Tetraose steroidal glycoalkaloids from potato provide resistance against Alternaria solani and Colorado potato beetle

Elife. 2023 Sep 26:12:RP87135. doi: 10.7554/eLife.87135.

Abstract

Plants with innate disease and pest resistance can contribute to more sustainable agriculture. Natural defence compounds produced by plants have the potential to provide a general protective effect against pathogens and pests, but they are not a primary target in resistance breeding. Here, we identified a wild relative of potato, Solanum commersonii, that provides us with unique insight in the role of glycoalkaloids in plant immunity. We cloned two atypical resistance genes that provide resistance to Alternaria solani and Colorado potato beetle through the production of tetraose steroidal glycoalkaloids (SGA). Moreover, we provide in vitro evidence to show that these compounds have potential against a range of different (potato pathogenic) fungi. This research links structural variation in SGAs to resistance against potato diseases and pests. Further research on the biosynthesis of plant defence compounds in different tissues, their toxicity, and the mechanisms for detoxification, can aid the effective use of such compounds to improve sustainability of our food production.

Keywords: Alternaria solani; Colorado potato beetle; Solanum commersonii; Solanum tuberosum; plant biology; plant immunity; steroidal glycoalalkaloids.

Plain language summary

Farmers often rely on pesticides to protect their crops from disease and pests. However, these chemicals are harmful to the environment and more sustainable strategies are needed. This is particularly true for a disease known as the early blight of potato, which is primarily treated using fungicides that stop the fungal pathogen responsible for the infection (Alternaria solani) from growing. An alternative approach is to harness the natural defence systems that plants already have in place to protect themselves. Like humans, plants have an immune system which can detect and destroy specific pathogens. On top of this, they release defence compounds that are generally toxic to pests and microbes, stopping them from infiltrating and causing an infection. In 2021, a group of researchers discovered a wild relative of the potato, known as Solanum commersonii, with strong resistance to early blight disease. Here, Wolters et al. – including some of the researchers involved in the 2021 study – set out to find how this plant defends itself from the fungus A. solani. The team found that two closely linked genes are responsible for the resistant behaviour of S. commersonii, which both encode enzymes known as glycosyltransferases. Further experiments revealed that the enzymes protect S. commersonii from early blight disease by modifying steroidal glycoalkaloids, typical defence compounds found in potato and other plants from the same family. The glycosyltransferases alter glycoalkaloids in S. commersonii by adding a sugar group to a specific part of the compound called glycone. Wolters et al. found that the glycoalkaloids from S. commersonii were able to slow the growth of other fungal pathogens that harm potatoes when tested in the laboratory. They also made plants resistant to another common destroyer of crops, the Colorado potato beetle. These findings could help farmers breed potatoes and other crops that are more resistant to early blight disease and Colorado potato beetle, as well as potentially other fungi and pests. However, further experiments are needed to investigate how these glycone-modified glycoalkaloids affect humans, and how variants of glycoalkaloids are produced and degraded in different parts of the plants. Acquiring this knowledge will help to employ these defence compounds in a safe and effective manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternaria
  • Animals
  • Coleoptera*
  • Plant Breeding
  • Solanum tuberosum*
  • Steroids

Substances

  • Steroids

Supplementary concepts

  • Alternaria solani

Associated data

  • SRA/PRJNA792513

Grants and funding

The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication.