Systematics and the Impact of Invasive Fungi on Agriculture in the United States

Fungi introduced into the United States have had and continue to have a profound impact on many aspects of US agriculture. Through human activities, fungi are moved effectively and efficiently to new areas. Most pathogens of US agricultural crops were introduced inadvertently along with their host plants (Yarwood 1983), many before the nature or cause of diseases, or the way in which they are spread, was understood. Although some introduced, plant-inhabiting fungi have a positive effect—mycorrhizal fungi, for example—this paper focuses on those that cause disease in plants occurring naturally in the environment and in crops cultivated for food or fiber or for use as ornamentals. The economic impact of these fungi derives from crop or yield loss; decreased quality of the plant or plant product, which could impair its exportability; and the costs of control, which may call for continuous monitoring, fungicide application, and breeding. Introduced invasive fungi also have a social impact. Late blight of potato is a striking example: The disease caused the Irish potato famine and led to the death or emigration of more than 3 million people (Large 1940, Schumann 1991). Moreover, introduced diseases can adversely impact native plants and sometimes change an entire ecosystem; for example, the introduction of chestnut blight in the early part of the 20th century led to the devastation of the North American chestnut trees (Anagnostakis 1987). This article discusses examples of plant pathogenic fungi that have been introduced into the United States, how they were introduced, and their effects on US agriculture, beginning with background information on fungal biology. The article concludes with a discussion of the importance of systematics—the science of discovering, organizing, and interpreting biodiversity—with emphasis on its role in making appropriate plant quarantine decisions in order to prevent future introductions of invasive fungi (Palm 1999). All plants, whether diseased or healthy, are hosts to a variety of fungi that can be categorized broadly in several biological groups (Alexopoulos et al. 1996). Fungi that obtain their nutrition by utilizing already-dead organic matter are called saprotrophs; those that grow on living plants, animals, or other fungi are called parasites. Many fungi are either facultative saprotrophs, which cause diseases in living plants but can survive in dead plant material, or facultative parasites, which usually are saprotrophic but sometimes become parasitic. Fungi that cannot grow without their living host plant, such as rusts, smuts, downy mildews and powdery mildews, are called obligate parasites or biotrophs (Alexopoulos et al. 1996). Research over the past two decades on the biology of fungi in woody and herbaceous dicotyledonous plants has revealed that some fungi, called endophytes, do not fit easily into those general biological categories. Endophytes, which occur within nearly all living plants, are generally defined as fungi that cause no apparent harm to the plant (Redlin and Carris 1996). The distinction between an endophyte that does not cause disease and a latent plant pathogen that elicits disease symptoms is not clear. It has been suggested, however, that the endophyte and plant are in a balanced antagonism, whereas the pathogen and plant are in an unbalanced antagonism in which the pathogen can suppress the plant's defense reaction and cause disease (Rodriguez and Redman 1997, Schulz et al. 1999). Can the same fungus have both lifestyles or are they mutually exclusive? Many fungi that have been isolated from apparently healthy plants, and therefore considered to be nonpathogenic endophytes, are morphologically similar to fungi that are plant pathogens. Are some of these apparently nonpathogenic endophytes actually latent pathogens that could cause disease under certain conditions? Or are there two distinct biological groups, one that is always nonpathogenic and another that is latent but can be pathogenic under the right conditions? If there are two distinct groups—nonpathogenic endophytes and latent pathogens—how can they be distinguished from each other? Answers to these questions are vital for making policies and decisions that are scientifically sound in order to protect plant resources from the introduction of latent—but potentially active—invasive pathogens. Obligate parasites are nearly always host-specific and mycologists and plant pathologists had thought that most plant pathogenic fungi, even facultative saprotrophs, were host-specific as well. Thus many plant-associated fungi were described and identified solely on the basis of host. However, recent molecular studies of taxa such as Phomopsis and Phyllosticta have shown that some species in these genera can infect multiple hosts. What had been considered to be separate species were genetically identical and therefore a single species that could infect many different plant genera and families (Rehner and Uecker 1994, Farr et al. 1999). This discovery, coupled with the fact that many Phomopsis and Phyllosticta species have been isolated as apparently nonpathogenic endophytes from asymptomatic plants, makes plant quarantine decisions more challenging. Making an accurate identification based on morphology is difficult, and new methods for identifying these species must be developed so that potential invasive pathogens can be distinguished from nonpathogenic endophytes. Fungi spread from one plant to another and from one location to another in several ways. Most pathogens produce spores, either through asexual or sexual reproduction, that aid in the dissemination of the fungus. These spores may be moved by wind, insects, or water, in which case the diseases generally spread over relatively short distances. However, sorghum ergot caused by Claviceps africana recently spread over a broad geographic area very quickly by way of wind-borne spores. This disease was first observed outside of Africa and Asia in 1995 in Brazil and in 1996 in Australia (Bandyopadhyay et al. 1998). The fungus that causes sorghum ergot may have spread to these new continents via infected seed. It spread rapidly in South America, and by 1997 it had been found in