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Evolution and stasis in plant-pathogen associations.


Plant-pathogen interactions provide perhaps the best example of coevolution. Infection can have a major impact on the fitness of both host and pathogen, and the compatibility between partners typically has a genetic basis. A single allelic substitution may spell the difference between a virulent or avirulent pathogen and a susceptible or resistant host (Flor 1971, Thompson and Burdon 1992). Most empirical data and theoretical models, however, are based on only a subset of plant-pathogen interactions, namely annual or short-lived plants infected by discrete, lesion-forming pathogens. While these associations predominate in agriculture, and have rightfully received the greatest research attention, they are atypical of many associations that may exhibit very different ecological and coevolutionary interactions.

The purpose of this paper is to consider plant-pathogen associations where the host is systemically infected by a single pathogen genotype. The selective forces acting on an association where the pathogen is completely dependent on a single host plant and where the pathogen, by virtue of its systemic growth, can control or manipulate the host's growth and reproduction, are likely far different than for interactions where a host plant is infected by large numbers of different pathogen genotypes. We develop the hypothesis that many systemic pathogens directly alter the host's recombination system to decrease the probability of producing resistant progeny. Much of the discussion is based on results from clavicipitaceous fungal parasites of grasses and sedges, particularly the interaction between the fungus Atkinsonella hypoxylon and Danthonia grasses, but the general idea is relevant for a wide range of systemic plant parasites such as rusts and smuts.


The numerical relationship of host and pathogen genotypes varies among associations. Hosts can be infected by only a single pathogen genotype or by multiple pathogen genotypes. Similarly, a pathogen genotype may infect only a single host plant or many host genotypes. Four combinations of plant-pathogen interactions are therefore possible. Two clavicipitaceous fungi infecting grasses illustrate the case where each host genotype is infected with a single pathogen genotype, Balansia obtecta infecting sandbur grass (Cenchrus echinatus) and Atkinsonella hypoxylon infecting Danthonia spicata (Diehl 1950). In the first case a given fungal genotype infects only one host genotype, while in the second one a fungal genotype can infect many plant genotypes when it is transmitted vertically to seed progeny (Clay 1994). Some smuts and ergot (Claviceps purpurea) are examples of multiple pathogen genotypes infecting a single host genotype. While each smut genotype infects only a single plant, e.g., smuts dispersed as diploid spores that later germinate and conjugate with other mating types to form a dikaryotic mycelium that actually infects the host plant (Alexander et al. 1993), an ergot genotype may infect many hosts. Asexual conidia in the "honey dew" of Claviceps can be transmitted by insects to many other plants (Campbell 1958).

TABLE 1. Summary of differences between systemic and nonsystemic fungal parasites of plants.
Characteristic           Systemic             Nonsystemic

Location of infec-   throughout plant       highly localized
Number of geno-          one or a few           many
types infecting
Occurrence of la-        common                 uncommon
tent infections
Parasite generation      long                   short
Duration of infec-       perennial              annual
Propagation within       by hyphal growth       by spores
Effect on host sur-      minimal                detrimental
Location of parasite     specific locations     site of vegetative
fruiting                                           growth
Effect on host de-       induced changes        no changes
Frequency of seed        often common           rare
Frequency of con-        low                    high
tagious spread
Frequency of epi-        rare                   common

Where multiple genotypes infect the same host, the genotype that can most efficiently convert plant biomass into contagious propagules will have the greatest reproductive success. Intrahost competition among pathogens can favor the most virulent genotypes and have a consequent debilitating effect on the host (Ewald 1987, Bonhoeffer and Nowak 1994, Lenski and May 1994). Multiple infections can severely reduce host survival and growth (Parker 1986, Paul and Ayres 1987). In contrast, where infection is caused by a single pathogen genotype host survival and/or growth may be enhanced (Clay 1991, Wennstrom and Ericson 1991; see also Table 2). Evidence that hosts are infected by only a single pathogen genotype includes uniformity of genetic markers (Leuchtmann and Clay 1989a), lack of sexual reproduction of pathogens in isolated plants (Bultman and White 1987), and uniformity of symptoms throughout the entire plant (Diehl 1950).


