G. A. Forbes J. A. Landeo




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Chapter 8

Late Blight

G. A. Forbes

J. A. Landeo

Late blight (Phytophthora infestans [Mont.] de Bary) is the most devastating disease of potato worldwide. CAB International (Anonymous, 2003) currently lists 122 countries where late blight has been reported, but it certainly occurs in more countries for which no report has been made. The economic and social impact of this disease was best experienced during the Irish famine in the 1840s when millions of Irish people either died or emigrated (Bourke, 1993) due to starvation caused by killing of potato crop by P. infestans. At present, about $77 million are spent only on fungicides per season throughout the United States for control of this disease (Guenther et al., 2001). Yearly fungicide usage for late blight control in Europe is estimated to be about $150 million (H. Schepers, personal communication). International Potato Center (CIP) estimated fungicide use in developing countries at $750 million (Anonymous, 1997). Based on these estimates, about $1 billion per year is spent on the fungicides to control late blight in the United States, Europe, and developing countries. These huge social and economic consequences of late blight have attracted considerable attention of the research workers. This chapter reviews the current state of knowledge and advances made in understanding and controlling this most dreaded malady of potatoes.



Causal Agent

Morphology

Phytophthora infestans (Mont) De Bary—the causal agent of potato late blight is a coenocytic oomycete, which produces ellipsoid to lemon shaped sporangia with a small pedicel. Sporangium length ranges between 29 and 36 µm and width between 19 and 22 µm. Zoospores (ca. 7-12 per sporangium) have two flagella, one tinsel type that is directed forward and a second whiplash type that is directed backward. Zoospores are usually uninucleate, but binucleate zoospores have also been detected.

The pathogen is hetrothallic and requires two mating types namely A1 and A2 for sexual reproduction. In culture the mycelium is white and the colony is somewhat slow growing. Growth rates can vary dramatically among isolates, but fast growing isolates can cover a 9 cm plate within about one week. Some isolates grow irregularly, producing a lumpy appearance in agar, which has sometimes been associated with A2 mating type. P hytophthora infestans can grow on a variety of culture media, but not all isolates will grow on all media. Commonly used media are rye agar, V-8 juice agar, pea agar, cornmeal agar, corn seed agar, and lima bean agar. Recipes for many media have been presented by Erwin and Ribeiro (1996).



Taxonomy

The genus Phytophthora, its closely related genus Pythium, and the downy mildews (i.e., Bremia, Sclerospora, Plasmopara, Peronspora, etc.) belong to the oomycetes, which are unrelated to true fungi, such as ascomycetes and basidiomycetes. Oomycetes are stramenopiles, a group that includes golden and brown algae and that are characterized by zoospores propelled by heterokont flagella (of unequal length). Nuclei in vegetative cells are generally diploid even though polyploidy has been detected (Tooley and Therrien, 1991). Sexual reproduction occurs via oospores that develop from the joining of oogonia and antheridia. Oomycetes have cellulose in their cell walls. Erwin and Ribeiro (1996) discussed the changes in the understanding of taxonomic position of this group of organisms. Many pathologists now consider the following as the correct taxonomic classification of P. infestans:



Phytophthora infestans (Mont.) de Bary—Kingdom Chromista, Phylum Oomycota, Order Peronosporales, Family Peronosporaceae, Genus Phytophthora, of which it is the type species (Birch and Whisson, 2001).

Origin and Spread

P. infestans is thought by most researchers to have originated in the highlands of central Mexico (Grünwald et al., 2001) because both mating types (A1 and A2) were present when the disease was discovered in that location and there is a high genetic diversity for the pathogen in this region (Goodwin and Drenth, 1997; Grünwald et al., 2001). In contrast, only the A1 mating type and low genetic diversity had been found outside Mexico until the mid-1980s (Hohl and Iselin, 1984; Goodwin et al., 1992). An alternative hypothesis proposed the Andes, center of origin of the cultivated potato, as the center of origin for P. infestans (Abad and Abad, 1997). This hypothesis is based primarily on historical accounts of potato diseases in the Andes, but appears to have no support from the scientific literature.

Until recently, most isolates of P. infestans found outside North America belonged to the US-1 clonal lineage. This led to a hypothesis that US-1 had caused the original epidemics in Europe in the 1800s (Goodwin et al., 1994) and then spread globally, presumably with seed trade (Fry et al., 1993). Originally researchers proposed that US-1 had spread from Mexico to the United States and then from the United States to Europe (Goodwin et al., 1994). Alternatively, some researchers proposed that US-1 was introduced into Europe directly from South America (Andrivon, 1996). However, recent analyses of mitochondrial DNA of P. infestans in herbarium material presented evidence that a genotype different from US-1 was involved in the original epidemics in Europe (Ristaino et al., 2001). During the 1980s, the A2 mating type of P. infestans was detected in Europe (Hohl and Iselin, 1984) along with several new alleles for known markers. Global migration of new races of P. infestans has taken place and their status in selected regions is presented in Table 8.1. The pathogen population in Europe is now highly diverse and there is evidence for sexual reproduction in several European countries (Drenth, 1994; Andersson et al., 1998; Flier, kessel et al., 2002).



