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Although there is an enormous variety of pathogens, an important distinction can be made between those which rapidly kill all or part of their host and others which co‐exist with host tissues for an extended period without inflicting severe damage. The former category, referred to as necrotrophs, are often opportunist pathogens which invade wounds and juvenile or debilitated plant tissues. They grow intercellularly, producing cytolytic factors and then utilize the dead host tissues as a resource. The ability to attack a living host distinguishes these organisms from the saprotrophs which subsist exclusively on organic debris. In contrast, biotrophs do not kill their host immediately. They are, in fact, dependent upon viable host tissue to complete their development. Extreme biotrophy resembles mutualism in that it is difficult to discern any marked pathogenic effects.

Figure 2.2 shows two contrasting diseases of faba beans, both caused by fungi. In the first, chocolate spot caused by Botrytis fabae, the main symptom is dark necrotic lesions in which host cells have died. As the disease progresses the lesions expand and eventually coalesce to destroy the whole leaf. In the second, bean rust caused by Uromyces viciae‐fabae, the leaves are covered with pustules producing rust‐colored spores, but the tissues around the pustules are still green and alive The rust penetrates living cells and absorbs soluble nutrients that are then transported back into the center of the pustules to fuel spore production. Over time, this process will impact on the physiology and development of the host plant, but tissues are not directly destroyed by the pathogen.

Figure 2.2 Faba bean leaves infected by Botrytis fabae (left) showing necrotic lesions, and bean rust, Uromyces viciae‐fabae (right) with pustules producing rust‐colored spores.

Table 2.1 Main characteristics of necrotrophic and biotrophic pathogens.

Necrotrophs	Biotrophs
Morphological and biochemical features
Host penetration via wounds or natural openings	Host penetration direct or via natural openings
Few special parasitic structures formed	Special parasitic structures, e.g., haustoria, typically formed
Host cells rapidly killed	Living host–pathogen interface
Toxins and cytolytic enzymes produced	Few or no toxins or cytolytic enzymes produced
Nutrients obtained from breakdown of host substrates	Nutrients diverted from host cells
Destruction of host resistance	Suppression or evasion of host resistance
Ecological features
Wide host range	Narrow host range
Able to grow saprophytically away from host	Unable to grow away from host
Attack juvenile, debilitated or senescing tissues	Attack healthy hosts at all stages of development

The contrasting features of necrotrophs and biotrophs are summarized in Table 2.1. Biotrophs, in keeping with their more specialized parasitism, usually attack only a limited range of hosts. Biotrophic fungi like the rusts form differentiated infection structures including modified intracellular hyphae termed haustoria (see Chapter 6). Generally, these fungi do not produce large quantities of extracellular enzymes or toxins; during their co‐evolution with the host, synthesis of hydrolytic enzymes may have been repressed or limited to localized sites where host cells are penetrated. Eventually, the ability to elaborate such enzymes may have been lost altogether.

An alternative view of these different lifestyles is that necrotrophs may have evolved from biotrophs through an increasing ability to produce enzymes capable of degrading complex substrates. This theory proposes that the first fungi were dependent on living plants, but gradually evolved independence by developing enzyme systems able to deal with polymeric carbon sources in plant litter. Such schemes can therefore be extended to include free‐living saprotrophs but in the absence of any adequate fossil record, both versions are speculative. The advent of techniques for analyzing genome structure and molecular phylogeny may, however, provide fresh evidence to support or refute such evolutionary models.

A human analogy for these contrasting types of parasite has been proposed, as follows: necrotrophs are “thugs” while biotrophs are “con artists,” reflecting their more devious way of obtaining resources from the host plant. However, the original idea that necrotrophs are unsophisticated pathogens is now being revised as we learn more about their strategies for invading plants and overcoming host defense. It turns out that some have the capacity to hijack host pathways, leading to programmed cell death, thereby releasing nutrients for their own use.

The impression may have been given that biotrophy and necrotrophy represent absolute categories; in reality, there is a continuous gradation between the two types of pathogen. At one extreme are the viruses, which can replicate only within living cells, and fungal biotrophs, such as the rusts and powdery mildews. At the other extreme are necrotrophs, such as the damping‐off fungi and soft‐rot bacteria. In between, one encounters pathogens with intermediate characteristics. For instance, the potato late blight pathogen Phytophthora infestans exhibits a high degree of host specificity and other biotrophic features such as haustoria, but it also causes relatively rapid necrosis of invaded tissues. Many pathogens pass through both a biotrophic and a necrotrophic phase during their life cycle. Plant pathogenic bacteria such as Pseudomonas syringae initially proliferate in intercellular spaces in leaves or fruits without apparent damage to host cells, but water‐soaked lesions which become necrotic then appear. The apple scab fungus Venturia inaequalis grows beneath the cuticle of host leaves for several days without causing obvious necrosis, but as the lesions age, the host tissues are eventually killed and the typical scabs develop (Figure 2.3). Some species of the anthracnose fungus, Colletrotrichum, penetrate directly into host cells which remain alive for several days (see Chapter 6, Figure 6.9); subsequently, necrotic, spreading lesions are formed. The term hemibiotroph has been used to describe such behavior. The factors responsible for this switch from a balanced mode of parasitism to rapid killing of host cells have in many cases not yet been identified.

In nature, necrotrophs may grow on both living and dead host tissues. Pathogens such as Pythium and Rhizoctonia may be found growing actively in soil or on subterranean or aerial plant surfaces in competition with the natural microflora. In the absence of a suitable host, they may successfully complete their life cycle by utilizing dead organic resources. The ability of biotrophs to compete for dead organic matter is very limited or even nonexistent. These differences in patterns of natural occurrence of pathogens are reflected in their growth on laboratory culture media. Most necrotrophs are nutritionally undemanding; they grow well on a wide range of simple media. Biotrophs, on the other hand, have traditionally been regarded as fastidious organisms and in extreme cases cannot be grown on any known culture media.

Figure 2.3 Apple scab disease caused by Venturia inaequalis. (Left) Scab lesions on fruit. (Right) Scanning electron micrograph of apple leaf fractured through a scab lesion, showing sporulation of the fungus on the surface, and intact, uncolonized host tissues beneath. Bar = 10 μm.

Source: Courtesy of Alison Daniels.

Figure 2.4 Nutritional modes in heterotrophic microorganisms.

Distinctions based on the criterion of culturability are used to divide pathogens into two nutritional types: facultative and obligate parasites. A further refinement of this scheme distinguishes pathogens which are able to grow relatively well in pure culture, but which in nature are unable to compete with nonparasitic microbes. Such parasites are termed ecologically obligate in contrast to biochemically obligate organisms which are unable to grow apart from the living host either in vivo or in vitro. The basis of obligate parasitism remains largely unresolved; such microorganisms may be unable to synthesize essential metabolites and therefore have to obtain them from the host, lack particular nutrient uptake mechanisms, or may require developmental cues that are only provided in the presence of the host plant.

Figure 2.4 summarizes these different relationships and modes of nutrition in heterotrophic microorganisms.