Breeding Disease-Resistant Horticultural Crops

By Paul W. Bosland and Derek W. Barchenger

Breeding Disease-Resistant Horticultural Crops is a complete and comprehensive resource for understanding the concept of breeding disease resistant crops, especially horticultural crops. Breeders of horticultural crops face distinct challenges that are different from agronomy/row crops, and these crops do not benefit from the vast body of literature available for agronomic crops. This book covers the basic theories that underpin breeding for disease resistance and features extensive real-world examples. Both classical and biotechnical breeding methods are covered, with an emphasis on how these methods are adapted for horticultural species.

Presented in a logical flow for the reader, this book addresses historical perspectives and context as it relates to breeding for disease resistance. It highlights treatments of resistance in the context of the phenotype, the genotype, the pathogen, the environment interaction, sources of resistance, and the deployment of resistance to obtain a durable resistance.

• Explores the definition of horticultural "resistance", how it is inherited, and how resistance can be manipulated through breeding
• Highlights the importance of the interaction among crops, pathogens, and environmental elements
• Provides the latest references and insights as a foundation for further research

• Language: English
• Publisher: Academic Press
• Release date: Sep 8, 2023
• ISBN: 9780443152795

Paul W. Bosland

Prof. Bosland is recognized internationally as one of the foremost experts on breeding disease resistant crops. He led the chile pepper breeding and genetics research program at New Mexico State University with the goal of releasing disease resistant chile peppers. In addition, he taught a graduate level course on Breeding for Disease Resistance for more than 3 decades. He has co-authored 8 books, 22 book chapters, and more than 100 research articles. He has received many honors and awards including named a Fellow of the American Society of Horticultural Science, the NMSU College of Agriculture and Home Economics Distinguished Researcher Award, inclusion in Who's Who in America, Wilson's Guide to Experts in Science and Technology, 2000 Outstanding Scientists of the 20th Century, and the Distinguished Award for Graduate Teaching/Achievement Gamma Sigma Delta. He was honored by the European Scientific Committee on Capsicum and Eggplant by being the first American ever selected to serve on this Committee.

Book preview

Preface

This book evolved from a course taught for more than three decades by P.W. Bosland at the New Mexico State University. On the first day of class the students hear that nothing will be harder for them in their careers as plant breeders than breeding disease-resistant plants. This is one area of plant breeding where understanding the genotype by environment interaction is crucial and essential; then add another layer of complexity, the genetic diversity of the pathogen causing the disease, and here is a relationship between a plant and a pathogen that is extraordinarily complex.

Breeding disease-resistant plants is not an end-all, but a beginning because of the ability of pathogens to overcome a plant’s resistance. Plants and pathogens interact on a physical, chemical, and molecular level and changes in the genetics of either affect their interaction. With resistance, this results in a constant battle in which the pathogen evolves to overcome the resistance, instigating what has been called an evolutionary arms race between the pathogen and the plant. Depending on the complexity of the interaction between the pathogen and the host, the resistance may lose its efficacy rapidly or be durable through time.

In addition, climate change will affect durable resistance in crops and will require both a greater knowledge of pathogen population dynamics and plant host responses to temperature by the plant breeder. The alarming spread of devastating diseases, such as the bacterium Xylella fastidiosa that attacks olives (Olea europaea) and woody crops in southern Europe and the United States, or the ug99 strain of stem rust fungus Puccinia graminis f. sp. tritici that affects wheat (Triticum aestivum) across parts of Africa, Asia, and the Middle East is attributed in part to warmer climates and presents a complex biogeographical and epidemiological problem. Because the environment plays a significant role in the development of disease and conversely the manifestation of resistance, changes in temperature can cause shifts from the resistant phenotype to a susceptible phenotype.

