|  In

Contributions of Plant Pathology to the Life Sciences

Dating back to the 1858 text book, Die Krankheiten der Kulturgewaechse, ihre Ursachen und ihre Verhuetung by Julius Kuehn, plant pathology as a field of study is at least 150 years old.  Yet compared with the medical and veterinary sciences, it remains relatively unknown within the life sciences and virtually unknown among the public at large. Even those considered to be leaders in the discipline debated as recently as the 1950s as to whether plant pathology is a science in its own right or only the application of other fields of science.

This debate occurred in spite of many firsts, including: the 1803 report of I. B. Provost on the infectious nature of covered smut of wheat made 73 years before the demonstration by Robert Koch in 1876 that Bacillus anthracis could cause anthrax in cattle; the 1886 paper by Adolf Mayer on transmission of the mosaic disease of tobacco by an agent that could not be seen or cultured, done at the same time Pasteur was attempting to understand the cause of rabies; the 1892 paper read by Dmitrii Ivanowski before the Academy of Science of St.-Petersbourg on the filterable nature of the mosaic disease of tobacco, now accepted as the first report of the filterability of either a plant or animal virus; first use of the term virus, by M. W. Beijerinck in 1898, in reference to the disease-causing agent in the contagium vivum fluidum responsible for the tobacco mosaic; and purification and crystallization of tobacco mosaic virus by Wendell Stanley in 1935, 20 years before the first animal virus (poliomyelitis) was crystallized.

Has the urgent need to control diseases delayed development of plant pathology as a basic science?

Some have asked whether the need to apply the science, i.e serve agriculture generally and farmers more specifically, has interfered with the development of plant pathology as a science.   No doubt the urgent needs to control the myriad of diseases on the hundreds of crops has contributed to what Luis Sequeira referred to as the “lost opportunities in plant pathology,” the result being that some of the major scientific advances have been by investigators from other disciplines that saw opportunities for research in plant pathology.  Indeed, the discoveries on the molecular biology of the plant host/pathogen interaction more than any other area in the plant sciences have led the emergence and growth of plant molecular biology over the past 20 years.  While botany gave rise to plant pathology in the 19th century, plant pathology gave rise to plant molecular biology in the 20th century.  Further to the question of basic versus applied plant pathology, it is significant that, of the two Nobel laureates in plant pathology, Stanley received the Nobel prize in chemistry for fundamental contribution to science—purification and characterization of TMV—and Norman Borlaug, a plant pathologist, received the Nobel Peace prize for his work on the application of science, namely his development of high-yielding varieties of wheat with resistance to rust that sparked the “Green Revolution.”

The contributions listed below to, respectively, virology, mycology, bacteriology, and nematology, represent my list of fundamental contributions that go beyond plant pathology as a science and helped to expand our knowledge in the life sciences more broadly.

Contributions to Virology

Just as advances in molecular plant pathology have set the pace in plant molecular biology, so advances in virology have set the pace in biology.  Some of the key contributions from plant virology include:

  • Stanley’s 1935 report of the chemical purification and crystallization of TMV;
  • First proof that RNA serves as a source of genetic information, based on research by Bawden and associates in the late 1930s on the nucleic acid of TMV;
  • Discovery by T.O. Diener of viroids (infectious, circular, single-stranded RNA), first shown to cause potato spindle tuber formerly thought to be caused by a virus;
  • Development of density gradient ultracentrifugation by Myron Brakke to purify a plant virus, that became a major tool in the development of molecular biology;
  • First demonstration that a plant virus could multiply in an insect vector;
  • Discovery of multipartite viruses; and
  • Discovery of small RNA-based silencing (RNAi) in plants.

