A scientific detective story

Our latest paper required a deep dive into the history of plant pathology

Today my colleagues and I are pleased to present our new paper on the Geometry and Evolution of the Ecological Niche in Plant-Associated Microbes in Nature Communications. The paper describes the temperature responses and host ranges of hundreds of fungi and oomycetes that attack agricultural crops and trees. There are three main findings:

  1. The temperature range at which biological processes occur in plant pathogens is narrower when they are interacting with the plant host than when they are growing in culture. We interpret this as direct experimental evidence that the realized niche is smaller than the fundamental niche. In the past, the narrower realized niche has largely been inferred from geographical species distributions.
  2. The differentiation between ecological specialists and generalists does not hold. The literature on ecological niche breadth rarely considers that the niche, according to G. E. Hutchinson, can be thought of as an n-dimensional hypervolume where each dimension represents an abiotic condition or biotic resource on which the species may specialize. By comparing niche breadth of temperature responses with niche breadth of host range, we show that pathogens can be generalists or specialists independently on either axis. We term this “Jack of some trades, master of others“, compared with the usual description of generalists as “Jack of all trades, master of none”.
  3. The niche is evolutionarily labile. By comparing the phylogenies of Phytophthora species, we showed that the niches can evolve rapidly in plant pathogens, making them formidable enemies to farmers and foresters.

Our methods and findings are described in great detail in the article and supporting materials, which are freely available online. Here we’ll focus on the main dataset we compiled, which is also available on the Data Dryad repository here (NB the data set is still being prepared by Dryad hence may not be available for a few days).

Back in 2014 I was reading about plant pathogen epidemiological models, specifically those employing temperature as predictors of disease risk. An excellent paper by Roger Magarey and colleagues at North Carolina State University had compiled cardinal temperatures (i.e. minimum, optimum and maximum) of infection by a number of plant pathogens, for use in a simple infection model. The paper also mentioned a book which contained similar data for hundreds of plant pathogens. That book was Biological characters of plant pathogens: temperature relations by Kogo Togashi, published in 1949 by Meibundo press in Japan.

Biological Characters of Plant Pathogens: Temperature Relations by Kogo Togashi (1949)

Intrigued, I searched Abebooks and found a single copy for sale, from antiquarian scientific bookseller Hermann L. Strack in France. Paying my £49.28, I awaited the arrival of The Book. It was genuinely exciting to open this treasure trove of historical data. Hundreds of pages of experimental data and results obtained from a literature review conducted by Togashi in the 1930s. According to the frontmatter:

The author has sought to assemble the data on the temperature relations of a large number of bacterial and fungal plant pathogens, which are arranged in alphabetical order and supplemented by an extensive bibliography and a list of synonyms. The manuscript of this valuable compilation was completed in 1935 and has been revised down to the end of 1936, mostly at the Departments of Plant Pathology of the Universities of Wisconsin and Cornell.

K. Togashi (1949)

Kogo Togashi was a fungal plant pathologist working at the Morioka Imperial College of Agriculture and Forestry from the 1930s to the 1950s (judging from his online publication record). The beautiful building is now the Historical Museum for Agricultural Education of the Faculty of Agriculture, Iwate University.

The former Morioka Imperial College of Agriculture and Forestry

The book came with another interesting historical note. The inside cover contains a rather lovely Ex Libris sticker of one J. Nash-Wortham, who was a pathologist at the Alice Holt research station of Forest Research in the UK.

Former owner of The Book

While the data within the book were very old, collected a century ago or more, we were relatively confident that those scientists were more than capable of measuring temperatures accurately (comparison of the data with more recent estimates confirmed this). SWBIO DTP doctoral student Tom Chaloner bravely took up the challenge of digitizing the data in the book. This monumental task, which involved deep and extensive cross-referencing of species names that have often changed several times over the past century, finally resulted in the dataset we have submitted to Dryad and the paper we published today.

In the era of climate change and growing concern over global food security, understanding plant pathogen temperature responses is an important part of predicting and managing their impacts on crop production. We hope that the Togashi Dataset will serve as a focal point for continued improvement of our understanding of these important microbes.

References

Chaloner, T. M., Gurr, S. J., & Bebber, D. P. (2020). Geometry and evolution of the ecological niche in plant-associated microbes. Nature Communications, 11(1), 2955. https://doi.org/10.1038/s41467-020-16778-5

Bebber, D. P., Chaloner, T. M., & Gurr, S. J. (2020). Fungal and Oomycete cardinal temperatures (the Togashi dataset) (Version 4, p. 2424892 bytes) [Data set]. Dryad. https://doi.org/10.5061/DRYAD.TQJQ2BVW6

Togashi, K. (1949). Biological characters of plant pathogens: temperature relations. Meibundo.

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