Another recent example is Fusarium oxysporum f. sp. apii race 4, a pathogen of celery (Apium graveolens var. dulce) that causes an emerging disease in California, United States. In approximately 2013 F. oxysporum f. sp. apii race 4 was noticed. This is highly aggressive at temperatures above 22°C. It has been spreading its geographic distribution within California and currently cannot be controlled via either host resistance or economical methods that reduce the pathogen abundance in infested soil. Although the organism F. oxysporum f. sp. apii has long been recognized, it is not as well-known as other forma speciales, such as f. sp. lycopersici on tomato (Solanum lycopersicum), f. sp. cubense on banana (Musa acuminata), and f. sp. conglutinans on cabbage (Brassica oleracea var. capitata). Lynn Epstein at the University of California-Davis believes that climate change will likely exacerbate Fusarium wilt disease severity and incidence in coastal California. At temperatures between 22°C and 26°C, F. oxysporum f. sp. apii race 4 is more aggressive than F. oxysporum f. sp. apii race 2, leading to the conclusion that the predicted climate change in California will increase the F. oxysporum f. sp. apii race 4 disease threat. Furthermore, climate change in California will also have a significant impact on the growth of multiple pathogens and consequently the need for disease-resistant crops in California.

Successful breeding for disease resistance is paramount for sustainable food production. Furthermore, a disease-resistant plant makes it possible to avoid or lessen the use of pesticides. Breeding disease-resistant plants can be considered a form of biological control, and their use is the first step in an integrated disease management program. Disease-resistant horticultural plants are a cornerstone of best management practices for organic growers. The development of disease-resistant plants is approached through both conventional breeding, where resistant traits are selected and incorporated into breeding lines over multiple generations, and through genetic engineering where genes for resistance are introduced into the plant genome. It is important to place breeding disease-resistant plants into the perspective of the whole cropping system. Resistance alone is not the sole means to achieve a disease-free crop and may lead to a rapid loss of the function of the resistance genes. One must use a resistant cultivar as part of an integrated system of production management.

Succinctly, one can say resistance is the absence of susceptibility, but it turns out not to be so simple or rational. There are a multitude of avenues to reach the phenotype called resistant. However, growers see the concept of resistance and susceptibility as two sides of the same coin. Nevertheless, the importance of breeding disease-resistance plants cannot be overstated. The ever-growing world population plus rapidly evolving pathogen populations have increased the urgency of this task.

1

Introduction to breeding disease-resistant horticultural plants

Abstract

Breeding for disease-resistant horticultural crops is a broad concept and a worthwhile goal. Using breeding for disease resistance, the plant breeder participates in a strategy that aids the grower to achieve a sustainable and profitable production system. There is no questioning that the plant breeder has an arduous task when breeding for disease-resistant horticultural crops. Thankfully, breeding for disease-resistance horticultural plants has been successful and will continue to be beneficial in the future. The plant breeder will require and use all the breeding tools available to them. An educated plant breeder is the first step to filling this tool kit.

Keywords

Breeding strategy; history; Koch's postulates; terminology

Overview

US President Thomas Jefferson famously said, the greatest service which can be rendered any country is to add a useful plant to its culture. Today, one can further elaborate adding a disease-resistant plant is a godsend to a farmer. The Food and Agriculture Organization of the United Nations (FAO) estimates that between 20 and 40% of global crop yields are lost each year due to the damage wrought by plant pests and diseases. Whether it is a highly virulent strain of bacterial wilt of tomato (Ralstonia solanacearum), late blight of potato (Phytophthora infestans), or Panama disease (Fusarium oxysporum f.sp. cubensis) threatening banana (Musa acuminata) fields, disease is historically a multifarious menace to crop production.

