Partners in root nodule symbiosis respond uniquely to heavy metal stresses in a host genotype-dependent manner

Authors: CHAKRABORTY, SANHITA - Texas A&M University Institute For Advancing Health Through Agriculture; SHARMA, REENA - Brookhaven National Laboratory; BHAT, ADITI - Brookhaven National Laboratory; Curtin, Shaun; WEN, JIANGQI - Oklahoma State University; MYSORE, KIRANKUMAR - Oklahoma State University; Paape, Timothy

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/27/2025
Publication Date: 9/29/2025
Citation: Chakraborty, S., Sharma, R., Bhat, A., Curtin, S.J., Wen, J., Mysore, K.S., Paape, T.D. 2025. Partners in root nodule symbiosis respond uniquely to heavy metal stresses in a host genotype-dependent manner. Scientific Reports. 15. Article 33518. https://doi.org/10.1038/s41598-025-17827-z.
DOI: https://doi.org/10.1038/s41598-025-17827-z

Interpretive Summary: Our study investigated how the root nodules of Medicago truncatula, the root organ where nitrogen-fixation occurs, responded to heavy metal stress caused by cadmium (a non-essential metal) and zinc (an essential metal), and how these responses differ between host genotypes. Specifically, we examined the symbiotic interaction between the host-plant and its bacterial partner (Sinorhizobium meliloti), focusing on the role of the ATP-binding cassette (ABC) transporter, MtABCG36, which plays a role in metal ion transport and hormone regulation in roots. Our experiment used dual transcriptomics to analyze gene expression profiles of both the host plant and the microsymbiont under stress from cadmium and zinc. The study compared two genotypes of M. truncatula: a wild-type and a mutant with a compromised nodule formation due to mutations in an ABC transporter gene (Mtabcg36). The results revealed that the plant’s transcriptome responded strongly to both metal treatments, with significant changes in genes encoding ion transporters, transcriptional regulators, symbiosis related genes, but the bacterial response was much less pronounced. Our findings also suggest that the MtABCG36 gene may play a role in auxin and iron homeostasis during heavy metal stress. Finally, quantified metal retention in the nodules using Inductively Coupled Plasma Mass Spectrometry (ICP-MS) and found that the mutant plants retained more cadmium in their nodules compared to wild-type plants under cadmium stress, suggesting a role for ABC transporters in managing metal retention.

Technical Abstract: Heavy metal toxicity damages nitrogen-fixing root nodules composed of plant and bacterial cells. Several ATP-Binding Cassette (ABC) transporters export heavy metals such as cadmium out of cells. We investigated the relative responses of the symbiotic partners in nodules to a non-essential (cadmium) and essential (zinc) heavy metal and the contribution of the host genotype to the responses. We performed dual transcriptomics from nodules following cadmium and zinc stresses using two host genotypes: wild-type Medicago truncatula and an ABC transporter gene mutant (Mtabcg36) with compromised nodule formation. We quantified metals in the nodules using Inductively Coupled Plasma Mass Spectrometry (ICP-MS). The host plant transcriptome strongly responded to both metal treatments in the wild-type nodules, while the microsymbiont showed very few regulated genes in response to either metal. The host response to the stresses required auxin and iron homeostasis, in a genotype-dependent manner. ICP-MS revealed a higher retention of cadmium in mutant compared to wild-type nodules under cadmium treatment. Our findings revealed that the partners in root nodule symbiosis respond to stresses caused by an essential and non-essential heavy metal uniquely, and in a host genotype-dependent manner. These results have potential implications in agricultural management systems.