Practical Biodiversity: Keeping Oat on Farms by Helping Farmers Enhance Disease Resistance

Increased domestic production of oat with its economic and environmental benefits is impeded by oat susceptibility to crown rust (Puccinia coronata Corda). Simple variety blends have recently been successful in rice, wheat, and barley: blend components were all top agronomic varieties and combining them reduced disease. The epidemiological mechanisms of blend effects entail that this approach be tested in very large plots as are used in on-farm research.

We evaluated 19 commercially available oat varieties for their resistances to specific pathogen isolates and chose to test the blend of three that were divergent. In three years of on-farm testing at eight locations per year (four in Minnesota and four in Iowa) the blend experienced significantly less rust severity and yielded significantly more than the average of the component varieties grown in pure stands. While we believe that this simple ecological diversity technology could benefit farmers who grow oats, the infrastructure for collecting and disseminating the necessary information and knowledge are not trivial.

Introduction:

The loss of crop diversity in the Upper Midwest has lead to increased pathogen and insect pest problems in the remaining crops. Though Midwest agriculture has turned away from oat (Avena sativa L.), it has a long history on farms in the U.S. and remains a critical component of most sustainable farms. An oat crop breaks weed and pathogen cycles, builds soil tilth, protects soil from erosion, scavenges nutrients left from other crops, can serve as a nurse crop for the establishment of forages, and provides an irreplaceable feed ingredient for young livestock. Disruption of corn and soybean pests by oat reduces input costs and increases yields of these crops and improves returns to farmers while oat also diminishes the row crops’ potential negative environmental impacts.

Increased domestic production of oat with its economic and environmental benefits is impeded by oat susceptibility to crown rust (Puccinia coronata Corda). While crown rust is not always severe, it can be devastating, and this variability may dissuade farmers from planting oat. Yield statistics understate the economic impact of rust epidemics, which can lower grain quality below market grade. Breeders have sought to enhance oat crown rust resistance using single-gene resistances introgressed from wild relatives. The pathogen, however, has rapidly evolved virulence to all such single-gene approaches. Thus, the use of genetic resistance for disease management poses two problems. First, how can resistance be used to minimize disease severity in the crop? Second, how can the evolution of pathogen virulence be managed? Increasing host-crop diversity by planting variety blends rather than single varieties can reduce disease severity and delay the evolution of pathogen virulence and has been long recognized but insufficiently explored. In the 1950s, an ecological approach was pursued against crown rust: “multiline” oat varieties were bred for diversity in disease resistance but uniformity in other traits. Though multilines managed both disease severity and virulence evolution, they were not adopted because they performed less well agronomically and were expensive to maintain. Simple variety blends, however, have recently been successful in rice, wheat, and barley: blend components were all top agronomic varieties and combining them dramatically reduced disease. The epidemiological mechanisms of blend effects entail that this approach be tested in very large plots as are used in on-farm research.

A significant proportion of variety improvement efforts are devoted to increasing crop resistance. We review crop-pathogen interactions, at the level of the plant then, from an ecological perspective, at the level of the plant population. We discuss approaches to improve resistance within the constraints imposed by the biology and genetics of resistance.

Plants possess mechanisms of resistance that are either simply inherited (monogenic resistance), or that derive from multiple genes and their interactions with each other and the environment (polygenic resistance). In single gene resistances, the gene in the host plant enables it to recognize the product of a single gene in the pathogen; this form of resistance is called gene-for-gene resistance. A salient feature of single-gene resistances is the dramatic differences in virulence that they elicit between pathogen races. In particular, pathogen races that carry the gene whose product the host recognizes are avirulent, while genotypes that do not carry such a gene can be highly virulent. There are no accepted models for the mechanisms that underlie polygenic resistances to disease. These resistances differ in their phenomenology in two important ways from single-gene resistances. First, the resistance is generally not complete, but partial. Second, differences among pathogen races in virulence are not as great against polygenic as against monogenic resistances. In addition to these plant-level resistances, a population-level mechanism contributes to preventing explosive disease epidemics. Natural populations of a plant species exist as complex blends of genotypes in which components differ in their single-gene and polygenic resistances. There are many mechanisms through which blends protect components from disease, which we will detail below.

These characteristics of resistances have had important consequences on breeding approaches to disease resistance. Incorporating monogenic resistances provides the easiest and most rapid solution. Single-gene resistances have therefore been used longest and most widely by plant breeders. The reliance on single-gene resistances has met with short-term success but long-term failure. When a novel single gene is introduced into a variety, the dramatic resistance that it provides often leads that variety, or others possessing the same gene, to be grown over large areas. At the same time, pathogen races that are virulent against that gene have a very strong selective advantage and proliferate, “defeating” the resistance gene. Shifts in crown rust populations that defeat resistance genes have been swift: single genes, once released in varieties, have lost effectiveness in less than five years.

