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1. Sinorhizobium meliloti succinylated high‐molecular‐weight succinoglycan and the Medicago truncatula LysM receptor‐like kinase MtLYK10 participate independently in symbiotic infection

   https://doi.org/10.1111/tpj.14625  

   Maillet, Fabienne ; Fournier, Joëlle ; Mendis, Hajeewaka C. ; Tadege, Million ; Wen, Jiangqi ; Ratet, Pascal ; Mysore, Kirankumar S. ; Gough, Clare ; Jones, Kathryn M. ( January 2020 , The Plant Journal)

   The formation of nitrogen‐fixing nodules on legume hosts is a finely tuned process involving many components of both symbiotic partners. Production of the exopolysaccharide succinoglycan by the nitrogen‐fixing bacteriumSinorhizobium meliloti1021 is needed for an effective symbiosis withMedicagospp., and the succinyl modification to this polysaccharide is critical. However, it is not known when succinoglycan intervenes in the symbiotic process, and it is not known whether the plant lysin‐motif receptor‐like kinase MtLYK10 intervenes in recognition of succinoglycan, as might be inferred from work on theLotus japonicusMtLYK10 ortholog, LjEPR3. We studied the symbiotic infection phenotypes ofS. melilotimutants deficient in succinoglycan production or producing modified succinoglycan, in wild‐typeMedicago truncatulaplants and inMtlyk10mutant plants. On wild‐type plants,S. melilotistrains producing no succinoglycan or only unsuccinylated succinoglycan still induced nodule primordia and epidermal infections, but further progression of the symbiotic process was blocked. TheseS. melilotimutants induced a more severe infection phenotype onMtlyk10mutant plants. Nodulation by succinoglycan‐defective strains was achieved byin transrescue with a Nod factor‐deficientS. melilotimutant. While the Nod factor‐deficient strain was always more abundant inside nodules, the succinoglycan‐deficient strain was more efficient than the strain producing only unsuccinylated succinoglycan. Together, these data show that succinylated succinoglycan is essential for infection thread formation inM. truncatula, and that MtLYK10 plays an important, but different role in this symbiotic process. These data also suggest that succinoglycan is more important than Nod factors for bacterial survival inside nodules.

    

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2. A newly evolved chimeric lysin motif receptor‐like kinase in Medicago truncatula spp. tricycla R108 extends its Rhizobia symbiotic partnership

   https://doi.org/10.1111/nph.18270  

   Luu, Thi‐Bich ; Ourth, Anna ; Pouzet, Cécile ; Pauly, Nicolas ; Cullimore, Julie ( June 2022 , New Phytologist)

   Rhizobial lipochitooligosaccharidic Nod factors (NFs), specified bynodgenes, are the primary determinants of host specificity in the legume–Rhizobia symbiosis.

   We examined the nodulation ability ofMedicago truncatulacv Jemalong A17 andM. truncatulassp.tricyclaR108 with theSinorhizobium meliloti nodF/nodLmutant, which produces modified NFs. We then applied genetic and functional approaches to study the genetic basis and mechanism of nodulation of R108 by this mutant.

   We show that thenodF/nodLmutant can nodulate R108 but not A17. Using genomics and reverse genetics, we identified a newly evolved, chimeric LysM receptor‐like kinase gene in R108,LYK2bis, which is responsible for the phenotype and can allow A17 to gain nodulation with thenodF/nodLmutant. We found thatLYK2bisis involved in nodulation by mutants producing nonO‐acetylated NFs and interacts with the key receptor protein NFP. Many, but not all, naturalS. melilotiandS. medicaestrains tested requireLYK2bisfor efficient nodulation of R108.

   Our findings reveal that a newly evolved gene in R108,LYK2bis, extends nodulation specificity to mutants producing nonO‐acetylated NFs and is important for nodulation by many naturalSinorhizobia. Evolution of this gene may present an adaptive advantage to allow nodulation by a greater variety of strains.

    

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3. Methylated chalcones are required for rhizobial nod gene induction in the Medicago truncatula rhizosphere

   https://doi.org/10.1111/nph.19701  

   Wu, Wenjuan ; Zhuang, Yuxin ; Chen, Dasong ; Ruan, Yiting ; Li, Fuyu ; Jackson, Kirsty ; Liu, Cheng‐Wu ; East, Alison ; Wen, Jiangqi ; Tatsis, Evangelos ; et al ( June 2024 , New Phytologist)

   Legume nodulation requires the detection of flavonoids in the rhizosphere by rhizobia to activate their production of Nod factor countersignals. Here we investigated the flavonoids involved in nodulation ofMedicago truncatula.

   We biochemically characterized five flavonoid‐O‐methyltransferases (OMTs) and a lux‐basednodgene reporter was used to investigate the response ofSinorhizobium medicaeNodD1 to various flavonoids.

