PAN-AMERICAN ADVENTURE: Chapingo, Mexico

Beyond GMO … the REAL answer to healthy, disease resistant crops
Down in Mexico, two plant scientists, despite lack of funding and support, are staging a true green revolution. By using a strategy called horizontal resistance to breed bean plants with broad genetic resistance to diseases and pests, they are outperforming GMO and commercial crop varieties … without the need for pesticides! This is a must read piece. Be patient with the science and you’ll be richly rewarded.

By Don Lotter, Ph.D.

Posted November 9, 2004, Chapingo, Mexico. Dr. Roberto Garcia opens the trunk of his car and reveals piles of cloth bags of bean seed, labeled with such names as Atimegaya, Hogar, and Huesonapan. “This is how I get the beans from my program to the farmers. I am the extension system as well as the researcher,” says Garcia. This is surprising, considering the impressive data he has shown me on the yields of the disease resistant bean cultivars (field beans, Phaseolus vulgaris) from his 10-year old breeding program. Most successful crop breeding programs like his have an extension system, or at least a full time employee, for getting seed out to farmers.

Garcia, professor at the Colegio de Postgraduados in Chapingo, outside of Mexico City, has no extension system support and no funding for seed dissemination (or for other activities fundamental to a breeding program) because he sits, despite successful results, on the wrong side of an unnecessary chasm that divides two different approaches to plant breeding.

In a society that calls itself democratic, open, and merit-based, it is always surprising, even shocking, to hear about a situation in which a proven technology or a solution to one of society’s problems has been ignored or even suppressed because it didn’t fit into the existing philosophy. Of course, those of us in the organic farming and food movement are all too familiar with such scenarios, but when I hear about it happening, as a scientist, it still pushes me hard.

Garcia’s development of high-yielding bean varieties that need no inputs of pesticides has been accomplished using an approach to plant breeding that literally turns the green revolution approach on its head. His approach is called horizontal or quantitative resistance breeding. (Terminology note: The mainstream plant breeding community uses the term quantitative when referring to this aspect of plant genetics. However, as a gesture of respect to those scientists who have used the term horizontal resistance breeding and who have persevered in establishing it as an indispensable approach to crop improvement, I am keeping the term horizontal.)

Horizontal resistance breeding can be of enormous value to the North American organic and sustainable agriculture community, and could prove to be the basis of the development of many, if not most organic crop lines in the future.

To learn more about horizontal resistance Raoul Robinson's classic text on plant breeding to reduce pesticide use, Return to Resistance, is out of print. In keeping with the principles of participatory plant breeding and democratic information sharing, however, Robinson has recently made several of his works available through the Canadian free e-books site, www.sharebooks.ca. The books carry copyright protection but can be downloaded for personal, non-commercial use. Included on the site are Return to Resistance in both English and Spanish versions; Self-Organising Agro-Ecosystems, described as the technical companion volume to Return to Resistance; and the Amateur Potato Breeder's Manual. Also available is the Amateur Plant Breeder's Handbook 2004, an expanded, cross-linked version of the glossary of technical terms included in the original print edition of Return to Resistance. If you just can't give up the pleasures of books in book form, copies of Robinson's books can also be found through on-line second-hand book sites like Abebooks.com or Bookfinder.com.

On the other side of the chasm from the horizontal approach to plant breeding sits (with all the money) what is known as vertical or qualitative resistance, dominant for some 100 years over the crop breeding milieu. Vertical disease resistance generally involves one or just a few genes, and the vertical approach to breeding involves the transfer of one or a few genes from plant to plant to bring about desired traits like disease resistance.

This approach to crop development is the basis for the genetic engineering industry, and is heavily invested in a proprietary orientation to crop development (ownership of genes and cultivars).

Garcia has seen his funding pulled by both international and Mexican funding sources, despite developing bean cultivars, via his horizontal resistance breeding program, that have increased yields by 2-5 times that of the existing cultivars in the Mixteca bean growing region of Mexico. The funding cuts came despite the fact that Garcia not only eliminated the need for pesticides, but showing that his new cultivars consistently yield on par or better than the newest “improved” green revolution varieties, all of which need pesticides.

The Mexican agricultural ministry and the international funding agencies are all staffed by mainstream plant breeders, invested in the vertical resistance paradigm, according to Garcia. “They simply refuse to believe that horizontal resistance breeding has any value,” says Garcia.

Garcia’s disease resistant bean data, showing yields of 1,500 to 2,400 kg of beans per hectare, with no pesticides, vs. former yields of 350 to 600 kg per hectare, are not just one year’s data. These are consistent yields from replicated trials, year after year for the past half dozen years. And the yields of the horizontal resistant cultivars are still climbing with each breeding cycle of hand cross-pollinations and screening.