Great strides have been made in developing disease-resistant horticultural cultivars that combine resistances to multiple diseases and pests. For example, a packet of tomato (Solanum lycopersicum) seeds may have the designation AVFFNT on it, indicating the cultivar has resistance to (A) anthracnose (Colletotrichum phomoides), (V) verticillium wilt (Verticillium albo-atrum), (FF) fusarium wilt (two races) (F. oxysporum f. sp. lycopersici), (N) nematodes (Meloidogyne incognita), and (T) tomato mosaic virus (ToMV; Tobamovirus). Other examples include garden pea (Pisum sativum), which may possess resistance to powdery mildew (Erysiphe pisi), fusarium wilt (F. oxysporum f. sp. pisi), pea enation mosaic virus (PEMV; Enamovirus), pea seedborne mosaic virus (PSbMV; Potyvirus), and bean leafroll virus (BLRV; Luteovirus), and cucumbers (Cucumis sativus) with resistance to angular leaf spot (Pseudomonas syringae pv. lachrymans), Alternaria leaf spot (Alternaria alternata f.sp. cucurbitae), anthracnose (Colletotrichum orbiculare), downy mildew (Pseudoperonospora cubensis), powdery mildew (Erysiphe cichoracearum), Ulocladium leaf spot (Ulocladium cucurbitae), target spot (Corynespora cassiicola), scab (Cladosporium cucumerinum), cucumber mosaic virus (CMV, Bromoviridae), papaya ringspot virus (PRSV; Potyvirus), watermelon mosaic virus (WMV; Potyvirus), and zucchini yellow mosaic virus (ZYMV; Potyvirus).

There are still many disease challenges waiting for the plant breeder to conquer. As disease-resistant horticultural plants are deployed, evolution that is always occurring changes the pathogen population. Resistance makes it harder for the pathogen to survive and multiply, creating selection pressure for individuals in the pathogen population to develop novel ways to overcome the plant’s resistance. It is said that a never-ending arms race drives coevolution between pathogen and host.

A second issue arises when crop production systems change. When cropping systems intensify and become more uniform, the microenvironment changes and pathogens may find a more optimal environment. For example, green bean (Phaseolus vulgaris) producers are using higher populations in the field to achieve higher yields, but greater plant densities create an environment favorable for white (Sclerotinia sclerotiorum) and gray mold (Botrytis cinerea).

Lastly, diseases can move to new locations by climatic events, such as typhoons, hurricanes, or transglobal winds; or with the assistance of animals, such as birds and most perilously humans moving seeds and plant parts. Viruses can be introduced by insect vectors spreading through a region. The oomycetes P. infestans that causes late blight on potatoes (Solanum tuberosum) can reproduce and spread both asexually (clonally) and sexually. Sexual reproduction occurs when induvial strains from different mating types (A1 and A2) are in proximity. While late blight has been present in the United States since at least the 1830s, there has historically been only one mating type (A1), so no sexual genetic recombination occurred. This made the pathogen remain uniform genetically, and resistance in the host remained effective and durable. In the 1990s, a new mating type (A2) arrived from Mexico, allowing for sexual recombination and the development of more virulent races.

An emerging viral threat to global tomato (S. lycopersicum) production is the tomato brown rugose fruit virus (ToBRFV, Tobamovirus). This is a new highly infectious virus that is currently causing great concern as it spreads to new tomato production areas. As stated earlier, monoculture conditions, intensive selection, international trade of infected propagating material and climate changes favor the rapid spread of new diseases. Among the different pathogens, viruses are the most threating, because of their rapid diffusion and production losses.

In 2015 ToBRFV was isolated for the first time in Jordan from greenhouse-grown tomato plants. The plants showed mild foliar symptoms and strong brown rugose symptoms on fruits, with a disease incidence close to 100%, suggesting a viral etiology based on symptoms. The tomato cultivars carrying the Tm-22 resistance gene that confers resistance to tobacco mosaic virus (TMV, Tobamovirus) and ToMV (Tobamovirus) showed mosaic patterns on leaves and occasionally narrowing of leaves and yellow-spotted fruits.

After the initial findings on tomato plants in Israel and Jordan, several reports were recorded in Europe, North America, Middle East, and Asia. Further concern about the tomato brown rugose fruit was raised when it was reported in pepper (Capsicum sp.) plants grown in Jordan, Italy, Turkey, Syria, and Lebanon. Since the first identification in 2015, laboratory inoculation experiments show that under certain circumstances, ToBRFV, can infect common grasses and weeds. Illustrating that weeds can act as a reservoir for the ToBRFV, which then could infect commercially cultivated crops. Weeds are often present in the production areas and, therefore, can act as potential sources of virus inoculum, representing a greater danger, especially if they are asymptomatic.

Dispersal of ToBRFV is mainly mechanical, but it can be carried for long distances, say from one country to another via contaminated seeds and fruits. During production, short-distance transmission occurs through infected propagation material, for example, cuttings and grafts. Direct plant-to-plant contact between an infected and a neighboring uninfected plant and in the process of ordinary cultivation practices, through wounds made to leaves or to the root system of seedlings. Infection can also happen through the transfer of infected sap from different surfaces, such as human body, clothes, work tools, gloves, shoes, and poles, as well as through irrigation or drainage water and/or nutrient solutions. Likewise, after harvesting, ToBRFV inoculum can remain infectious on surfaces and materials in a greenhouse, such as wires, glass, concrete, and soil. After transplanting in a greenhouse, only two infected plants are sufficient to reach a 100% infection rate because of the high plant-to-plant transmission rate.

The Tm-22 gene that for 50 years effectively controlled ToMV and TMV infections is ineffective against ToBRFV. Because the ToBRFV is capable of overcoming all known tobamovirus-resistance genes. Before ToBRFV, another tobamovirus that raised concern because of its rapid spread on resistant tomato genotypes was the tomato mottle mosaic virus (ToMMV, Tobamovirus), first described in 2013, infecting tomato crops in Mexico. It was subsequently found in the Americas, Asia, and Europe, causing infections on tomato and pepper crops. As ToMMV is an emerging virus with similarities to the ToBRFV, the European and Mediterranean Plant Protection Organization Panel on Phytosanitary Measures recommended that both be added to the European and Mediterranean Plant Protection Organization Alert List.

ToMMV raises less concern than tomato brown rugose fruit because some tomato genotypes were found to be totally resistant to ToMMV. In fact, an undefined genotype E of tomato, with resistance to ToMV and TMV, was also extremely resistant to ToMMV, although it is not specified in the work which tobamovirus-resistance gene is involved in the control of the virus.

Recently, Dr. Avner Zinger and colleagues (2021) at the Institute of Plant Sciences, Volcani Center, Israel, evaluated 160 genotypes for tolerance and resistance to ToBRFV, resulting in the identification of an unexpectedly high number of tolerant genotypes and a single genotype resistant to the virus. An analysis of the genetic inheritance revealed that a single recessive gene controls tolerance, whereas at least two genes control resistance.

The discovery of this resistance, determined by additive effects of a recessive gene and a dominant gene, represents a novelty in tomato genetics, because effective resistance to viruses described so far is controlled by single dominant genes, except for the resistance to Potato virus Y (PVY, Potyviridae) and tobacco etch virus (TEV, Potyviridae), both controlled by the same single recessive gene pot-1.

In the last few decades, ToMV, having spread rapidly throughout the world, has induced plant breeders to select tomato cultivars with genes of resistance to ToMV. This has led to the gradual abandonment of local cultivars. Similarly, the ToBRFV will motivate plant breeders to breed plants resistant to this pathogen.

Plant viruses spread by seed, such as ToBRFV, are particularly dangerous because of the possibility of long-distance movement of infected material in an extremely short time. Therefore suitable integrated management of ToBRFV requires monitoring of potential secondary hosts, hygiene, and prophylactic measures by agricultural personnel when handling plant material and other farm activities, followed by the removal of infected plants, and continuous monitoring of cultural practices. Unfortunately, even with the adoption of phytosanitary measures, ToBRFV was able to establish itself in production systems. Therefore the hope for the future is to introduce resistance of ToBRFV in tomato lines and hybrids, especially for those intended for cultivation in protected environments where the problem is particularly evident.

Resistance must not be observed as an either–or effect, rather it is a continuum of a resistance phenotype. The key take-home message for breeding disease-resistant horticultural plants is that components of resistance are like components of yield. Genes for yield do not exist per se; there are only genes for components of yield, and components of yield differ among crops. For example, the components of yield for sweet corn (Zea mays) depend on the number of plants per hectare, ears per plant, kernel rows per ear, kernels per row, and the kernel weight, while for peaches (Prunus persica), it depends on the weight of each fruit, number of flowers per fruiting shoot, number of fruiting shoots per branch, number of branches per tree, and the number of trees per hectare.

