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Risk of heart attack in the orange groves

Citrus sudden death kills trees in a few weeks, threatens production, and challenges researchers

Two years ago, in the orange groves of the Minas Gerais municipality of Comendador Gomes, a few kilometers from the border with São Paulo, a strange disease that seemed like a heart attack was identified for the first time. In a matter of months, sometimes in just a week, the leaves of the trees that have been hit by the unknown malady would lose their color, and the plants would die, deprived of nutrients and water – probably as a result of the generalized clogging up of the system (the phloem) that takes the sap produced from the canopy to the roots. With luck, the moribund tree would still provide one crop of oranges, the juice of which is not affected by the ailment, but the demise of the plant would be just a question of time. Not much time. Due to its fulminating effect, the new threat was baptized as citrus sudden death (CSD) and was rapidly promoted to the condition of today’s number one enemy of citriculture.

Last month, the Ministry of Agriculture and the government of São Paulo, with the collaboration of the citrus fruit growers and research institutes, created a task force to try to hold back the advance of the disease, which has already hit 1 million orange trees from a dozen municipalities from the south of Minas Gerais and the far north of São Paulo, according to the most recent forecast carried out by the Sanitary Defense of the State and the Fund for Citrus Plant Protection (Fundecitrus), a private institution maintained by producers and juice industries. Over 90% of the confirmed cases of the disease are in the region of the Triangle of Minas Gerais (South of the State of Minas Gerais), apparently the cradle of this sudden death, where only 17 municipalities are dedicated to citriculture.

In São Paulo, the state that has 70% of the country’s orange groves, which are spread over more than 300 municipalities, the situation is less serious, for the time being. The presence of the ailment is restricted to the northernmost tip of the state, but it is on its way southwards at a speed estimated at from 30 to 40 kilometers a year. “Thirty percent of São Paulo’s citriculture lies within a distance of 100 kilometers from the outbreaks of the infection”, explains Ademerval Garcia, president of the Brazilian Association of Citrus Exporters (Abecitrus).

With the grim reaper of sudden death scratching the heart of the groves in São Paulo, Fundecitrus swiftly mobilized over a dozen research institutes from here and even from abroad to study the new ailment. In spite of all the efforts, the knowledge of this sudden death is still more empirical, the fruit of observations of the disease in the field, than properly scientific, a sign that a lot of work still lies ahead. Little is known about the ailment. Its causal agent, probably a virus, is still unknown. Perhaps it is a mutation or a more aggressive reintroduction of the citrus tristeza virus, a disease that in the 40’s decimated over 80% of the orange trees in the São Paulo hinterland and used to show signs similar to those of sudden death.

“Except that the trees infected by tristeza could live for as long as six years, whereas those attacked by sudden death perish far more quickly”, comments agronomist engineer Marcos Antônio Machado, from the Sylvio Moreira Citrus Center, an institution located in Cordeirópolis, upstate São Paulo, and linked to the Campinas Agronomy Institute (IAC). The form of transmission of this illness that is reminiscent of a heart attack in citrus fruit is also a mystery, although there is evidence that the ailment is disseminated through the air, possibly by an insect.

Changes in sight
In this scene of uncertainties, one idea is taking shape among researchers and producers of citrus fruit: Brazilian citriculture – which is the largest in the world, a little ahead of the United States – will not be the same after sudden death. There is no catastrophic sense built into the above phrase. Although there is still no cure in sight for sudden death, the orange groves are not going to disappear because of the new ailment. But, for sure, they will have to undergo transformations to beat the intriguing illness that, according to Fundecitrus, has already brought about losses of some US$ 20 million for the sector, which generates annual exports in the order of US$ 1.3 billion, above all in the form of concentrated juice, and employs 400,000 persons in São Paulo alone.

And therein lies the good news: if the cause and the form of transmission of CSD have not yet been discovered, the researchers now have in hands the means for minimizing or avoiding the disease spread. As sudden death attacks exclusively varieties of oranges grafted onto the Rangpur lime, by far the most common in São Paulo and in the south of Minas, it seems that the replacement of this part of the plants can hold back the advance of the symptoms of the disease in trees that have already been contaminated, and perhaps even avoid the propagation of sudden death in healthy orchards. It may not even be the solution for the problem, but it is, in the worst of the scenarios, a way of gaining time and reducing the speed that the disease progresses until more effective solutions are found.

