Food and Fertilizer Technology Center - publications

Jun. 01, 2003

Citrus Greening and Virus Diseases

Virus Diseases of Citrus

Citrus is one of the most important fruit crops in the Asian and Pacific region. However, most citrus orchards are now suffering severe losses from virus diseases, particularly tristeza and tatter leaf, and the virus-like citrus greening ("huanglongbin").

All of these diseases are highly infectious and incurable. Once an orchard has become infected, there is no effective chemical control. The trees gradually decline in vigor and yield, until finally they die. The average life span of citrus orchards in tropical countries is less than ten years, mainly because of these diseases.

Realizing how important this problem is to citrus growers, FFTC has sponsored since 1997 more than four training programs on how to diagnose and detect these diseases, using diagnostic molecular probes. The Center has also held training courses on shoot-tip micrografting techniques for eliminating viruses and greening pathogens in citrus foundation stock (
Fig. 1

Disease Incidence

It is greening disease which does most damage to citrus orchards in their countries. Transmission is through infected planting materials, and by the vector, the Asian citrus psyllid. Citrus tristeza virus is generally the second most important disease problem. It is transmitted by several species of vector aphids. Fortunately, most of the methods used to control citrus greening are also effective against tristeza and other viruses.

Control of the Diseases

Control of the Vector

Control of citrus greening and other diseases transmitted by insects is based on control of the vector. This in turn requires a good understanding of the population dynamics of the vector insects. Continued heavy effective applications of chemical pesticides are expensive and not very effective, as well as harmful to the environment. Spraying should be prophylactic, on the first young growth as soon as populations begin to increase at sprouting time.

Mineral Oils

Mineral oils are at least as effective in controlling the citrus psyllid as a range of synthetic chemicals. Mineral oils also have the advantage that they are broad-spectrum, controlling other pests such as citrus red mite, aphids, scale insects, and fungus diseases such as greasy spot. They also kill algae, leaving the trees and fruit clean. Heavier oils seem to be more effective than light ones under tropical conditions.

The pest control effect is largely the result of suffocation, as the oil moves into the spiracles of insects. However, more recently it has been realized that the control is also behavioral. For example, leafminer females do not lay eggs on oil deposits. Mineral oil can also reduce the transmission of virus by aphids. With non-persistent viruses, the oil interferes with the retention of virus by aphids, whitefly and thrips. (Unfortunately, transmission of citrus greening by phyllids is persistent).

One problem with mineral oils is that heavy applications may injure the tree (phytotoxicity). In recent years, it has been realized that reducing the concentration from 2% to 1% halved the risk of phytotoxicity without reducing the effectiveness.

Recently, experiments in Sarawak have found that more frequent sprays using an even lower concentration of mineral oil (0.5%) did not induce phytotoxicity. Since the climate is warm, the growth rate is faster. The oil disappeared more quickly than when it is used as a spray in cooler climates.

Disease-Free Seedlings

Many countries have begun programs to produce disease-free seedlings. There was a general consensus among participants that the private sector has an important role in a disease-free nursery system, often in cooperation with the government. In Taiwan and Sarawak, farmers' associations are actively involved in the mass production of disease-free seedlings. In Sarawak, production is done by the private sector and distribution by the farmers' association.

In Taiwan, the farmers' associations produce the seedlings themselves. Some of them are doing a good job, but others have poor operations. The government is now encouraging the private sector in Taiwan to become involved in the production of disease-free seedlings.

In several cases, the government has funded the expensive facilities such as screenhouses (
Fig. 2
) and also the disease-free foundation stock, needed to produce disease-free seedlings, (
Fig. 3
), while the actual day-to-day operations have been entrusted to the private sector. This is because the private sector can manage production more efficiently, and produce seedlings at a faster rate and for a lower cost. This combination of government-owned facilities, operated by the private sector under contract, seems to be a very successful model, especially in less industrialized countries where it is difficult for the private sector to raise large amounts of capital. Ownership of facilities by the government ensures that quality standards are maintained, and that the interests of farmers in the sale of seedlings takes priority over increasing the profits.

Management of Disease-Free Orchards

Once the healthy seedlings are planted out in the field, the next step is to keep them free of disease as long as possible. Achieving this is based on an integrated management system. The aim is to monitor the orchard for pests, particularly vector insects, and spray only to prevent population build-up, particularly at the time of growth flushes.

Prompt eradication of inoculum sources, including infected citrus trees and alternative host plants, is very important. To minimize chemical sprays, growers use field practices to control pests and diseases.

Overall, the emphasis is on improving the orchard environment. The layout and design ensure good ventilation and exposure to sunlight. Soil management is emphasized, including an efficient fertilization program, and grassy cover in orchards where rainfall is heavy. While these practices may not keep the trees free of greening and virus diseases indefinitely, they will prolong their useful lifespan, and keep the trees productive for some years even after they have been infected.