Similarly, genes for resistance differ among horticultural crops. While there are certain gene families that are often associated with host resistance, such as nucleotide-binding leucine-rich repeats (NB-LRR), there is no universal gene for resistance. There are genes that keep a pathogen from establishing itself on a plant, and these genes can be bred into a plant to make it a disease-resistant plant.

Breeding for disease-resistant horticultural crops is a broad concept. The first step is to learn everything about your crop. This includes production practices and quality components, the primary pathogens, and new and secondary pathogens that cause disease to the crop. There are many ways to learn this information. First is to attend everything from small meetings to large conferences dealing with the horticultural crop. With the advent of the internet, it has become easier to talk to people internationally. In fact, the best reference library is your computer and emailing colleagues, as they will know of new and evolving disease issues long before one reads about them in a scholarly journal.

A key step in setting up the disease-resistance breeding program is to set priorities; not every disease is an issue that must be addressed. For example, in New Mexico, USA, chile wilt caused by Phytophthora capsici is a prevalent disease, with every production field having the causal agent established in the soil. Breeding for disease-resistant chile peppers (Capsicum annuum) (Fig. 1.1) to phytophthora wilt is a major objective at New Mexico State University, while bacterial leaf spot caused by four species of Xanthomonas is not a breeding objective in the New Mexico State University program because even though it is a major disease in the southeastern United States, it is less common in the semiarid region of New Mexico. This is because the pathogen favors 24°C–30°C and high humidity. In New Mexico, the temperature is warm, but the humidity is low; thus the disease is rare. When a chile pepper field does have infected plants, it is because either the grower planted contaminated seeds or the grower did not practice crop rotation. Thus breeding for bacterial leaf spot resistance in chile peppers is not a high priority in New Mexico.

Figure 1.1 Bountiful plates and plants of healthy peppers (Capsicum sp.) at the World Vegetable Center. Courtesy of World Vegetable Center.

The plant breeder must also be aware of cryptic diseases. These are diseases that are always present, and the crop must have resistance to be productive and profitable. For example, ToMV (Tobamovirus) has occurred in tomato (S. lycopersicum) for more than 75 years in the United States and the Netherlands and now occurs wherever tomato crops are grown, becoming a serious constraint on tomato production in most parts of the world. To the plant breeder’s displeasure, ToMV has many host species and is readily spread mechanically. In addition, ToMV persists in seeds, plant debris, greenhouse benches, and clothing worn by people coming in contact with the infected plants. A study in the Netherlands disclosed that ToMV persisted for more than 3 years on clothing stored in a dark enclosed space. A survey of clothes worn by workers in tomato-growing nurseries showed that workers’ outer clothing is seldom cleaned and is often worn from one season to the next. Fortunately, infection by ToMV is controlled by the durable resistance Tm-22 gene, and growers plant only resistant cultivars, so one does not see symptoms and could wrongly assume that ToMV is not an issue.

Breeding disease-resistant horticultural crops is part of a strategy to assist the grower to achieve a sustainable and profitable production system. As the following chapters will illustrate, the plant breeder has an arduous task. Nevertheless, breeding for disease-resistance horticultural plants has been successful in the past and will be successful in the future using all the tools available to the plant breeder. An educated plant breeder is the first step to accomplishing this worthwhile goal, and it is our goal for this book to serve as a resource for plant breeders in developing disease-resistant cultivars of horticultural crops.

Historical perspective

A review of the history of breeding disease-resistance plants is important because it allows us to understand our past, which in turn, allows us to understand our present situation and plan for the future. If one studies the successes and failures of the past, it is possible to learn from the errors and avoid repeating them in the future, and the future looks promising for plant breeders using both classical and recent technologies to improve disease-resistance horticultural plants.

