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  1. Summary

    Symbiotic nitrogen fixation in legumes is mediated by an interplay of signaling processes between plant hosts and rhizobial symbionts. In legumes, several secreted protein families have undergone expansions and play key roles in nodulation. Thus, identifying lineage‐specific expansions (LSEs) of nodulation‐associated genes can be a strategy to discover candidate gene families.

    Using bioinformatic tools, we identified 13LSEs of nodulation‐related secreted protein families, each unique to eitherGlycine,ArachisorMedicagolineages. In theMedicagolineage, nodule‐specific Polycystin‐1, Lipoxygenase, Alpha Toxin (PLAT) domain proteins (NPDs) expanded to five members. We examinedNPDfunction usingCRISPR/Cas9 multiplex genome editing to createMedicago truncatulaNPDknockout lines, targeting one to fiveNPDgenes.

    Mutant lines with differing combinations ofNPDgene inactivations had progressively smaller nodules, earlier onset of nodule senescence, or ineffective nodules compared to the wild‐type control. Double‐ and triple‐knockout lines showed dissimilar nodulation phenotypes but coincided in upregulation of aDHHC‐type zinc finger and an aspartyl protease gene, possible candidates for the observed disturbance of proper nodule function.

    By postulating that gene family expansions can be used to detect candidate genes, we identified a family of nodule‐specificPLATdomain proteins and confirmed that they play a role in successful nodule formation.

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  2. Abstract

    In the legume‐rhizobia mutualism, the benefit each partner derives from the other depends on the genetic identity of both host and rhizobial symbiont. To gain insight into the extent of genome × genome interactions on hosts at the molecular level and to identify potential mechanisms responsible for the variation, we examined host gene expression within nodules (the plant organ where the symbiosis occurs) of four genotypes ofMedicago truncatulagrown with eitherEnsifer melilotiorE. medicaesymbionts. These host × symbiont combinations show significant variation in nodule and biomass phenotypes. Likewise, combinations differ in their transcriptomes: host, symbiont and host × symbiont affected the expression of 70%, 27% and 21%, respectively, of the approximately 27,000 host genes expressed in nodules. Genes with the highest levels of expression often varied between hosts and/or symbiont strain and include leghemoglobins that modulate oxygen availability and hundreds of Nodule Cysteine‐Rich (NCR) peptides involved in symbiont differentiation and viability in nodules. Genes with host × symbiont‐dependent expression were enriched for functions related to resource exchange between partners (sulphate/iron/amino acid transport and dicarboxylate/amino acid synthesis). These enrichments suggest mechanisms for host control of the currencies of the mutualism. The transcriptome ofM. truncatulaaccessionHM101 (A17), the reference genome used for most molecular research, was less affected by symbiont identity than the other hosts. These findings underscore the importance of assessing the molecular basis of variation in ecologically important traits, particularly those involved in biotic interactions, in multiple genetic contexts.

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