Transcriptional reprogramming and microbiome dynamics in garden pea exposed to high pH stress during vegetative stage.

Abstract

Main conclusion: High soil pH induces the upregulation of genes involved in oxidative stress and nutrient transport, while the enrichment of beneficial microbes (Variovorax, Chaetomium, and Pseudomonas) highlights their potential role in promoting stress adaptation. High soil pH severely impacts plant growth and productivity, yet the transcriptomic changes and microbial dynamics underlying stress adaptation in garden pea (Pisum sativum ssp. hortense) remain unclear. This study demonstrates that high soil pH leads to stunted growth, reduced biomass, impaired photosynthesis, and nutrient status in garden pea. Further, disruption in key nitrogen-fixing bacteria (Rhizobium indicum, R. leguminosarum, and R. redzepovicii), along with the downregulation of NifA and NifD genes and upregulation of NifH in nodules highlights the critical role of micronutrient balance in legume-microbe symbiosis and a compensatory response to maintain nitrogen status. RNA seq analysis revealed extensive transcriptional reprogramming in roots, characterized by the upregulation of oxidative stress response genes (e.g., oxidoreductase and glutathione transferase activities, metal ion transporters) and the downregulation of genes related to ammonia-lyase activity and ion binding, reflecting broader disruptions in nutrient homeostasis. KEGG pathway analysis identified enrichment of MAPK signaling pathway, likely interacting with other pathways associated with stress tolerance, metabolic adjustment, and structural reorganization as part of adaptive responses to high pH. Root microbiome analysis showed significant enrichment of Variovorax, Shinella, and Chaetomium, suggesting host-driven recruitment under high pH stress. Stable genera, such as Pseudomonas, Novosphingobium, Mycobacterium, Herbaspirillum, and Paecilomyces, displayed resilience to stress conditions, potentially forming core microbiome components for adaptation to high pH. In a targeted study, inoculation of plants with an enriched microbiome, particularly C. globosum, under high pH conditions improved growth parameters and increased the abundance of Stenotrophomonas and Pseudomonas in the roots. It suggests that these bacterial genera may act as helper microbes to C. globosum, collectively promoting stress resilience in pea plants suffering from high pH. These findings provide a foundation for microbiome-aided breeding programs and the development of microbial consortia to enhance the adaptation of pea plants to high pH conditions.