A separate but related horizontal resistance breeding program at the University of Chapingo, under the direction of Dr. Luis Serrano, has achieved the similar levels of bean yields, also showing superior yields to the green revolution varieties.

History of the chasm between vertical and horizontal resistance breeding

The history of the chasm between horizontal resistance breeders and the dominant alternative, vertical resistance breeding, goes back to the first decade of the 20th century, to the discovery of the neglected work of Gregor Mendel. Mendel had discovered that single genes could be inherited as recessive or dominant alleles as part of homologous chromosomes, forming the basis for single gene selection and breeding of organisms for traits based on selected genes. The transfer into crop cultivars of genes with characteristics such as disease resistance or short stature became the focus of crop breeding programs.

The problem is that a majority of the time that a gene for disease resistance was bred into a crop, the disease pathogen would develop new races that were virulent against the newly bred “resistant” cultivar. The breakdown of resistance based on single genes has been a continual problem in crops since vertical resistance breeding began. In wheat, resistance to leaf rust, stem rust, stripe rust (Puccinia spp.) and scab (Fusarium) have broken down one after another. The most recent breakdown of stem rust in wheat was announced in 1999 when a virulent biotype developed on wheat in Uganda, causing concern for wheat crops around the world.

The traits that were of interest to the Mendelian disease resistance breeders were generally for genes with total resistance to disease. However, it was known, even before the discovery of Mendel’s work, that there was a quantitative aspect to disease resistance in plants, and that within populations there could be found plants with anything from zero to near total resistance to a disease and everything in between. This quantitative type of disease resistance was not as spectacular as single gene resistance and receded into the shadows of plant breeding.

In 1963 a South African plant pathologist, J.E. Vanderplank, elucidated these two types of disease resistance, vertical and horizontal, in his classic book Plant Diseases: Epidemics and Control. The terms vertical and horizontal were based on graphical depiction of the two phenomena (Fig. 1).

The vertical resistance system is actually a system of matching co-evolved genes between the plant and the pathogen. Horizontal resistance is polygenic; many genes are involved in the resistance to the disease, thus the terms vertical/qualitative and horizontal/quantitative.

FIGURE 1:

Dr. Raoul Robinson, British/Canadian plant pathologist and author of Return to Resistance, probably the staunchest defender and strongest promoter of horizontal/quantitative resistance breeding of crops, uses various metaphors to describe vertical and horizontal resistance. In my own adaptation of his description, vertical resistance can be likened to a door lock on a house, where the pathogen has to have the key to enter. But the house has other doors through which other races of the pathogen may enter, if they find the plant, in which case vertical resistance breaks down.

Horizontal/quantitative resistance is akin to having unlocked doors on the house, with soldiers in the house to fight off the pathogens when they enter. It is characterized by many genes which can fight off any local races of pathogen. Horizontal resistance, according to Robinson, does not break down, because there is no lock and key gene-for-gene mechanism as with vertical resistance. It can vary from very low levels of resistance to nearly complete, and thus is known as quantitative resistance.

When vertical resistance is isolated by taking a narrow genetic slice of a spectrum of genes from a wild population, and then bred into a crop, as is done in mainstream resistance breeding, the resistance, in isolation, cannot be sustained, and in most cases eventually breaks down. Potato illustrates another case. Early in the 20th century potatoes were bred almost entirely for vertical resistance to late blight, the devastating fungus that hit Ireland in the 1840s. It was found however, that it took the late blight fungus about four years to overcome the vertical resistance while it took eight years to breed the vertical resistance. After that, resistance breeding was largely given up and control of late blight brought about by copper compounds.

Dr. John Niederhauser, working in Toluca, Mexico, discovered that polygenic, quantitative (horizontal) resistance was much more successful and sustainable against late blight of potato. In 1991 he was awarded the World Food Prize for his pioneering work.

The chasm between horizontal and vertical breeding is not all black and white, and many crop breeding programs incorporate quantitative resistance into their regimens. However, most are based substantially on gene transfer and vertical resistance, while horizontal/quantitative resistance remains a minor player. Much of the alienation of the Raoul Robinson-trained horizontal resistance breeders from the mainstream may be due to Robinson´s approach of eliminating vertical resistance from crop lines in resistance breeding programs (described below and outlined in his books Return to Resistance and in Self-Organizing Agroecosystems).

Robinsons’s practice of completely eliminating vertical resistance from parental lines appears to have merit, however. Vanderplank discussed in his book--and Niederhauser further showed--how in potato, vertical resistance to late blight could, over many breeding generations, cause a near complete loss of horizontal resistance to late blight, just as happens when fungicides are consistently applied over many sexual generations. The plant, minus any pressure from late blight, in a sense says “Why do the work to produce these (horizontal resistance) defense mechanisms when there is no late blight attacking me?” When the vertical resistance broke down in this particular variety of potato, called Vertifolia, late blight completely and utterly devastated it, as it now had neither vertical nor horizontal resistance. This Vanderplank called the Vertifolia Effect. It is for this reason that the Robinson school of plant breeding first eliminates vertical resistance from parental lines of crops, as they don’t want any masking of horizontal resistance.