Contributions to Mycology

More than any other field in the life sciences, plant pathology has set the pace in mycology going back to the origins of these fields in the mid 1800s.  Some of the specific contributions include:

  • Major and ongoing advances in fungal and oomycete taxonomy;
  • Establishment of aerobiology as a field of science in its own right;
  • Advances in medical and veterinary mycology through research on mycotoxins, and their effects on livestock, allergies caused by fungal spores, ryegrass toxicity to livestock, and many other illnesses of humans and animals caused by fungi;
  • Characterization of specialization in parasitism at the levels of subspecies and sub-subspecies, breeding for disease resistance, clarification of obligate vs. necrotrophic parasistism, and first disease-resistance gene cloned;
  • Flor’s gene-for-gene model for understanding host-parasite genetics, demonstrated first with flax rust, but subsequently shown to also apply to phytopathogenic bacteria, oomycetes, viruses, some insect pests, and plant parasitic nematodes.

Contributions to Phytobacteriology

Phytobacteriology began with the early 20th century debate between the American plant pathologist Erwin F. Smith, who held that bacteria caused plant diseases, and the German microbiologist Alfred Fischer, who held that bacteria were only contaminants and secondary colonists of plant tissues infected by fungi or injured by other causes.  Even with the proof that bacteria cause plant diseases, starting with the 1882 report of T. J. Burrill on the cause of fireblight, early bacterial taxonomists treated bacterial pathogens of plants as a separate taxon, namely the tribe Erwiniaceae [1st edition of Bergey’s Manual], described simply as “plant pathogens.”  Recent seminal contributions of plant pathology to bacteriology include:

  • First avirulence gene cloned and its product characterized, namely the gene responsible for race-specific incompatibility of Pseudomonas syringae pv. glycinia on soya;
  • Discovery of plant-transformation as the basis for the crown gall phenotype, now the basis for production of new crop plant genotypes through “genetic engineering;”
  • Discovery of the type IV secretion systems in bacteria, used in the crown gall bacterium Agrobacterium tumefaciens for transfer of NA;
  • Discovery of ice-nucleating-active (INA) bacteria as incitants of frost injury in plants and now used to make artificial snow;
  • Discovery of the wall-less, helically-shaped motile prokaryotes named spiroplasmas as agents of disease and a new taxon of bacteria, first shown to cause corn stunt, now classified along with mycoplasma-like organisms (MLOs) as  phytoplasma;
  • Discovery of plant growth-promoting rhizobacteria in the rhizospheres of plants.

Contributions to Nematology

Plant pathology has provided the scientific “home” for the origin and growth of nematology as field within the life sciences.  For example, N. A. Cobb (1859-1932) trained as a marine nematologist inGermany, devoted his career the study of plant parasitic nematodes as part of plant pathology inAustraliaand thenHawaiibefore joining the U.S Department of Agriculture and is considered the “father” of nematology.

The serendipity of science – Flor’s gene-for-gene model for understanding the genetics of host-pathogen interaction and discovery of plant-transformation as the basis for the crown gall phenotype are arguably the two most fundamental contributions of plant pathology to the life sciences.  H. H. Flor was doing “mission-linked” research focused on genetic control of flax rust in the North Central states of theUSA.  His proposed model went on to effect a paradigm shift of thinking conceptionally of the diseased tissue as a single phenotype produced by two separate genotypes in the same way that mycorrhizae and lichens are single phenotypes produced by the genotypes of two taxonomically and phylogenetically distinct organisms living as one.  Flor’s model also laid the foundation for research into our modern-day understanding of the molecular biology of host-pathogen interactions, including of innate resistance in plants to pathogens, placing plant pathology at the cutting edge of this area of research within the life sciences.  Surprisingly, this revolutionary understanding of the genetics of host/pathogen interaction has not advanced the ability of plant breeders to manage the ever-adapting populations of plant pathogens beyond the strategies developed by E. C. Stakman dating back to the 1920’s.