Hosts

Erwin and Ribeiro (1996) list 89 host species of P. infestans, but more than 25 percent of these were based only on artificial inoculations. Some of the hosts mentioned have only been reported once and others may have been attacked by morphologically similar species of Phythophthora, which have been identified only recently. Species of both Ipomea and Mirabilis are listed as hosts by Erwin and Ribeiro (1996), but disease on these may have been caused by P. ipomeae (Flier, Grünwald et al., 2002) and P. mirabilis (Goodwin et al., 1999), respectively.

Of the nontuber-bearing Solanum hosts, tomato, S. lycopersicum, is the most important economically. Other domesticated Solanum species are also hosts of P. infestans, including pepino (S. muricatum), tree tomato (S. betaceum) (Oliva et al., 2002), and naranjilla (S. quitoense) (Unpublished data). Eggplant has also been reported as an occasional host of P. infestans (Hooker, 1981), but lack of disease reports in this very cosmopolitan crop puts its host status in doubt. P. infestans is undoubtedly also a pathogen of the wild Solanum species closely related to tomato (Abad et al., 1995), but there are few reports on these. A recent study in South America listed 6 wild nontuber-bearing Solanum species and one species complex attacked in nature by P. infestans. However, some isolates of the pathogen associated with certain hosts are so unusual that they may actually be new species of Phytophthora (Adler et al., 2004). A study in Canada showed that the nightshades, S. dulcamara and S. sarrachoides were infected while black nightshade, S. nigrum, was not (Platt, 1999). In Europe, natural infections were found on S. nigrum, S. dulcamara, and S. sisymbriifolium (Flier et al., 2003b). One study in California showed that 11 Solanum species got infected by inoculation in a greenhouse, however, only one of these, S. sarrachodes, was found naturally infected in the field (Vartanian and Endo, 1985).

There have also been references to infection in Solanaceous plants outside the genus Solanum. Nolana species are apparently attacked on the coast of Peru during the wet winter season (Turkensteen, 1978; Abad et al., 1995). Datura species have been reported as hosts of P. infestans (Sunita and Sen, 1997), but it is not clear if infections occur naturally in the field. Extensive sampling in Ecuador, where Datura spp. are common weeds has not produced any indication that this genus is a host (Adler et al., 2004). Brugmansia anguinea is also attacked by P. infestans in South America, but lesions have only been found on flower petals (Adler et al., 2004). P. infestans also attacks Petunia (Platt, 1999).

Several species from Africa have been cited as hosts of P. infestans. Kori (1972) reported that S. indicum, S. incanum, and S. aculosturm were all infected in the field. Natural infection in S. incanum and S. indicum were confirmed by Nattrass and Ryan (1951) as well as infection in one unidentified species of Solanum. A cultivated crop, garden huckleberry (S. scabrum) was reported as a host of P. infestans in Cameroon (Nkengaka, 2000).

Disease Symptoms

The disease appears first as water-soaked irregular pale-green lesions mostly near tips and margins of leaves. These lesions rapidly grow into large brown to purplish black necrotic spots. During morning hours a white mildew, which consists of sporangia and spores of the pathogen, can be seen on lower surface of infected leaves especially around the edges of the necrotic lesions (Figure 8.1A). The symptoms thus can vary depending on the age of lesion and the environmental conditions prior to observation and the tissue infected. Very young lesions are small (2-10 mm) and irregularly shaped, and may be surrounded by a small halo (collapsed, but green tissue bordering the dark necrotic lesion). As lesions grow they become more circular until they are limited by the leaflet margins. They are usually not delimited by the veins and older lesions are typically surrounded by a chlorotic hallow.

When late blight attacks the stem it can cause girdling and the leaves wilt above the point of infection. Light to dark brown lesions on stems or petioles elongate and encircle the stems (Figure 8.1B). Stem lesions become brittle and the stem frequently breaks at that point. Rain-borne sporangia from the diseased foliage can also infect tubers in the soil. The infected tubers show irregular reddish brown to purplish slightly depressed areas that extend deep into internal tissue of the tubers (Figure 8.1C). The infected tubers are initially hard, dry, and firm but may be invaded by other pathogens, mainly bacteria, leading to soft rot. A pungent putrid smell is often associated with heavily infected fields. This is due to rotting of dead tissue and is not a direct consequence of late blight.

Late blight lesions can be mistaken for several other diseases. Under especially wet conditions, Botrytis cinerea can cause rot of lower leaves of potato plants in such a manner that they resemble late blight lesions, however sporulation from B. cinerea is gray (see Figure 9.1 Chapter 9). When conditions become quite dry and late blight lesions dry out, they can be mistaken for dried lesions caused by B. cinerea or sometimes by lesions caused by Alternaria solani (early blight). However, early blight lesions are typically zonate with a definite outer margin, whereas active late blight lesions are surely not zonate and typically without a definite outer margin. Certain types of frost damage as it occurs in the highland tropics can resemble late blight.



