Tristeza represents one of the biggest threats to citrus production around the globe. The severity of the strains can change, and the tolerance of certain scion/rootstock combinations to this virus can no longer be taken for granted. Careless introduction of severe strains, such as the orange stem pitting strain of tristeza recently found in Queensland, is a constant risk.

There are more than 30 virus and virus-like diseases of citrus known in the world, of which citrus tristeza virus (CTV) is arguably the most destructive. In 1981, the total world loss attributable to this disease was estimated at 50 million trees⁽¹⁾. CTV is spread in the field by aphid species, which transmit the disease with varying degrees of efficacy. The most efficient vector of CTV is the black citrus aphid (Toxoptera citricida), which is widespread in New Zealand. The high degree of efficacy of this aphid as a CTV vector was demonstrated by the rapid spread of the disease in South America immediately after the introduction of the disease.

Symptoms
The most economically important symptom is the quick decline or death of orange, grapefruit and mandarin trees on sour orange rootstock. Virus infection in the scion causes dieback of the phloem in the sour orange rootstock below the bud union. This results in the rootstock being girdled and therefore starved as the starch reserves are depleted. A second symptom of the disease is a 'slow decline' where the trees decline in health over a period of years. This decline is accompanied by a loss in productivity but the tree does not necessarily die. A third common symptom is stunting where the virus does not kill the tree, but the tree does not grow. In areas where Toxoptera citricida is present, some CTV strains cause stem pitting which may give a bumpy appearance to the trunk and limbs of the tree. Either deep pits are present under depressed areas of the bark, or more severe strains may cause a more general distribution of the stem pitting, with a thickening of the bark and many fine pits. The virus may also have a latent form which gives no symptoms.

Stem pitting symptoms caused by citrus tristeza virus.

World History
CTV apparently originated in Asia where it existed for centuries unrecognised, possibly because the commonly grown citrus cultivars were highly tolerant. Citrus was first introduced to Europe and the New World as seed, and since CTV is not seed transmitted, these trees were free of the virus. The major diseases of concern at this time were Phytophthora gummosis and root rot, and consequently trees were grafted onto the highly adaptable Phytophthora-resistant sour orange rootstock. This decision has contributed to the dramatic effect that CTV has had on world citrus production. The first tristeza disaster was reported in the 1930's in Argentina, where 90% of the citrus was planted on sour orange rootstock.

Quick decline was first identified in Australia and New Zealand in 1940. This was preceded by similar symptoms being noted in South Africa in 1900, Java in 1928, Argentina in 1930, Brazil in 1937 and then California in 1939. It was originally thought to be an 'incompatibility problem', for example, Australian nurserymen were reporting total failure of sour orange rootstock as early as 1928⁽²⁾. The famous Avondale nurseryman, Hayward Wright, spent many frustrating years in the 1930s and 40s attempting to grow citrus on sour orange stock. A case of 'quick decline' was recorded in New Zealand at Mt Albert Research Centre in 1954⁽³⁾, when buds of Washington navel orange were worked on to sour orange stocks as part of a rootstock trial. It was not until the outbreak of 'incompatibility' symptoms in South America that the phenomenon was better understood, and then finally in 1946 linked with a virus causal agent^(4&5).

CTV is today widespread in Israel, Morocco, India, China, Japan, Southern California, Florida, Argentina, Brazil, South Africa, Australia and southern Spain, and is moving into previously free, northern Spain. Corsica is currently free of CTV, although three low-efficiency aphid vectors (Aphis spiraecola, A.gossypii and Toxoptera aurantii) occur there. Italy is supposedly free of CTV, although some infected trees had been detected in southern areas. Again, the three vector species listed above also occur in Italy. Surprisingly, sour orange continues to be the main rootstock used in Italian nurseries.

New Zealand Situation
In the late 1950's the spread of tristeza in Spain reached epidemic proportions, resulting in the death of 15 million trees on sour orange rootstock, with several million more in different stages of decline. Countries such as Spain all experienced devastating losses from CTV because of widespread use of a susceptible rootstock. However, in New Zealand all our citrus is today grown on rootstocks which historically are tolerant of CTV - Poncirus trifoliata, citranges and sweet orange. What then is the risk of CTV to the New Zealand citrus industry?

Recently, an outbreak of CTV has occurred in the Central Burnett area of Queensland⁽⁶⁾. Alarmingly, this strain of CTV affects Valencia orange, Joppa orange, Navel orange and Ortanique tangor in increasing order of severity. This severe orange stem pitting (OSP) isolate is believed to be of exotic origin i.e. it was probably brought in on illegally imported budwood. The most characteristic symptoms are a brittleness of twigs and branches, due to fine pitting and yellow staining of the wood, resulting in a honeycomb effect. Other symptoms are curling, mottling and size reduction of leaves, small fruit and a reduction in tree size. A disturbing fact of this disease is that the orchard spread has continued despite the removal of obviously infected trees. The Queensland Citrus Budwood Scheme was wound up this year because of the fear of spreading infected budwood.

In Japan and South America a similar OPS strain of CTV develops symptoms in Minneola tangelo and Swingle citrumelo rootstock. In Peru, the navel orange industry has been devastated by an OSP strain introduced on satsuma budwood from Japan. This suggests that our CTV tolerant rootstocks might not be as foolproof an insurance policy as we once thought.

Large numbers of citrus nursery trees were imported into New Zealand from Australia during the 1930's and 40's, during which time quarantine restrictions were non-existent. It is probable therefore that the New Zealand CTV strains are similar to those present in Australia. It is suspected that CTV strains have not caused major reductions in tree growth and yield in our orchards because we are using tolerant scion/stock combinations, and because a degree of mild strain cross-protection is taking place. However, CTV is not limited only to certain stionic combinations, and our current state of bliss could be shattered by a similar situation to that in Queensland.

