
From Enemy to Ally: Harnessing CPR1 for Soybean Defense Strategies
- Meenu Singla-Rastogi †
- Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A.
Soybean (Glycine max) is one of the most widely grown crops globally and is extensively studied, making significant contributions to both agriculture and the economy. Other than being an important source of protein and oil, soybean is widely used for sustainable agricultural practices, as it fixes soil nitrogen, improves soil health, and reduces the need for chemical fertilizers (Aneece and Thenkabail 2018). These belowground functions are mainly executed through the interaction with soil microbes, which could potentially be dampened by environmental threats or pathogens. Soybean cyst nematode (SCN; Heterodera glycines) is one such pest, affecting soybean crops worldwide, causing estimated losses exceeding $1.5 billion in North America alone (Arjoune et al. 2022). Crop rotation with nonhost plants and the use of resistant soybean varieties have been deployed for SCN management to alleviate major yield losses. However, the reliance on these resistant soybean varieties has led to the emergence of strains that are virulent on these varieties, thereby impacting their efficacy (Allen et al. 2017; Niblack et al. 2008).
Alternatively, the Innes Laboratory has been developing new approaches to engineer genetic-based disease resistance in soybeans through the identification of decoy substrates of proteases secreted by pathogens (Helm et al. 2019; Pottinger et al. 2020). They had previously discovered that the nucleotide-binding leucine-rich repeat (NLR) disease resistance protein Resistance to Pseudomonas 5 (RPS5) of Arabidopsis is activated by proteolytic cleavage of another Arabidopsis protein, AvrPphB Susceptible 1 (PBS1), which is targeted by an effector protease from Pseudomonas syringae, AvrPphB (Shao et al. 2003). Activation of RPS5 in turn triggers a localized hypersensitive response (HR) as part of the plant defense response. Substitution of the AvrPphB cleavage sequence within the activation loop of PBS1 with cleavage sequences specific to proteases of other pathogens has been deployed to change the specificity of RPS5, thereby conferring resistance to new pathogens (Helm et al. 2019; Kim et al. 2016; Pottinger and Innes 2020). The PBS1 decoy technology has previously been used to confer resistance to viruses (Pottinger et al. 2020), but whether it can be used to engineer resistance to other classes of pathogens is not known.
In this issue of Molecular Plant-Microbe Interactions, Margets et al. (2024) lay the groundwork to extend PBS1 decoy technology to engineer resistance to SCN. First, the researchers identified and characterized a secreted protease effector from SCN, which they named CPR1 (Cysteine Protease 1). CPR1 was selected, in part, because it was found to be conserved amongst all SCN populations with available genome sequence information (>10), indicating that it is essential to SCN viability. This, in turn, suggests that SCN will not be able to easily lose CPR1 protease activity, so a resistance mechanism based on the detection of CPR1 protease activity should be durable. They further demonstrated that CPR1 suppresses plant immune responses, highlighting its role in facilitating nematode infection. Using biotin-based proximity labeling, the researchers identified candidate targets of CPR1 in soybean roots, providing a more accurate depiction of how effectors operate during infection. The authors show that CPR1 partially localizes to the mitochondria and interacts with the mitochondrial protein GmBCAT1 (Fig. 1). Based on its proteolytic activity, they further postulated that this effector could modify soybean metabolism in the infected tissue, thereby enhancing SCN's ability to infect plants. The authors also found that silencing of CPR1 in SCN inhibits the pathogen from penetrating soybean roots, while overexpression of CPR1 in soybean roots significantly enhances SCN infection, demonstrating that CPR1 contributes to virulence.

Fig. 1. Illustration of the secretion of Cysteine Protease 1 (CPR1, a secreted effector) by soybean cyst nematode (SCN) into the infected root cells and its downstream interaction with the mitochondrial target protein, GmBCAT1. Upon secretion, CPR1 is processed into a mature active form and partially localizes to mitochondria. When and where processing occurs is not yet known. Although the expression of CPR1 (mat denotes mature form) in the host leads to the suppression of immune responses, further investigation to identify the potential cleavage sequence of CPR1 (which is still unknown, marked with an asterisk) would allow better characterization of this secreted protease effector and provide insights into the downstream CPR1-mediated virulence mechanisms. The illustration was prepared using BioRender.
The present work provides important new insights into the molecular interactions between SCN and soybean. This study emphasizes the importance of elucidating the mechanism of action of pathogen effectors, such as CPR1, that are highly conserved among various nematode species. Going forward, identification of CPR1’s target cleavage sequence within GmBCAT1 (or other host targets) is needed to engineer resistance to SCN using PBS1 decoy technology. This work paves the way to developing durable and broader pathogen resistance in crops, thereby addressing a significant challenge in agriculture and food security.
The author(s) declare no conflict of interest.
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M. Singla-Rastogi is an Assistant Feature Editor serving on the MPMI Editorial Board.
Linked article: This article refers to Margets et al. (2024). To view this article, please visit https://doi.org/10.1094/MPMI-06-24-0068-R.
The author(s) declare no conflict of interest.
Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.