If you were asked to tally up all the diseases you’ve ever heard of, chances are that you would think of animal rather than plant infections. Except when they have created widespread problems—think of the potato blight that affected British and Irish farmers in the mid-19th century—plant pathogens have typically been interesting only to the farmers whose livelihoods have depended on quickly recognising, reacting to, and preventing the spread of these diseases. More recently, agriculturalists have been assisted in their efforts by plant geneticists and phytopathologists (researchers who specialise in the field of plant disease) tasked with developing disease-resistant crops and reducing the spread of infection between various plants and fields.
However, despite the efforts of these individuals—not to mention the millions of dollars that the agriculture and horticulture industries have poured into phytopathology research—we still lack a fundamental understanding of plant disease. In some cases we haven’t even identified the agents responsible for certain sicknesses; where these have been found, we don’t always know why they have suddenly become problematic, or how widespread the infection might ultimately become.
One way of predicting where, when and under what conditions plant infections will appear and spread is to examine the characteristics of emerging infectious diseases (EIDs)—those that have recently become more visible to us, either because they are newly evolved or discovered, have changed their method of infection, or are found in higher numbers or over a broader geographical area. An improved understanding of the mechanisms that allowed these pathogens to become so successful could not only have huge agricultural (and therefore economic) implications, but also inform conservation and management decisions relevant to sensitive or endangered wild species.
Emerging infectious diseases in plant
Plants, like animals, can be infected by a variety of microorganisms, such as viruses (the most common type of EID, causing nearly half of infections), fungi, bacteria and nematodes (the least common form of EID, responsible for ~1% of infections). Perhaps counterintuitively, a discussion of the factors responsible for the emergence of phytopathogens is best initiated with a summary of the mechanisms that prevent pathogens from running rampant in the first place. First and foremost among these is the evolution of tolerance or even complete resistance in potential host species. Though pathogens are likely to eventually develop new characteristics that allow them to break through these genetic defenses, mutation and recombination (a process by which DNA is broken and then re-joined in new patterns) both allow plants to adapt to these changing infectious circumstances. Thanks to this ‘arms race,’ neither host nor pathogen is generally ever able to completely gain the upper hand.
Another important characteristic of natural ecosystems is their diversity. Even though a habitat may offer an abundance of a particularly good host, it may also be home to plenty of terrible hosts that represent dead-ends for even the most infectious (transmissible) and virulent (harmful) of pathogens. Likewise, high biodiversity can negatively impact pathogens that rely on ‘vectors’, or organisms that shuttle infectious agents from a reservoir (an organism in which the pathogen is ‘stored’) to a host; where there are many alternative vectors, infectious agents may not end up at their intended destination. An abundance of natural predators and parasites may also waylay pathogens before they are able to infect any hosts. A number of abiotic factors can also keep pathogens in check. Physical and geographical barriers—even something as simple as a few feet between an infectious host and its uninfected neighbour—can prevent or reduce the spread of disease. Further, changing weather conditions can kill off pathogens that are highly sensitive to temperature and moisture, while a lack of wind or hard rain can prove problematic for microorganisms that rely on these events to create injuries through which they can invade their hosts.
Given these natural checks on pathogen spread, it is not surprising that both habitat disturbances (including those caused by humans) and changes in vector populations have been identified as major players in the emergence of phytopathogens. Recombination can also play a role, since it can—temporarily, at least—allow either plants or pathogens to pull ahead in their evolutionary arms race. Fluctuating weather patterns are thought to be responsible for approximately one-quarter of emergences; many of these variations are likely tied to climate change facilitated by anthropogenic activities.
By far the most important factor, however, is the introduction of non-native species—of both hosts and pathogens. On average, introductions are responsible for just over one-half of all emerging diseases. However, the exact figure varies from one type of pathogen to the next; viruses seem particularly skilled at capitalising on interactions with organisms they have not previously encountered. Whether introductions are accidental or deliberate, things tend to go very badly for plants exposed to pathogens to which they have no innate defense.