How scientists breed for horizontal/quantitative resistance

The methods used for breeding for horizontal resistance are such a radical departure from conventional plant breeding that the reader is likely to do a double-take when introduced to them. They literally turn the classical plant breeding paradigm on its head. (Note: Not all crops are conducive to horizontal resistance breeding, a subject that Robinson discusses in his book Return to Resistance.)

After collecting as wide a spectrum of crop germplasm as possible, the collected lines are planted, and inoculated with or exposed to two or three of the worst diseases or insect pests for that particular crop. The next step is the controversial one. The surviving plants (the disease and pest inoculations should be designed to be sub-lethal) are then selected for on the basis of susceptibility. This may be completely counterintuitive, but it is one of the most important steps in horizontal resistance breeding. The objective is to completely eliminate any vertical resistance, which is easy to identify because the plants will be completely free of the disease or pest.

In Garcia’s breeding program in Mexico, he selected 71 of the best bean cultivars from the Mixteca region, exposed them to three of the worst bean diseases - bean common mosaic virus (BCMV), the common blight bacterium (Xanthomonas), and the fungus Macrophomina, a soil-borne root pathogen.

He then selected seven of the most diseased lines out of the 71. The seven lines were so diseased that some of them had just one or two pods.

When Drs. Garcia and Robinson were working together at the susceptibility selection stage in the first year of project, they visited the selection site with the field operations manager. Diseased plants were everywhere.

“What a mess!” said the field ops guy. “On the contrary, it’s a beautiful sight!” countered Robinson.

After the initial stage of selection for susceptibility, every subsequent generation is subject to selection for resistance, measured by yield, since disease pressure is intense due to the pathogen inoculations. The common bean is 95% self-pollinated. Therefore, starting with the seven selected susceptible lines, hand cross-pollination was carried out to cross each of the selected lines with the other, an extraordinarily laborious task. The progeny lines (there are some 49 families, including self-pollinations) are grown out and subjected to the same disease screening, this time for resistance. Only 1% to 10% of plants are selected (each family has hundreds of plants, and there is high variability between the plants within those families.) This is known as recurrent mass selection, and the resistance selected for is entirely horizontal/quantitative. With each subsequent generation, all selected lines are crossbred with each other to generate new lines, exposed to the pathogen screening, and 1-10% of plants selected.

On the average there is a 20% increase in yield from the lines selected in each subsequent breeding cycle (Fig. 2). The breeding cycle often takes more than one year, since it involves crosses which yield just a few seeds. Those seeds need to be increased for one or two generations to obtain enough seed for another round of selection.

After the 3rd breeding cycle, the selected cultivars are taken from the university experiment station to the bean growing region, where dozens of bean diseases and insect pests are endemic, and are planted in the most disease and insect pest prone areas that can be found. Therefore, according to Garcia, selection from the 4th cycle onwards was not only for resistance to the inoculated diseases, but also for other pests and diseases as well. This is the great strength of horizontal resistance breeding. Resistance to all locally active pests and diseases is selected for after the 3rd breeding cycle.

Since at least half of the generations occur in the target location of the crop, horizontally resistant crop lines are generally regional and local in their resistance characteristics. Transfer to another region which has a different complex of pests and diseases will give variable results, depending on how much the pests and diseases vary from the original site of selection. Thus, horizontal breeding programs have a local and regional focus. This is a distinct difference from the green revolution approach, which attempts to develop crops that have resistance to a few major diseases and pests for widespread inter-regional use.

Unplanned but later built into Garcia’s breeding program was horizontal resistance to soil borne diseases – the classic heavy hitters of so many crops – Fusarium, Pythium, and Rhizoctonia. These pathogens hit the research plots during the 4th breeding cycle, nearly wiping out the entire experiment. Garcia then went on to select for resistance to the soil borne diseases, in addition to BCMV and blight. In subsequent years, these pathogens were inoculated to screen for resistance. Garcia now has bean lines that are completely resistant to these soil-borne diseases.

Garcia loses funding because he doesn’t fit into the dominant paradigm

When Garcia’s project, which was funded by the International Development Research Center of Canada, came up for review, the referees who were sent to review his program were all from the CIAT (Centro Internacional de Agricultural Tropical) bean program, a green revolution center. According to Garcia, the scientist referees, who had spent their entire careers developing vertical resistance and gene-transfer type breeding programs, were threatened by his success in breeding high yielding varieties that competed with the green revolution varieties. Either that or, for inability to perceive the benefits of horizontal resistance breeding, they had the program funding ended.

