The Poetry of Mycological Accomplishment and Challenge

fungal biology reviews 25 (2011) 3e13 journal homepage: www.elsevier.com/locate/fbr Keynote Paper 5 The poetry of mycological accomplishment and challenge John W. TAYLOR Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102, USA article info abstract Article history: Adaptation is the evolutionary process that has given us the remarkable diversity of fungi Received 18 January 2011 and I cannot think of a theme better suited to bringing together the wide variety of topics at Accepted 18 January 2011 this congress: pathogenicity, cell biology, genomics, evolution and ecology. It is also a timely theme because the latest biological innovation, genomics, has stimulated new Keywords: thinking about the types of genetic variation and subsequent selection that enable adapta- Adaptation tion. For more than half a century the Modern Synthesis of natural selection and genetics Biotrophs has provided the framework for evolutionary inquiry as reviewed by Kutschera and Niklas Complex multicellularity (2004). The Modern Synthesis is focused on point mutations as the mode of genetic varia- Comparative genomics tion, but genomics has emphasized the role of gene loss and gene gain by duplication or Evolutionary cost horizontal transfer in generating genetic variation. Likely, the Modern Synthesis can be Gene family expansion and stretched to accommodate these new processes, as it was to accommodate neutral evolu- contraction tion (Pigliucci, 2007). However, there are those who are calling for a new synthesis and I Necrotrophs encourage mycologists to take a look at these proposals because fungi may be the organ- Septal pores isms of choice in testing these ideas (Koonin, 2009a, b). Woronin bodes ª 2011 Published by Elsevier Ltd on behalf of The British Mycological Society. Adaptation in fungi is a theme with an abundance of mate- An’ lea’e us nought but grief an’ pain rial due to the efforts of many mycologists and I have time For promis’d joy! for just three stories that showcase these accomplishments. At the same time, great challenges remain and I aim to I’m ashamed to admit that when I spring this poem on my highlight these, as well. My title promises more than friends in Berkeley, they ask, as often as not, “It’s Shake- science, it promises poetry. There being a rich tradition of speare, isn’t it?” That is not a mistake that would be made poetry in Scotland, I’ll begin with the most famous stanza in Edinburgh because To a Mouse is the work of the bard of of what is possibly the most famous Scottish poem, “To Scotland, Robert Burns (Fig. 1). aMouse.” 1. Pathogenesis But Mousie, thou art no’ thy lane, In proving foresight may be vain: Keeping Burn’s thoughts in mind, I’ll begin with a story of The best-laid schemes 0’ Mice an’ Men, Gang aft agley, adaptation in pathogenesis. We’ll start with flax rust, the 5 The opportunity to open an International Mycological Congress is a singular honor and I offer my sincere thanks to Nick Read, Chair of the IMC9 program committee, and its membership: Simon Avery, Nicholas Clipson, Geoff Gadd, Neil Gow and Geoff Robson. Thanks also are due to Neil Gow for his thoughtful introduction and Nina Cosgrove and her crew from Elsevier for implementing the committee’s vision for this glorious congress. E-mail address: [email protected] 1749-4613/$ e see front matter ª 2011 Published by Elsevier Ltd on behalf of The British Mycological Society. doi:10.1016/j.fbr.2011.01.005 4 J. W. Taylor Fig. 1 e Portrait of Robert Burns by Alexander Nasmyth 1787, Scottish National Portrait Gallery. Fig. 2 e Flax rust, Melampsora lini Lev., showing orange uredinia on flax, Linum sp. Reproduced from the cover of the Plant Cell, Ellis et al. (2007). disease of Linum species caused by the rust, Melampsora lini (Fig. 2), and follow it to North Dakota. The gene-for-gene hypothesis to explain host resistance and pathogen aviru- et al., 2010; Stukenbrock and McDonald, 2007). Of course, lence was developed in that state by Flor in mid-twentieth there is a cost to resistance (Korves and Bergelson, 2004; century. It was the first study of the genetics of both host Tian et al.,2003), and questions about this cost have arisen and parasite and represents one of the great accomplish- as plans are made to add stacks of resistance genes to ments of mycology (Flor, 1971). For biotrophic pathogens, crops (Rausher, 2001; Stuiver and Custers, 2001), although like rusts and powdery mildews, the recognition of pathogen-produced avirulence gene products (effectors) by plant-produced resistance gene (R genes) products, and the ensuing plant hypersensitive response, has driven a tremendous amount of basic research and practical plant breeding (Chisholm et al., 2006; Jones and Dangl, 2006). We now know that molecules associated with fungi, for example, chitin or ergosterol, collectively known as pathogen-associated molecular patterns (PAMPs), are recog- nized by plants, which then mount generalized