Plant breeders face a conundrum when it comes to plant diseases. The most powerful disease resistance genes, if not managed well, will quickly become useless.
Plants have an innate immune system that recognizes certain molecules that are typically found on pathogens. When a microbe presenting a typical molecular signature enters a plant, the plant basically bleaches the area using highly reactive oxygen compounds. The plant then activates genes that insure the microbe will not spread. However, successful pathogens overcome the innate immune system using molecules called “effectors” that disable components of the plant’s detection or response system.
The story does not end there, though. Thanks to Darwinian evolution, plant populations can develop resistance to pathogens. A dramatic form of resistance is the so-called R gene, the major resistance gene. If a pathogen possessing a single potent effector arrives, it will run rampant in a population of its host species. However, natural plant populations are typically very diverse. Any individual plant that happens to have an R gene that matches the pathogen’s effector allows it to recognize the effector and turn on its so-called hypersensitive response. Microbes with effectors are considered so dangerous that the plant will go crazy bleaching the point of entry until all cells in the area, pathogen and host, are dead. The result is an inconspicuous dot of dead tissue that shows where a pathogen attempted penetration.
In a natural population, the plant with the R gene will outlive its susceptible neighbors and pass this gene on to its progeny. In agriculture, this type of gene is highly sought by breeders aiming to develop resistant crop lines. A field of plants with the R gene will stand firm against the onslaught of a pathogen, growing robustly and giving their full yield where susceptible plants would turn out stunted, discolored, deformed, or dead.
In a further turn of evolution, however, the pathogen population can include individuals with a novel effector gene that allows them to disable a plant’s R gene and carry out its invasion of the plant’s tissues. These individual pathogens will reproduce thousands of progeny that are able to infect all the resistant plants. The pathogen has broken through the resistance. This is a common event, as a pathogen’s lifestyle depends on infecting plants, and therefore it is built to evolve new effectors quickly.
Another type of resistance is partial resistance, termed QTL, for Quantitative Trait Loci. In this case, instead of a single gene in the plant that acts as a tripwire for the pathogen’s effector, the plant has various traits that make it harder for the pathogen to carry out its lifecycle. Perhaps the plant’s external surface is harder for the pathogen to traverse, or one of the plant’s targeted enzymes is only partially disabled, or the plant produces a metabolite that slows the pathogen’s growth. Any single gene for partial resistance buys the plant only a partial or temporary escape from the ravages of the disease, but if many of these genes are present in an individual, that individual can be as resistant to the pathogen as if it had the appropriate R gene.
As you can imagine, partial resistance genes are more work for plant breeders. The QTL-resistant crop varieties they release must have multiple genes bred into them, or “stacked”. There is an advantage, though, in that the odds of any pathogen individual having enough genetic mutations to overcome all the resistance genes is essentially zero. In fact, breeders could stack multiple R genes in the crop varieties they release as well and enjoy the same odds against breakthrough, but expediency often overrules prudence when disease threatens. Furthermore, if one breeder expends the time and resources to stack R genes while other breeders release varieties with single R genes, the pathogens may break through the single R genes one by one, and the crop line with the stacked R genes may end up with few or just one functioning resistance gene. In that case, the pathogen population may be only one mutation away from breaking through the stack.
Plant pathologists are thus perennially concerned about release of resistance genes in seeds to farmers, but releases are often out of the control of the plant pathology commmunity. The network structure of plant pathologists, breeders, non-profit germplasm repositories, agribusiness corporations, and farmers presents a complex adaptive system where each actor has its own incentives, all of whom interact to produce the dynamics of resistance gene diffusion across the globe, both prudent and expedient. Karen Garrett and her plant pathology and plant breeding colleagues have looked into these dynamics using an epidemiological approach, published recently in Phytopathology.
Garrett et al. examine network structure for four staple crops: cassava, potato, rice, and wheat. The result is four abstract diagrams, evocative respectively of a double spiderweb, the tentacles of a sea anemone, a time-lapse photo of flocks of birds taking flight, and spaghetti with cheese flowing off a plate, all with colorful circles and squares on the periphery and black ones in the center. The central black circles show the centrality of the non-profit International Agricultural Research Centers, the IARCs. The other colors are codes for the continents where the different actors are located. Arrays of black squares represent private multinational companies, clustered near the center for potato and wheat, less obtrusive for cassava and rice.
