing and defoliation, then died within 4 to 5 weeks.

Researchers have been trying to identify the cause(s) of this serious problem since August 2000. Many of the affected trees were removed and the roots washed with a handgun sprayer. The roots showed extensive insect feeding injury (channeling) and symptoms of severe Phytophthora root rot. The channels varied from 1.25 to more than 30 cm long and up to 1.25 cm wide.

Scientists identified the white larvae (grubs) found in the soil as the blue-green citrus root weevil, Pachnaeus spp., and the sugarcane root stalk borer weevil, Diaprepes abbreviatus. Adult D. abbreviatus were captured in “Tedders traps” placed in the orchard. Also, larvae of D. abbreviatus were collected from the soil near affected trees.

Soil and root analysis have confirmed the presence of the Phytophthora fungus. Thus far, D. abbreviatus has been found in two LRGV orchards and surrounding dooryard properties. However, this type of tree damage exists in several locations.

In these other locations, 4.1 percent of the 1,768 trees surveyed were either dead or declining. One grower pushed out more than 145 dead trees; in another orchard, 20 percent of the trees died, but D. abbreviatus was not confirmed as the cause.

Studies to identify the cause(s) of tree death found that the problem was associated with a complex of Phytophthora-Diaprepes root weevil interaction. Diaprepes abbreviatus, a root weevil introduced into Florida in 1964, is now considered the worst long-lasting threat to the citrus industry in that state. There is no effective management program for its control and even partially effective programs cost more than $250/acre.

When the weevil larvae feed on the root system, the damage increases the incidence of Phytophthora. When Diaprepes is involved, there is a several-fold higher incidence of tree decline as a result of Phytophthora infection. This weevil can feed on many different hosts. Moreover, the reproductive capacity of Diaprepes is extremely high: A female can produce more than 20,000 adults in 4 years.

This is the first report of this serious new root weevil-Phytophthora disease complex in Texas citrus. The affected area is under quarantine by the Texas Department of Agriculture.

In a 2001 survey on citrus root weevil (Diaprepes abbreviatus) and fungus Phytophthora distribution in orchards, psorosis incidence was found up to 13.6 percent in a mixed planting of two old-line grapefruit cultivars and a navel orange. In another orchard that had D. abbreviatus, Phytophthora and poor soil conditions, though the psorosis incidence was low, the trees exhibited a compounding effect.

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4. Viral Diseases

Citrus tristeza virus (CTV)
Citrus tristeza disease is the most important citrus disease in the world. A major CTV disaster was reported in 1930 in the province of Corrientes, Argentina. In 1937, the disease was named tristeza – the sadness disease – in Brazil, where about 30 million citrus trees on sour orange rootstock were lost to CTV infection.

The term CTV covers different virus strains that produce at least five distinct biological reactions in citrus, depending on the cultivar and the environment:

The mild type isolates produce no noticeable symptoms on most commercial scion-rootstock combinations. However, they may cause slight stem pitting, vein clearing and flecking on Mexican lime plants kept in a cool greenhouse.

The seedling yellows (SY) type isolates may cause severe chlorosis and dwarfing of sour orange, lemon and grapefruit maintained in a greenhouse. SY type reaction is normally found in greenhouse-grown trees or in field trees top-worked with a susceptible cultivar.

The sour orange decline type isolates produce tree decline symptoms of sweet orange on sour orange rootstock. Grapefruit and tangerine cultivars are also commonly affected.

Field symptoms include a gradual or quick decline of trees on sour orange rootstock. Infected trees show leaf yellowing, wilting, defoliation and fruit hanging on dead trees. The bud union area may show needlelike pegs in the wood and pinholes in the bark. They may also show a brown line at the bud union.

The stem pitting on grapefruit type isolates produce chlorosis, stunting and stem pitting on the stems. In the field, grapefruit and pummelo may show large longitudinal ridges or ropes, and the fruit on infected trees are rather small.
The stem pitting on sweet orange type isolates produce chlorosis, stunting and stem pitting. In the field, sweet orange trees also produce small fruit that are not marketable as fresh, and the twigs may become brittle and break easily.

