Abstract
Main conclusion
Lysin motif (LysM)-receptor-like kinase (RLK) and leucine-rich repeat (LRR)-RLK mediated signaling play important roles in the development and regulation of root nodule symbiosis in legumes.
Abstract
The availability of water and nutrients in the soil is a major limiting factor affecting crop productivity. Plants of the Leguminosae family form a symbiotic association with nitrogen-fixing Gram-negative soil bacteria, rhizobia for nitrogen fixation. This symbiotic relationship between legumes and rhizobia depends on the signal exchange between them. Plant receptor-like kinases (RLKs) containing lysin motif (LysM) and/or leucine-rich repeat (LRR) play an important role in the perception of chemical signals from rhizobia for initiation and establishment of root nodule symbiosis (RNS) that results in nitrogen fixation. This review highlights the diverse aspects of LysM-RLK and LRR receptors including their specificity, functions, interacting partners, regulation, and associated signaling in RNS. The activation of LysM-RLKs and LRR-RLKs is important for ensuring the successful interaction between legume roots and rhizobia. The intracellular regions of the receptors enable additional layers of signaling that help in the transduction of signals intracellularly. Additionally, symbiosis receptor-like kinase (SYMRK) containing the LRR motif acts as a co-receptor with Nod factors receptors (LysM-RLK). Cleavage of the malectin-like domain from the SYMRK ectodomain is a mechanism for controlling SYMRK stability. Overall, this review has discussed different aspects of legume receptors that are critical to the perception of signals from rhizobia and their subsequent role in creating the mutualistic relationship necessary for nitrogen fixation. Additionally, it has been discussed how crucial it is to extrapolate the knowledge gained from model legumes to crop legumes such as chickpea and common bean to better understand the mechanism underlying nodule formation in crop legumes. Future directions have also been proposed in this regard.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The datasets generated or analyzed during the current study are presented in the article.
References
Ané J-MM, Kiss GB, Riely BK et al (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science (80-) 303:1364–1367. https://doi.org/10.1126/science.1092986
Antolín-Llovera M, Ried MK, Parniske M (2014) Cleavage of the symbiosis receptor-like kinase ectodomain promotes complex formation with nod factor receptor 5. Curr Biol 24:422–427. https://doi.org/10.1016/j.cub.2013.12.053
Arrighi J, Barre A, Amor B et al (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142(1):265–279. https://doi.org/10.1104/pp.106.084657
Bensmihen S, de Billy F, Gough C (2011) Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE. https://doi.org/10.1371/JOURNAL.PONE.0026114
Bozsoki Z, Gysel K, Hansen SB et al (2020) Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity. Science 369:663–670. https://doi.org/10.1126/science.abb3377
Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7:191–226. https://doi.org/10.1146/annurev.cb.07.110191.001203
Broghammer A, Krusell L, Blaise M et al (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109:13859–13864. https://doi.org/10.1073/pnas.1205171109
Capoen W, Goormachtig S, De Rycke R et al (2005) SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102:10369–10374. https://doi.org/10.1073/pnas.0504250102
Cerri MR, Wang Q, Stolz P et al (2017) The ERN1 transcription factor gene is a target of the CCaMK/CYCLOPS complex and controls rhizobial infection in Lotus japonicus. New Phytol 215:323–337. https://doi.org/10.1111/nph.14547
Chakraborty S, Nguyen B, Wasti SD, Xu G (2019) Plant leucine-rich repeat receptor kinase (LRR-RK): structure, ligand perception, and activation mechanism. Molecules 24:3081. https://doi.org/10.3390/MOLECULES24173081
Charpentier M, Bredemeier R, Wanner G et al (2008) Lotus japonicus Castor and Pollux are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479. https://doi.org/10.1105/tpc.108.063255
Charpentier M, Sun J, Martins TV et al (2016) Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352(6289):1102–1105. https://doi.org/10.1126/science.aae0109
Chen T, Zhu H, Ke D et al (2012) A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24:823–838. https://doi.org/10.1105/tpc.112.095984
den Herder G, Yoshida S, Antolín-Llovera M et al (2012) Lotus japonicus E3 ligase SEVEN IN ABSENTIA4 destabilizes the symbiosis receptor-like Kinase SYMRK and negatively regulates rhizobial infection. Plant Cell 24:1691–1707. https://doi.org/10.1105/tpc.110.082248