There are myths and historical accounts of disastrous disease epidemics. The ancient Romans had a festival called Robigalia, which was named for their God Robigus, where sacrifices were made to protect the wheat (Triticum aestivum) fields from a serious disease, rust (Puccinia tritcina) (Fig. 1.2). The concept of disease resistance may have started around 300 BCE when Theophrastus, the Greek philosopher, discussed that plants differed in resistance to disease. He observed that plants in low-lying areas of the field had higher levels of disease than those on higher ground. At the time, however, it was not realized that a pathogen caused the disease. The common concept was that disease arose from decaying plant material, an association with the idea of spontaneous generation. It was a common belief at the time that the causes of plant disease included divine power, religious belief, superstitions, and the effects of stars and wrath of God. Slowly, these ideas were replaced with the concept that other organisms caused plant diseases.

Figure 1.2 Blessing of the Wheat at Artois by Jules Breton (1857). Christian feast of Rogation replaces the Roman Robigalia on April 25 of the Christian calendar. Courtesy Wikiart, public domain.

In 1807 Isaac Benedict Prevost in Switzerland proved conclusively that the wheat bunt disease was caused by a fungus (Tilletia tritici) and could be controlled by dipping seed in copper sulfate. Unfortunately, the notion was not widely accepted until the German botanist and mycologist Heinrich Anton de Bary established that rusts and smut diseases are caused by pathogens. It would take a few more decades before the concept that bacteria can cause the disease would be accepted in 1877, when Thomas Burrill at the University of Illinois established that bacteria caused fire blight (Erwinia amylovora) of pear (Pyrus communis).

Robert Hermann Koch, a German physician, developed Koch's rules (today Koch's postulates) in 1882, stating that for an organism to cause disease, it needed to satisfy a set of three rules later changed to four rules by Erwin Frink Smith at the US Department of Agriculture.

Koch's postulates

1. An organism believed to cause disease must always be present in the host when the disease occurs.

2. The organism must be isolated and grown in pure culture.

3. The organism obtained from pure culture when inoculated must produce the symptoms of the disease.

4. (E. F. Smith added) An organism believed to cause the disease must be reisolated from the diseased plant and compared with the organism first isolated.

However, for some diseases, there are exceptions to Koch's postulates: obligate parasites, viruses, nematodes, and noninfectious causal agents (low temperatures, mineral excess, air pollution, etc.).

In 1894 Jakob Eriksson, a prominent Swedish mycologist and plant pathologist, using wheat rust (Puccinia triticina) showed that pathogens, although morphologically similar, differed from each other in their ability to attack different related host species. Eriksson’s discovery of formae speciales (f.sp.) provided an enhancement to understanding the inheritance of resistance.

In 1900 the laws of inheritance developed by Gregor Mendel, an Augustinian friar and abbot, and biologist, were rediscovered, and the birth of genetics began aiding plant breeders to better understand the inheritance of resistance. Unfortunately, the new era of explaining disease-resistance traits by genetics had its distractors. The British botanist, mycologist, and plant pathologist, Harry Marshall Ward in 1902 promoted the bridging-host hypothesis. His theory encompassed the idea that bromegrass (Bromus sp.), grown for several generations with moderate resistance, allows the pathogen to become highly virulent. Thus the pathogen is plastic or malleable, and no matter what type of resistance the plant host has, the pathogen will overcome resistance in time. His observations had some legitimacy because resistance does fail, illustrating that not all resistance is durable.

