Diverse triggers, common outcome: Senescence in Fix⁻ Medicago truncatula nodules

Pál, Alexandra and Lima, Rui and Tiricz, Hilda and Ayaydin, Ferhan and Kereszt, Attila and Kondorosi, Éva and Ábrahám, Edit (2025) Diverse triggers, common outcome: Senescence in Fix⁻ Medicago truncatula nodules. PLANT PHYSIOLOGY, 199 (3). No. kiaf518. ISSN 0032-0889

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Abstract

Nodule senescence in barrel medic (Medicago truncatula) can occur as a natural, developmentally regulated process or be triggered prematurely by environmental stress or ineffective symbiotic interactions. In this study, we examined five M. truncatula Fix⁻ mutants (dnf4, dnf7-2, TR183, TRV36 and TR36) that fail to fix nitrogen to determine whether they share common senescence-related traits. Our findings reveal that, despite distinct genetic defects, all mutants exhibit similar hallmarks of premature senescence: a rapid decline in the transcription of nitrogen-fixation-related genes (as indicated by DINITROGENASE REDUCTASE (NifH) expression), early degradation of bacteroids and symbiotic cells, recolonization of nodules by saprophytic rhizobia, premature closure of the nodule endodermis, impaired post-mitotic differentiation of the symbiotic cells, and upregulation of senescence marker genes (CYSTEINE PROTEASE 2 (CP2), CYSTEINE PROTEASE 6 (CP6), CHITINASE 2 and PURPLE ACID PHOSPHATASE 22 (PAP22). Neither symbiotic maintenance genes (DEFECTIVE IN NITROGEN FIXATION 2 (DNF2), Symbiotic CYSTEINE-RICH RECEPTOR-LIKE KINASE (SymCRK) and REGULATOR OF SYMBIOSOME DIFFERENTIATION (RSD) that inhibit plant defense responses nor the defense-related gene PATHOGENESIS-RELATED PROTEIN 10.1 (PR10.1) were upregulated, suggesting that premature senescence in these mutants is driven primarily by proteolytic activities rather than immune responses. These results indicate that early nodule senescence is a common feature of ineffective M. truncatula-Sinorhizobium medicae interactions, independent of the specific genetic mutation. Understanding nodule longevity and functionality may contribute to the development of strategies to enhance symbiotic efficiency in legumes for sustainable agriculture. © The Author(s) 2025. Published by Oxford University Press on behalf of American Society of Plant Biologists.

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