AgronomyWar and Peace, Verticillium Style

War and Peace, Verticillium Style


[deck]Insights into the complex relationship between potato plants and this pathogen are helping to advance development of resistance cultivars.[/deck]

Verticillium dahliae, a soil-borne fungus, causes wilt, yellowing, necrosis and early dying in potato. This yield-robbing pathogen is tough to manage, has a broad host range, and is known to survive in the soil for up to about five years.

Potato cultivars with improved resistance to Verticillium would be a great tool for growers.

Now, research into the complicated interactions between potato plants and this pathogen has come up with a more effective way to select for Verticillium-resistant cultivars.

“The fungus life cycle starts with the production of hardened overwintering structures called microsclerotia. When a potato plant or other host plant species starts to root, the roots produce a compound that stimulates the microsclerotia to germinate,” says Dr. Helen Tai, a research scientist with Agriculture and Agri-Food Canada (AAFC) who is leading this research.

This close-up shows Verticillium dahliae microsclerotia (the dark spots) and fungal strands (the clear, sparkly things).

“The germinating fungi penetrate the roots and then get into the vascular system of the plant. A plant’s vascular system draws water and nutrients upwards from the roots to the leaves, and the pathogen moves through the plant by hitchhiking a ride in the vascular system to the plant’s vine. The wilting and chlorosis of the vine are the first symptoms to become noticeable.”

The early dying symptom is the critical aspect of the disease for potato crops because it can result in yield impacts of 30 to 50 per cent. “[Normally] the potato vine gets bigger and bigger, and then a signal goes down to say to the underground extensions of the stem, which are called stolons, to swell up and become tubers. The tubers bulk up and become bigger because they are receiving nutrients from the vine. So the vine actually undergoes a natural dying to allow for resources to move underground for tuber bulking,” says Tai.

“By inducing the plant to die early, Verticillium causes the plant to have a smaller vine, which leads to lower bulking. The pathogen wants the plant to die because the pathogen needs a dead plant to make its microsclerotia.”

Tai and her colleagues have been getting down to the nuts and bolts – the genes and genomics – of exactly what is happening in Verticillium dahliae-induced early dying. As part of this research, they created a special crossbred population of potato plants for mapping the genes that control tolerance and resistance to the pathogen.

“We called this ‘War and Peace’ genetic mapping to represent the two kinds of relationships between the plant and the pathogen.”

Some potato plants are at war with Verticillium. In this conflict relationship, the plant develops a way to resist the pathogen, and then the pathogen evolves a way to resist against the plant’s resistance. So there’s a back-and-forth arms race between the pathogen and the plant.

Other potato plants have a peace pact with Verticillium. They tolerate the pathogen, harbouring high pathogen loads without developing early dying. So, instead of having cycles of resistance of one organism against the other, the plant and pathogen have a more stable relationship. But in agriculture, tolerant crop plants are quite risky because the resulting higher pathogen loads could spell big trouble for subsequent host crops that are not tolerant or resistant to the pathogen.

The researchers planted their diverse mapping population in a Verticillium-infested field and a greenhouse, scored the plants for early dying symptoms and tested them for Verticillium infection levels.

Some plants in the mapping population were resistant to the disease, so they weren’t infected. Some were tolerant, so they were infected but didn’t show any symptoms of early dying. Some were very susceptible and had severe symptoms. “So we had a range of symptoms in the population and a range of infection levels. However, the infection levels were not necessarily related to the symptom levels,” says Tai.

Next, the researchers genotyped the individual plants in their mapping population. Then they used a statistical technique called quantitative trait loci (QTL) mapping, associating the genotypes with early dying levels. In this way, they identified the locations (loci) on the potato chromosomes associated with early dying.

“We found the major locus controlling the amount of early dying was actually a locus that had a gene within it that controlled maturity and tuberization. We also found a second locus that was co-located with the Verticillium resistance gene,” notes Tai. Dr. Larry Kawchuk at AAFC Lethbridge had identified this Verticillium resistance gene in previous research.

“So we found the Verticillium resistance gene in our mapping, but we also found this maturity and tuberization gene,” adds Tai. “That prompted us to do an analysis of gene interactions to see if different forms of the maturity and tuberization gene were more or less responsive to the resistance gene. And that is where we made a very novel discovery, which was that some forms of the gene controlling tuberization are responding to the pathogen differently.”

This discovery is important for several reasons. “First of all, it suggests that the pathogen is co-opting [the maturation] process that is already occurring in the plant,” says Tai. “The pathogen sends out a false signal to the plant that tricks the plant into going through its own natural senescence pathway [earlier than it would have normally].”