Two great contributions of plant pathology as a science and the application of science

The breakthrough-research on crown gall was entirely “curiosity driven” and done in laboratories (the Max Plank Institute in Germany and the University of Washington and Washington University in the USA) quite apart from mainstream agricultural research.  Yet immediately upon the realization that crown gall is the product of the pathogen inserting its own genes into the host genotype so as to “engineer” its host to produce a source of nutrients (the amino acids opine and nopine) unique to its needs, scientists realized the potential of Agrobacterium tumefaciens as a vehicle to move foreign genes into economically important plants.   In slightly more than 10 years (1996), the first of many genetically engineered crops made their appearance in commercial agriculture.  Today, these crops are grown on some 400 million acres in 29 countries.  Discovery of the basis for the crown gall phenotype, while curiosity driven,  has  led to some of the most important and useful applied research in the history of agriculture with potential to both increase food production and reduce the foot print of agriculture on the environment.

Selected Reading

Bawden, F. C., Pirie, N.W., Bernal, J.D.C. and Fankuchen, I.  1936.  Liquid crystalline substances from virus infected plants.  Nature 188:1051.

Black, L.M.  1981.  Recollections and reflections.  Annu. Rev. Phytopathol. 19:1-19.

Brakke, M.K.  1988.  Perspectives on progress in plant virology.  Annu. Rev. Phytopathol. 26:331-350.

Chilton M-D., Drummond, M.H., Merlo, D.I, Scianki, D., Montoyakm A.L., et al.  1977.  Stable incorporation of plasmid DNA into higher plant cells:  the molecular basis of crown gall tumorgenesis.  Cell 11:263-271.

Clay, Keith and Kover, P. X.  1996.  The Red Queen hypothesis and plant/pathogen interactions.  Annu. Rev. Phytopathol. 34:29-30.

Davis, R.E., Worley, J.F., Whitcomb, R.F., Ishijima, R., and Steere, R.L. 1972. Helical filaments produced by a mycoplasmalike organism associated with corn stunt disease.  Science 176:521-523

Flor, H.H.  1955.  Phytopathology 45:680-685.

Gelderblom WCA, Marasas WFO, Vleggaar R, Thiel PG, Cawood ME.  Fumonisins: Isolation, chemical characterization and biological effects.  Mycopathologia 117:11-16.

Goldbach, R. W.  1986.  Molecular evolution of plant RNA viruses.  Annu. Rev.  Phytopathol.  24:289-310.

Kelman, A.  1995.  Contributions of plant pathology to the biological sciences and industry.  Annu. Rev. Phytopathology 33:1-21.

Lindow SE, Arny DC, Upper CD. Distribution of ice nucleation-active bacteria on plants in nature. Appl Environ Microbiol. 1978 Dec; 36:831–838.

Leach, J.E. and White, F.F.  1996.  Bacterial avirulence genes.  Annu. Rev. Phytopathol. 34:153-159.

Marasas WFO, Kellerman TS, Gelderblom WCA, Coetzer JAW, Thiel PG, Van der Lugt JJ. 1988. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme.  Onderstepoort J. Vet. Res. 55:197- 203

Sequeira, L. 2000. Legacy for the millennium:  A century of progress in plant pathology.  Annu. Rev. Phytopathol.  38:1-17.

Stanley, W.M.  1935.  Isolation of a crystalline protein possessing the properties of tobacco mosaic virus.  Science 81:644-645.

Staskawicz, B.J., Dahlbeck, D. and Keen, N.T. 1984.  Cloned avirulence gene of Pseudomonas syringae pv. glycinia determines race specific incompatibility of Glycine max (L.) Merr. Proc. Nat. Acad. Sci. 81:6024-6028.

Starr, M. P. 1984.  Landmarks in the development of phytobacteriology.  Annu. Rev. Phytopathology 22:169-188.

Synder, W.C. 1960. No Apologies.   President’s column Phytopathology 51:865.

Van Larabeke, N., Engler, G., Holsters, M., Van der Elsacker, S., Zaenen, I, Schilperoort, R.A., and Schell, J.  1974.  Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability.  Nature 252:169-170.