Despite its global dominance, the common potato suffers tremendous losses due to disease - losses that translate into billions of dollars in wasted resources and lost sales both in the US and abroad every year.
Among potato's most persistent pathogens is the late blight causing, Phytophthora infestans, a fungus-like oomycete related to brown algae. P. infestans originated as a local pest of wild potato and tomato relatives in the Toluca Valley of central Mexico. Perhaps best known for its role in the Irish Potato Famine of the mid-nineteenth century, P. infestans continues to be one of the most devastating of all plant pathogens. It infects all parts of potato and spreads quickly - it can completely destroy a healthy field in just one week. This spread is enhanced by the fact that potato is generally propagated by tuber cuttings (lateral buds) rather than by seed, allowing pathogens like P. infestans to be easily transmitted from one crop generation to the next.
For years, pesticides have been used to combat P. infestans - a practice that pollutes the soil, ground water and surrounding ecosystems, and is often ineffective, as P. infestans evolves rapidly and often emerges resistant to commercially available pesticides.
Potato has several insect, virus, and worm pathogens as well. The Colorado Potato Beetle (commonly called the potato bug) feeds on the leaves of plants and is extremely destructive.
Another insect, the potato leafhopper, interferes with the normal physiology of the plant. Its salivary secretions cause leaf-cell hypertrophy that impairs transport of sugars. The resulting sugar accumulation in the leaves destroys chlorophyll and causes the leaves to turn brown and die. This injury, termed hopper burn, can result in the complete loss of a potato crop if not controlled.
The witches' broom virus causes the infected plant to produce numerous buds on the above-ground stems of the potato plants. Long, slender stolons resembling aerial roots that are covered with hairs develop from these buds.
The Columbia root-knot nematode, Meloidogyne chitwoodi, is another serious pest of potato, concentrated mostly in the Pacific Northwest and in Holland. Newly hatched nematode juveniles penetrate tubers causing the formation of blackened sectors and hypertrophy of flesh resulting in galls on the tuber surface. Presently, M. chitwoodi is controlled by the severe method of soil fumigation. This practice presents a formidable cost to potato growers and creates a large toxic burden for the soil and groundwater.
Disease resistance analysis may lead to viable alternatives to pesticide use and soil fumigation, offering growers more economically feasible and ecologically sound growing practices. While S. tuberosum, the species to which commercial potato cultivars belong, is highly susceptible to disease, there are several wild potato species that resist not only P. infestans and M. chitwoodia, but a number of other pathogens as well. These species bear a diverse set of resistance traits that are clustered in particular genomic regions--resistance "hot spots". Evidence suggests that if introduced, these traits could easily function in common potato cultivars.
Phytophthora infestans
Phytophthora infestans belongs to the Oomycetes, a group of organisms causing many plant diseases. Surprisingly, recent data resulting from the use of biochemical and molecular techniques, unambiguously illustrated the large evolutionary distance between the Oomycetes and the true fungi. Because Oomycetes differ from the true fungi by numerous biochemical characteristics, it will be of interest to compare R genes for P. infestans to those for true fungal pathogens.
P. infestans is best known as a pathogen of potato, Solanum tuberosum. However, P. infestans is also a major pathogen of tomatoes ( Lycopersicon esculentum ) and of pear melon ( Solanum muricatum , a cultivated host in the Andes Mountains). Additionally, P. infestans is a pathogen of many tuber-bearing wild species of Solanum. Up to 20 such species have primary or secondary centers of diversity in the central highlands of Mexico, where this host/parasite system probably evolved. Interestingly, S. tuberosum probably evolved from Andean progenitors. It seems highly probable that late blight on "Irish" potatoes is less than two centuries old.
On potatoes and tomatoes, P. infestans is a hemi-biotrophic pathogen. For the first 24 hrs after initial penetration (by either a germinating zoospore or a directly-germinating sporangium), susceptible host cells have little detectable response. From 24-48 hrs, some of the earliest affected cells become necrotic. After 48 hrs (longer in more resistant hosts), the lesion can consist of necrotic cells in the center, surrounded by apparently healthy tissue in which the pathogen is growin - hence the hemi-biotrophic designation. Necrosis is characteristic of the later stages of pathogenicity in most hosts.
