Dept. of Plant Pathology, Physiology, and Weed ScienceVirginia Tech, Blacksburg, VAabaudoin@vt.edu
The graphic representation shown in Figure 1, the plant disease “doughnut”, has been very helpful to me in discussions of terms such as disease, disorder, injury, and the causes of plant problems as well as to explain that the term “disease” is used with two distinct meanings. To my knowledge, the idea of arranging pathogens in a circle originated with Gary R. Hooper, when he taught introductory plant pathology at Virginia Tech many years ago. I inherited a set of notes from him, including a handwritten sheet with the various kinds of pathogens arranged on a line, and a note to the secretary instructing her to connect the ends of the line into a circle. In hopes that there would be an interesting story here, something similar to Kekulé's dream about a snake eating its own tail and thus conceiving of the ring nature of the benzene molecule, I asked Gary recently whether he remembered how he came up with the circle, but he wrote that his recollection was fuzzy on this point.
Definitions of disease diverge with respect to the range of pathogens included. When I ask students whether they believe hail damage or nitrogen deficiency is a “disease,” most of them don’t think so. In this, they agree with Windham and Windham (2004): “A disease is the result of a dynamic, detrimental relationship between an organism (emphasis added) that parasitizes or interferes with the normal processes of cells or tissue, or both, of the plant. The organism that incites or causes the disease process with the host is called a pathogen. … Plant stresses or plant injuries are not diseases because they are not dynamic; that is, they do not change over time.”
This definition limits “disease” largely to the upper right one-third of Figure 1. This corresponds with plant pathological daily practice. Plant pathology meetings are attended by scientists working with fungi, prokaryotes, viruses, and nematodes, but by very few who focus on abiotic conditions. Almost all publications in plant pathology journals deal with biotic pathogens, whereas abiotic stresses are the purview of agronomic, horticultural, and plant physiological publications.
However, the definition of disease in many other textbooks is much broader. For example, G. N. Agrios (2005, Glossary p. 890) defines disease as "Any malfunctioning of host cells and tissues that results from continuous irritation by a pathogenic agent or environmental factor and leads to development of symptoms.” The Merriam-Webster Online Medical Dictionary (Anonymous 2005) defines disease as: “an impairment of the normal state of the living animal or plant body or one of its parts that interrupts or modifies the performance of the vital functions, is typically manifested by distinguishing signs and symptoms, and is a response to environmental factors (as malnutrition, industrial hazards, or climate), to specific infective agents (as worms, bacteria, or viruses), to inherent defects of the organism (as genetic anomalies), or to combinations of these factors.”
These broader definitions include virtually the entire doughnut (Figure 1), and correspond to medical and clinical practice: we would feel put off if we went to the doctor with an ailment and he or she would say: “Oh, that is abiotic, or a mere injury, I don’t deal with that.” Meetings and journals of the medical profession provide ample coverage of noninfectious diseases such as obesity, hip fracture, malnutrition, bullet injuries, and many cancers.
The same dichotomy is seen in the use of the term pathogen, although broader or narrower use does not always correlate with the broader or narrower concept of disease. Windham and Windham (2004, see above) limit the use of pathogen to organisms. So do Holliday (1998) (pathogen: “an organism, often a micro-organism, a virus or viroid, which causes disease.”), Kenaga (1974) (“A pathogen is an agent that incites infectious disease”), and Agrios (2005) (“pathogenic microorganisms, i.e., the transmissible biotic (=living) agents that can cause disease and are generally referred to as pathogens, usually cause disease in plants by disturbing the metabolism … Environmental factors cause disease in plants when abiotic factors … occur at a level above or below a certain range tolerated by the plants.”). However, Horsfall and Dimond (1960) recognized both animate and inanimate pathogens, and recommended that the term be applied to the latter as well.
Just as the disease triangle can be used in a simple manner to illustrate an important concept, but can also be elaborated upon (Francl 2001), likewise, the disease doughnut can be used to simply illustrate the broad and narrow definitions of plant disease and plant pathogen, but also to discuss a number of additional aspects surrounding these concepts.
