PlantView Supports Dual Stress Resistance Research: A symbiont fungal effector relocalizes a plastidic oxidoreductase to nuclei to induce resistance to pathogens and salt stress

New progress has been made in elucidating the molecular mechanism by which the beneficial endophytic fungus Serendipita indica enhances plant resistance.

Professor Weixing Shan from the College of Agronomy, Northwest A&F University, recently published his latest findings in “ Current Biology” (IF = 8.1, Q1 journal).

This study reveals a novel mechanism whereby the fungal effector SIE141 relocalizes a plant chloroplast thioredoxin-like protein to the nucleus, thereby simultaneously enhancing resistance to both pathogen infection and salt stress.

Pathogen infections, such as those caused by Phytophthora species, and abiotic stresses including salinity severely limit crop productivity in agricultural systems. Developing sustainable and efficient strategies for stress resistance has therefore become a major priority in modern agriculture. Serendipita indica, a beneficial root endophytic fungus, establishes symbiotic associations with a wide range of plant species and significantly improves host tolerance to both biotic and abiotic stresses. However, the molecular mechanisms underlying its stress-protective effects have remained largely unclear.

Fungal effectors, which are small secreted proteins, are known to interact with plant proteins to regulate host physiological processes. The activation of systemic acquired resistance in plants depends on the salicylic acid signaling pathway, in which the master regulator NPR1 must dissociate from its inactive oligomeric form into active monomers. Thioredoxin-like proteins can facilitate NPR1 monomerization through redox regulation. However, whether fungal effectors enhance stress resistance through the manipulation of these proteins has not been clearly elucidated. In addition, the thioredoxin-like protein CDSP32 has been implicated in non-host resistance and thermotolerance, but its role in fungus-mediated stress resistance has remained poorly understood.

The study revealed that the S. indica effector SIE141 regulates dual stress resistance through a unique molecular mechanism. SIE141 specifically interacts with the conserved plant thioredoxin-like protein CDSP32 and interferes with the function of its chloroplast transit peptide (CTP), causing CDSP32 to relocate from chloroplasts to the nucleus. This nuclear relocalization is essential for the stable interaction between SIE141 and CDSP32 and for the activation of stress resistance functions.

Furthermore, SIE141 significantly enhances the redox activity of CDSP32, enabling it to efficiently mediate the monomerization and activation of NPR1, a key regulator of systemic acquired resistance. This process subsequently activates plant defense responses against pathogens such as Phytophthora. In addition, SIE141 improves plant salt tolerance. This function is partially dependent on CDSP32-mediated redox homeostasis and partially achieved through other pathways, including the regulation of hormone signaling networks.

This study is the first to demonstrate a novel mechanism by which a fungal effector simultaneously activates resistance to both biotic and abiotic stresses through the relocalization of a plant chloroplast protein to the nucleus. The findings establish CDSP32 as a promising candidate gene for stress-resistance breeding and provide important theoretical support for the development of new biological agents and sustainable agricultural practices.

Experiments using Plantview

In the study, the researchers used luciferase complementation imaging (LCI) assays to investigate the interaction between the symbiotic fungal effector SIE141 and the plant thioredoxin-like protein CDSP32. Imaging was performed using the PlantView Plant In Vivo Imaging System developed by Guangzhou Biolight Biotechnology.

DOI: 10.1016/j.cub.2024.05.064