   We found that chalcone‐OMT 1 (ChOMT1) and ChOMT3, but not OMT2, 4, and 5, were able to produce 4,4′‐dihydroxy‐2′‐methoxychalcone (DHMC). The bioreporter responded most strongly to DHMC, while isoflavones important for nodulation of soybean (Glycine max) showed no activity. Mutant analysis revealed that loss of ChOMT1 strongly reduced DHMC levels. Furthermore,chomt1andomt2showed strongly reduced bioreporter luminescence in their rhizospheres. In addition, loss of both ChOMT1 and ChOMT3 reduced nodulation, and this phenotype was strengthened by the further loss of OMT2.

   We conclude that: the loss of ChOMT1 greatly reduces root DHMC levels; ChOMT1 or OMT2 are important fornodgene activation in the rhizosphere; and ChOMT1/3 and OMT2 promote nodulation. Our findings suggest a degree of exclusivity in the flavonoids used for nodulation inM. truncatulacompared to soybean, supporting a role for flavonoids in rhizobial host range.

    

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4. A Medicago truncatula Autoregulation of Nodulation Mutant Transcriptome Analysis Reveals Disruption of the SUNN Pathway Causes Constitutive Expression Changes in Some Genes, but Overall Response to Rhizobia Resembles Wild-Type, Including Induction of TML1 and TML2

   https://doi.org/10.3390/cimb45060293  

   Schnabel, Elise L. ; Chavan, Suchitra A. ; Gao, Yueyao ; Poehlman, William L. ; Feltus, Frank Alex ; Frugoli, Julia A. ( June 2023 , Current Issues in Molecular Biology)

   Nodule number regulation in legumes is controlled by a feedback loop that integrates nutrient and rhizobia symbiont status signals to regulate nodule development. Signals from the roots are perceived by shoot receptors, including a CLV1-like receptor-like kinase known as SUNN in Medicago truncatula. In the absence of functional SUNN, the autoregulation feedback loop is disrupted, resulting in hypernodulation. To elucidate early autoregulation mechanisms disrupted in SUNN mutants, we searched for genes with altered expression in the loss-of-function sunn-4 mutant and included the rdn1-2 autoregulation mutant for comparison. We identified constitutively altered expression of small groups of genes in sunn-4 roots and in sunn-4 shoots. All genes with verified roles in nodulation that were induced in wild-type roots during the establishment of nodules were also induced in sunn-4, including autoregulation genes TML2 and TML1. Only an isoflavone-7-O-methyltransferase gene was induced in response to rhizobia in wild-type roots but not induced in sunn-4. In shoot tissues of wild-type, eight rhizobia-responsive genes were identified, including a MYB family transcription factor gene that remained at a baseline level in sunn-4; three genes were induced by rhizobia in shoots of sunn-4 but not wild-type. We cataloged the temporal induction profiles of many small secreted peptide (MtSSP) genes in nodulating root tissues, encompassing members of twenty-four peptide families, including the CLE and IRON MAN families. The discovery that expression of TML2 in roots, a key factor in inhibiting nodulation in response to autoregulation signals, is also triggered in sunn-4 in the section of roots analyzed, suggests that the mechanism of TML regulation of nodulation in M. truncatula may be more complex than published models. 

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5. Paired Medicago receptors mediate broad-spectrum resistance to nodulation by Sinorhizobium meliloti carrying a species-specific gene

   https://doi.org/10.1073/pnas.2214703119  

   Liu, Jinge ; Wang, Ting ; Qin, Qiulin ; Yu, Xiaocheng ; Yang, Shengming ; Dinkins, Randy D. ; Kuczmog, Anett ; Putnoky, Péter ; Muszyński, Artur ; Griffitts, Joel S. ; et al ( December 2022 , Proceedings of the National Academy of Sciences)

   Plants have evolved the ability to distinguish between symbiotic and pathogenic microbial signals. However, potentially cooperative plant–microbe interactions often abort due to incompatible signaling. The Nodulation Specificity 1 ( NS1 ) locus in the legume Medicago truncatula blocks tissue invasion and root nodule induction by many strains of the nitrogen-fixing symbiont Sinorhizobium meliloti . Controlling this strain-specific nodulation blockade are two genes at the NS1 locus, designated NS1a and NS1b , which encode malectin-like leucine-rich repeat receptor kinases. Expression of NS1a and NS1b is induced upon inoculation by both compatible and incompatible Sinorhizobium strains and is dependent on host perception of bacterial nodulation (Nod) factors. Both presence/absence and sequence polymorphisms of the paired receptors contribute to the evolution and functional diversification of the NS1 locus. A bacterial gene, designated rns1 , is required for activation of NS1 -mediated nodulation restriction. rns1 encodes a type I-secreted protein and is present in approximately 50% of the nearly 250 sequenced S. meliloti strains but not found in over 60 sequenced strains from the closely related species Sinorhizobium medicae . S. meliloti strains lacking functional rns1 are able to evade NS1 -mediated nodulation blockade. 

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