The word “Piwi” increasingly needs no explanation. It has become a trend term in winegrape growing. Piwi is an abbreviation of the German Pilzwiderstandsfähige Rebsorten, meaning fungus-resistant grape varieties. These varieties are presented as having been given resistance to the fungal diseases that are the chief enemies of winegrapes, above all powdery mildew and downy mildew.
Resistance is acquired mainly through crossing between varieties. Powdery mildew and downy mildew originated in North America, so the European species Vitis vinifera carries no resistance to them. Breeders therefore confer resistance by artificially crossing V. vinifera with North American species and others that do carry resistance to these diseases.
Simple crossing of two varieties predates the use of the name “Piwi.” Yet such varieties, though called hybrids, are not called Piwi. What makes a Piwi a Piwi is that these varieties are classified as V. vinifera under the varietal categories of wine law. In the early days of breeding, debate over their classification remained. In more recent generations, however, repeated crossing (backcrossing) has brought them to be classified as V. vinifera.
Wine law in most jurisdictions stipulates that the grape varieties permitted for wine production must belong to V. vinifera. A hybrid produced by simple crossing is not classified as V. vinifera under wine law, and so it violates this provision. Varieties treated as Piwi, by contrast, are classified as V. vinifera, with the exception of some early breeding lines. They can therefore be used as winemaking material without running afoul of the regulation.
What the “Resistance” of Piwi Really Is
Descriptions of Piwi make frequent use of the term resistance to disease. Piwi does indeed carry resistance to fungi. Organizations promoting the spread of Piwi report in their materials that some varieties can cut the number of spray treatments by up to 75 percent. So where does this resistance come from?
As the explanation that resistance is acquired through crossing already makes clear, resistance is conferred by genes. The presence or absence of a resistance gene is, directly, the presence or absence of resistance to the target disease. Put simply, European V. vinifera varieties are prone to powdery mildew and downy mildew because they lack the resistance genes.
Resistance genes differ from disease to disease. A resistance gene matched to powdery mildew exists for powdery mildew, and one matched to downy mildew exists for downy mildew. For downy mildew, the group known as the Rpv genes provides resistance; Rpv3, Rpv3.1, Rpv3.2, Rpv10, and Rpv12 are among the specific resistance genes identified. For powdery mildew there is likewise a group called the Ren/Run genes, and resistance genes such as Run1, Ren3, and Ren9 are known.
In Piwi breeding, incorporating several of these resistance genes into a single variety is set as one of the goals. This design approach is called gene pyramiding. Pyramiding aims to achieve higher resistance by stacking multiple resistance genes against a single disease. Early Piwi such as Regent and Rondo carried only a single resistance gene against each disease. Later breeding generations, by contrast, stack multiple resistance genes, and they also pursue resistance architectures that draw on a wider range of genotypes.
The logic of pyramiding resembles defending a castle by digging a moat, raising high walls, mounting gun emplacements on them, and erecting watchtowers as well. Even if one line of defense is breached, the attack is stopped somewhere along the defenses that follow. A variety with a greater degree of such stacked defenses is treated as one with higher resistance.
The Safety of Resistance Genes
The resistance of a Piwi is secured by the resistance genes built into it. The effect of these genes, however, is not absolute.
Consider Regent, a variety developed early among Piwi. Regent carried a resistance gene, but it was a single one, and no pyramiding had been done. Its disease resistance therefore fell short of what could be called true resistance and remained weak. In such varieties, even if the incidence of disease was somewhat lower than in susceptible varieties, it was not low enough to allow a large reduction in spray treatments. Even with a resistance gene present, the risk of contracting disease always remains.
The same holds for the most recent varieties, in which more advanced pyramiding has been carried out. The presence of resistance genes does lower the risk of disease, but it never reduces that risk to zero.
The Expiry Date on Safety
Once planted, a grapevine is cultivated for decades. Even from the standpoint of first harvest, a newly established vine does not yield fruit until three to five years later. This is not annual cropping, in which a vine is harvested the year it is planted and replaced with a new one the next. What is expected of a Piwi, therefore, is that it continue to exercise its disease resistance for decades after establishment.
As already shown, the resistance of a Piwi is conferred by resistance genes. An established vine does not, as a rule, undergo large changes in its genetic makeup thereafter. The resistance genes built into it therefore keep exerting their effect for as long as the vine survives. The environment inside the vine does not change. What changes is the environment outside it.
Simple resistance conferred by a single gene is easily overcome, and quickly, by shifts in the pathogen population; this has long been pointed out. Across many crops, more than 260 resistance genes have already been reported to have lost their effect when deployed singly. And the overcoming of resistance genes by pathogens has already begun even in Piwi.