Epidemiology and Disease Cycle

The occurrence of late blight varies spatially and temporally depending on inoculum sources and weather. P. infestans survives on tubers in storage, or within soil or a refuse pile. The two most important sources of initial infection in the temperate zone are refuse piles (Zwankhuizen et al., 1998) and infected seed (van der Zaag, 1956; Marshall and Stevenson, 1996). It is not clear which of these is more important. However, seed tubers play an important role in the long-distance dispersal of P. infestans (Fry et al., 1993).

In most temperate zones, P. infestans generally reproduces asexually, which means there are no overwintering spores. New epidemics each year must start from the abovementioned inoculum sources. In subtropical and highland tropical areas, potatoes are produced round the year and the pathogen is always present, hence the disease is also always present, even though often limited to only humid microenvironments. For this reason, late blight generally occurs in the tropics as soon as the rains begin.

Most potato growers know the general conditions that favor late blight development. Within months of the appearance of late blight in Ireland in 1845, David Moore, curator of the Royal Dublin Society’s Botanic Gardens, (cited in Nelson, 1995) wrote that “damp is conducive to the progress of the disease … dryness retards it.” The disease has been associated historically with “cool wet weather,” but optimum temperatures are probably near 20C (Harrison, 1992), although the disease can occur over a range from about 5C to 30C.

A number of authors have reviewed the effects of the external environment on one or more aspects of the biology of P. infestans (Harrison, 1992; Mizubuti et al., 2000). The principal factor determining sporangial germination appears to be temperature, although the exact effect of temperature probably depends on the pathogen’s genotype being evaluated. Regardless, 15C appears to be a point of differentiation, below which germination is indirect, and above which it is direct. Interestingly, germination and zoospore activity can occur at very low temperatures, near 0C, although at a very slow rate. Above 30C, sporangia do not germinate (Crosier, 1933). Most phases of P. infestans cannot survive temperatures above 30C (Harrison, 1992), but the pathogen is more robust when it is inside plant tissue and has survived temperatures of 40C in stem tissue (Kable and Mackenzie, 1980).

Similarly, the effect of humidity on the pathogen development, and subsequent disease, is complex. Generally, saturated air or leaf wetness is required for sporangia to germinate and for zoospore motility (Harrison, 1992). After infection has occurred, the mycelium is relatively protected from low humidity, but high ambient humidity, near saturation, is needed for sporangia formation (Harrison, 1992).



There is inconsistency in the literature relating to sporangial sensitivity to drying. Most studies found that once dried, sporangia were no longer viable (Warren and Colhoun, 1975). However, Minogue and Fry (1981) showed that sporangia could gain viablilty after drying if rehydrated gradually. Because of the putative sensitivity of sporangia to drying, early workers considered rain splashing as one of the primary dispersal modes for this pathogen (Hirst, 1958). More recent studies indicate that sporangia are dispersed in air and are generally released during the day when relative humidity is lower (Aylor et al., 2001). Because of this wind-borne mode of dispersal, the sensitivity of sporangia to ultraviolet light is an important issue. Under high light conditions, most sporangia are killed within 1 h, but sporangia can last for very long periods on cloudy days (Mizubuti et al., 2000). Long-distance wind dispersal can virtually be inferred by the extremely rapid rate of overland and oversea movement detected when P. infestans was introduced to Europe in 1845 (Bourke, 1991). Factors other than temperature and humidity are also known to affect sporangia germination, for example, pH and osmotic potential of water.

P. infestans has a complex pre-infection process involving sporangial germination, zoospore movement, encystment, cyst germination, germ tube development, appresorium formation and penetration. These steps may be further divided into substeps. For example, penetration may involve both physical pressure from the infection peg, as well as enzymatic activity. Sporangia of P. infestans germinate either directly with a germ tube or indirectly by liberating zoospores. Germ tubes can also form secondary sporangia, which may serve to increase the longevity of the spore (Harrison, 1992). Germ tubes can penetrate most leaf epidermal cells, but various authors have detected that infection on the leaf surface is not random and that successful infections more readily occur near the stomatal complexes (Coffey and Gees, 1991). Germ tubes do not penetrate host tissue directly, but rather via formation of an appresorium and subsequently an infection peg. After penetration, the pathogen forms a specialized hyphal structure, sometimes referred to as an infection vessel. Hyphae extend from this and begin colonization of plant tissue intercellularly. Intercellular hyphae form haustoria that penetrate cells to absorb nutrients (Hohl and Suter, 1976). After a certain amount of time, sporangiophores grow out of stomatal openings (Figure 8.2).

Lesions become visible within a few days, the time taken depends on temperature, and the genetics of the host and pathogen. Under optimal conditions (18-22C), and with a susceptible potato cultivar, infections can be visible in less than three days. Within a day or two after the lesion first becomes visible, the pathogen is capable of sporulation. Moderate temperatures (10-25C) and wet conditions (100 percent RH) are required for sporulation. Within 8-12 h of favorable conditions sporangia are borne on indeterminate sporangiophores. Sporangia dislodge during changing relative humidity and can be captured in air currents or splash dispersed. As sporangia can survive for hours in unsaturated atmospheres when protected from solar radiation (Mizubuti et al., 2000), dispersal to hundreds of kilometers are possible. Under favorable conditions, large numbers of sporangia can be produced from a single lesion (more than 100,000 sporangia/lesion).

