Interactions: What guided your decision to dedicate the next stage of your research career to MPMI?
Detlef Weigel: My path to MPMI was rather circuitous. Genetics is my first love, and genetic phenomena of any kind appeal to me. Almost 15 years ago, Janne Lempe and Kirsten Bomblies in my lab discovered a syndrome of Arabidopsis hybrid weakness that we at first interpreted as a developmental abnormality. We quickly learned that this syndrome was not specific to Arabidopsis spp. and that it was already well known from many wild and cultivated plants, for which it is called “hybrid necrosis.” Anybody in the MPMI field knows that necrosis is often a hallmark of pathogen infection. Nevertheless, we were apparently the first ones to recognize that inappropriate immune reactions in the absence of pathogens were most likely the defining characteristics of this phenomenon, rather than developmental defects.
For us, one of the attractions of studying hybrid necrosis was that we thought it would teach us about speciation, but after many thousands of crosses and having cloned quite a few of the causal genes, we realized that hybrid necrosis has much more to do with how the plant balances the demands on its immune system. With too little immunity, the plant will succumb too quickly to infection, but with too much immunity, the plant will damage itself. Hybrid necrosis occurs when components of the immune system are mismatched, and these components begin to signal even if there is no pathogen trigger. Satisfyingly, the molecular observations in Arabidopsis spp. seemed to match similar observations in several other species. As a matter of fact, with hindsight we realized that the first case of hybrid necrosis that was molecularly understood predated our own work in Arabidopsis—namely, the study of the tomato Cf-2/Rcr3 system by Jonathan Jones.
In parallel with our efforts to clone the causal genes for hybrid necrosis in Arabidopsis spp., we could confirm through our whole-genome resequencing and sequencing studies that immune genes—particularly those of the NLR class but also of other smaller families—are the most diverse genes in the Arabidopsis genome. This, in turn, made us wonder what drives this diversity—hence, our current obsession with trying to understand the relationship between Arabidopsis and its natural pathogens in the real world.
I: What do you see as the next big challenge in this field of research?
DW: The MPMI field has already revealed in exquisite detail many of the molecular mechanisms that allow pathogenic and symbiotic microbes to infect plants, as well as a plethora of mechanisms that plants use to either accommodate or ward off microbes. It is also clear that many of these molecular interactions are evolutionarily very fluid—perhaps the best example being the ease with which pathogens often jettison effectors. However, what this means in an ecological context is much less obvious. I therefore see as a big challenge how we can integrate the advanced molecular knowledge with an understanding of the interaction between wild plants and their microbes in the real world and how this changes over ecological and evolutionary time scales. To begin to dissect these, we need to know much more not only about the spatial and temporal distribution of hosts and microbes but also about their fine-scale genetic variation in effectors, resistance genes, and so on. My dream is to learn how genetic diversity in wild plant species maps onto the diversity of their microbiota (and vice versa) and what genetic, molecular, and ecological mechanisms relate the two. To this end, we recently started an ambitious effort, which we call “Patho(gens in Arabi)dopsis,” or “Pathodopsis” for short, to generate such foundational data. It would be fantastic to initiate such efforts in many other species. So far, the focus has mostly been on local populations, such as the impressive long-term studies by Anna-Liisa Laine in Finland and Jeremy Burdon and colleagues in Australia. I would love to see the sorts of insights they have gathered across the entire geographic ranges of many different plant species.
I: Symbiotic relationships between plants and microbes have been occurring for hundreds of millions of years, and we are only studying a tiny “snapshot” in the history of these interactions. How can we extrapolate our observations to better understand MPMI and improve the resistance capacity of agricultural crops?
DW: I agree that we need to have a better understanding of how wild plant pathosystems are different from agricultural systems. Whether the information from the wild systems is directly useful for agricultural systems is difficult to know beforehand, although it is probably safe to assume that increased immune system diversity in individual agricultural fields would most likely be helpful—an idea that has been advocated, for example, by Bruce McDonald. I like to think that with agriculture, we have often “broken” long-term stable interactions, and we need to learn what confers long-term stability before we can fix the broken state. I realize that to this end, I need to learn a lot more ecology, and I am benefitting in this area greatly from my collaboration with Joy Bergelson.
I: Your recent paper in PLoS Genetics highlights how interactions between NLRs from different species might affect the fitness of progeny. Do you feel that NLR interactions are a driving force in speciation?
DW: It is an attractive hypothesis, and I would not be surprised if there are cases of speciation or population divergence caused by inappropriate NLR interactions, but they are unlikely to be major drivers, because NLR variants typically do not become fixed in species. Having said this, there is a minority of NLR genes that seem to have very little, if any, variability, and these highly conserved NLR genes probably deserve more attention.
I: Do you plan to continue your research on plant development and adaptation? What do you hope to gain from your IS-MPMI membership?
DW: There is very little developmental work going on in my lab these days, as we have pivoted almost completely to genomic variation and plant immunity. As plant biologists, we are sometimes annoyed when animal biologists lump us all together simply because we all study plants, but I actually see this as a great advantage of our field. Beginning with the very first Arabidopsis conference that I attended in 1990, a large fraction of the plant meetings I have gone to have included at least a bit of plant immunity. Moreover, at the Salk Institute, I worked next to the late Chris Lamb, who was an important early figure in MPMI, and I have been lucky enough to have had Jeff Dangl as a friend for many years—a friendship that eventually turned into a very productive and enjoyable long-term collaboration. In addition, I have had the good fortune of having served on the board of The Sainsbury Laboratory (TSL) for several years, where I have received a tremendous education in MPMI from colleagues such as Cyril Zipfel, Sophien Kamoun, Silke Robatzek, David Baulcombe, and John Rathjen.
Even though I’m still somewhat of an amateur when it comes to MPMI, it is what I think about most these days, so it seemed only natural to join IS-MPMI. Not a small contributor to this step was that I have come to know the work of the three most recent IS-MPMI presidents very well: Sophien Kamoun’s work because of my association with the TSL and also through several collaborative projects, Sheng Yang He’s work because of my recently emerged interest in Pseudomonas biology, and Regine Kahmann’s work because she is a Max Planck colleague with whom I meet very regularly.
I: Much of your research engages interdisciplinary and international interactions. What methods/tools do you use to initiate and foster these interactions?
DW: Tool number 1: an open mind. I strongly believe that almost everybody we meet can teach us something—both inside and outside science. In other words, if one respects others and their research, even if it’s not automatically one’s own “cup of tea,” then productive interactions with a wide range of colleagues, both in different disciplines and in a wide range of institutions, are essentially preprogrammed.
I: Many students and some early post-docs are undecided on their ultimate career paths academia/industry/government/other). What advice do you give students and early post-docs in your research group who might need help making this decision?
DW: Many colleagues, both old and young, equate science only with academia, which is very shortsighted. Science has many different incarnations, from blue-sky discovery to translational and applied research, but also when we use the tools of scientific thinking and reasoning to make the world around us a better place. In the end, it is about personal proclivities and what career paths best fit one’s own personality along with the demands of family and friends. Somebody who is geographically more constrained because of a partner or parents must, of course, be more open minded about different careers—which is perfectly OK!