Most, if not all, of the examples where hosts are infected by a single pathogen genotype involve fungi that form systemic infections of plants, yet these types of infections have received relatively less research attention than typical lesion-type plant-pathogen interactions. Other important differences between systemic and nonsystemic fungal parasites of plants are outlined in Table 1. These are generalizations and many exceptions exist. The relative life-spans of systemic and nonsystemic pathogens often differ. Many nonsystemic pathogens begin to sporulate a few days or weeks after the initial colonization event and do not persist for more than a single growing season (e.g., lesions on deciduous leaves) (Agrios 1969). In contrast, many systemic pathogens are long lived, exceeding the life-span of their host. Systemic infections are often initiated at the seed or seedling stage, and in some cases are transmitted to progeny through the maternal plant (Clay and Jones 1984, Clay 1986). Pathogens that fruit in the flowers or inflorescences of their hosts, such as loose smut of barley (Ustilago nuda), anther smut of many Caryophyllaceae (U. violaceae), and choke (Epichloe typhina) of grasses, are dependent upon hosts reaching reproductive maturity for their transmission, which may take many years in perennial plants. A long latent period between infection and flowering would favor relatively avirulent systemic fungi and/or fungi that can induce precocious flowering or increase flower numbers (Wilson 1977, Alexander and Maltby 1990). Any pathogen genotype that killed or debilitated its host in such a way as to delay or prevent host flowering would be at a selective disadvantage compared to other genotypes whose hosts have higher survival and/or flowering rates. Gill and Mock (1985) have described a similar situation in the red-spotted newt infected by trypanosomes that cannot reproduce until adults return to water several years after they migrated into terrestrial habitats.

Systemic and nonsystemic pathogens differ in their ability to spread contagiously. Van der Plank (1959) suggested that the maximum rates of multiplication of systemic pathogens were 10-fold a year on tree hosts and 10000-fold per year on herbaceous plant hosts compared to up to one-billion-fold per year for lesion-forming pathogens such as Phytopthora infestans. Poor powers of contagious spread would favor longer associations with a particular host plant genotype allowing repeated fruiting over many years. Systemic pathogens do spread contagiously (Alexander 1990, Clay 1990, Wennstrom and Ericson 1990), but they are generally incapable of the explosive spread of many lesion-forming nonsystemic pathogens (Burdon 1987).

Perhaps the most frequent feature of systemic pathogens is their ability to alter the reproductive biology of their hosts. Many examples exist of systemically infected plants that do not flower (Marks and Clay 1990, Wennstrom and Ericson 1991, Roy 1993), whose flowers are aborted (Bradshaw 1959, Verma and Petrie 1980, Clay 1984), or whose flowers are transformed into completely different structures, typically for the dissemination of the fungus (Fischer and Holton 1957, Clay 1986, Alexander and Maltby 1990). Induced structures that mimic flowers, but are actually organs for attraction of insect visitors and fungal reproduction, represent another example of developmental control (Roy 1993). The occurrence of systemic fungi throughout the plant and around meristematic areas, and the ability to alter nutrient relations or hormonal balances, provide the opportunity to control and alter host development (Porter et al. 1985, Clay 1986). The dramatic changes seen in some associations, such as the production of spore-filled anthers by female Silene plants (Alexander 1990), suggest that systemic fungi may alter gene expression and regulation in host plants. The diversity of fungal genotypes infecting one host in nonsystemic associations, plus their highly localized occurrence, does not appear to allow a similar level of coordinated developmental control of host plants. Even if they could control host development they would be vulnerable to "cheaters," pathogens that benefit from altered host development without the cost of inducing such alterations.