According to Garcia, the basic premise of the vertical resistance breeders’ objections to the horizontal resistance approach is that it is characterized by “Garbage in, garbage out”. They maintain that you simply cannot base a breeding program on crop lines whose original parents were selected for on the basis of susceptibility to disease. It is simply antithetical to them.

This is a perfect example of how philosophical blinders work in science, as the data shows unequivocally it is possible to develop resistance from such parental lines.

Garcia counters this criticism: “We didn’t start with garbage. We started with 71 of the best varieties, out of hundreds, in the Mixteca region. The seven cultivars we selected in the susceptibility stage were susceptible to diseases, but they had good genes.”

When Garcia put together an international conference on bean pathology, his approach to bean improvement, despite data that showed success, was largely ignored. “The mainstream breeders had such an arrogant attitude,” says Garcia, “they declined to even to take a short field trip to look at my trials.”

Dr. Luis Serrano of the University of Chapingo, whose bean horizontal resistance breeding program has achieved very similar results as those of Garcia at Colegio de Postgraduados, has the same things to say about the chasm between his program and the mainstream breeders. His funding was ended by the Mexican government, whose agronomists and geneticists are all mainstream, green revolution types. Serrano now manages his program with his own salary and with the scores of students that come through his classes. The plant breeding and agronomy courses at the university involve dozens of hours of field and fieldhouse work by students to manage the breeding program.

Serrano showed me boxes of envelopes of seeds, 400 bean lines in each of six types of beans – black, pink, yellow, tan, white and mottled. He is working on horizontal resistance to the bean’s worst pest in Latin America, the Mexican bean beetle. He also showed me data in which his horizontally resistant bean cultivars are compared in replicated trials to the best green revolution and commercial cultivars. His horizontally resistant cultivars came out well above the others, with yields of 2,000 to 2,400 kg per hectare compared to 1,500 for the commercial and green revolution varieties.

The CIAT bean program web page shows that yields of their improved varieties in commercial plantings in Mexico and Central America range from 800 to 1,500 kg per ha, with low to moderate levels of pesticide inputs.

The entire agricultural extension system in Mexico is, for the most part, set up to promote green revolution and capital intensive type approaches to agriculture. The bean lines that Garcia and Serrano have developed do not interest them.

The inability to patent and make proprietary (to own) the genes and cultivars in a horizontal breeding system, which is polygenic, is likely another reason for the rejection of horizontal resistance breeding by mainstream agriculture. The entire basis of the genetic engineering industry is the ownership and ability to transfer of one or a very few genes from crop to crop and cultivar to cultivar.

Additionally, programs which develop crop lines that don’t need agrichemicals are not going to get much support in an agricultural system that is heavily invested in the use of agrichemicals either.

Other crops are currently the target of horizontal disease and pest resistance breeding at the University of Chapingo – mainly onions and, just at its inception, tomatoes. Niederhauser’s former program for potato horizontal resistance apparently continues in Toluca, southwest of Mexico City, and has spawned at least one potato breeding program in the US at Michigan State.

Bean breeders from international centers and universities who I contacted had not heard of the Mexican bean horizontal resistance breeding program. At least one had heard of the Raoul Robinson horizontal resistance approach, but had only cursory knowledge of it.

A student plant breeding club to the rescue

Traditionally, beans are a central part of the diet in Mexico and Central America. Along with corn they form the main food source of the poor. In the category of basic grains, beans are second only to corn in area planted, and are the number one source of farm income in Mexico. The market for beans has grown substantially in recent decades as urban populations swell with migrants from the countryside.

Figure 2 Dr. Roberto Garcia’s horizontal resistant bean yields in the Mixteca bean growing region of Mexico, at the end of the first breeding cycle and the 3rd to the 6th. This year he finishes the 7th cycle and is seeing another increase of 20% in yields, which substantially outperform green revolution varieties, without the use of pesticides.

With the help of Raoul Robinson, Serrano has developed a rather innovative way of getting his bean lines out into the field all over the country – the student breeding club.

Students from farms all over the country come to Serrano’s program, participate in the development of bean cultivars, and when they go home, take many of the cultivars with them, as well as bring local cultivars back to Chapingo for putting into the screening and breeding program.

“Our bean lines have been planted in a dozen states all over Mexico via what is now officially called the Raoul Robinson Breeding Club, and we have collected a very large assortment of bean lines via the students,” says Serrano. “It’s not a perfect extension system, because many times we don’t hear back from the students once they have gone with our beans, but it works at our level of funding.”

“Plus, we are putting out hundreds of students who know the value of horizontal resistance breeding, not just from our telling them, but from firsthand experience. This is good for the future of horizontal resistance breeding.”