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Nature 406, 140-141 (13 July 2000) | doi:10.1038/35018202

Plant pathology: The bugs from Brazil

Michael Bevan

The list of organisms whose genomes have been sequenced is growing fast. The latest addition comes from a Brazilian consortium: the organism concerned is Xylella fastidiosa, a bacterium that attacks citrus trees.

Agricultural crops are under constant threat from disease and the vagaries of climate, and in many areas of the world much human suffering stems from crop failure. Couple these factors with the demands of expected increases in human population, the continued encroachment on virgin and marginal land for agriculture, and decreasing water quality, and it is plain that food producers have a considerable challenge on their hands.

Genome sequencing is a potent new tool in the biologist's armoury, and it is being applied to a wide variety of organisms that directly or indirectly affect food supplies. A striking and welcome example of the approach comes on page 151 of this issue1, where a Brazilian sequencing consortium report the first public sequence of a free-living plant pathogen. The organism concerned is the bacterium Xylella fastidiosa (Fig. 1), the cause of citrus variegated chlorosis, a serious disease of citrus fruit. Certain strains of X. fastidiosa also affect other commercially important produce such as coffee, nuts and other fruits2.

Figure 1: Xylella fastidiosa, a bacterium that causes severe damage to citrus trees and the citrus industry.
Figure 1 : Xylella fastidiosa, a bacterium that causes severe damage to
citrus trees and the citrus industry. Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, or to obtain a text description, please contact npg@nature.com

Its genome sequence, now published1, shows it to be highly adapted to life in a plant's water-conducting system.

High resolution image and legend (62K)

The X. fastidiosa genome sequence is one of 24 complete bacterial genomes now available3. Each reveals a gene complement and organization that reflects in marvellous detail the specific adaptations and lifestyles of the organism concerned.

The X. fastidiosa bacterium is highly specialized. It multiplies in the foregut of sharpshooter leafhoppers, which feed on sap in a plant's xylem, the main water-conducting tissue. The insect carrier delivers bacteria directly into the xylem system of host plants. There they multiply and cause symptoms of chlorosis — cholorophyll loss and yellowing — and the premature production of fruit which are small, tough and therefore worthless. The disease is potentially devastating; the most effective control is to produce healthy bacteria-free material for plant propagation. Brazil produces around one-third of the world's orange fruit, and nearly half of the orange-juice concentrate. So the citrus and other fresh-fruit industries are of great national significance, and research into disease control has a high priority.

The gene complement of X. fastidiosa reflects its life in plant xylem in three main ways. First, the bacterium is adapted to use a variety of free sugars found in xylem sap, and to supplement these sugars with glucose derived from the breakdown of cellulose, the main component of plant cell walls. Adding to the picture of a honed-down metabolism, genes encoding the enzymes needed to make sugars from amino acids and other metabolites are missing; this shows that the organism has a strict requirement for carbohydrates as the sole energy provider and source of building blocks for all biosynthetic reactions.

Second, no fewer than 67 genes are devoted to the uptake of iron and other transition metals from xylem sap, and the authors suggest that depletion of these micronutri- ents contributes to symptoms of infection. Third, X. fastidiosa produces two distinct cell- adhesion systems. One comprises a matrix of extracellular polysaccharides, synthesized by the appropriately named gum genes, that embed the bacteria in a matrix in the xylem, eventually leading to blockage of xylem flow and host water-stress. The other system is for bacterial adhesion to the gut and mouthparts of the insect vector, and is specified by 26 genes encoding the so-called fimbral proteins that are needed for bacterial adhesion and translocation across cell surfaces.

The consortium1 also identified genes encoding other molecules involved in cell adhesion that were previously associated only with human and animal pathogens. This is further evidence that disease-causing bacteria of humans and plants have common mechanisms of pathogenicity4.

One of the barriers to breeding and engineering plant resistance to X. fastidiosa is a comparative lack of knowledge of its interplay with its citrus hosts. Usually, host– pathogen specificity is conferred by interactions between avirulence factors encoded by the pathogen and host resistance factors. Suprisingly, however, X. fastidiosa lacks recognizable avirulence genes and the secretion system that injects them directly into host cells. The authors1 suspect that the direct injection of bacteria into host cells by the insect carrier bypasses avirulence gene function, and that the host ranges of X. fastidiosa are defined by other molecules. Exploring this aspect of the bacterium's biology will provide new perspectives on host–pathogen interactions, with the ultimate general goal of developing tolerance and resistance in crop plants.

The impending completion of several other bacterial and fungal plant-pathogen sequences, and the initiation of genome sequencing of Rhizobium meliloti (the nitrogen-fixing symbiont of legumes), adds further to the exciting possibilities in agricultural genomics. Moreover, the near-completion of the sequence of the favoured model plant Arabidopsis and the start of rice genome sequencing, along with farm-animal genome projects that draw strongly on mouse and human genome sequencing, are establishing a solid foundation for research. This is research with eminently practical ends: tackling current or imminent problems in food production, human nutrition and environmental degradation. For example, disease-resistant crops, and plants better adapted to grow in extreme conditions, are nearly ready for large-scale use.

Finally, to return to South America, this first implementation of large-scale sequencing in Brazil is only a harbinger of things to come. The same consortium is now sequencing another plant pathogen, Xanthomonas citri. This is the cause of citrus canker, a worldwide disease that can severely damage citrus crops unless strict quarantine zones are enforced. The citrus industry in Florida is currently under threat from X. citri spread by a tornado in 1996 (ref. 5). The successful sequencing of X. fastidiosa also shows that genome projects are a highly effective tool for science policy. Such projects provide a strong direction to and framework for biological investigations; they direct disparate areas of biology towards common themes; and they result in the distribution of the latest technologies to many laboratories, allowing scientific talent to flourish more widely.

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References

  1. Simpson, A. et al. Nature 406, 151–157 (2000). | Article | PubMed | ISI | ChemPort |
  2. Machado, M. A. http://www.dcc.unicamp.br/genoma/xylella.html (1997 ).
  3. Genomes OnLine Database http://wit.integratedgenomics.com/GOLD/
  4. Rahme, L. G. et al. Science 268, 1899– 1902 (1995). | PubMed | ISI | ChemPort |
  5. Gabriel, D. W. http://www.biotech.ufl.edu/~pcfcl (2000).

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