A wide range of associations between systemic fungi and plants are characterized by the complete or partial suppression of outcrossing or sexual reproduction and an increase in clonal growth in hosts compared to uninfected plants (Table 2). The taxonomic diversity of hosts indicate that these interactions are not limited to certain plant families or life histories. Further, a wide range of fungal groups is involved, including rusts, smuts, clavicipitaceous fungi, and others, again indicating that plant pathogens that suppress sex are taxonomically diverse. Given the relatively small number of wild plant-pathogen systems that have been subjected to detailed research, many more similar systems likely exist.

Ecological advantages accruing to parasites that eliminate host sexual reproduction are reported from several animal systems. Parasitic castration, or the specific destruction of host gonads, can result in bigger, longer lived hosts that support larger numbers of parasites with higher reproductive rates (Baudoin 1975). Hosts, on the other hand, typically are incapable of reproduction by either sexual or asexual means and have a finite life-span. Parasitic castration can be viewed as a type of resource allocation where the parasite shifts host resources from reproduction to growth, ultimately enhancing parasite reproduction. The greater survival and growth of parasitically castrated plants (see Table 2) could also be explained by resource real-location.

TABLE 2. Examples of systemic fungal pathogens affecting the balance between sexual and asexual reproduction of host plants.
Example                                    Reference(*)

Greater or equivalent survival compared to
uninfected plants

Tolumnia variegata infected by Sphenosphora
saphena                                          11
Pulsatilla pratensis infected by Puccinia pul-
satillae                                         17
Danthonia spicata infected by Atkinsonella hy-
poxylon                                           4
Cyperus virens infected by Balansia cyperi        6

Floral transformations and/or loss of sexual

Arabis holobellii infected by Puccinia monoica   12
Tridens flavus infected by Balansia epichloe      9
Silene spp. infected by Ustilago violacea     1, 18
Cruciferae infected by Albugo candida        15, 16

Enforced self-fertilization

Danthonia species infected by Atkinsonella hy-
poxylon                                           4
Viola spp. infected by Puccinia violae            3

Enhanced vegetative growth

Grasses infected by Epichloe typhina           2, 8
Arabis holboellii infected by Puccinia monoica   12
Grasses infected by various smuts                 7
Pulsatilla pratensis infected by Puccinia pul-
satillae                                         17
Cyperus rotundus infected by Balansia cyperi     13

Induction of novel structures for asexual

Cyperus virens infected by Balansia cyperi       5
Andropogon glomerata infected by Myrioge-
nospora atramentosa                              5
Zea mays infected by Sphacelotheca reiliana     10
Pennisetum typhoides infected by Sclerospora
graminicola                                     14

* Reference numbers are as follows: (1) Alexander 1990, (2) Bradshaw 1959, (3) U. Carlsson, personal communication, (4) Clay 1984, (5) Clay 1986, (6) Clay 1990, (7) Fischer and Holton 1957, (8) Harberd 1961, (9) Marks and Clay 1990, (10) McGee 1988, (11) Melendez and Ackerman 1993, (12) Roy 1993, (13) Stovall and Clay 1988, (14) Tarr 1972, (15) Verma and Petrie 1980, (16) Alexander and Burdon 1984, (17) Wennstrom and Ericson 1991, (18) Carlsson et al. 1990.

Unlike most animals, plants are capable of reproducing by outcrossing, self-fertilization, and/or vegetative reproduction. Clones can be very large and long lived (Harberd 1967) and, depending on the species, are capable of considerable dispersal (Holm et al. 1977). The loss of sexual reproduction is little or no impediment to species with alternative methods of reproduction. The prevention of flowering itself can stimulate clonal growth through resource reallocation (Peterson et al. 1958). Indeed, many thousands of widespread and aggressive plants depend entirely on apomixis or clonal reproduction for their persistence (Holm et al. 1977).