Endre G, Kereszt A, Kevei Z et al (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966. https://doi.org/10.1038/nature00842
Ferguson BJ, Indrasumunar A, Hayashi S et al (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52:61–76. https://doi.org/10.1111/j.1744-7909.2010.00899.x
Fonouni-Farde C, Tan S, Baudin M et al (2016) DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nat Commun 7:1–13. https://doi.org/10.1038/ncomms12636
Frugier F, Kosuta S, Murray JD et al (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120. https://doi.org/10.1016/j.tplants.2008.01.003
Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300. https://doi.org/10.1128/mmbr.68.2.280-300.2004
Gamas P, Brault M, Jardinaud MF, Frugier F (2017) Cytokinins in symbiotic nodulation: when, where, what for? Trends Plant Sci 22:792–802. https://doi.org/10.1016/j.tplants.2017.06.012
Gherbi H, Markmann K, Svistoonoff S et al (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932. https://doi.org/10.1073/pnas.0710618105
Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693. https://doi.org/10.1105/tpc.106.043778
Göttfert M (1993) Regulation and function of rhizobial nodulation genes. FEMS Microbiol Rev 10:39–63. https://doi.org/10.1111/J.1574-6968.1993.TB05863.X
Haney CH, Riely BK, Tricoli DM et al (2011) Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23:2774–2787. https://doi.org/10.1105/tpc.111.086389
Hayashi T, Shimoda Y, Sato S et al (2014) Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca 2+ spiking. Plant J 77:146–159. https://doi.org/10.1111/tpj.12374
He J, Zhang C, Dai H et al (2019) A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Mol Plant 12:1561–1576. https://doi.org/10.1016/j.molp.2019.10.015
He C, Gao H, Wang H et al (2021) GSK3-mediated stress signaling inhibits legume–rhizobium symbiosis by phosphorylating GmNSP1 in soybean. Mol Plant 14:488–502. https://doi.org/10.1016/j.molp.2020.12.015
Indrasumunar A, Wilde J, Hayashi S et al (2015) Functional analysis of duplicated Symbiosis Receptor Kinase (SymRK) genes during nodulation and mycorrhizal infection in soybean (Glycine max). J Plant Physiol 176:157–168. https://doi.org/10.1016/j.jplph.2015.01.002
Isidra-Arellano MC, Pozas-Rodríguez EA, Rocío Reyero-Saavedra M et al (2020) Inhibition of legume nodulation by Pi deficiency is dependent on the autoregulation of nodulation (AON) pathway. Plant J 103:1125–1139. https://doi.org/10.1111/tpj.14789
Jin Y, Liu H, Luo D et al (2016) DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat Commun 7:1–14. https://doi.org/10.1038/ncomms12433
Kalo P, Kaló P, Gleason C et al (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science (80-) 308:1786–1789. https://doi.org/10.1126/science.1110951
Kawaharada Y, Kelly S, Nielsen MW et al (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–312. https://doi.org/10.1038/nature14611
Kawaharada Y, James EK, Kelly S et al (2017a) The ethylene responsive factor required for nodulation 1 (ERN1) transcription factor is required for infection-thread formation in Lotus japonicus. Mol Plant-Microbe Interact 30:194–204. https://doi.org/10.1094/MPMI-11-16-0237-R
Kawaharada Y, Nielsen MW, Kelly S et al (2017b) Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia. Nat Commun 8:1–11. https://doi.org/10.1038/ncomms14534
Ke D, Fang Q, Chen C et al (2012) The small GTPase ROP6 interacts with NFR5 and is involved in nodule formation in Lotus japonicus. Plant Physiol 159:131–143. https://doi.org/10.1104/pp.112.197269
Kelly S, Sullivan JT, Kawaharada Y et al (2018) Regulation of Nod factor biosynthesis by alternative NodD proteins at distinct stages of symbiosis provides additional compatibility scrutiny. Environ Microbiol 20:97–110. https://doi.org/10.1111/1462-2920.14006
Kevei Z, Lougnon G, Mergaert P et al (2007) 3-Hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:3974–3989. https://doi.org/10.1105/tpc.107.053975
Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421. https://doi.org/10.1016/0968-0004(94)90090-6
Kosuta S, Held M, Hossain MS et al (2011) Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J 67:929–940. https://doi.org/10.1111/j.1365-313X.2011.04645.x
Krusell L, Sato N, Fukuhara I et al (2011) The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation. Plant J 65:861–871. https://doi.org/10.1111/j.1365-313X.2010.04474.x
Lévy J, Bres C, Geurts R et al (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science (80-) 303:1361–1364. https://doi.org/10.1126/science.1093038
Li H, Chen M, Duan L et al (2018) Domain swap approach reveals the critical roles of different domains of SYMRK in root nodule symbiosis in Lotus japonicus. Front Plant Sci 9:697. https://doi.org/10.3389/fpls.2018.00697