When individuals of opposite mating type (A1 and A2) colonize the same substrate (plant tissue or agar), sexual structures (antheridia and oogonia) are produced by each thallus and meiosis occurs in the gametes. After fertilization, the oogonium develops into an oospore, which can survive adverse conditions better than other forms of the pathogen. After a period of dormancy (weeks or months) oospores become capable of germination. Germination in the lab occurs in water or 1.5 percent agar at 18C in the presence of blue light. It is clear that oospores can survive winter in temperate zones (Turkensteen et al., 2000), but the conditions stimulating germination are not yet precisely known. Oospores germinate via a germ sporangium. This sporangium may then either liberate zoospores or may germinate directly giving out a germ tube.

The problem of tuber blight predates the relatively recent international spread of oospores and is thought to develop from sporangia and zoospores coming from foliage infection. There appears to be little evidence that oospores present in the soil are significant sources of tuber infection (Flier, Kessel et al., 2002). Infection in tubers generally occurs at eyes, lenticels, or through wounds (Adams, 1975). Most researchers agree that sporangia wash down through soil and infect tubers directly or indirectly via zoospores (Andrivon, 1995). There appear to be few studies on sporangial transport in soils, but one study done in a sandy loam demonstrated that 0.6 cm of water could carry sporangia to a depth of 40 cm (Dubey and Stevenson, 1996). Lacey (1967) demonstrated the important role of channels within the soil and especially those formed by the stem. He found more infection near the stolon end of the tubers and attributed this to water running down the stem. Studies (Dubey and Stevenson, 1996) indicate that sporangia arrive to the vicinity of tubers through various means in the soil and do not necessarily require channels. These researchers found that mulching, high hilling, and chemical treatment of soil could reduce but did not eliminate tuber infection when foliage infection was present.



Disease Management

Cultural

Eliminating the sources of initial inoculum is the first step in the control of any disease. So, use of healthy seed and destruction of infected foliage prior to harvest may help in reducing the incidence of late blight in the next season. Tubers left in the ground sprout leading to an early emergence of the volunteer plants that may become infected very early. Lesions on these plants sporulate and can cause disease in potato crop. Removal or destruction of volunteer plants is a common component of most late blight management strategies. Alternative hosts are other potential sources of initial infection (Flier et al., 2003b). However, alternative hosts frequently have specialized pathogen populations and therefore may not always be involved in potato disease development (Oyarzún et al., 1998).

Areas that remain wet because of excess soil moisture or heavy shading are potential hot spots for late blight. Planting potato crop only in sunny and well-drained fields can thus reduce the incidence of late blight. High hilling has been associated with reduced foliage severity (Boyd, 1980). This is probably due to improved drainage and better aeration, which dries foliage quickly. Hilling also reduces tuber blight by increasing the barrier between tubers and spores washing out of foliage. Some traditional techniques in the Andes such as raised beds or a similar technique in Colombia and Ecuador called “Huacho Rozado" (unpublished), have been associated with reduced late blight. Within a given season, the time of greatest late blight can often be avoided by opportune planting (Devaux and Haverkort, 1987). In the highland tropics, a large number of farmers escape the major late blight season by either planting the crop before or after rains. Planting date can reduce the time the plants are exposed to the disease potential. Green sprouting also known as diffused light sprouting, presprouting, or chitting, can create a more uniform crop that can be harvested earlier thereby reducing the period of exposure to late blight.

Data generated on the effects of plant density and plant nutrition on late blight incidence are not consistent. According to Garrett and Dendy (2001), the effect of plant density on potato late blight appears to be minimal. Several authors found that increased doses of phosphorous and potassium reduce late blight (Awan and Struchtemeyer, 1957) whereas nitrogen increases late blight incidence (Carnegie and Colhoun, 1983). Phosphorous and nitrogen apparently have contrasting effects on tuber blight. Nitrogen delays tuber maturation, resulting in more blight whereas phosphorous reduces incidence by accelerating maturation (Herlihy, 1970). A study in the highland tropics (Juarez et al., 2001) demonstrated that fertilization effects on late blight were much smaller than yield effects and therefore farmers would make decisions based on yield.

Acid soils and high aluminum availability in soils, commonly found in the tropics, have been shown to inhibit P. infestans in soil (Andrivon, 1995). Tuber blight incidence is also checked by early removal or destruction of foliage prior to harvest, and harvesting and storing of tubers under dry conditions.

Chemical

The use of chemicals to control late blight began about a century ago. Initially materials such as sodium chloride, lime, and sulfur were used, but these were not very effective (Schwinn and Margot, 1991). The first effective compound was Bordeaux mixture, which was discovered in the 1880s and is made of copper sulfate and lime. Bordeaux mixture was widely used on potatoes until other copper compounds were shown to be more effective in the 1930s. One of these, copper oxychloride is still used for control of blight.



In the 1940s the ethylenebisdithiocarbamates (often referred to as EBDCs), were first introduced into the market. Several of these, zineb, maneb, metiran, mancozeb, and propineb make up the group of fungicides most frequently used against late blight in many parts of the world.