The presence of CTV isolates in general can be detected by enzyme linked immunosorbent assay (ELISA), which is a laboratory test that can detect disease-causing agents. CTV in the field is naturally transmitted by aphids, especially the brown citrus aphid. In addition to aphids, people transmit CTV and other viruses and viroids in nature. The inadvertent use of budwood from CTV-infected but symptomless trees to propagate new trees would increase the incidence of CTV in the field.

The most efficient insect vector of CTV is the brown citrus aphid (BrCA). It originated in China and moved to several countries, including the United States. It probably reached South America in the 1930s or before, spread naturally northward to the Caribbean Basin and arrived in Florida in 1995. In Belize, its presence was confirmed in 1996; it was detected in southern Mexico in 2000.

It is possible that it will soon reach Texas either from Florida or Mexico. The BrCA efficiently transmits CTV in many parts of the world, contributing to the decline of several million citrus trees grown on sour orange rootstock.

The rate of BrCA-related tree loss can be best illustrated by the case study reported from Venezuela. BrCA entered Venezuela in 1976 through the southeast (Colombia) and southwest (Brazil) borders. The aphid was well established by 1978 and resulted in the death of more than 6 million trees on sour orange rootstock.

CTV was detected in noncommercial citrus cultivars in the 1950s in the Lower Rio Grande Valley. Later surveys in the 1990s using ELISA detected the virus in commercial orchards, nurseries and dooryard plantings. CTV has been also found in East Texas.

CTV was detected in noncommercial samples collected since 1994 in the LRGV and from areas northeast of the Valley. CTV transmission studies done with local aphids have shown that the spirea aphid, Aphis spiraecola, transmitted CTV isolates in the LRGV.

Citrus psorosis virus (CPsV)

Psorosis disease of citrus has been reported to be spread in Texas orchards planted with nucellar, virus-free trees. Psorosis symptoms have also been reported in virus-free Rio Red grapefruit trees, which suggests that this virus may be transmitted naturally in Texas. It is our hypothesis that had it not been for the four tree-killing freezes in the past 50 years, the psorosis incidence in Texas would have been higher.

Psorosis disease of citrus has been known since 1896 and its viral etiology since 1933. The term “psorosis” has been used to describe several diseases that are transmissible through grafts and that produce leaf flecking in indicator plants. However, some have been characterized as being caused by different viruses.

It is the oldest citrus virus that is known and historically led to the establishment of a virus-free budwood programs in several citrus-producing states. The disease is caused by citrus psorosis virus (CPsV), with the genus name Ophiovirus.

The disease produces bark scaling that is different from that caused by fungus Phytophthora or Rio Grande gummosis diseases. This disease may also cause ring spots on leaves and fruit. However, many trees may grow in the field as symptomless carriers.

Reports from Argentina and Texas on the increase in the incidence of psorosis symptoms suggest that this virus may be transmitted naturally. Specifically, in Texas, the incidence of psorosis symptoms in nucellar, virus-free orchards increased from 0 to 11 trees within 7 years (1971-78). The percentage of psorosis disease increased from 0.7 to 2.0 in five orchards totaling about 3,400 trees. Vector transmission of psorosis has been suspected but not yet confirmed.

The Texas citrus industry in the LRGV dates back to the fruiting season of 1919-20, with a production of 12,000 boxes of fruit. The acreage and fruit production continued to increase for many years.

However, between January 1951 and December 1989, four tree-killing freezes occurred in Texas. These freezes crippled the acreage to as low as 12,000, but production has always been reestablished. Among the three or four grapefruit cultivars, Rio Red is planted in more than 70 percent of the area.

The tree-killing freezes drastically reduced the citrus acreage in the LRGV. This natural calamity probably helped reduce the incidence of prososis symptoms in commercial orchards.

In addition, the development and commercial success of a new (psorosis-free) grapefruit cultivar, Rio Red, through a mutation breeding also helped to reduce the overall impact of psorosis disease in Texas.

But in the past 6 years, field symptoms of psorosis have been found in new plantations (post-1989), old plantations (trees pruned after the 1983 freeze), dooryard trees (post 1983) and nucellar trees. Psorosis symptoms have been detected in Rio Red orchards that originated from a single source of psorosis-free trees, which implies that natural transmission is possible.

