Alfalfa transcriptomic responses to the field pathobiome

Authors: Nemchinov, Lev; Irish, Brian; Grinstead, Samuel; Postnikova, Olga

Submitted to: Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/4/2025
Publication Date: 4/15/2025
Citation: Nemchinov, L.G., Irish, B.M., Grinstead, S.C., Postnikova, O.A. 2025. Alfalfa transcriptomic responses to the field pathobiome. Plant Biology. https://doi.org/10.1111/plb.70021.
DOI: https://doi.org/10.1111/plb.70021

Interpretive Summary: Pathobiome is a comprehensive biotic environment that includes a community of all disease-causing organisms within the plant. With the development of modern high-throughput sequencing approaches, it replaces traditional “one microbe - one disease” concept. Pathobiome may not only promote disease development and define symptom manifestations in the field, but also prompt unique genetic responses in the host. In this work, we used a novel “field host genomics” approach to estimate host genetic responses to a collective pathobiome in the natural field environment. It is expected that this study will be of interest to scientists involved in research on alfalfa improvement, plant pathologists, virologists, extension specialists and breeders.

Technical Abstract: In this work, we applied a novel “field host genomics” approach toward the study of alfalfa transcriptomic responses to a collective field pathobiome represented by viral, bacterial, and fungal organisms. Identified pathogenic species included alfalfa mosaic virus, pea streak virus, beal leafroll virus, Pseudomonas viridiflavia, Agrobacterium rubi, Acidovorax sp., Alternaria sp., Stemphylium sp., Ascochyta medicaginicola, Cladosporium herbarum, Claviceps purpurea and other microorganisms. Plants were also infected with cryptic and not fully characterized viruses, beneficial and non-pathogenic bacterial and fungal species. A microbiome of asymptomatic and symptomatic alfalfa field plants was found to be comparable, rather than distinct. This fact suggests that healthy-appearing plants may exhibit tolerance to the multi-pathogenic infections and are able to reduce the effect of pathobiome on their overall fitness. Various reasons can potentially contribute to alfalfa tolerance to the pathobiome: 1)tolerance observed in asymptomatic plants appears to be under genetic control; 2) tolerant plants maintained at the upregulated level specific cellular processes, classified into enriched GO categories photosynthesis, thylakoid, photosynthetic membrane, and oxidoreductase activity. In other words, robust response of chloroplasts to multi-pathogenic infection may be critical for the establishment of tolerance, as defense against microbial attack requires energy provided by photosynthesis; 3) in addition to genes involved in photosynthesis, genes encoding proteins localized in chloroplasts and known to modulate defense responses were upregulated in tolerant plants, such as calcium-sensing receptor, thylakoid formation 1 protein, and light-harvesting complex-like protein; 4) genes not involved in photosynthesis also participated in tolerant response. Among those were HAD, regulating phosphate homeostasis during phosphorus (Pi) deficiency stress; 40S ribosomal protein S3a with many roles including host-pathogen interactions; disease resistance proteins; plasma membrane ATPase participating in plant immune responses: WRKY TF, known for their role in plant immunity, and others. While combination of all relevant factors is important, chloroplasts appear to play a major role in promoting alfalfa’s ability to reduce the effect of multi-pathogenic infections on the plant fitness. Knowing genes controlling this important and likely polygenic trait can provide an alternative to host resistance-based management practices of plant diseases.