Another important group of fungicides are the tin compounds, such as fentin acetate and fentin hydroxide. These fungicides are effective and last for a long time on foliage. The main disadvantage is that they can be phytotoxic so they should be used on mature plants. Chlorothalonil is another effective protectant fungicide and it has low plant toxicity.

In the 1970s systemic fungicides greatly increased the efficacy of chemical control. The most effective of these are the phenylamides, such as metalaxyl, ofurace, oxadyxil, and benalaxyl. Of these, the most effective is metalaxyl (Schwinn and Margot, 1991). These fungicides have a strong curative effect, that is, they can kill the pathogen even after it is in the plant. The main disadvantage of the phenylamides is that resistance readily develops in the pathogen population. To avoid this problem guidelines have been developed for the use of phenylamide fungicides.

Some more protective and systemic fungicides have been released in the past 20 years that offer growers a much larger array of options (Table 8.2). Many of the protective fungicides have similar levels of effectiveness and durability on the leaf. The best period to use them, therefore, may depend on their levels of phytotoxicity.

The most commonly used means of protecting tubers against infection is by applying fungicides to foliage. In theory, this approach can reduce tuber blight in three ways: (1) reducing sporulation; (2) reducing viability of spores on leaves, and (3) when repeated applications leave residues in the soil, formation or motility of zoospores is inhibited (Schepers and van Soesbergen, 1995). As may be expected, not all fungicides are equally effective in controlling tuber blight via foliar application (Schepers and van Soesbergen, 1995).

Forecasting

One rather old but still active area of research is that of forecasting of disease or decision support systems (DSS) for timing prophylactic fungicidal sprays. Forecasting models were developed as early as the 1940s and numerous models now exist. A description of this research in general chronological order has been made by Fry and Doster (1991).

Forecasting models have also been tested in developing countries (Katsurayama and Boneti, 1996; Gómez et al., 1999; Grünwald et al., 2000; Singh et al., 2000) but there appears to be little evidence that they are being used effectively. This is probably because most of these systems require weather-measuring devices and/or computers, which are not within the economic reach of poor farmers.

Host Resistance

Reports of potato cultivars with resistance to late blight date back to the 1700s, and apparently breeding was an important activity in Ireland during the decades following the famine (Dowley, 1995). A number of cultivars with resistance to late blight were available in Europe by the late 1800s (Umaerus et al., 1983). In 1882, the French Professor Pierre Millardet discovered that a mixture of copper sulfate and lime (later named Bordeaux mixture), used to deter people from stealing grapes, also protected plants from fungal and oomycete pathogens. According to Robinson (1996), this discovery had a profound negative effect on potato breeding for resistance to late blight. Robinson’s hypothesis is supported by the fact that during the Bordeaux mix era, from the 1880s until the First World War, several highly susceptible varieties (e.g., Bintje, Russet Burbank) were developed, which would have been difficult to produce without chemical protection.

Potato genotypes also differ in their resistance to tuber blight (Wastie et al., 1987), but the level of resistance currently available is not sufficient to protect plants from tuber blight. Resistance mechanisms apparently differ for foliage and tuber blight and in parts of Europe the pathogen population varies in its aggressiveness on tubers (Flier et al., 2003a)



Traditional Andean farmers have used high host diversity for centuries, either in the form of cultivar mixtures or by intercropping (Thurston, 1990) to reduce late blight severity. Research to test the effect of host diversity on late blight severity has given surprising results. Cultivar mixtures have consistently reduced blight severity in North America and Europe (Andrivon and Lucas, 1998; Garrett and Mundt, 2000) but the effect is much smaller in the highland tropics (Garrett et al., 2001). This has been attributed to a much higher amount of outside (coming from other fields) inoculum in the highland tropics that tends to cause uniform infection foci throughout the field.

Nature of Host Resistance



Until recently, there was a fairly general consensus that most resistance to P. infestans could be classified into two types. The first governed by single dominant genes with major effects, and a clear discontinuous segregation in progeny; and the second governed by several or many genes, called minor genes, with small cumulative effects and continuous distribution of resistant genotypes. Major gene resistance has also been described as vertical resistance, R-gene resistance, qualitative resistance, specific resistance, race-specific resistance, unstable resistance, and complete resistance. Minor gene resistance has been described with contrasting names, as horizontal resistance, polygenic resistance, quantitative resistance, general resistance, nonrace-specific resistance, stable resistance, partial resistance, field resistance, and rate-reducing resistance. Some reviews discuss terminology used to describe these types of resistance (Thurston, 1971; Umaerus et al., 1983). For consistency, we will use the terms “specific resistance” and “general resistance” in this chapter.

By definition, general resistance was considered effective against all races of the pathogen (Vanderplank, 1984). Some authors, however, proposed an alternative hypothesis for resistance, in which some degree of race specificity exists for all resistance types (Parlevliet and Zadoks, 1977), and pathogen adaptation to plant genotypes with general resistance has been identified for some diseases (Parlevliet, 1989).