Clonal reproduction results in genetic copies of parental plants bearing the same genes conferring resistance, or susceptibility, to plant pathogens. Sexual reproduction, in contrast, results in more variable progeny, although obligate self-fertilization will give rise to completely uniform, homozygous lines in a few generations. According to the Red Queen hypothesis, sexual recombination increases the probability of progeny escape from parasites adapted to common host genotypes by producing offspring with rare genotypes. Therefore, pathogens ultimately favor the maintenance of outcrossing and not just sexual reproduction. The fact that clonally propagated crop species (e.g., sugar cane, bananas) incur greater economic losses from pathogen damage than do self-fertilized crops, which in turn incur more losses than outcrossing crops (Stevens 1948, Adams et al. 1971) supports this prediction. Several plant-insect studies have also found that selfed or clonal progeny suffer greater damage than out-crossed progeny (Rice 1983, Schmitt and Antonovics 1986). Genetically based resistance has been demonstrated repeatedly (Keen 1990, Long and Staskawicz 1993), although the genetic mechanism of resistance is still not completely understood. Among crop plants there is evidence for Flor's (1956) gene-for-gene model, but under the Red Queen hypothesis a "matching-allele" model is assumed (Hamilton 1980, Frank 1993). Although gene-for-gene resistance will not give rise to frequency-dependent selection necessary for the long-term advantage of sexual recombination (Parker 1994), outcrossing will still be advantageous. In the gene-for-gene model single gene resistance to a particular pathogen race is typically a dominant trait. An infected plant would therefore be a homozygous recessive. Selfing or clonal reproduction can generate only susceptible progeny, whereas outcrossing will produce resistant progeny as a function of the frequency of resistance alleles in the population. Variation in quantitative resistance of progeny is expected to exhibit a similar trend; selfed or clonal progeny would exhibit resistance patterns more similar to the parent than outcrossed progeny.

There may be other, nongenetic advantages of host castration for systemic parasites, such as increased transmission (Stouthamer et al. 1990) or greater nutritive value of reproductive, compared to vegetative, tissues (White et al. 1991). However, these bases for parasitic castration do not predict a correlation between genetic similarity and host-parasite compatibility.


The interaction between the fungus Atkinsonella hypoxylon (Ascomycota, Clavicipitaceae) and grasses in the genus Danthonia is an ideal system for examining the hypothesis that parasites can benefit from, and enforce, genetic uniformity in their hosts. Danthonia is a worldwide genus of perennial caespitose grasses. Four species in eastern North America (D. compressa, D. epilis, D. sericea, and D. spicata) represent the entire known host range of A. hypoxylon (Diehl 1950; K. Clay, unpublished data). Atkinsonella grows epiphytically on meristems, leaf axils and inflorescences, forming a systemic infection (Leuchtmann and Clay 1988). As the host flowers, hyphae rapidly proliferate to produce a fungal fruiting body (stroma) that aborts the terminal inflorescence. Infected plants can exhibit greater survival, growth, and interspecific competitive ability compared to uninfected conspecifics (Clay 1984, Kelley and Clay 1987).

Both Atkinsonella and Danthonia can reproduce two ways [ILLUSTRATION FOR FIGURE 1 OMITTED]). The grass produces dimorphic seeds from terminal panicles of potentially outcrossed flowers and self-fertilized cleistogamous flowers in the lower leaf sheaths (cleistogenes) (Weatherwax 1928, Clay 1983, Cheplick and Clay 1989). The basal cleistogamous flowers are not aborted by infection and produce viable seeds vertically infected from the maternal plant (Clay 1984, 1994, Clay and Jones 1984). A quantitative genetic study of D. spicata revealed that cleistogamous progeny were less variable within families for 12 quantitative traits compared to progeny from terminal inflorescences (Clay and Antonovics 1985). Atkinsonella hypoxylon also has two mechanisms of reproduction. In addition to vertical transmission through the basal cleistogamous seeds, fruiting bodies borne on aborted inflorescences produce infective spores (Leuchtmann and Clay 1989b).

Seedling inoculation studies conducted with different populations and hosts of A. hypoxylon have shown that there are genetic differences in compatibility among plant-fungal combinations (Leuchtmann and Clay 1988, 1989c). Recent studies have revealed with-in-population variation in compatibility with certain isolates exhibiting significantly higher infection rates than other isolates from the same population (K. Clay and I. Frentz, unpublished data). Moreover, many seedlings inoculated with isolates from the same population often exhibit extensive lignification and cell death in areas adjacent to the epiphytic hyphae around the meristematic region, which ultimately leads to the death of the seedling. This suggests that there is genetically based resistance to infection in Danthonia populations, although the genetic mechanism of resistance is not known.