responses, such as, callose deposition to thicken cell walls or the production of reactive oxygen species, in a process termed PAMP-triggered immunity (PTI). Not surprisingly, biotrophic fungi have evolvedeffectors,whichdisrupt the PTI. Equally not surprisingly, plants have evolved R genes to recognize effectors and, through subsequent pro- grammed cell death, kill the plant cell harboring the biotroph, thereby starving it (termed effector-triggered Fig. 3 e Diagram of the evolution of plant immunity begin- immunity, ETI). Studies of the evolution of effectors and ning with pathogen-associated molecular patterns (PAMPS) R genes document the evolutionary back and fourth that lead to PAMP-triggered immunity and progressing to (Fig. 3) associated with avoidance of detection by the path- effectors, plant resistance genes (Avr-R) and effector-trig- ogens and restoration of detection by the plant (Anderson gered immunity. Modified from Jones and Dangl (2006). Mycological accomplishment and challenge 5 farmers seem willing to suffer a known, regular loss to cell biology, I am going south to England for a poem oft found avoid a catastrophic one. in American middle-school anthologies, Percy Bysse Shelly’s Alas, most of the work on gene-for-gene hypothesis has Ozymandias. Shelly and his poet friend, Horace Smith, considered the interaction of just one pathogen and one competed to write a sonnet about the statue of Ramesses II host, but plants in nature face more than one parasite and in the British Museum (Fig. 4). Shelly’s, below, is viewed as not all of them are biotrophs. Consider the necrotrophs, path- one of the most perfect sonnets ever written. ogens that kill plant cells with toxins and then feast on the Ozymandias. dead cells (Govrin and Levine, 2000). Recently it has been shown that the toxins produced by these fungi, e.g., Phaeos- I met a traveller from an antique land phaeria nodorum and Pyrenophora tritici-repens (many of them Who said: Two vast and trunkless legs of stone seem to be Dothideomycetes), are akin to elicitors and they Stand in the desert. Near them, on the sand, target plant resistance genes to turn on the plant hypersensi- Half sunk, a shattered visage lies, whose frown tive response (Friesen et al., 2008). Whereas killing the cell in And wrinkled lip, and sneer of cold command which the fungus resides is a good strategy for stopping a bio- Tell that its sculptor well those passions read troph, it is exactly the wrong response for a necrotroph. As Which yet survive, stamped on these lifeless things, expected, in this inverse gene-for-gene system there is The hand that mocked them and the heart that fed: evidence for evolutionary “arms races” or “trench warfare” And on the pedestal these words appear: with a premium for plants whose resistance genes now fail “My name is Ozymandias, king of kings: to interact with elicitors turned toxins, and fungal toxins Look on my works, ye Mighty, and despair!” that keep pace with changes in resistance genes Nothing beside remains. Round the decay (Stukenbrock and McDonald, 2009). When both biotrophs Of that colossal wreck, boundless and bare and necrotrophs are considered, the true cost of extra R genes The lone and level sands stretch far away becomes apparent, because each additional R gene that protects against a biotroph invites a new necrotroph. In fact, I chose this poem because it deals with a large, complex the effect of additional R genes is additive for necrotrophs; structure, the statue of Ozymandias, which I will liken to the the more interactions between R genes and effectors that act large complex fruiting bodies made by Pezizomycotina and like toxins, the more disease (Friesen et al., 2007). The Agaricomycotina (Fig. 5). I also like it because it addresses emphasis on resistance for biotrophs has contributed, along hubris, here defined as a lack of humility before the gods. In with changes in tillage and climate, to an emergence of ancient Greece, hubris did not go unpunished. Punishment necrotrophs. Clearly, the challenge is to develop crops that was the task for Nemesis, who, with her lamp and sword, resist both biotrophs and necrotrophs. However, current tracked the transgressors. I’ll come back to Nemesis because research suggests that it will not be simple. Take oat, for some cell biologists are venturing perilously close to hubris. example, where the same R gene acts to protect against the biotroph, Puccinia coronata var. avenae, and enable the necrotroph, Cochliobolus victoriae (Lorang et al., 2007). To sum up the conundrum of protecting against biotrophs and necrotrophs, it is hard to do better than the Scottish Bard, “The best laid plans of mice and men gang aft aglay .” As a last thought about pathogenesis, could there be rele- vance of the findings about plant pathogens to medical mycology? The plant R genes are typically cell surface molecules with nuclear binding, lysine rich repeats (Jones and Dangl, 2006).

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