Second, the results show the Verticillium resistance gene and the maturity and tuberization gene are both involved in early dying, and both need to be considered in order to develop potato cultivars with good resistance. The researchers found the maturity and tuberization gene, which is called CDF1, interacts with the Verticillium resistance gene, and the nature of this interaction depends on which particular variant – which allele – of the CDF1 gene is involved. The resistance gene needs to partner with the CDF1 gene to provide resistance to Verticillium, and only certain CDF1 alleles will work for this; with some other CDF1 alleles, the resistance gene doesn’t provide very much protection against the pathogen. Also, some CDF1 alleles are insensitive to the pathogen’s attempt to trick the plant into early dying. Those plants are tolerant to the pathogen, which leads to higher pathogen loads in the soil.

So simply selecting potato lines for reduced early dying symptoms is not enough. Tai says, “You need to select for reduced pathogen levels through selecting for resistance genes together with tuberization genes. Then you can get more stable and reliable reduction in early dying.”

Races and Strains

Another complicating factor for breeding Verticillium-resistant cultivars is that the pathogen has two different races, race 1 and race 2, and each race has various strains.

Both race 1 and race 2 have been identified in Canada. Tai is part of a team of scientists from universities, provincial government labs and AAFC who recently submitted a proposal for a cross-Canada survey of the races and strains of Verticillium dahliae as well as the fungal species Verticillium albo-atrum and the nematode species Pratylenchus penetrans, which are part of the Verticillium wilt disease complex with Verticillium dahliae.

She says, “We need this kind of survey, especially now that we are realizing that the Verticillium fungi are variably aggressive. The resulting information will be very helpful in developing resistant cultivars and disease control strategies.”

Beneficial Microbes and More

Tai is also investigating several possibilities for controlling the Verticillium pathogen by using endophytes, microbes that live within plants without harming the plants.

“We know peaceful relationships can occur between Verticillium and the potato plant. We’ve seen that in certain genotypes of our potato plants. Now we’re wondering if there are certain genotypes of Verticillium that will be peaceful with all genotypes of potato,” she notes.

 This concept comes from research at the University of Guelph by Dr. Jane Robb. Tai explains, “She took a Verticillium strain from eggplant and infected tomato with it. She found that the strain could infect to a very high level but didn’t produce symptoms, meaning that the tomato plant was tolerant to that strain. Then she took that tomato plant that had been infected with the eggplant strain and re-infected it with a highly virulent Verticillium strain from tomato and found the plant had reduced symptoms.”

Tai and her research team are just beginning to explore whether such Verticillium strain interactions might occur in potato. At this point, they are still looking for a strain that causes moderate symptoms in potato. Such a strain might be found if a national Verticillium survey is conducted.

Tai is also working with her AAFC colleague Claudia Goyer to identify other microbial endophyte species that could help the potato plant fight Verticillium. “A whole microbial community lives within the plant, as we are finding in our studies, and that community contains some microbes that antagonize pathogens like Verticillium.”

For this work, the researchers extract naturally occurring endophytes from potato plants and then grow those endophytes with the pathogen in culture dishes to see which ones stop the pathogen’s growth. In the future, this research could lead to development of biological control strategies and to development of cultivars that can host microbial communities that provide protection against Verticillium.

Another avenue of Tai’s research concerns nitrogen. Nitrogen fertilizers are known to delay maturity and tuberization, and her research shows that high nitrate levels affect the same genes controlling the maturity and tuberization pathway that Verticillium affects. So she and her research team are starting to look at how nitrogen stimulates that pathway, compared to how Verticillium stimulates it. This research might eventually lead to improved nutrient management strategies to help protect potato plants from the disease.

“A lot of growers have observed that you can offset the symptoms of early dying with nitrogen fertilizer, but there are environmental risks to overapplication of nitrate fertilizers that need to be considered,” she notes. “More study on the role of nitrogen in controlling maturity and tuberization is needed.”

Tai’s Verticillium research is funded by AAFC. In addition to Goyer, Tai has been collaborating on some of her studies with other scientists at AAFC including Benoit Bizimungu, Bernie Zebarth and David De Koeyer (currently with the International Institute of Tropical Agriculture), and with Dennis Halterman from the University of Wisconsin and Kåre Lehmann Nielsen from Aalborg University in Denmark.

Tai’s findings on the relationship between the Verticillium resistance gene and the maturity and tuberization gene could give potato breeders a better way forward in finding and selecting for Verticillium resistance. Some of her other studies could lead to additional strategies for developing resistant lines.

Overall, her research has the potential to contribute to the development of better tools for growers to manage Verticillium wilt and potato early dying.

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