It so happens that abandoning the main rootstock for grafting will lead to quite a change in citriculture. At the same time palliative and preventive, this measure will have serious implications from the point of view of productivity. “The Rangpur lime is today what gives our citriculture its competitiveness, given that this kind of rootstock, more rustic, dispenses with irrigation, even in areas with a dryer climate”, Machado reckons. “To escape from sudden death, we are going to have to change the rootstock of roughly 160 million trees (some 85% of the groves in São Paulo and Minas Gerais are grafted on Rangpur lime rootstocks) and in many cases turn to cultivation under irrigation”, reckons Ademerval Garcia da Abecitrus.

What does adopting rootstocks that are more tolerant to sudden death have to do with the use of irrigation in the orange plantations? Of the four rootstocks that have up till now proved tolerant to the causal agent of citrus sudden death, whatever that agent is, three – the Cleopatra mandarin, the Sunki tangerine and the Swingle citrumelo – need an extra dose of water, besides the water that comes from the rain, to sustain a productive orange tree. Only the Volkamer lemon, another candidate to take the place of the Rangpur lime rootstocks, dispenses with irrigation. It so happens that this rootstock is incompatible with the Sweet Pera orange, one of the most important varieties of citrus cultivated here.

“To abandon the Rangpur lime rootstocks and migrate to other rootstocks, citriculture will need to be under irrigation or to move to places with a more rainy climate”, explains Juliano Ayres, Fundecitrus’s scientific manager. This line of thought is particularly valid for the south of Minas Gerais and the northernmost part of São Paulo, areas of great hydric stress, within an ecosystem that is typical of the cerrado (savanna), where citriculture has only arrived successfully thanks to the vigor of the Rangpur lime rootstock. Coincidentally (or not), it was precisely in this region that CSD originated.

The productivity in irrigated groves can be two or three times more than in areas without this resource. On the other hand, the cost of implanting and maintaining these artificial systems calls for greater planning and heavier investments.

Among the major citrus producing countries in the world, such as the United States and Spain, Brazil is the only one that does not have to resort massively to irrigation. Unless a cure or a way of controlling the advance of CSD that dispenses with the generalized exchange of orange tree rootstocks comes out of the research laboratories quickly, citriculture in São Paulo (and nationwide) will have to be redesigned rapidly. The ideal is for the reform to be carried out without affecting productivity, a difficult objective to be attained. “We are going to have to change the tire with the car in movement”, is Garcia’s comparison.

Challenge for science
Luckily, the cultivation of citrus is one of the most dynamic segments in Brazilian agriculture, with an ample tradition of getting round, or at least learning to live with, challenging diseases and a good track record of integration and investments in the area of research. For years, citrus canker and Citrus Variegated Chlorosis (CVC), two diseases with a great economic impact for orange producers, have been the target of several works, some at a world-wide level, in research institutes, universities and at Fundecitrus. The famous sequencing of the genome of the Xylella fastidiosa bacterium, the causal agent of CVC, for example, was carried out by Onsa, the virtual network of genomic laboratories created and maintained by FAPESP.

For having been the first complete sequencing of the genome of a pathogen that attacks plants, the work on Xylella made he cover of Nature, the most important scientific magazine in the world, on July 13, 2000. The good job done by the São Paulo researchers with the CVC-causing bacterium led the United States Department of Agriculture (USDA), a body equivalent to a Ministry of Agriculture in the USA, to commission, before the end of 2000, the sequencing of the genome of a variety of X. fastidiosa that attacks the grapevines of California, the main wine producing American state. The deciphering of the grape Xylella ‘s DNA has just been published in an international scientific magazine.

Being a totally new disease, without any record in any other part of the world except the south of Minas and far north of São Paulo, sudden death is, for the while, specific to Brazilian producers – and to the research centers set up here that started to study it less than two years ago. Scientists from Spain, France and the United States are collaborating with some lines of study of CSD, but, patriotism aside, the greater part of the investigations is going to continue to be carried out on Brazilian soil. Generally speaking, the researchers’ efforts aim at expanding the basic knowledge of the hidden enemy that puts in risk the vigor of the orange groves – always with the prospect of supplying some element that may be useful in controlling the disease.

The first question to which an answer is sought: what causes citrus sudden death? “Bacteria, fungi, nematoids, viroids (tiny pathogens devoid of genes) and phytoplasms have already been excluded”, Machado explains. “That leaves the viruses.” To be more precise, the hypothesis left over is that the causal agent of this sort of heart attack in the orange trees is a mutation (or a new introduction) of the citrus tristeza virus.