Basic research aimed at elucidating the genetic and physiological basis of resistance has not demonstrated clear mechanistic differences between general and specific resistance. Until recently, specific resistance was closely associated with the hypersensitive response (HR), which is a particular type of programmed cell death that enables plants to limit invading pathogens. Several cells near the infection point die rapidly, severely restricting or stopping the infection process. The most commonly accepted model suggests that R genes in the plant trigger HR when they recognize elicitors (signal molecules) coming from the pathogen, which are encoded by avirulence (Avr) genes (Kamoun et al., 1999). It is the specificity between the Avr gene in the pathogen and the R gene in the host that causes the race-specificity of specific resistance. The exact way in which R genes and Avr genes interact is not yet known but different models have been proposed (Dangl and Jones, 2001).



R genes were not traditionally associated with general resistance, and therefore neither was HR. However, histological studies, some done decades ago, have consistently found rapid necrosis occurring during the infection process in plants with general resistance (Gees and Hohl, 1988; Coffey and Gees, 1991; Vleeshouwers et al., 2000b). HR has also been associated with nonhost resistance in potato (Vleeshouwers et al., 2000b). Kamoun et al. (1999) proposed that resistance in all plants against oomycetes might always involve HR. In general resistance, HR occurs somewhat later and allows the pathogen to escape, with HR often trailing behind colonization by the pathogen (Vleeshouwers et al., 2000b). Based on histological observations, Vleeshouwers et al. (2000b) proposed that general resistance is conferred by weak interactions between R genes and Avr genes. Weak R genes producing a phenotype that mimics general resistance had been identified in the past (Landeo and Turkensteen, 1989). At the cellular level, resistance of weak R genes resembles general resistance (Vleeshouwers et al., 2000b).

General resistance in potato is also associated with basal levels of pathogenesis-related (PR) proteins (Vleeshouwers et al., 2000a), as well as with other defense-related genes (Trognitz et al., 2002). Callose formation on cell walls, which may hinder colonization of the plant tissue by the pathogen, was observed in histological studies of resistant cultivars ( Wilson and Coffey, 1980; Gees and Hohl, 1988).

Another area of research that has tended to blur the apparently clear field effects of general and specific resistance is that carried out on residual effects of R genes. Some plant pathologists have hypothesized that “defeated” (no longer effective) R genes have residual effects, that is they contribute additively to general resistance. Putative residual effects were demonstrated for some diseases (Pedersen and Leath, 1988), but not for others (Young et al., 1994). Recently, potato progeny of several crosses were compared in the field in Scotland. On the average, those genotypes with a defeated R gene were slightly more resistant than those without the R gene (Stewart and Bradshaw, 2001). In an evaluation of 882 breeding clones, Darsow et al. (1987) found that the clones that had R genes also had more general resistance. These authors interpreted their data as an indication of linkage between R genes and general resistance. It is difficult to differentiate between a direct effect of defeated R gene and an effect of genes that might be tightly linked to the R gene (Anderson, 1982). In a large population in which an R gene was segregating, there was no relationship between lesion expansion rate, and the presence of the R gene (Ordoñez et al., 1998) when inoculated with a compatible isolate. Similar to the effects of pathogen specificity to general resistance discussed earlier, residual effects, if they exist, are probably small and difficult to measure.

Pathogen's Adaptation to Host Resistance

Studies on pathogen adaptation to host resistance have produced inconclusive results. Pathogen adaptation to general resistance to P. infestans was observed after successive culturing on potato tubers by some authors (Caten, 1974), but in one study host specialization did not occur after 90 cycles of subculturing on tubers (Paxman, 1963). Host specialization was demonstrated for incubation period on detached leaves (Jeffrey et al., 1962) and field studies demonstrated a small hostpathogen interaction for epidemic rate (Latin et al., 1981), but the latter did not prove consistent over years. In field studies carried out by James and Fry (1983), host specialization was not measured. Recently, a series of studies on tuber and foliage infection concluded that plant genotypes carrying different levels of general resistance react differentially against new aggressive genotypes of the pathogen (Flier et al., 2003a). These authors hypothesized that they were able to measure host specificity because the pathogen population they studied involves both asexual and sexual reproduction (Turkensteen et al., 2000). General resistance might be more stable in areas where clonal pathogen populations exist and less stable with sexual populations. However, a recent assessment of historical data of Mexican cultivars grown in Toluca, an area of high pathogen variability resulting from sexual reproduction, demonstrated that the resistance was generally stable (Grünwald et al., 2002).

Inconsistency in studies on host specialization to general resistance may be due to the fact that specialization is partial and difficult to measure (Turkensteen, 1993). The constancy of resistance ratings of potato cultivars over time (Colon et al., 1995; Inglis et al., 1996; Grünwald et al., 2002; Landeo, 2002) probably indicates that the host specificity, to the extent that it occurs, is smaller than the general effects of host resistance.