Central America, the Caribbean, and North America. The pathogen produces copious amounts of wind-borne secondary spores, and Bandyopadhyay et al. (1998) note that “even if seed-borne inoculum sources were eliminated, the disease would have spread between countries via the airborne inoculum.” Fungi are moved most effectively and efficiently to new areas, both accidentally and deliberately, through human activities. Many food crops were introduced to the United States by early explorers and settlers, who brought the seeds and plants of their home countries. Other new food crops and plants were introduced and continue to be introduced under the auspices of US government, industry, and aca demia. For example, from 1764 to 1775 Benjamin Franklin sent plant material to the United States from his diplomatic post in England (Yarwood 1983); US diplomats and representatives overseas were encouraged to do the same by President John Quincy Adams. Undoubtedly this plant material carried with it a number of associated fungi, some as harmless endophytes, some as beneficial mycorrhizae, and some as pathogens. Since its establishment in 1862, one of the responsibilities of the US Department of Agriculture (USDA) has been plant exploration and introduction. The Office of Plant Introduction was established in USDA in the latter part of the 19th century, and its history was chronicled by its first director, David Fairchild (1938). By 1923 an estimated 50,000 kinds of plants had been introduced by USDA (Yarwood 1983), and these introductions have contributed to the highly successful development of agriculture and horticulture in the United States. However, many USDA scientists recognized that disease-causing fungi and other pests might be introduced along with these plants, and they pointed out the need for a mechanism to prevent introduction of such pests. Following the introduction of such devastating diseases as chestnut blight and white pine blister rust, the US Congress enacted legislation—the Plant Quarantine Act of 1912—to protect plant resources. Puccinia graminis, an obligate parasite and the causal agent of wheat stem rust, is one of these plant pathogens introduced by human activity into the United States centuries ago. Wheat was brought to the United States as early as 1621, and wheat stem rust was probably in the United States as early as 1660 (Yarwood 1983). The disease was definitely here in 1832, based on observations of the fungus on wheat straw (Yarwood 1983). Puccinia graminis was probably introduced through infected wheat seed, infected barberry (the alternate host), or wheat straw (Yarwood 1983). This disease has been present in the United States for so long that it probably does not come to mind when one thinks of introduced diseases, but wheat stem rust continues to have an adverse economic effect on US agriculture (Schumann 1991). Dogwood anthracnose, a recently discovered disease, may have been introduced into the United States. Flowering dogwood (Cornus florida) and pacific dogwood (Cornus nuttallii) are important native understory trees in the East and Pacific Northwest, respectively. Dogwood anthracnose (Figure 1) first was observed in the 1970s (Daughtrey et al. 1996) and has spread rapidly throughout much of the range of both hosts. A previously unknown fungus, Discula destructiva, has been found to be the causal agent of the disease (Redlin 1991). The appearance of this new and lethal disease on both coasts, the rapid spread of the pathogen, and the relatively low genetic diversity within populations of the pathogen suggest that the fungus was introduced recently (Trigiano et al. 1995, Daughtrey et al. 1996). Additional studies of the genetic differences between the fungal populations from each coast suggest that the introductions on the two coasts were concurrent but separate events (Caetano-Anollés et al. 1996, Yao et al. 1996). One pathway for the introduction of this fungus may have been asymptomatic seeds or plants of kousa dogwood (Cornus kousa) imported from its native Asia. There the fungus may be a weak pathogen or an endophyte of that dogwood species. In the latter case, the fungus would not be observed during plant quarantine inspections of germ plasm exported to the United States. Among other recently introduced plant pathogens are powdery mildew fungi, which cause diseases of ornamental plants. These include powdery mildew of cascading petunias, New Guinea impatiens, poinsettia, and sedum. Powdery mildew fungi are obligate parasites in the order Erysiphales and host specific at the plant genus or species level. They usually are evident by their white, threadlike hyphae on the surface of plants, giving the plants a mildewed appearance (Figure 2). As novel plants are introduced and ornamental production spreads to new areas of the world, the opportunities for disease introductions multiply: For example, new powdery mildew diseases have become a serious problem for the ornamentals industry over the past decade (Figure 3). Why have so many new powdery mildew diseases been discovered in so short a time? Poinsettias for the US market used to be propagated mainly in the United States, but now they are propagated in other countries and cuttings are shipped to the United States for further development and marketing. Although all plant materials are subject to inspection by the USDA Animal and Plant Health Inspection Service (APHIS) before entering the United States, powdery mildew infections of young poinsettias can be inconspicuous (Celio and Hausbeck 1998), especially on cuttings, and could be overlooked during phytosanitary inspections. Thus, some of these powdery mildews may have been introduced on asymptomatic plant cuttings used for propagation (Margery Daughtrey [Cornell University], personal communication, 1999). Other powdery mildews of ornamentals might have been introduced on cuttings of plant varieties relatively resistant to the disease and therefore without obvious visible effects (Margery Daughtrey [Cornell University], personal communication, 1999). When those seemingly healthy cuttings were brought into greenhouse production near a susceptible variety, the fungus could have infected the less-resistant variety and only then—after the time for preventing introduction of the fungus