An unusual suspect is responsible for susceptibility of barley to devastating fungal disease

A collaboration between US and German researchers has revealed the surprising identity of a plant factor responsible for susceptibility to fungal disease in the USA’s top barley-growing region. Their study is published in the journal New Phytologist.

Both barley leaves have been inoculated with the fungus causing spot blotch. The upper one is sensitive, while the lower one is resistant.  © Shaobin Zhong

Barley is one the world’s most important grain crops with 155 million tonnes produced worldwide every year, the majority being used for animal feed. As with other crops, barley is also targeted by pathogenic microorganisms that cause severe yield losses. One of the most devastating of these is responsible for a disease called spot blotch, which is caused by a necrotrophic fungus – meaning that it kills infected plant cells – and which is characterized by dark, chocolate-coloured blotches that result in leaf drying. In the 1990s a devastating new strain of spot blotch reached the main barley-growing region in the USA in North Dakota. Curiously, some barley plants were very susceptible to the new strain, while others were not.

To determine the gene or genes responsible for the susceptibility, the team of Shaobin Zhong, based at North Dakota State University in Fargo applied a substance that causes random mutations in genes to barley seeds. Analysis of plants that were now no longer susceptible to spot blotch revealed that they all share mutations in a gene called Scs6. When Scs6 was genetically transferred to resistant barley lines, they then became highly susceptible. Thus, 30 years after the new spot blotch strain first caused havoc in North Dakota, the gene that makes some barley plants highly susceptible was finally identified.

One mystery remained though: When the sequence of Scs6 was deciphered, it was found to belong to the MLA family of immune receptors, which are well known to provide immunity against biotrophic pathogens, i.e., those that require living plant hosts. What was going on?

To answer this question, Zhong’s group teamed up with the group of Paul Schulze-Lefert in Germany. Schulze-Lefert’s group, based at the Max Planck Institute for Plant Breeding Research in Cologne, have long-standing experience in the study of immune receptors. Here, graduate student Florian Kümmel performed experiments to try and understand why an immune receptor was paradoxically responsible for making plants more susceptible to spot blotch infection. Zhong’s group had previously found that an atypical type of molecule called a non-ribosomal peptide is responsible for the virulence of the barley spot blotch. The researchers suspected that the pathogen uses this unusual molecule to target and activate the Scs6 immune receptor, which then executes a cell death response that is intended to fend off biotrophic invaders. When wash-out from infected barley leaves was injected into healthy leaves of barley with the Scs6 gene, this resulted in a cell death response. Importantly, when Kümmel performed the same experiment in leaves of another plant species induced to express Scs6 but no other barley proteins, he also observed cell death. Thus, the cell death elicited by Scs6 seems to be due to a direct interaction between it and the non-ribosomal peptide.

Barley domestication and breeding for resistance has led to the enrichment of many immune receptor genes such as Scs6 in commercially grown barley elite varieties. Could this be a doubled edge sword? As co-first author Kümmel points out: ″Evolution has seemingly led some pathogens to hijack host immune receptors, turning the plants weapons against themselves to make them more susceptible to disease. In breeding for resistance to one type of disease, we need to ensure that we are not inadvertently making our crops more susceptible to other pathogens.″­­

Original Publication

Leng, Y., Kümmel, F., Zhao, M., Molnár, I., Doležel, J., Logemann, E., Koechner, P., Xi, P., Yang, S., Moscou, M. J., Fiedler, J. D., Du, Y., Steuernagel, B., Meinhardt, S., Steffenson, B. J., Schulze-Lefert, P., Zhong, S.

A barley MLA immune receptor is activated by a fungal nonribosomal peptide effector for disease susceptibility

New Phytologist (2024)

Source    DOI