Genetic innovations underlying the evolution of root nodule symbiosis in Leguminosae

Tengfei Liu; Hao Lin; Zhixi Tian

doi:10.1016/j.jgg.2025.09.008

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Genetic innovations underlying the evolution of root nodule symbiosis in Leguminosae

doi: 10.1016/j.jgg.2025.09.008

a. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China;
b. Yazhouwan National Laboratory, Sanya, Hainan 572024, China

Funds:

This work was supported by The National Natural Science Foundation of China (32300512), and the Xplorer Prize.

Received Date: 2025-07-28
Accepted Date: 2025-09-24
Rev Recd Date: 2025-09-24

Available Online: 2025-10-10

Abstract

Abstract

Root nodule symbiosis (RNS) is a mutualistic association formed between nitrogen-fixing rhizobia or Frankia and host plants limited to four orders within Rosid I—Fabales, Fagales, Cucurbitales and Rosales—which comprise the so-called ‘Nitrogen Fixing Nodulation Clade’ (NFNC). The majority of nodulation studies have focused on Leguminosae, given their agricultural and environmental importance, as well as the widespread occurrence of nodulation among members of this family. Endowing cereal crops with nitrogen fixation, like Leguminosae, presents a strategy to reduce the detrimental effects of synthetic fertilizer overuse. Different hypotheses on the origin of RNS have been proposed, however key genetic innovations underlying the evolution of RNS, even in Leguminsoae, have been rarely reported. In this review, we begin by examining current knowledge of genetic innovations—including gene gain, gene loss, and the acquisition or loss of conserved noncoding sequences (CNS) in preexisting genes. We explore the available evidence supporting these genetic innovations underlying the evolution of RNS in Leguminosae and offer the phylogenomics approach that could be applied to uncover these genetic innovations. Finally, we conclude by proposing a model of genetic innovations underlying the evolution of RNS in Leguminsoae and consider the potential implications for the development of nitrogen-fixing crops.
- Root nodule symbiosis,
- Leguminosae,
- Genetic innovations,
- Gene gain,
- Gene loss,
- Conserved noncoding sequences,
- Phylogenomics

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References(102)

References

Albalat, R., Canestro, C., 2016. Evolution by gene loss. Nat. Rev. Genet. 17, 379-391.

Aravind, L., Watanabe, H., Lipman, D.J., Koonin, E.V., 2000. Lineage-specific loss and divergence of functionally linked genes in eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 97, 11319-11324.

Arrighi, J.F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L.C., Mirabella, R., de Carvalho-Niebel, F., Journet, E.P., Gherardi, M., Huguet, T., et al., 2006. The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265-279.

Arrighi, J.F., Godfroy, O., de Billy, F., Saurat, O., Jauneau, A., Gough, C., 2008. The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc. Natl. Acad. Sci. U. S. A. 105, 9817-9822.

Azani, N., Babineau, M., Bailey, C.D., Banks, H., Barbosa, A.R., Pinto, R.B., Boatwright, J.S., Borges, L.M., Brown, G.K., Bruneau, A., et al., 2017. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: The Legume Phylogeny Working Group (LPWG). Taxon 66, 44-77.

Bergthorsson, U., Andersson, D.I., Roth, J.R., 2007. Ohno's dilemma: Evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. U. S. A. 104, 17004-17009.

Bowles, A.M.C., Paps, J., Bechtold, U., 2022. Water-related innovations in land plants evolved by different patterns of gene cooption and novelty. New Phytol. 235, 732-742.

Cai, L., Arnold, B.J., Xi, Z., Khost, D.E., Patel, N., Hartmann, C.B., Manickam, S., Sasirat, S., Nikolov, L.A., Mathews, S., et al., 2021. Deeply altered genome architecture in the endoparasitic flowering plant Sapria himalayana Griff. (Rafflesiaceae). Curr. Biol. 31, 1002-1011.e9.

Campbell, M.A., Zhu, W., Jiang, N., Lin, H., Ouyang, S., Childs, K.L., Haas, B.J., Hamilton, J.P., Buell, C.R., 2007. Identification and characterization of lineage-specific genes within the Poaceae. Plant Physiol. 145, 1311-1322.

Capoen, W., Sun, J., Wysham, D., Otegui, M.S., Venkateshwaran, M., Hirsch, S., Miwa, H., Downie, J.A., Morris, R.J., Ane, J.-M., et al., 2011. Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl. Acad. Sci. U. S. A. 108, 14348-14353.

Castro, L.F., Goncalves, O., Mazan, S., Tay, B.H., Venkatesh, B., Wilson, J.M., 2014. Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history. Proc. Biol. Sci. 281, 20132669.

Cathebras, C., Gong, X., Andrade, R.E., Vondenhoff, K., Hayashi, M., Keller, J., Delaux, P.M., Griesmann, M., Parniske, M., 2022. A novel cis-element enabled bacterial uptake by plant cells. bioRxiv, 2022.03. 28.486070.

Cerri, M.R., Wang, Q., Stolz, P., Folgmann, J., Frances, L., Katzer, K., Li, X., Heckmann, A.B., Wang, T.L., Downie, J.A., 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.

Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., Parniske, M., 2008. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467-3479.

Chen, H., Yu, H., Yuan, L., Kong, L., Li, S., Cao, X., Li, Y., Wang, Y., Lin, L., Guo, R., et al., 2025. A naturally occurring SNP modulates thermotolerance divergence among grapevines. Nat. Commun. 16, 5084.

Ciren, D., Zebell, S., Lippman, Z.B., 2024. Extreme restructuring of cis-regulatory regions controlling a deeply conserved plant stem cell regulator. PLoS Genet. 20, e1011174.

Clark, J.W., 2023. Genome evolution in plants and the origins of innovation. New Phytol. 240, 2204-2209.

Combier, J.P., Vernie, T., de Billy, F., El Yahyaoui, F., Mathis, R., Gamas, P., 2007. The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiol. 144, 703-716.

Dakovic, N., Terezol, M., Pitel, F., Maillard, V., Elis, S., Leroux, S., Lagarrigue, S., Gondret, F., Klopp, C., Baeza, E., et al., 2014. The loss of adipokine genes in the chicken genome and implications for insulin metabolism. Mol. Biol. Evol. 31, 2637-2646.

de Faria, S.M., Ringelberg, J.J., Gross, E., Koenen, E.J.M., Cardoso, D., Ametsitsi, G.K.D., Akomatey, J., Maluk, M., Tak, N., Gehlot, H.S., et al., 2022. The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes. New Phytol. 235, 2365-2377.

De Smet, R., Adams, K.L., Vandepoele, K., Van Montagu, M.C., Maere, S., Van de Peer, Y., 2013. Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl. Acad. Sci. U. S. A. 110, 2898-2903.

Delaux, P.M., 2017. Comparative phylogenomics of symbiotic associations. New Phytol. 213, 89-94.

Demuth, J.P., Hahn, M.W., 2009. The life and death of gene families. Bioessays 31, 29-39.

Domonkos, A., Kovacs, S., Gombar, A., Kiss, E., Horvath, B., Kovats, G.Z., Farkas, A., Toth, M.T., Ayaydin, F., Boka, K., et al., 2017. NAD1 controls defense-like responses in Medicago truncatula symbiotic nitrogen fixing nodules following rhizobial colonization in a BacA-independent manner. Genes 8, 387.

Dong, R., Wang, W., Luo, N., Li, H., Liu, J., Wang, Y., Ye, Y., Zhu, H., Li, F., Yu, H., et al., 2025. MtNAD1 associates with the autophagy complex to contribute to the degradation of immunity-related proteins in Medicago truncatula nodules. New Phytol. 245, 2186-2201.

Dong, W., Zhu, Y., Chang, H., Wang, C., Yang, J., Shi, J., Gao, J., Yang, W., Lan, L., Wang, Y., et al., 2021. An SHR-SCR module specifies legume cortical cell fate to enable nodulation. Nature 589, 586-590.

Ehrhardt, D.W., Atkinson, E.M., Long, S.R., 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256, 998-1000.

Emms, D.M., Kelly, S., 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238.

Feng, J., Lee, T., Schiessl, K., Oldroyd, G.E.D., 2021. Processing of NODULE INCEPTION controls the transition to nitrogen fixation in root nodules. Science 374, 629-632.

Gage, D.J., 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280-300.

Gleason, C., Chaudhuri, S., Yang, T., Munoz, A., Poovaiah, B.W., Oldroyd, G.E.D., 2006. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149-1152.

Gogarten, J.P., Townsend, J.P., 2005. Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3, 679-687.

Griesmann, M., Chang, Y., Liu, X., Song, Y., Haberer, G., Crook, M.B., Billault-Penneteau, B., Lauressergues, D., Keller, J., Imanishi, L., et al., 2018. Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361, eaat1743.

Guijarro-Clarke, C., Holland, P.W.H., Paps, J., 2020. Widespread patterns of gene loss in the evolution of the animal kingdom. Nat. Ecol. Evol. 4, 519-523.

Guo, K., Yang, J., Yu, N., Luo, L., Wang, E., 2023. Biological nitrogen fixation in cereal crops: Progress, strategies, and perspectives. Plant Commun. 4, 100499.

Hakoyama, T., Niimi, K., Yamamoto, T., Isobe, S., Sato, S., Nakamura, Y., Tabata, S., Kumagai, H., Umehara, Y., Brossuleit, K., et al., 2012. The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225-236.

Hendelman, A., Zebell, S., Rodriguez-Leal, D., Dukler, N., Robitaille, G., Wu, X., Kostyun, J., Tal, L., Wang, P., Bartlett, M.E., et al., 2021. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection. Cell 184, 1724-1739.e16.

Herridge, D.F., Peoples, M.B., Boddey, R.M., 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311, 1-18.

Hirsch, S., Kim, J., Munoz, A., Heckmann, A.B., Downie, J.A., Oldroyd, G.E.D., 2009. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21, 545-557.

Hubisz, M.J., Pollard, K.S., Siepel, A., 2010. PHAST and RPHAST: phylogenetic analysis with space/time models. Briefings Bioinf. 12, 41-51.