Resistance to Late Blight
Two types of resistance to late blight have been described and used in potato breeding. One kind, "gene-for-gene" resistance, is conferred by a series of dominant resistance genes that render the host resistant to specific races of the pathogen. Eleven such R genes have been identified and have originated in Solanum demissum, a hexaploid native to Mexico. A second type of resistance, which is quantitative in nature and race non-specific (Quantitative Trait Loci, QTL), is thought to be much more durable. This resistance has been reported in several different species of Solanum.
Several late blight R genes have been mapped. R1 has been located on chromosome 5, R2, on chromosome 4 and R3, R6, and R7 on chromosome 11. Two additional late blight R genes in tomato have been localized. Ph-1 on chromosome 7 and Ph-2 is on the long arm of chromosome 10, which is highly co-linear with the potato map.
Data are emerging that suggest that QTLs for resistance traits may often cluster near known resistance genes. For example, the R1 locus on chromosome 5 is flanked by the two RFLP markers, GP21 and GP179. This region also harbors a major QTL conferring non-race-specific field resistance to P. infestans. Furthermore, the region harbors a major QTL conferring resistance to the potato cyst nematode Globodera rostochiensis line Ro5-22 and to the G. pallida population Pa2-D383, as well as partial resistance to the G. pallida population Pa3-Rookmaker. In addition, the region contains the Gpa hypersensitive resistance gene to G. pallida, the Potato Virus X extreme resistance gene Rx2 and the hypersensitive resistance gene Nb. The region also contains genes for resistance to insects.
The quantitative and race non-specific resistance has been termed "partial" or "field" resistance. Because this resistance is much smaller in magnitude than R gene resistance, detection has been difficult. The general phenotype is to slow the progress of an epidemic. This is accomplished by slowing pathogen development (expressed in different stages of the disease cycle). The contributing plant components are detectable statistically through QTL analysis. Some QTLs have been mapped in analyses of progeny from different inter-specific crosses. 11 QTLs on nine chromosomes for late blight resistance assessed through a leaf disc assay identified a multi-allelic locus for late blight resistance in tetraploid potato. This locus was at the proximal end of chromosome 8, in the same region to which a single resistance gene analogue had been mapped. QTLs for "field" resistance have also mapped in backcross progeny involving S. tuberosum and S. berthaultii, using a "field" bioassay (individual epidemics in small plots of potatoes - a technique demonstrated to be reliable and reproducible and reflective of the phenotype sought.
A new and important broad-spectrum resistance to the devastating late blight disease has been described and the gene specifying this broad-spectrum resistance has been recently isolated by John Helgeson and Jiming Jiang and their colleagues. This is an important finding because RB is the only resistance gene to encode effective broad-spectrum resistance to all P. infestans strains tested.
R-gene mediated resistance and signaling networks
All plants have evolved several different types of defense and resistance mechanisms that provide protection against pathogen-induced disease including preformed physical and chemical barriers, non-host resistance, basal defense and gene-for-gene resistance (Dangl and Jones, 2001).
In the last decade, rapid progress towards the identification of pathogen and host gene products that determine the outcome of these encounters has occurred, particularly for the latter two categories of resistance responses. As a consequence, more than 30 host R genes, and 30 pathogen avirulence (Avr) genes have been characterized.
Five classes of plant R genes have been proposed based on structural features, four of which contain leucine-rich repeats (LRR), which are considered the most important determinant of specificity based on mutational analyses and evolutionary studies. R protein-mediated recognition results in induction of common defense responses and suggests that fundamental signaling mechanisms may underlie R gene-mediated pathogen resistance.
Defense responses include host cell death, termed the hypersensitive response (HR), an oxidative burst, inhibition of pathogen spread, and systemic plant signaling for heightened defense against secondary pathogen infection, termed systemic acquired resistance (SAR).
Genetic dissection of R gene signaling has helped identify resistance pathway components (Dangl and Jones, 2001). However a complete picture of the genes required for disease resistance is lacking. Therefore, a more comprehensive genetic approach for dissection of disease resistance is needed.
J.L. Dangl, J.D. Jones, Nature 411, 826-33. (2001).