Li X, Zheng Z, Kong X et al (2019) Atypical receptor kinase RINRK1 required for rhizobial infection but not nodule development in Lotus japonicus. Plant Physiol 181:804–816. https://doi.org/10.1104/pp.19.00509
Liang P, Stratil TF, Popp C et al (2018) Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains. Proc Natl Acad Sci USA 115:5289–5294. https://doi.org/10.1073/pnas.1721868115
Limpens E, Franken C, Smit P et al (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science (80-) 302:630–633. https://doi.org/10.1126/science.1090074
Limpens E, Mirabella R, Fedorova E et al (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380. https://doi.org/10.1073/pnas.0504284102
Madsen EB, Madsen LH, Radutoiu S et al (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640. https://doi.org/10.1038/nature02045
Madsen EB, Antolín-Llovera M, Grossmann C et al (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J 65:404–417. https://doi.org/10.1111/j.1365-313X.2010.04431.x
Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor- kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:e68. https://doi.org/10.1371/journal.pbio.0060068
Mbengue M, Camut S, de Carvalho-Niebel F et al (2010) The medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22:3474–3488. https://doi.org/10.1105/tpc.110.075861
Mergaert P, Uchiumi T, Alunni B et al (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103:5230–5235. https://doi.org/10.1073/pnas.0600912103
Moling S, Pietraszewska-Bogiel A, Postma M et al (2014) Nod factor receptors form heteromeric complexes and are essential for intracellular infection in Medicago nodules. Plant Cell 26:4188–4199. https://doi.org/10.1105/tpc.114.129502
Monahan-Giovanelli H, Pinedo CA, Gage DJ (2006) Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol 140:661–670. https://doi.org/10.1104/pp.105.072876
Murakami E, Cheng J, Gysel K et al (2018) Epidermal LysM receptor ensures robust symbiotic signalling in Lotus japonicus. Elife 7:e33506. https://doi.org/10.7554/eLife.33506
Nishida H, Suzaki T (2018) Nitrate-mediated control of root nodule symbiosis. Curr Opin Plant Biol 44:129–136. https://doi.org/10.1016/j.pbi.2018.04.006
Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume–rhizobial symbiosis. Annu Rev Genet 45:119–144. https://doi.org/10.1146/annurev-genet-110410-132549
Ott T (2017) Membrane nanodomains and microdomains in plant–microbe interactions. Curr Opin Plant Biol 40:82–88. https://doi.org/10.1016/j.pbi.2017.08.008
Ouma EW, Asango AM, Maingi J, Njeru EM (2016) Elucidating the potential of native rhizobial isolates to improve biological nitrogen fixation and growth of common bean and soybean in smallholder farming systems of Kenya. Int J Agronomy 2016:1–7. https://doi.org/10.1155/2016/4569241
Pan H, Stonoha-Arther C, Wang D (2018) Medicago plants control nodulation by regulating proteolysis of the receptor-like kinase DMI2. Plant Physiol 177:792–802. https://doi.org/10.1104/pp.17.01542
Peiter E, Sun J, Heckmann AB et al (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145:192–203. https://doi.org/10.1104/pp.107.097261
Radutoiu S, Madsen L, Madsen E et al (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425(6958):585–592. https://doi.org/10.1038/nature02039
Ried MK, Antolín-Llovera M, Parniske M (2014) Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases. Elife 3:1–17. https://doi.org/10.7554/eLife.03891
Rutten L, Miyata K, Roswanjaya YP et al (2020) Duplication of symbiotic Lysin Motif-receptors predates the evolution of nitrogen-fixing nodule symbiosis. Plant Physiol. https://doi.org/10.1104/pp.19.01420
Saha S, Paul A, Herring L et al (2016) Gatekeeper tyrosine phosphorylation of SYMRK is essential for synchronizing the epidermal and cortical responses in root nodule symbiosis. Plant Physiol 171:71–81. https://doi.org/10.1104/pp.15.01962
Sánchez-López R, Jáuregui D, Nava N et al (2011) Down-regulation of SymRK correlates with a deficiency in vascular bundle development in Phaseolus vulgaris nodules. Plant Cell Environ 34:2109–2121. https://doi.org/10.1111/j.1365-3040.2011.02408.x
Schallus T, Jaeckh C, Fehér K et al (2008) Malectin: a novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation. Mol Biol Cell 19:3404. https://doi.org/10.1091/MBC.E08-04-0354
Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195. https://doi.org/10.1038/46058
Schroeder JI, Delhaize E, Frommer WB et al (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66. https://doi.org/10.1038/nature11909
Singh J, Valdés-López O (2022a) A nodule peptide confiscates haem to promote iron uptake in rhizobia. Trends Plant Sci 28:125–127. https://doi.org/10.1016/j.tplants.2022.11.005