The incidence of psorosis in nucellar trees (from the 1970s to present) and in Rio Red grapefruit plants (current) in Texas suggests that the virus may be transmitted naturally. We believe that the incidence of psorosis in Texas would have been higher if not for the tree-killing freezes. A new virus-free program will help reduce the incidence of graft-transmissible psorosis.

Stem pitting and gum deposits typical of Cachexia viroid disease.

 

Citrus tatter leaf virus (CTLV)

Citrus tatter leaf virus (CTLV) was first discovered in California in 1962 on Meyer lemon trees introduced from China. This disease was also reported from other places in the 1960s and ‘70s. In Texas, CTLV-like symptoms were discovered in indicator plants inoculated with tissue from Meyer lemon.

Most citrus species and commercial cultivars are symptomless carriers of this virus. A bud-union crease (with or without fluting of the stem) may develop when infected scions are grafted to trifoliate orange or its hybrids. When the bud-union crease is severe, the tops may shear off at the union in high winds.

Citrus tatter leaf virus is an important disease that growers should take into consideration when replacing sour orange with rootstocks of trifoliate orange or its hybrids. Always use virus-free plants for propagation. CTLV-free Meyer lemon is already available in Texas, and nurseries are encouraged to use only virus-free budwood.

The presence of CTLV is generally detected based on reactions of indicator plants such as Citrus excelsa and citranges. The common symptoms of CTLV infection are tattering of young leaves, chlorosis and asymmetric leaf distortion.

Viroid Diseases

Citrus exocortis viroid (CEVd)
Field symptoms are rare among commercial citrus trees in Texas. This is because the common rootstock, sour orange, is tolerant to CEVd. However, commercial citrus on tolerant root­stock can be stunted to some degree. Susceptible rootstocks that show field symptoms include trifoliate orange and its hybrids. These rootstocks show bark scaling and tree dwarfing. In the 1990s, several samples suspected to have CEVd were collected from commercial plantings. The presence of CEVd was tested by indexing on to ‘Etrog’ citron indicator plants. Of 45 suspected samples, 16 were found to carry CEVd based on the reaction of Etrog citron indicator plants for CEVd.

Cachexia

Cachexia (also called xyloporosis) is another viroid disease of citrus. Unlike exocortis, it affects the scion part of mandarins, tangelos and Palestine sweet lime trees. Cachexia produces wood pitting and gumming in the bark and distorted leaves in mature trees. Although this viroid is present in many citrus-producing areas, the disease symptoms are more prevalent in some of the Mediterranean countries.

Citrus Nematode

 Citrus nematode, Tylenchulus semipenetrans Cobb, is an important pest in the LRGV. It feeds on young root tissue, using a spear or stylet (a slender probe) protruding from the “head.” Feeding by an inconceivably large number of nematodes often results in the general decline of tree health and the production of fewer and smaller fruit. Affected trees do not die from citrus nematode infection alone. The effect of citrus nematode is often referred to as “slow decline.” Sour orange, the predominant rootstock used in the Valley, is susceptible to attack by citrus nematodes. The greatest concentration of nematodes is in the upper 1 foot of soil.

A typical life cycle of citrus nematode can take 1 to 2 months. Eggs that are destined to be males do not develop a stylet and therefore cannot feed on root tissue. Female juvenile larvae feed on root surface cells, each larva often embedding 1⁄4 of its anterior body into root tissue (this is about 4 to 5 cells deep). Adult females penetrate deep into roots. Thus, a typical feeding nematode becomes a sedentary pest that feeds and develops a comparatively larger body (the posterior part) outside the root tissue. Females excrete gelatin and deposit many eggs into it. Nematode populations are influenced by such factors as climate, soil type and root mass. Peaks in citrus nematode population in soil and roots are often associated with new growth of roots. Therefore, spring is an ideal time to have soil samples tested for nematodes.
The best strategy to control citrus nematode is prevention. Start with buying and planting trees grown in nematode-free soil. Unfortunately, most nurseries in the Valley have no programs to eliminate nematodes or to plant trees in nematode-free nursery plots.

In soils heavily infested with nematodes, the preferred control method is to fumigate the orchard site before planting. In dooryard situations, nematode populations can be managed by solarizing the soil with plastic mulch before planting.

When managing nematode problems, remember:

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