Resistance Genes That Get Overcome
In 2005, severe downy mildew was confirmed on the variety Bianca at a trial station in the Czech Republic. Bianca is a white grape variety bred in Hungary in 1963. The spread of downy mildew on this variety pointed to the existence of a pathogen capable of overcoming a resistance gene.
Bianca carried Rpv3 as a resistance gene and was known for its high resistance to downy and powdery mildew. Cases of Piwi varieties such as Regent and Solaris contracting downy or powdery mildew had been reported before, but these had been attributed to fungal strains more virulent than the conventional ones, and it had been thought that the resistance gene itself had not been overcome. The Bianca case, however, clearly demonstrated the existence of a pathogen acting specifically against a resistance gene.
The study that examined the Bianca case used downy mildew strains collected and isolated from vineyards under three different sets of conditions. It tested how each strain acted on individuals carrying Rpv3 and on those lacking it. The strain isolated from the diseased Bianca was confirmed to act specifically on individuals carrying Rpv3. This result strongly suggested that, for a strain that has overcome the resistance gene, the gene no longer exerts any effect at all: the Piwi ceases to function as a Piwi. Under such conditions, reducing the number of spray treatments yields the same result as applying no treatments to a conventional variety without resistance. In other words, the very premise that the variety is a Piwi may, as a consequence, raise the risk of contracting disease.
The Time-Limited Risk in Disease Resistance
The downy mildew infection on Bianca was observed in 2005. This case clearly suggested that even a resistance gene can be overcome through the evolution of the pathogen. It did not, however, immediately render Rpv3 meaningless. A resistant strain was confirmed in the Czech vineyard, but that did not amount to the strain being distributed worldwide. Even if resistant strains are bound to arise eventually, Rpv3 can be expected to keep providing disease resistance until then.
The problem is that no one knows when a resistant strain will appear. It may hold up for ten years, or it may break out worldwide, suddenly, tomorrow. Given recent climatic conditions, however, expecting to pass safely through the decades between planting and the next replanting may be too optimistic.
Rising Resistant Strains, Neutralized Resistance Genes
For downy mildew, strains that overcome multiple resistance genes have already been confirmed. These are reported to overcome not only single resistance genes but even some pyramided combinations. Pyramiding is certainly an effective means of improving resistance, but it is not absolute. In particular, stacking resistance genes of the same lineage, such as Rpv3.1 and Rpv3.2, has been observed to make resistant strains more likely to arise. The troublesome thing about resistant strains is that, for some of them, the resistance gene has become something that can be ignored.
The action of a resistance gene resembles that of an immune system. It functions as a defense by recognizing a target to be attacked. Under high virulence, disease appears because the effect of the fungus outweighs the defense even after that defense has operated. In a resistant strain, however, the resistance gene may fail to recognize the target for attack in the first place. When that happens, the relevant resistance gene is, for the resistant strain, as good as absent. A great bridge now spans the moat that was dug, and beyond it the wall has a hole one can walk straight through. In that state, no matter how many resistance genes have been stacked by pyramiding, the variety is likely to become, for the fungus, no different in standing from a conventional grape variety carrying no resistance genes.
Looking Behind the Safety Myth
This is not to say that pyramiding is meaningless. Combining several different types of resistance genes has been reported to yield higher efficacy than stacking genes of a single lineage. The point is only that the possibility of a resistant strain arising that overcomes even this cannot be ruled out.
The recent direction of Piwi breeding is toward more complex pyramiding. This reflects not only the aim of raising efficacy but also the fact that, without it, the varieties are becoming unable to hold out against resistant strains. Piwi breeding is often discussed in terms of coverage against a broader range of diseases and the expansion of varietal characteristics. At the same time, however, it is a game of cat and mouse to maintain resistance to downy and powdery mildew.
How long the resistance of a Piwi holds depends heavily on the environment in which the vine is planted. In regions where pathogenic fungi tend to be more active, the likelihood of resistant strains emerging tends to be higher. And once a resistant strain emerges, the disease-resistance advantage of the Piwi in that region drops sharply from then on, at least locally. Since the resistance of a Piwi rests entirely on resistance genes, no resistance beyond that can be expected once the defensive effect of those genes can no longer be counted on.
Piwi breeding continues, and each successive generation is expected to acquire higher resistance through more complex pyramiding. In the vineyard, however, one cannot keep replanting simply because a new generation of Piwi has appeared. In that sense, there is a need to think ahead about how to handle Piwi varieties that, at some future point, have lost their disease-resistance advantage.
Judging by the pattern in which resistant strains have appeared so far, placing excessive expectation on the resistance of a single Piwi variety is dangerous. What lies there is not the safety myth the world tends to describe, but a far closer-run fight. These circumstances should be understood correctly, and only then should one consider and choose how to use this new class of varieties.