The emergence of novel pathogens may also be facilitated by farming methodologies. Particularly problematic is the fact that we tend to grow monocultures comprising plants with a similar genetic makeup. This technique creates huge tracts of land covered by crops frequently lacking the resistance genes needed to combat that next big infection— whatever it might be. Modern farmers also tend to sow seeds fairly close together, thereby increasing the likelihood that infections will spread between grown plants. Recently, there has also been a move towards leaving plant remnants in the field once the harvest has been completed. While this helps enrich the soil, it also facilitates the spread of last year’s diseases to next year’s crops.
Compounding all of these problems is the fact that agricultural efforts have been intensifying in order to satisfy the demands of a growing human population. Given the flexibility of gene transfer amongst many pathogens, there is an almost endless supply of infectious agents available in the environment. Sooner or later, chances are good that we will experience the emergence of an infection that will be the next potato blight or cassava mosaic disease—two epidemics with extreme financial, social, and health repercussions
Emerging infectious diseases in wild plant
Although the bulk of phytopathogen research to date has focused mainly on domestic species, epidemics can, of course, also occur in wild plants. Detailed studies of native organisms have generally been pursued only in species acting as a reservoir for infections impacting crops or ornamentals. There are, however, two notable exceptions: the American chestnut blight (caused by the fungus Cryphonectria parasitica) and the spread of Dutch elm disease (caused by fungi in the genus Ophiostoma), each of which has been fairly well documented. In both cases, the infectious agents appear to have been introduced into new habitats after hitchhiking on exotic products; C parasitica was hiding in Japanese chestnut trees bound for an American nursery, while the original Ophiostoma species (from which two others eventually evolved) was stowed away in a shipment of lumber.
Anthropogenic activity also appears to be responsible for infections threatening eucalyptus species in Australia and dogwood trees in the United States. In both cases, the pathogens (both fungi) were introduced and spread by humans. Origins of other known plant diseases are more mysterious. The Florida torreya, a conifer native to the northern portion of the US state of Florida, has suffered an extreme population decline likely resulting from one or more fungal infections; it is now considered critically endangered. Researchers are still searching for the pathogen responsible for the severe decline of pondberry, a rare and endangered North American species that had already been hit hard by habitat loss when it also began to succumb to an unknown—probably fungal—infection.
Other recent notable EIDs include ash dieback (caused by the fungus Chalara fraxinea) and sudden oak death (caused by Phytophthora ramorum). The latter of these is only the most recent disease resulting from the activity of a species in the Phytophthora genus; previous victims have been the New Zealand kauri (collar-rot), a variety of ornamental rhododendrons (root rot), beeches (stem and leave rot), and several domesticated species, including strawberries, soybeans, coconuts, and cocoa.
Effects of climate change on phytopathology
One of the biggest questions in contemporary plant phytology is how the spread and emergence of disease are impacted by climate change. Analyses of ancient sediment and ice samples have revealed evidence that both the distribution and prevalence of pathogens have been affected by historical fluctuations in weather and climate patterns. Thus, there is every reason to believe that the high rates at which infectious plant diseases have been emerging over the past several decades may be related, both directly and indirectly, to climate change.
One factor that affects emergence is moisture: fungi and bacteria tend to benefit from increases in humidity and precipitation, while viruses and insect-borne diseases thrive under drier conditions. As certain habitats have become wetter or drier (patterns affected by numerous factors, including topography and proximity to the Equator), local conditions have likely shifted to favor new pathogens. Such shifts are expected to continue— and perhaps become even more common—over the next several decades.
Variations in temperatures and broader weather patterns may also benefit pathogens by altering the distributions and abundances of both vectors and hosts, allowing disease agents to move into new habitats. Some pathogens are free-living, capable of surviving in water or soil for long periods before encountering a suitable host. Even slight variations in environmental conditions can extend the length of time over which these organisms can lie in wait, thus increasing the likelihood that hosts will eventually become infected. Researchers have even suggested that thawing glaciers might release frozen pathogens that could either infect hosts directly or contribute pathogenic genes to other infectious agents in the environment.