had passed—become a clearly visible problem. Other powdery mildews may have been present for many years but did not become established immediately. After World War II growers applied protectant fungicides regularly (Margery Daughtrey [Cornell University], personal communication, 1999). Frequent use of Benlate, the first partially systemic fungicide, may have suppressed new powdery mildew introductions. The current integrated pest management practice—spraying only after a problem is detected—might have allowed the introduced disease to become established and evident as a new problem. Introduced pathogens have serious impacts in the economic, social, and ecological realms. Although Puccinia graminis was introduced into the United States at least 150—and possibly more than 300—years ago, this fungus still has a negative economic impact due to crop losses and the cost of breeding programs aimed at producing varieties of wheat that are resistant to wheat stem rust. Puccinia graminis can continually change genetically through sexual reproduction and the movement of wind-borne spores. These spores are often blown long distances (e.g., from the wheat-growing areas in the southern United States and Mexico to the northern US plains along the “Puccinia pathway”) (Schumann 1991). The USDA Agricultural Research Service Cereal Disease Laboratory in St. Paul, Minnesota, coordinates a continuous monitoring program of races of P. graminis. Wheat breeding programs are ongoing to provide new germ plasm when plant disease resistance is overcome by a new race of the pathogen. Introduced diseases can have social impacts. Scarcity of wheat caused by epidemics of wheat stem rust is the historical reason that the bread of central Europe is often made of rye and that cornbread is so popular in the southern United States (Horsfall 1983). One of the best-known examples of the social impact of a plant disease is the Irish potato famine in the mid-19th century, which resulted from an epidemic of potato late blight (Figure 4) caused by Phytophthora infestans. The potato had been introduced into many parts of the world from its native South America; the introduced pathogen is thought to have evolved in the Toluca Valley of Mexico, where there are many native potato relatives (Fry et al. 1993). The epidemic, caused by weather conditions conducive to the disease, had profound social and historical impacts, given the reliance of the Irish on the potato as a food source. Horsfall (1983) describes the famine as having affected the politics of England and the outcome of World War I. Interestingly, potato late blight has reemerged as a problem disease worldwide. Indeed, it is still the greatest potential disease threat to the world's potato crop (Cooke and Deahl 1998). Serious epidemics have occurred in the United Kingdom and northern Europe during the past decade; in the United States, too, the disease has become a severe problem, even in areas that formerly were relatively free of it (Cooke and Deahl 1998). This reemergence in the United States has been attributed to recent introductions of fungicide-resistant and more virulent strains of the pathogen, probably on tomatoes (Fry and Goodwin 1997). The introduction of these genotypes and of the opposite mating type of P. infestans, which is needed for sexual reproduction, and the movement of the fungus within the United States on tomato plants and in infected seed potatoes, has increased the opportunity for sexual recombination, which may result in destructive new genotypes (Goodwin et al. 1998). An example of an introduced disease that affected natural resources is chestnut blight, which permanently changed the eastern US forests (Anagnostakis, 1987). American chestnut (Castanea dentata) was a predominant forest tree and a widely planted shade tree in the eastern United States the first of the 20th of its resistance to the was used for and it was also used for and In chestnut blight was discovered to be the cause of the death of American chestnut trees in the New The disease spread rapidly within the entire native range of American years this forest tree was to a relatively (Anagnostakis and The introduction of chestnut trees in the latter part of the 19th century was as the of this devastating pathogen after found the fungus in chestnut trees (Castanea in and (Anagnostakis 1987). However, in those countries the fungus caused or no Plant and Quarantine is for preventing of invasive species into the United States. The in and in the coupled with over recent introductions of invasive such as the has made the need to its The Plant was to a of the current American Plant a of the and on how to and to more effectively protect US agriculture and plant resources from new invasive plant pests in the management is an in the and that phytosanitary and policies be based on a of that is in studies to of the of of fungi are present in the United States and their and to The more information the more the and the more effectively US plant resources can be from invasive is the science of discovering, and interpreting to of by of and studies 1994, The result is accurate that information the and that fungus and In even if a specific plant-inhabiting fungus is information by the biological of fungi could of the fungus in the that an and in a an is often based on the of whether a may as a pathway for the introduction of plant pests. These are the in the when a industry, or the opportunity to a plant or plant to the United States. The of the in on of the and biology of potential pests. The of as from South Africa to the United States as an of the plant to South Africa and produce that are by in the United States and the world and are highly in the industry (Figure In South Africa the industry is a in and is relatively at million but with potential for US growers new germ plasm to novel varieties and disease protect the US industry, and germ plasm exported to the United States must be free of pathogens not present in the but the United States must also of this to with and both of these through pest of the of fungi on in the United States and South These with the of a of fungi other to in South than of the million fungal species have been discovered and described and 1997). 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