Fortuitously, in 1905 Sir Rowland Biffen at the University of Cambridge, UK, demonstrated that resistance to yellow rust (Puccinia striiformis f. sp. tritici) in wheat (T. aestivum) was governed by a recessive gene segregating in a Mendelian ratio one resistant to three susceptible (1:3) in the F2 generation. However, the bridging theory was so strong it hampered Biffen's important work. At the time, traditional breeding programs were identifying resistance sources and introgressing resistance genes into crops by hybridizing and selecting for traits well before understanding the mechanism of action of resistance genes. Also, in 1905 mycologists found that fungi have mating systems—allowing for genetic recombination. Later, in 1911 Mortier F. Barrus of Cornell University, USA, working with beans (P. vulgaris) and anthracnose (Colletotrichum lindemuthianum) demonstrated that different isolates of a microorganism differed in their ability to attack different cultivars of the same host species, this finding is the basis for the concept of physiological races and/or pathotypes. Barrus distinguished two races, alpha and beta, of anthracnose. It was subsequently established that the ability of a pathogen to infect a host strain, that is, virulence, is genetically determined. Thus both the ability of the host to resist invasion by a pathogen as well as the ability of a pathogen to invade its host are genetically controlled.

The concept of physiological differentiation was extensively applied to wheat stem rust (Puccinia graminis f. sp. tritici) by Elvin C. Stakman in 1910 at the University of Minnesota, USA, who coined the phrase, physiological races, later to be shortened to race. Later in 1915 he coined the term hypersensitive response for the necrotic tissue reaction some plants show as resistance to a pathogen. Between 1918 and 1921, Paul R. Burkholder and Gordon P. McRostie, of Cornell University, USA, demonstrated the independent inheritance of resistance to different races of the pathogen. The understanding of disease resistance was heavily influenced in 1952, when Harold Henry Flor at North Dakota State University, USA, postulated the hypothesis of a gene-for-gene relationship between host and pathogen, which holds true in most cases and is widely accepted. His concept requires an avirulence (Avr) gene in the pathogen and a resistance (R) gene in the host plant for the resistant phenotype to manifest itself. At this point, the science of genetics could be applied to breeding for disease-resistant plants allowing breeders to consciously select for individual plants that had a resistant phenotype and know that at least some of that phenotype was genetically based. Usually, such resistance was developed as a second phase—a rescue operation—after new cultivars, selected primarily for high yield, was discovered to be susceptible to a particular disease. Plant breeders found early on that they could identify single genes (usually dominant) that conferred essentially complete resistance to the disease in question. Cultivars containing such excellent resistance were developed and released for large-scale use. But plant breeders then discovered, all too often, that the perfect resistance lost its effectiveness after a few seasons. They soon learned, with the aid of plant pathologists, that disease-causing pathogens are highly diverse genetically and that almost without fail a rare genotype will turn up that is not affected by the newly deployed resistance gene. The new pathogen genotype multiplies, and the horticultural crop’s resistance loses its effectiveness or in the vernacular breaks down.

Plant breeders change the genetic composition of horticultural crops as they select for disease resistance. One cannot say, categorically, that single gene resistance will always be undependable, or that multiple-factor resistance will always be durable. It is important to remember that the phrase stability of resistance refers to whether a previously resistant variety is overcome by a specific disease. A critical concept is that individual resistance genes do not lose their power to hold individual pathotypes in check. The resistance genes are stable and functioning, but previously undetected pathotypes appear, with types of virulence that are not curbed by the current resistance genes. The cultivar succumbs to the disease once again, albeit to a new race/pathotype/strain of the pathogen, and growers will say that the cultivar has broken down.

Toward the end of the 20th century, Brian J. Staskawicz and colleagues at University of California, Berkeley, USA, cloned the first avirulence gene in P. syringae pv. glycinea. Then in 1986 Roger N. Beachy and colleagues at Washington University, Missouri, USA created a transgenic plant expressing the coat protein of the TMV (Tobamovirus) that delayed the development of disease. Gurmukh S. Johal and Steven P. Briggs at Pioneer Hi-Bred International, Inc. reported the cloning of the first resistant gene, Hm1 (NADPH-dependent reductase) in maize (Z. mays) by transposon tagging in 1992. The next year a second resistant gene, Pto (kinase type) in tomato (S. lycopersicum) was cloned by positional mapping at Cornell University, USA. More resistant genes were cloned in the following years belonging to a different class of genes; the leucine-rich repeat (LRR) motifs with a nucleotide-binding site (NBS) were the most common class. The LRR motifs implicate protein-to-protein interactions, while NBS implies a role in signal transduction