Climate also influences host physiology, affecting fundamental processes such as respiration and metabolism. These are characteristics that can impact how easy it is for a pathogen to infect a host, as well as the speed and strength with which an infected individual can mount an immune response to an infection. Animal pathologists have recently identified several systems in which physiological processes likely played an integral role in linking climate change with disease emergence; in all likelihood, an analysis of plant data would yield similar results.
What will happen in the future?
Paolo Bacigalupi’s 2009 award-winning novel The Windup Girl envisions a future where the world has been re-shaped by the activity of phytopathogens; agriculture companies race to develop disease-resistant genetically modified crops, while ‘natural’ plant resources are all but depleted. It is a chilling scene made all the more frightening by the fact that we have already experienced outbreaks and destruction similar to those the author describes. Luckily, there are many ways for us to escape such a future.
Given the influence of introductions on disease emergence, one of the most important tactics will be improving our monitoring systems—especially those associated with the import and export of plants and plant-based products. Many regions and countries have already initiated more stringent procedures in response to outbreaks. For example, flour export is often banned from regions affected by the smut fungus Tilletia indica (the cause of Karnal, or partial bunt), which is so destructive that it is considered a biological weapon.
There are also a number of ways in which farmers could adjust their agricultural practices to reduce the likelihood of disease spread. A greater emphasis might be placed on native, rather than exotic, crop species. Alternatively, crops could be rotated more frequently in order to reduce infection rates (though this tactic would not work as well against pathogens that can infect multiple domestic species). The development of new pesticides and genetically modified crops could also be helpful; however, these techniques must be used carefully, as they could have negative implications for both humans and wildlife, and are currently heavily regulated in many parts of the world.
Seedbanks—stores of seeds from both cultivated and wild species—may also prove useful in preserving biodiversity in the face of pathogenic activity. Seedbanks have two main benefits. First, they can be used to reintroduce plants that can no longer be found growing in the wild. Second, if we preserve a variety of seeds from each species, the bank stocks can be used to reintroduce specific genes—for example, those conferring resistance to a particular infection—that may have vanished from extant populations.
One of the most important weapons against plant epidemics is, of course, knowledge. Further scientific research will be critical in helping us identify, predict, and respond to the activity of phytopathogens. There is growing interest in improving our understanding of plant disease not just in agricultural crops, but also in wild plants. Because mild infections in native species may become widespread outbreaks in agricultural crops—and vice versa—it is vital that we study infections in a broad range of organisms and habitats. It will be equally important to consider what might happen as various disease strains hybridise and produce novel infectious agents.
Finally, we need to elucidate the ways in which specific human activities alter disease dynamics— and how these anthropogenic effects might act in conjunction with each other and other stressors to impact the spread and emergence of phytopathogens. It will be particularly important to model the possible effects of climate change in a variety of scenarios that differ according to level of mitigation; it is unclear how soon or how intensely we will adjust our behaviour to prevent further climatic variation, and so we need to be prepared for a range of potential pathogenic responses.
Unlike other agents of widespread ecological change, we are in the unique position of being cognizant of our own effects on the natural world. We can significantly reduce the likelihood of plant diseases emergence and spread by making informed decisions about farming and gardening practices, shipment of plant materials, travel practices, and land management (among other things). Perhaps the most important goal, however, is education. By raising awareness and fostering an improved understanding of disease dynamics, we can initiate a broader discussion about what we need to do to prevent both domestic and wild plant species from being eradicated by phytopathogens.
Caitlin Kight is an editor, writer and educator affiliated with the University of Exeter’s Penryn Campus, email@example.com, http://www. caitlinkight.com.
Illustrations: Priya Sebastian
Photographs: International Maize and Wheat Improvement Center (CIMMYT), Ronnie Nijboer, Wikimedia