Singh J, Valdés-López O (2022b) Discovering the genetic modules controlling root nodule symbiosis under abiotic stresses: salinity as a case study. New Phytol 237(4):1082–1085. https://doi.org/10.1111/nph.18627
Singh J, Verma PK (2021) NSP1 allies with GSK3 to inhibit nodule symbiosis. Trends Plant Sci 26:999–1001. https://doi.org/10.1016/j.tplants.2021.07.001
Singh J, Verma PK (2023) Plant transcription factors and nodule development. In: Plant transcription factors. Elsevier, pp 175–196. https://doi.org/10.1016/B978-0-323-90613-5.00020-0
Singh S, Katzer K, Lambert J et al (2014) CYCLOPS, A DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:139–152. https://doi.org/10.1016/j.chom.2014.01.011
Singh J, Varshney V, Mishra V (2023) AUR1 and its pals: orchestration of intracellular rhizobia infection in legume for nitrogen fixation. Plant Cell Rep 1:3. https://doi.org/10.1007/s00299-023-02979-x
Smit P, Raedts J, Portyanko V et al (2005) NSP1 of the GRAS protein family is essential for rhizobial nod factor-induced transcription. Science (80-) 308:1789–1791. https://doi.org/10.1126/science.1111025
Smit P, Limpens E, Geurts R et al (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145(1):183–191. https://doi.org/10.1104/pp.107.100495
Soyano T, Kouchi H, Hirota A, Hayashi M (2013) NODULE INCEPTION directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet 9:e1003352. https://doi.org/10.1371/journal.pgen.1003352
Stracke S, Kistner C, Yoshida S et al (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962. https://doi.org/10.1038/nature00841
Takeda N, Maekawa T, Hayashi M (2012) Nuclear-localized and deregulated calcium- and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24:810–822. https://doi.org/10.1105/tpc.111.091827
Tirichine L, Sandal N, Madsen LH et al (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science (80-) 315:104–107. https://doi.org/10.1126/science.1132397
Tóth K, Stratil TF, Madsen EB et al (2012) Functional domain analysis of the remorin protein LjSYMREM1 in Lotus japonicus. PLoS ONE 7:e30817. https://doi.org/10.1371/journal.pone.0030817
Van Brussel AAN, Bakhuizen R, Van Spronsen PC et al (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of rhizobium. Science (80-) 257:70–72. https://doi.org/10.1126/science.257.5066.70
van Velzen R, Holmer R, Bu F et al (2018) Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. Proc Natl Acad Sci USA 115:E4700–E4709. https://doi.org/10.1073/pnas.1721395115
Vernié T, Kim J, Frances L et al (2015) The NIN transcription factor coordinates diverse nodulation programs in different tissues of the medicago truncatula root. Plant Cell 27:3410–3424. https://doi.org/10.1105/tpc.15.00461
Vernié T, Camut S, Camps C et al (2016) PUB1 interacts with the receptor kinase DMI2 and negatively regulates rhizobial and arbuscular mycorrhizal symbioses through its ubiquitination activity in medicago truncatula. Plant Physiol 170:2312–2324. https://doi.org/10.1104/pp.15.01694
Wais RJ, Galera C, Oldroyd G et al (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci USA 97:13407–13412. https://doi.org/10.1073/pnas.230439797
Wang D, Griffitts J, Starker C et al (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science (80-) 327:1126–1129. https://doi.org/10.1126/science.1184096
Wong JEMM, Nadzieja M, Madsen LH et al (2019) A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation. Proc Natl Acad Sci USA 116:14339–14348. https://doi.org/10.1073/pnas.1815425116
Wong JEMM, Gysel K, Birkefeldt TG et al (2020) Structural signatures in EPR3 define a unique class of plant carbohydrate receptors. Nat Commun. https://doi.org/10.1038/s41467-020-17568-9
Xie F, Murray JD, Kim J et al (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109:633–638. https://doi.org/10.1073/pnas.1113992109
Yoshida S, Parniske M (2005) Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J Biol Chem 280:9203–9209. https://doi.org/10.1074/jbc.M411665200
Yuan S, Zhu H, Gou H et al (2012) A ubiquitin ligase of symbiosis receptor kinase involved in nodule organogenesis. Plant Physiol 160:106–117. https://doi.org/10.1104/pp.112.199000
Zhu H, Chen T, Zhu M et al (2008) A Novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148:337–347. https://doi.org/10.1104/pp.108.119164
Acknowledgements
JS thanks the Council of Scientific & Industrial Research, Government of India, for the fellowship.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The author declare that there is no conflict of interest.
Additional information
Communicated by Gerhard Leubner.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Singh, J., Verma, P.K. Role of Nod factor receptors and its allies involved in nitrogen fixation. Planta 257, 54 (2023). https://doi.org/10.1007/s00425-023-04090-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04090-7