Fungus follows fertilization path

Fungal pathogens that infect plants and pollen making its way to the egg utilize some of the same molecular components, such that mutations in shared genes may provide resistance to infection, but also reduce fertility, according to a study published this week in Science.

Powdery mildew fungal infection
Image: Wikimedia commons, The Bugwood Network
University of Georgia and the USDA Forest Service

The results may offer new leads in the study of disease resistance and hold important implications for engineering pathogen-resistant crops."I think [it's] very interesting how a plant pathogen has managed to [take advantage of] an essential program in the plant for its own benefit and the completion of its own life cycle," said plant geneticist linkurl:Martin Parniske;http://www.genetik.biologie.uni-muenchen.de/people/parniske/index.html of the Institute of Genetics of the University of Munich, who was not involved in the research. Because some of the genes involved in infection and fertilization are the same, a plant cannot evolve resistance without hindering its own fertilization. "This research has important consequences for the way we think about plant-microbe interactions."Fungi that cause powdery mildew disease, a relatively common disease that can result in severe crop losses, infect plants by producing a tube-like feeding structure, which germinates from a fungal spore that has landed on an epidermal cell and penetrates the cell to access nutrients in the plant. Similarly, when pollen lands on a plant's stigma, it emits tubes that grow toward the ovary to deliver the sperm. In fact, the morphological parallels between these two processes led scientists to believe that pollen tubes were actually parasites until their role in reproduction was identified in the middle of the 19th century.Investigating the molecular pathways involved in the fertilization process of Arabidopsis plants, developmental geneticist linkurl:Ueli Grossniklaus;http://botserv1.uzh.ch/home/grossnik/groupmembers/ueli/ueli.html of the Institute of Plant Biology at the University of Z?rich and his colleagues discovered that the similarities between fertilization and fungal invasion go beyond looks.nortia mutants, for example, showed reduced fertility and had pollen tubes that did not stop growing when they reached the female gametophyte. This gene, it turns out, is a member of the mildew resistance locus o (MLO) gene family, originally discovered in barley and known to be important for powdery mildew susceptibility. Plants with mutations in certain MLO genes are resistant to the fungal infection, and breeding for such mutations has proven an effective strategy to protect barley crops, Grossniklaus said. But nortia is not expressed outside of the female gametophyte, suggesting that the MLO proteins involved in fertilization are different from those involved in infection. In fertilization, nortia appears to interact with another gene previously identified as important in fertilization, known as feronia, whose mutants show a remarkably similar phenotype to nortia mutants. Feronia, it seems, is important for redirecting Nortia within the female gametophyte when the pollen tubes arrive."We thought maybe if Feronia, together with Nortia, somehow regulates this pollen tube reception, maybe Feronia with other MLO proteins is involved in disease resistance," Grossniklaus said. Indeed, feronia mutants showed increased resistance to powdery mildew infection than wild-type plants, suggesting that in addition to its role in fertilization, feronia is involved in fungal invasion and necessary for susceptibility to the disease. With overlapping components like feronia, which helps pollen find the egg and fungi to invade epidermal cells, the two pathways essentially "work against each other," said plant pathologist linkurl:Francine Govers;http://www.php.wur.nl/UK/Staff/PermanentStaff/Govers/?wbc_purpose=Basic&WBCMODE=PresentationUnpublished of Wageningen University and the Centre For BioSystems Genomics in The Netherlands, who did not participate in the research. "If we are going to use these components for increasing resistance, we will reduce the fertility of the plants. On the other hand, if we modify these receptors [so] that they perform even better, then we make them more susceptible to pathogens." "But simply the awareness that these two things are connected is certainly helpful in our way of thinking about strategies of disease resistance," Parniske added. For example, researchers may be able to seek out components that are unique to the infection pathway to avoid affecting fertilization success, Grossniklaus noted.These findings also explain why plant geneticists have not been able to identify very many genes involved in powdery mildew susceptibility, Parniske said. A common way to identify important genes is to induce random mutations in plants, breed them to develop homozygous mutants, and look for plants that are more or less susceptible to the disease. But because many of the genes involved may also affect fertilization, the breeding part of this process may have hindered the discovery of such genes.Furthermore, this research points to a new direction for disease resistance research, said Govers, who wrote an accompanying perspective in Science. "We had no clue that receptor-like kinases [such as Feronia] had any involvement in resistance," she said. "So that's a new class that we need to investigate in more detail."S.A. Kessler, et al., "Conserved molecular components for pollen tube reception and fungal invasion," Science, 330: 968-71, 2010.
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[12th February 2008]