In the 40’s, tristeza killed nine of the 11 million orange trees that there were in the state of São Paulo. The disease only failed to raze completely the modest São Paulo citriculture of those days, which was then 20 times smaller than it is now, because it was noticed that one kind of rootstock, the Rangpur lime, was very resistant to the action of the pathogen. In those days, the citrus groves were grafted on the rootstock of the so-called bitter orange (Citrus aurantium). The discovery that the Rangpur lime rootstock – rustic, productive and adapted to dry climates – was resistant to tristeza ended up being the salvation of the groves. But, as far as everything indicates, what in the past served as the basis for citriculture to escape tristeza and grow in such a noteworthy way has become its Achilles heel in facing CSD.

The new disease only attacks orange trees grafted onto Rangpur lime rootstock, the one most used. There is yet another complicating factor in the fight against citriculture’s new hidden enemy. At the moment, the disease, whose unknown causal agent seems to remain incubated during at least two years in the infected plants, is only discovered when the orange trees start showing the symptoms of sudden death. In other words, the diagnosis of the disease is always late, which diminishes the chances of combating the ailment. This limitation may, though, have its days numbered. A Brazilian biotechnology company founded in March 2002, Alellyx, hopes to launch in a year at the most a DNA test capable of making an early diagnosis of the disease.

Researchers from the young private company – which is linked to the Votorantim group, which also controls a concentrated orange juice company, Citrovita – have sequenced the genome of hundreds of strains of the tristeza virus taken from healthy trees that do not show any symptoms of sudden death, and from diseased plants, and they believe that they have identified the mutation that could be responsible for the new disease. “We are patenting these sequences”, says Fernando Reinach, the interim president of Alellyx, which is investing some R$ 3 million in studies into sudden death. Healthy trees were inoculated with the mutation of the tristeza virus that is a candidate for being the pathological agent of the disease, but it is still very soon to know if these plants are going to develop the symptoms of the ailment. Another of Alellyx’s objectives is to create a vaccine or treatment to prevent or cure the new citrus malady.

Mutant virus
With his team at the biotechnology laboratory in the Sylvio Moreira Citrus Center, Machado is coordinating another group of scientists that is also seeking to isolate the pathogen that brings on sudden death. Amongst other hypotheses, the researcher is working with the possibility that sudden death is unleashed by an altered form of the tristeza virus. “But the fact of finding mutations of this virus in plants with sudden death does not necessarily mean to say that this pathogen is the causing agent of the malady”, the researcher explains.

This is because all orange trees, even the healthy ones, show a “soup” of mutant tristeza viruses that has become endemic in the country. This “soup”, which may contain from three to five different breeds of the virus, only fails to cause tristeza in today’s citrus because the rootstocks of these plants are more tolerant to the action of this pathogen. But some varieties of citrus, such as the Sweet Pera orange, are even today susceptible to the tristeza virus. For this reason, in this variety, a vaccine against the disease is applied. Finding mutations of the tristeza virus in orange trees is therefore common and expected. “What is difficult is to find which of the mutations leads to sudden death”, Machado ponders.

Tip for producers
While researchers are trying to discover CSD’s causal agent and to conceive lasting and effective strategies for combating the disease, Fundecitrus recommends, immediately, that producers with trees affected by the new malady resort to sub-grafts. That is, to put rootstocks known to be tolerant to sudden death, like the Volkamer lemon and the Sunki and Cleopatra mandarin tangerines, into the groves affected by the ailment. These extra rootstocks act as a sort of bypass graft. When the vessels of the original rootstock clog up and make it unserviceable, the new rootstocks take on the role of the degenerated tissue. “Carrying out subgrafting rapidly, it seems that it is possible to save trees with sudden death”, says Pedro Takao Yamamoto, from Fundecitrus. The promising, still preliminary, result was obtained from the first trees that were given a bypass graft.

Another tip for producers who want to escape from sudden death is not to by cuttings from areas affected by the disease. Talking of which, the State of São Paulo has prohibited the transport and marketing of citrus cuttings produced in the open air, which are very vulnerable to illnesses transmitted by aerial vectors. Now, only certified cuttings can be sold, produced in tile-covered nurseries. Some of the most serious citrus diseases, like the yellowing disease, the pathological agent of which, the X. fastidiosa bacterium, is carried by a sharpshooter, are propagated by means of insects. This must also be the case of sudden death. The suspicion is that the lice that transmit the tristeza virus may also be vectors of the new disease.