Breeding

Specific resistance due to single genes (R genes) was first discovered in the wild S. demissum, or the closely related species S. edinese and S. stoloniferum (Black, 1954) from Mexico. The first R genes were transferred from S. demissum to cultivated potato at the beginning of the last century (Wastie, 1991), but they were not really used in breeding programs until the 1920s (Bradshaw et al., 1995). Originally, four R genes were transferred into cultivated potatoes, but subsequently more R genes were discovered. A differential set of potato varieties containing 11 R genes (alone and in combinations) is commonly used to classify races of the pathogen (Perez, Gamboa et al., 2001). However, most breeding for R genes involved only the first four to be discovered, because it soon became evident that the resistance they conferred was not at all durable. Virulent races of the pathogen rapidly appeared to which the cultivars were highly susceptible. The ephemeral nature of R-gene mediated resistance became evident by the 1950s and 1960s (Bradshaw et al., 1995) and researchers recognized the need to emphasize general resistance (Vanderplank, 1956).

Breeding potatoes with general resistance is technically more difficult than breeding for resistance based on a few R genes with large effects. As mentioned earlier, general resistance is quantitatively inherited, which makes the achievement of high levels of resistance a slow process, usually requiring several cycles of recombination. This problem is compounded by the fact that R genes can easily mask, or otherwise interfere with general resistance (Turkensteen, 1993). Thus, screening for general resistance in plant populations in which one or more, large-effect R genes are segregating is particularly tricky.

One way potato breeders overcome this problem is by screening with a highly complex race of the pathogen. This was generally done by culturing large quantities of inoculum and inoculating plants in the field. Robinson (1996) used this technique in Africa and the International Potato Center (CIP) used inoculation with a complex race to screen for resistance in wild potatoes (Perez, Salas et al., 2001). There is a theoretical assumption underlying this practical application of plant pathology that should be considered when interpreting results. Breeders inoculate the populations with complex races to overcome any R genes that actually may have large effects that mask other resistance factors. The efficacy of this approach is based on the compatibility of the race with the parental material used to produce the potato genotypes being screened. Compatibility of a complex pathogen race on the plants used as parents should, in theory, ensure compatibility with all the progeny. This, however, is not always the case because some parental plants can harbor major genes that have been rendered ineffective by modifier genes (El Kharbotly et al., 1996; Ordonez et al., 1997). When these parental plants are crossed, the R gene might become effective by being separated from the modifier gene in the progeny.

Another way that potato breeders have attempted to overcome the problem of major R genes interfering with general resistance is by screening progeny in areas where the naturally occurring pathogen population is variable, at least for specific virulence (the ability to infect plants with different strong R genes). The principal location for this type of screening has historically been near Toluca, Mexico, which is the putative center of origin of the pathogen (Goodwin, 1997). The sexually derived population of P. infestans in Toluca is so variable that several different genotypes are often found within a single field (Flier, Grünwald et al., 2003). The utility of central Mexico as a “hot spot” for resistance screening has been borne out by a large number of resistant cultivars that have been developed fully or in part there (Bradshaw et al., 1992; Robinson, 1996). Because of the very high pathogen diversity in this location it is likely that any potato cultivar grown over a relatively large area will eventually become infected, regardless of the R gene(s) it may carry. How large this area must be for disease to occur would depend on the frequency of compatible isolates in the pathogen population. In small experimental plots, however, potato genotypes sometimes remain immune in Mexico throughout the duration of the season (unpublished data). For this reason, high levels of resistance in Mexico must be interpreted with caution if the plot size is small.

A third technique used to breed for general resistance in potato is the elimination of certain R genes from the host population. Turkensteen (1993) described the theoretical feasibility of this approach for potato and it has been implemented by the CIP (Landeo, 2002) since the early 1990s. This approach was actually implemented by the CIP in two different ways. The first was by using only parents from the putatively R gene-free tetraploid native cultivars from the Andes that are generally classified as Solanum tuberosum ssp. andigena (Landeo et al., 1995). Even though this species is considered free of R genes, selected parents are checked for the presence of strong R genes by greenhouse inoculation. Two inoculations are done separately, one with a highly compatible race of P. infestans and one with a race that does not infect any of the known 11 R-gene differentials. If a potato genotype reacts in a similar fashion to both races, then it is considered free of demissum R genes that react differentially to the avirulence genes in the avirulent isolate.

The dual inoculation method is also used for potato populations in which known R genes with qualitative effects are segregating. By the dual inoculation technique, individual plant genotypes are identified that do not react differentially to the two pathogen isolates. These plant genotypes are referred to as “R gene-free” (Landeo et al., 1995) but in fact they should be considered free of R genes that react to avirulence genes in the avirulent isolate.

Stability of general resistance across different locations is also difficult to study and has only been reported for late blight of potato on a few occasions and over a limited geographical area. Recently, sets of potato genotypes were evaluated at several locations in the United States in two separate studies ( Haynes et al., 1998, 2002). These authors found that the most resistant materials were generally stable but some of the intermediate clones were less stable. In an earlier study, the genotype Alpha was more resistant in New York State than in Toluca, Mexico, compared to three other varieties that behaved similarly at both locations (Parker et al., 1992).