The arrangement of pathogens around the doughnut is divided into an abiotic and a biotic side, but the separations are somewhat fuzzy. Although viruses are biotic, are they living? Should genetic abnormalities go on the left or the right side? They are biotic, but they are not transmissible or infectious. The same or even greater fuzziness occurs at the bottom of the circle: when an herbivore eats a plant, the injury could be considered mechanical damage (abiotic), or the herbivore could be considered a biotic agent. If a person (biotic) with a chain saw (abiotic) … well, even some of the broader definitions of disease do not include instances of instantaneous injury, and this is why the circular arrow in the center is left open at the bottom.
Going down the right-hand side of the doughnut, the agents (except for nematodes) are increasingly less likely to get much attention in a plant pathology course, but the separations are not sharp. Parasitic plants clearly fit the “continuous irritation” part of many disease definitions. Feeding by some nematodes causes mainly physical injury or damage, whereas others induce complicated physiological abnormalities that would meet anyone’s definition of disease; the same is true for insects. Hence, the separation between disease and injury is fuzzy, and placed to indicate that for nematodes and insects, each term can be appropriate depending on the characteristics of the specific system.
Similarly on the left-hand side, the separation between injury (considered here as acute injury, due to instantaneous events, although broader definitions exist) and disorder (a more protracted development of a condition) is by no means sharp. For example, chemical injury can develop very quickly (paraquat), or symptoms may require one or more weeks to develop (glyphosate).
The disease doughnut as presented here does not include all possible agents: plasmodiophorids, mollicutes, lightning, excess water (flooding), and others are not mentioned, in an effort to keep it reasonably simple. However, a Powerpoint version is available, which will make it easy to add, move, or delete text items. It may make for an interesting class discussion to ask students to come up with additional possibilities, or to give examples of conditions or symptoms caused by the pathogens shown. One important requirement for accurate diagnosis is to think of all the possibilities.
The doughnut is presented as a vehicle for discussion of concepts rather than to advocate a broader or a narrower definition of disease or pathogen, or to provide a literature review; a more comprehensive discussion with many literature citations may be found in Bos and Parlevliet (1995). Definitions need to be considered in context. In a plant pathology course or textbook, and as a science, we spend by far the most time on the upper right one-third of Figure 1. However, when we wish to diagnose plant problems, we must keep ALL possible causes or incitants in mind, the entire doughnut!
Acknowledgements: development of the original concept by Gary R. Hooper, and helpful suggestions by Wayne A. Sinclair and anonymous PHI reviewers are gratefully acknowledged.
Agrios, G.N. 2005. Plant Pathology (5th edition). Elsevier-Academic Press, San Diego, CA. 922 pp.
Anonymous, 2005. "disease." Merriam-Webster Online Dictionary. http://www2.merriam-webster.com/cgi-bin/mwmednlm?book=Medical&va=disease (accessed 3 Aug. 2007).
Bos, L., and J.E. Parlevliet. 1995. Concepts and Terminology on Plant/Pest Relationships: Toward Consensus in Plant Pathology and Crop Protection. Annual Review of Phytopathology 33:69-102.
Francl, L.J. 2001. The Disease Triangle: A plant pathological paradigm revisited. The Plant Health Instructor. DOI: 10.1094/PHI-T-2001-0517-01Holliday, Paul. 1998. A Dictionary of Plant Pathology. 2nd ed. Cambridge University Press, Cambridge, UK. 560 pp.
Horsfall, J.G. and A.E. Dimond. 1960. The pathogen: the concept of causality. Pages 1-18 in: Plant Pathology, An Advanced Treatise, vol. 2, J.G. Horsfall, and A.E. Dimond, eds. Academic Press, New York.
Kenaga, C. B. 1974. Principles of Phytopathology (2nd ed.). Waveland Press, Prospect Heights, IL. 402 pp.
Windham, M.T. and A.S. Windham. 2004. What is a Disease? Chapter 2 in: R.N. Trigiano, M.T. Windham, and A.S. Windham, eds. Plant Pathology, Concepts and Laboratory Exercises. CRC Press, Boca Raton, FL. 413 pp.