The dots and squares on the periphery are segregated by color, signifying a dearth of direct connectivity between continents or regions. In terms of resistance gene diffusion, this means that there is no easy way for resistance genes from one continent to be bred into another continent’s crop, potentially leaving some areas without optimum disease protection. However, from the perspective of pathogen evolution, it could be helpful to have different resistance gene profiles in different regions to reduce the likelihood of the emergence of a super-strain able to infect the entire world crop. Also, less movement of the plant material containing the resistance genes means less likelihood of bringing hitchhiking pests and pathogens to new regions.
The reason for the four diagrams’ different arrangements of black squares — representing the international-scale private breeders — is the privileged position of some of their non-profit counterparts, the IARCs. In the case of cassava, a staple in tropical Africa and Latin America, the entire network is small, making the lone black square look rather incongruous and with very few connections. Private corporations seek out crops with the largest markets, and cassava is not one of them. In the case of rice, the authors explain that the international centers have played such a dominant role in the development of major resistance genes toward bacterial blight and rice blast diseases that there has been little profit incentive for the entry of private companies into the network. On the opposite extreme is wheat, for which several multinational corporations have extensive germplasm collections and have highly connected black squares in the network diagram. For potato there are similarly black squares in a more central position, but a closer look also reveals a proliferation of red squares on one side of the abstract anemone, representing a large number of private interests in wealthy Europe.
The abstract diagrams and their underlying analysis is a work in progress. The idea is to provide insight into what-if questions, such as how resilient a network would be if a major hub should disappear, such as the recent abandonment of the seed collection at the International Center for Agricultural Research in the Dry Areas in Aleppo, Syria (the Center was reconstituted in Lebanon and Morocco with backup seeds from the Svalbard vault). This type of change in a network would be unfeasible to test in an experiment, but past performance of the existing networks in terms of R gene diffusion and lag times can provide insights into the robustness of the complex adaptive system, as well as whether the networks themselves can be shaped by institutions embedded within them, e.g. the IARCs.
An observation by the authors is that private breeders tend to weaken the structure of the overall network. Whereas non-profit breeders’ focus is on providing farmers with plant material containing resistance genes, and ideally getting feedback on their performance from the farmers, private breeders have an incentive to hoard crop germplasm resources and release only those resistance genes that will make them a profit. Because of pro-corporate intellectual property laws and the development of biotechnology and hybrid varieties, private breeders are proliferating. The authors point out that private breeders focusing on more profitable markets enjoy a funding advantage for research over the constrained resources of the international research centers, thus allowing them to more quickly coordinate the release of resistant material. Poorer farmers have derived some benefit in the past due to trickle-down effects of resources originally directed at richer farmers.
A response to the privatization trend is the rise of open-source breeding movements, but the authors are unable to evaluate the effect of these efforts on breeding networks. Another shortcoming of the analysis, and of the underlying networks themselves, is the emphasis on staple crops. Traditional agriculture depended on a dizzying diversity of crops that is hard to fathom from the perspective of modern agriculture. This diversity provided an economic resilience to farmers as well as environmental services that benefited the crop plants, both of which have been replaced in modern low-diversity agroecosystems by continuous subsidies, in forms that range from pesticide development to resistance-gene prospecting to famine relief. A research focus on a handful of crops has promoted this low diversity, to the detriment of not just the environment but also human diet. While a big-picture analysis of the diffusion of resistance genes is an improvement over uncoordinated efforts to fight local outbreaks or to make a profit, such analysis must also be viewed as a small piece of the overarching big picture that is agriculture.
I really appreciate the clear description of the R gene and how it works against plant pathogens, as well as the idea of stacking resistant genes. The potential for durable resistance is high. But as you also explain, modern agriculture’s emphasis on profit from private breeding and embedding this breeding in monoculture systems quickly breaks down resistance. Diversification is necessary, but food system change that promotes diversification must come first.