There is anecdotal evidence for and against the geographic stability of general resistance in potato to P. infestans. Several genotypes with appreciable levels of resistance are grown in different continents and generally maintain their resistance (Forbes and Jarvis, 1994). However, other genotypes have gained a reputation for being resistant in one location whereas being susceptible in another. One such genotype is Atzimba, which is thought to have an intermediate level of resistance in Mexico but is considered highly susceptible in Costa Rica. The study on Alpha, mentioned earlier, was inspired by the generalized opinion that this genotype is highly susceptible in Mexico but moderately resistant in upstate New York (W. E. Fry, personal communication). Anecdotal information, however, is extremely difficult to interpret because it seldom involves experimental comparison of two or more plant genotypes in the same region, which would permit an appreciation of a genotype by environment (G × E) interaction.

Molecular biology

The advent of molecular biology has enabled researchers to elucidate many aspects of the host-pathogen relationship, but much uncertainty remains about underlying mechanisms of putatively different resistance types. To date, at least five R genes that confer specific resistance to P. infestans have been located on a potato genetic map (Birch and Whisson, 2001). Several of these R genes are clustered and others are located near defense genes for other pathogens and nematodes (Meksem et al., 1995; de Jong et al., 1997;). Quantitative trait loci (QTL) segregating in several different breeding populations have also been located on the potato map (Ewing et al., 2000; Ghislain et al., 2001). Originally some QTL were associated with R genes and this led researchers to speculate that R genes may be highly effective allelic forms of QTL (Gebhardt, 1994). However, QTL that are not known to be associated with R genes have been identified in subsequent studies using plant material evaluated for resistance to late blight in the field (Collins et al., 1999; Oberhagemann et al., 1999; Ewing et al., 2000; Ghislain et al., 2001). QTL expression may be related to day length (Ghislain et al., 2001) and appears to be influenced by overall plant physiology, as QTL for resistance can also vary with vigor and rate of physiological development of the plant (Collins et al., 1999).

R genes have also been identified in species other than S. demissum. Two genes (apparently different) from the diploid species S. bulbocastanum were cloned and expressed after introduction into a susceptible potato genotype (Van der Vossen et al., 2002; Song et al., 2003). The sources of these genes were resistant against all known races of the pathogen, which has led to great speculation on their durability. Should these genes prove to be durable, they could provide a novel, and extremely effective disease control mechanism.

Gene expression probably constitutes the most active area of research on mechanisms of resistance. The complex recognition process between pathogen elicitors and host receptors is thought to up- and down-regulate many genes. Different techniques are being used to evaluate gene expression during the infection process. Using high throughput DNA sequencing, scientists are rapidly developing libraries of sequenced cDNAs (Expressed Sequence Tag or ESTs). Thousands of ESTs from P. infestans and potato are now housed at the Phytophthora Genome Initiative database (Waugh et al., 2000) and TIGR, respectively. Analyses of ESTs recently led to the discovery of novel necrosis inducing cDNAs from P. infestans (Torto et al., 2003). This research relied on high throughput bioassays to link a particular sequence with a phenotype.



Suppression subtractive hybridization (SSH), a PCR-based method for studying expressed genes, has the advantage of requiring only small amounts of biological material (Birch and Whisson, 2001). SSH has been used to study genes that are up-regulated in both compatible (Dellagi et al., 2000) and incompatible (Birch et al., 1999) reactions. PCR-based techniques were also used to identify genes differentially expressed in resistant and susceptible genotypes grown in the field in Peru (Evers et al., 2003). Some up-regulated genes associated with general resistance in this study had previously been identified in association with specific resistance (Birch and Whisson, 2001).

Microarray technology will enhance the ability of researchers to evaluate gene expression at different stages of the infection process. This technology has already been used to evaluate factors affecting adaptation of P. infestans to tomato (Smart et al., 2003).

The above account shows that there has been tremendous progress in understanding the late blight disease of potato. Though the disease has been controlled through the development and deployment of cultural and chemical means as well host resistance, yet it continues to be worldwide the most devastating disease of potato crop.

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TABLE 8.1. Distribution of A1 and A2 mating types and Phytophthora infestans populations in selected parts of the world*

Region

Country

Population

Africa

Ethiopia

A1, new population




Kenya

A1, clonal, host specific, old population




Uganda

A1, clonal, host specific, old population




Egypt

A1+ A2




Morocco

A1+ A2




South Africa

A1, clonal, old population

Asia and the Pacific

China

A1 + A2




India

A1 + A2




Japan

A1 + A2




Korea

A1 + A2




Nepal

A1 + A2




Pakistan

A1 + A2




Thailand

A1 + A2




Bangladesh

A1




Philippines

A1




Sri Lanka

A1




Taiwan

A1




Vietnam

A1




Indonesia

A2




Russia

A1+A2, clonal (Siberia) recombinant (near Moscow)

Latin America

Argentina

A1+A2, clonal, host specific




Brazil

A1+A2, clonal, host specific




Uruguay

A2, clonal




Bolivia

A2, clonal, host specific




Ecuador

A1 clonal, host specific




Peru

A1 clonal, host specific




Chile

A1 clonal




Colombia

A1, clonal




Costa Rica

A1, clonal




Venezuela

A1, clonal




Mexico

A1 + A2 recombinant
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