Chloroplast function impairment during phytoplasma infection in tomato

Phytoplasmas ‘Ca. P. solani’, represents a major threat to global crop production due to their unique biological features, complex transmission dynamics, and profound physiological impact on host plants. These cell wall-less bacteria, restricted to sieve elements, exploit the nutrient-rich and immune-privileged environment of the phloem while evading early detection and defense responses. Our integrative analysis combining transcriptomics, co-expression network analysis, and physiological characterization of S. lycopersicum cv. Micro-Tom revealed that ‘Ca. P. solani’ infection severely disrupts the host’s photosynthetic machinery through repression of key genes involved in chlorophyll biosynthesis, the electron transport chain, and carbon fixation. Central to this disruption is the impairment of chloroplast-mediated anterograde and retrograde signaling, which normally regulates the coordination between chloroplast function and nuclear gene expression. Importantly, our findings underscore the pivotal role of chloroplasts not only in energy metabolism but also as signaling hubs in plant immunity, influencing hormone biosynthesis, redox homeostasis, and defense gene activation. The differential physiological responses observed between Wild-type and Aurea mutant plants further emphasize that genetic background and photomorphogenic traits significantly influence host resilience. The Aurea mutant, with its altered light signaling and carbon allocation strategies, maintained a more stable physiological performance under infection, including improved water-use efficiency, sustained electron transport, and greater fruit biomass retention, highlighting genotype-specific mechanisms of tolerance. Together, this work provides new insights into how phytoplasmas interfere with core plant functions by targeting chloroplast signaling pathways and offers a physiological and molecular framework for understanding tolerance mechanisms. These insights may support the development of more targeted strategies for phytoplasma disease management, including the development of genotypes with enhanced chloroplast resilience and improved immune signaling.