Control Measures
It is hard not to sound alarmist when discussing the potential threat of vector-transmitted viruses such as CTV. But complacency about this problem could easily result in huge tree and production losses to our industry. In New Zealand, where the highly efficient vector Toxoptera citricida is wide spread, we need to be aware of two factors : (1) the need to stringently exclude any introduction of severe strains, and (2) the need for mild strain protection in the future.

Strict control by quarantine must be continued in order to prevent the introduction of more severe strains. Such strains may attack combinations other than those on sour orange or attack cultivars which are tolerant to strains already present. For growers and nurserymen, this means never, ever considering illegal importation of citrus budwood. MAF Quality Management at Lynfield has sound procedures and facilities for handling introduction and quarantine of citrus from high risk countries such as Japan. Any introduction of citrus budwood other than through Lynfield could be disastrous for our industry. If you have any knowledge of illegal budwood imports, please contact us immediately - you will be doing yourself and your industry a service.

Mild Strain Cross Protection
In recent years much effort has been devoted to mild strain cross protection research. Cross protection works upon the basis that if you inoculate trees with mild CTV isolate (symptomless or causing only mild symptoms) and later infect with a severe isolate, the symptoms of the severe isolate would not be expressed. This approach at present appears promising in controlling stem pitting symptoms in trees on tolerant rootstock varieties. It has not been effective in controlling decline of trees on sour orange rootstocks.

One of the best examples of the implementation of this research has been in Brazil⁽⁷⁾. Brazil is the largest exporter of citrus juice concentrate in the world. In the 1930's this country lost its entire industry, which is based to a large degree on the Pera sweet orange variety, because of decline due to CTV. Pera trees, even when planted on CTV tolerant rootstocks, become severely affected by the field strains of the virus. It was at this point that the preimmunization of trees with mild CTV isolates was proposed as a means of cross-protection.

The distribution of preimmunized budwood started two decades ago. Large scale propagation of cross-protected Pera by budding has neither altered the CTV strain severity, nor led to breakdown in protection.

Over the years, this method has been extended in Brazil to other citrus types and strain interactions. Based upon the excellent results obtained, it is suggested now that all budwood released to growers should be preimmunized. Increasing use of preimmunized plant material in any given region may lead to a change in the composition of the field CTV isolates, resulting in the mild strain predominating. This in turn should lead to a decrease in infection pressure by severe isolates, thereby reducing the risk of a breakdown of the cross-protection in those citrus types that are particularly sensitive to CTV. Preimmunization is also a standard routine for all citrus cultivars in South Africa, and for grapefruit in the NSW budwood scheme.

New Cultivar Introductions
All new cultivar imports must now meet rigorous quarantine standards, which require that the material which passes through quarantine is virus free. These virus free trees need to be protected from infection by severe strains of CTV. Our native strains could be devastating to any one of our new imported cultivars. Until such time as we can ascertain that these trees will not be debilitated by local orchard strains of CTV, or until we are able to preimmunize the trees with a selected mild strain, two trees of each virus-free cultivar will be housed in an aphid-proof glasshouse. This structure has been built at Kerikeri Research Centre, with funding supplied by the Citrus Sector of NZ Fruitgrowers Federation.

Summary
We believe that a calm but proactive approach to CTV should be taken by the New Zealand citrus industry. This should include the following measures :
(i) Continuing the maintenance of CTV-free trees of important commercial cultivars
    in an aphid-proof screenhouse
(ii) Initiating a project to define the severity and complexity of CTV strains in New Zealand,
    and to seek potential mild strains
(iii) Initiating a CTV mild strain preimmunization programme
(iv) Ensuring that we maintain technical awareness of world developments on CTV research.

HortResearch has identified NZ tristeza characterization and mild strain preimmunization as an important research area, and has allocated funding to it. Ted Dawson has been awarded a Queen Elizabeth II Technicians Study award to study CTV identification techniques in the laboratory of Pat Barkley at the Biological and Chemical Research Institute, Sydney. In this first year, we will focus on defining the severity and complexity of CTV strains in New Zealand citrus orchards.

Acknowledgments
We thank the Citrus Sector of the NZ Fruitgrowers Federation and the Ministry of Education (Queen Elizabeth II Technician Study Award) for financial assistance. We would also like to thank Pat Barkley for hosting Carol Jagiello during August and Ted Dawson during September/October of this year.

References
1. Bar-Joseph M., Roistacher C.N., Garnsey S.M. and Gumpf D.J. 1981. A review of
   tristeza, an ongoing threat to citriculture. Proc. Int. Soc. Citricul. 1:419-423.
2. Fraser L.R. 1959. The relation of seedling yellows to tristeza. In: Citrus diseases.
   [J.M. Wallace ed.]. University of California.
3. Chamberlain E.E. 1954. Plant virus diseases in New Zealand. Bull. NZ DSIR 108:205
4. Fawcett H.S. and Wallace J.M. 1946. Evidence of the virus nature of citrus quick decline.
   Calif. Citrogr. 32:50, 88-89
5. Meneghini M. 1946. Sobre a naturaleza e transmissibilidade de doenca "Tristeza" dos
   Citrus. O Biologico. 12:285-287
6. Owen-Turner J. 1990. Citrus Tristeza Virus. Queensland Citrus Bulletin. Department
   of Primary Industries.
7. Muller G.W. and Costa A.S. 1968. Further evidence on protective interference in citrus
   tristeza. [In: Childs ed]. Proc. IV Int. Org. Citrus Virol. Univ. Flo. Press.

Source:
The Orchardist, September 1992