In response to these pathogen population shifts, crop breeders have developed strategies that include gene pyramiding, selection for partial resistance, and the development of multilines. Gene pyramiding involves the introgression of two or more effective resistance genes into a single pure-line variety. Gene pyramids have sometimes retained effectiveness and sometimes have been defeated. Pyramids are more difficult to breed than single gene introgressions. Selection for partial resistances involves handling disease resistance as a quantitative trait, seeking to increase the frequencies of the genes that have small but favorable effects. The heritability of partial resistance is generally reported to be low. Selecting partial resistance in the presence of segregating single-gene resistances is difficult.

Two approaches to increasing host diversity have been considered, variety blends and multilines. Variety blends involve physically mixing the seed of varieties bred as pure lines. Multilines involve selecting a single agronomically adapted variety and creating several sublines of that variety, with each subline containing a distinct single-gene resistance. Each subline derives from the simple but time-consuming process of crossing the variety to a carrier of the single-gene resistance of interest, then repeatedly back-crossing progeny to the original variety. The subline becomes genetically almost identical to the original variety, with the exception of the new resistance gene. The multiline variety is then also produced by physically mixing the seed of the sublines. Given these different approaches, the individual oat plants of a field planted to a multiline will be virtually identical for their polygenic resistances. In contrast, the individual plants of a blend will differ in both their monogenic and polygenic resistances, and added diversity that may confer overall resistance benefits.

Variety blends enjoy several advantages over multilines. In the 1960's the Iowa Experiment Station released two multiline varieties that were quite effective in preventing economic losses from crown rust but never became popular because, by the time the multiline had been created, the single variety forming the basis of the multiline had become agronomically obsolete. A major breeding advantage of variety blends is that current agronomically competitive varieties can be used. Other advantages include that variety seed sources are easier and less expensive to maintain than multiline seed sources; creation of multilines are a burden to breeding programs that must also develop pure-breeding varieties; and most importantly, variety blends are controlled by farmers, who can tailor them to their farms, while multilines are controlled by breeding programs.

Biological Bases for Variety Blend Efficacy

The reduction in disease severity in variety blends may arise from several factors. Probably the most important cause of reduced disease is the reduction in the proportion of susceptible host plants available for infection. Because only a fraction of the pathogen population will be virulent on any component of a blend, pathogen infection efficiency decreases. The reduced frequency of susceptible plants also means that susceptible plants are physically further apart, which slows the spread of disease from plant to plant in the blend. Resistant host plants may also physically block the dispersal of inoculum between susceptible plants. Compensation and competition among host plants may also play an important role. Disease will affect competitive ability of blend components, leading to increased production by resistant components. Thus, the impact of an equal amount of disease may be less in the blend than in a monoculture.

Another possible mechanism of the blend effect in reducing disease may be induced resistance. An incompatible reaction around an infection site may prevent subsequent infection by an otherwise compatible isolate of the pathogen. Since blends may maintain more variable pathogen populations and high proportions of races avirulent to blend components, they may also enhance induced resistance effects. Competition between pathogen races may also play a role in the blend effect. Modeling of competition between races of stem rust (Puccinia graminis Pers. sp. tritici) of wheat has shown that the more competitive races may not be the most virulent. Finally, in a variety blend, even if two components lack major gene resistances, they will have different polygenic resistances to which some virulent races will not be adapted. Thus blends may have an important biological advantage over multilines: they provide diversity for polygenic and single-gene resistance. Similarly, the variety blend may also beneficial diversity for other traits. Diversity in resistance to other pests (e.g., insects) will make it more difficult for any pest population to adapt to the variety blend environment. Diversity in tolerance to weather-related stresses may make blends more stable in the face of unpredictable weather conditions. Compensating growth and yield of the blend components tolerant of the stress experienced in a specific season may cause a blend to out-perform or attain greater stability than a multiline from purely agronomic perspectives.

The importance of epidemiological factors in the effectiveness of blends has consequences for the empirical study of blend effects. In particular, these effects are most prominent when they can be assessed on large areas. In small plots, evaluation of the blend effect on the build up of the disease over the season can be swamped by border effects. Rather than assessing how the disease inoculum builds up in the blend itself, small plots ultimately show only how much disease built up elsewhere and blew in. This fact provides an important rationale for conducting the experiments we propose in large plots on farms. The most compelling examples of blend benefits come from studies over large areas.