Greening and virus diseases are difficult to diagnose on the basis of physical symptoms. Trees may have a latent infection with no visible symptoms. Where there are symptoms, their expression may differ from one variety to another, and according to whether the infection is a mild or virulent strain. Indexing, to identify diseased plants and distinguish them form healthy ones, is a vital aspect of disease control. This is especially important for foundation stock, but is also important for eliminating diseased plants as sources of inoculum in the field.

An important new innovation is a field testing kit for citrus tatter leaf virus (RNEasy Plant mini kit). A field testing kit for citrus tristeza virus has also been developed, and was demonstrated by Professor Hong-Ji Su at the Workshop. It shows whether a tree is healthy or infected with tristeza virus within a few minutes. It will soon be produced commercially. It is important that the sample tested is made up of small pieces of leaves taken from different parts of the plant. This is because like greening bacteria, the tristeza virus particles are unevenly distributed in the tree.

PCR tests, which are carried out in a laboratory, have been developed by Professor Su and his colleagues for citrus tatter leaf virus, citrus exocortis virus and citrus greening. These are faster and more accurate than the traditional indexing on indicator plants. However, PCR testing is technically difficult, and also rather expensive. Work is now underway at Dr. Su's laboratory to develop a rapid field test for citrus greening.

Establishment of Disease Free Foundation Stock

Greening disease and virus diseases can only be controlled if the seedlings planted out in the field are free of disease. This in turn depends on a supply of foundation stock which is free of infection, whether active or latent. The foundation stock supplies the scions for grafting. The rootstock are grown from seed, which breaks the cycle of virus transmission.

A national scheme of citrus budwood certification has been operating in Taiwan since 1983. The citrus rehabilitation program is extending a similar system to other Asian countries. Many changes and improvements have been made over the past two decades. Pathogen-free foundation stocks are established through a shoot-tip micro-grafting system.

The production of pathogen-free citrus seedlings is performed by using virus-free scions propagated from the foundation stock trees. This is a very efficient way of using foundation stock, since each year a single mother tree can provide buds for dozens of grafted plants. In Taiwan, some of the foundation stock have been kept in a screenhouse for more than ten years and are still free of disease.


There is no easy solution to the problem of citrus greening and virus diseases. Control must be based on the mass production of disease-free planting stock. These are always going to be more expensive than ordinary cuttings grown by marcotting or sidegrafting. If price is an important factor, especially in low-income countries, governments may need to subsidize their production cost. This is being done effectively in many Asian countries by government investment into facilities such as screenhouses, with actual operations being carried out by the private sector.

Indexing and diagnosis is an essential technology, since only these can show definitely whether a tree is diseased or healthy. Field test kits for virus diseases are a new development which will be immensely useful. For the first time, trees can be tested out in the field, rather than in the laboratory. Furthermore, the tests are simple and cheap, and give results in a few minutes. It is to be hoped a field test kit can also be developed for greening disease.

The final step, the management of a disease-free orchard, is also the most difficult. It follows an integrated approach that begins with layout and design, and continues with good soil and water management, as well as pest control. Constant monitoring allows growers to apply prophylactic sprays at an early stage of pest buildup, to keep pest populations at a minimum for minimum pesticide input. Good pruning and canopy management are important for sprays to be effective.

However, even with the best pest control practices, it is impossible to eradicate aphids and citrus psyllids from tropical and subtropical orchards. Success must be seen in the life span of the orchards, not in the unachievable goal of 100% healthy trees and 100% eradication of the vector.

The life span of orchards in tropical Asia without proper control measures against greening and virus disease is about 5-6 years. Using the control measures, the life span can be extended to twelve years or even more. However, it is important that growers are coordinated in their efforts. One infected orchard, or even one infected tree, can do great damage to the control efforts in neighboring orchards.

International FFTC Workshop on Rehabilitation of Citrus Orchards in Tropical Asian Countries

Held at the Phuong Dong Hotel, Vinh, Nghe An Province, Vietnam on November 5-6

No. of countries participating: 8 (Australia, Japan, Korea, Malaysia, Philippines, Taiwan, Thailand, Vietnam)

No. of papers presented: 12

No. of participants: 20 plus observers

Co-sponsors: Ministry of Agriculture and Rural Development, Vietnam National Inst. for Plant Protection (NIPP),

Vietnam People's Committee of Nghe An Province, Vietnam

Index of Images

  • Figure 1 Young Nursery Tree Already Has Greening Disease

    Figure 1 Young Nursery Tree Already Has Greening Disease

  • Figure 2 Some of the Thirteen Screenhouses, Insect-Proof Screenhouses for Disease-Free Seedlings in Nghe an Province, Vietnam

    Figure 2 Some of the Thirteen Screenhouses, Insect-Proof Screenhouses for Disease-Free Seedlings in Nghe an Province, Vietnam

  • Figure 3 Foundation Stock in a Screenhouse, Insect-Proof Screenhouses for Disease-Free Seedlings in Nghe an Province, Vietnam

    Figure 3 Foundation Stock in a Screenhouse, Insect-Proof Screenhouses for Disease-Free Seedlings in Nghe an Province, Vietnam

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