The abortion of potentially outcrossing flowers and the transmission of the fungus through cleistogamous seeds, combined with intrapopulation variation in resistance, could have an important effect on the population genetic structure of Danthonia. Because host plants produce only obligately self-fertilized cleistogamous flowers they are reproductively isolated from uninfected plants. Moreover, since the fungus is transmitted through the self-fertilized seeds and has the same effect on the reproductive system of the subsequent generation of infected plants, lineages of infected, self-fertilized plants are created. Multiple generations of infection-induced self-fertilization would generate highly homozygous lines infected by a single fungal genotype within the more randomly breeding uninfected members of the population.


The Red Queen hypothesis suggests that a major reason for the prevalence of sexual reproduction, despite its significant genetic disadvantages, is that the constant production of novel genotypes each generation increases the probability of producing resistant progeny (Hamilton et al. 1990, Lively et al. 1990). Sexual reproduction creates a moving target that is more difficult for parasites to hit. This hypothesis, which has garnered a large amount of empirical and theoretical support, is host centric and views parasites as being trapped in a perpetual arms race. The effects of systemic fungi that enforce selfing or asexual reproduction, reducing genetic diversity, suggest that they have "captured" the Red Queen by limiting the host's evolutionary ability to respond to infection. This can be tested through field and laboratory experiments and investigations of the population genetic structure of interacting plant and pathogen populations.

The Red Queen Captured hypothesis is not a challenge to the original hypothesis and indeed is dependent on the basic premise. If outcrossing is advantageous to hosts to reduce pathogen infection among genetically variable offspring, it follows that pathogens with high transmission rates to its host's progeny (due to vertical transmission, systemic growth, or spatial clumping) will benefit by preventing their host from outcrossing. Systemic pathogens, as opposed to lesion-forming pathogens, are both more likely to be able to directly alter reproductive development and to reap the benefits of those changes.

With respect to Danthonia we predict that outcrossed chasmogamous progenies will, on average, contain a higher frequency of resistant progeny than self-fertilized cleistogamous progenies when inoculated with the maternal fungal strain [ILLUSTRATION FOR FIGURE 1 OMITTED]. This is currently being tested. Past research has shown that plants are infected by a single genotype, the rate of contagious transmission is low relative to vertical transmission through cleistogamous seeds, there is genetic specificity for compatibility, and significant outcrossing occurs in chasmogamous flowers. What remains to be investigated is whether infected lineages persist in natural populations for multiple generations, indicating that the fungus is maintaining genetically uniform and highly susceptible host lines in an evolutionary stalemate.


Recent interest in plant-pathogen systems by ecologists and evolutionary biologists has largely centered on the relative fitnesses of infected and uninfected plants and the genetic basis of their interaction. It is widely recognized that pathogens can indirectly affect the population genetic structure of hosts by acting as a selective agent favoring resistant genotypes. It is less often recognized that plant pathogens can directly affect the genetic structure of host populations by changing plant reproductive systems toward increased clonal spread and decreased genetic variability. Where host resistance to infection has a genetic basis, the loss of sexual recombination is the loss of a valuable weapon in the coevolutionary interaction with pathogens. The genetic uniformity and enhanced clonal spread of hosts relative to uninfected plants may allow long-lived systemic pathogens with poor powers of contagious spread to persist and dominate in many plant populations.


This paper is based on a talk given at the symposium "The ecology of diseases" (L. Real, organizer) at the 1993 Ecological Society of America annual meeting in Madison, Wisconsin. We thank two anonymous reviewers for their helpful comments. Research on Danthonia and Atkinsonella has been supported by NSF grant BSR906858 to K. Clay.


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Author:Clay, Keith; Kover, Paula
Date:Jun 1, 1996
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