Jiang, S., Jardinaud, M.F., Gao, J., Pecrix, Y., Wen, J., Mysore, K., Xu, P., Sanchez-Canizares, C., Ruan, Y., Li, Q., et al., 2021. NIN-like protein transcription factors regulate leghemoglobin genes in legume nodules. Science 374, 625-628.

Jones, K.M., Kobayashi, H., Davies, B.W., Taga, M.E., Walker, G.C., 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5, 619-633.

Kaessmann, H., 2010. Origins, evolution, and phenotypic impact of new genes. Genome Res. 20, 1313-1326.

Kaessmann, H., Zollner, S., Nekrutenko, A., Li, W.H., 2002. Signatures of domain shuffling in the human genome. Genome Res. 12, 1642-1650.

Kang, H., Chu, X., Wang, C., Xiao, A., Zhu, H., Yuan, S., Yang, Z., Ke, D., Xiao, S., Hong, Z., et al., 2014. A MYB coiled-coil transcription factor interacts with NSP2 and is involved in nodulation in Lotus japonicus. New Phytol. 201, 837-849.

Kates, H.R., O’Meara, B.C., LaFrance, R., Stull, G.W., James, E.K., Liu, S.Y., Tian, Q., Yi, T.S., Conde, D., Kirst, M., et al., 2024. Shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants. Nat. Commun. 15, 4262.

Keeling, P.J., Palmer, J.D., 2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618.

Kvon, E.Z., Kamneva, O.K., Melo, U.S., Barozzi, I., Osterwalder, M., Mannion, B.J., Tissieres, V., Pickle, C.S., Plajzer-Frick, I., Lee, E.A., et al., 2016. Progressive loss of function in a limb enhancer during snake evolution. Cell 167, 633-642.e11.

LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371-379.

Lee, U., Arsala, D., Xia, S., Li, C., Ali, M., Svetec, N., Langer, C.B., Sobreira, D.R., Eres, I., Sosa, D., et al., 2024. The three-dimensional genome drives the evolution of asymmetric gene duplicates via enhancer capture-divergence. Sci. Adv. 10, eadn6625.

Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ane, J.M., Lauber, E., Bisseling, T., et al., 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361-1364.

Li, L., Stoeckert, C.J., Jr., Roos, D.S., 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189.

Li, X., Liu, M., Cai, M., Chiasson, D., Groth, M., Heckmann, A.B., Wang, T.L., Parniske, M., Downie, J.A., Xie, F., 2023. RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus. PLoS Genet. 19, e1010621.

Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., Geurts, R., 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630-633.

Lin, H., Moghe, G., Ouyang, S., Iezzoni, A., Shiu, S.H., Gu, X., Buell, C.R., 2010. Comparative analyses reveal distinct sets of lineage-specific genes within Arabidopsis thaliana. BMC Evol. Biol. 10, 41.

Lin, Z., Chen, L., Chen, X., Zhong, Y., Yang, Y., Xia, W., Liu, C., Zhu, W., Wang, H., Yan, B., et al., 2019. Biological adaptations in the Arctic cervid, the reindeer (Rangifer tarandus). Science 364, eaav6312.

Liu, J., Rutten, L., Limpens, E., van der Molen, T., van Velzen, R., Chen, R., Chen, Y., Geurts, R., Kohlen, W., Kulikova, O., et al., 2019. A remote cis-regulatory region is required for NIN expression in the pericycle to initiate nodule primordium formation in Medicago truncatula. Plant Cell 31, 68-83.

Liu, T., Liu, H., Xian, W., Liu, Z., Yuan, Y., Fan, J., Xiang, S., Yang, X., Liu, Y., Liu, S., et al., 2024a. Duplication and sub-functionalization of flavonoid biosynthesis genes plays important role in Leguminosae root nodule symbiosis evolution. J. Integr. Plant Biol. 66, 2191-2207.

Liu, T., Liu, Z., Fan, J., Yuan, Y., Liu, H., Xian, W., Xiang, S., Yang, X., Liu, Y., Liu, S., et al., 2024b. Loss of Lateral suppressor gene is associated with evolution of root nodule symbiosis in Leguminosae. Genome Biol. 25, 250.

Madsen, E.B., Madsen, L.H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., et al., 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640.

Masson-Boivin, C., Sachs, J.L., 2018. Symbiotic nitrogen fixation by rhizobia-the roots of a success story. Curr. Opin. Plant Biol. 44, 7-15.

Messinese, E., Mun, J.-H., Yeun, L.H., Jayaraman, D., Rouge, P., Barre, A., Lougnon, G., Schornack, S., Bono, J.-J., Cook, D.R., et al., 2007. A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant-Microbe Interact. 20, 912-921.

Miller, J.B., Pratap, A., Miyahara, A., Zhou, L., Bornemann, S., Morris, R.J., Oldroyd, G.E.D., 2013. Calcium/Calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 25, 5053-5066.

Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E.D., Long, S.R., 2004. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. U. S. A. 101, 4701-4705.

Oldroyd, G.E.D., Downie, J.M., 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546.

Oldroyd, G.E.D., Murray, J.D., Poole, P.S., Downie, J.A., 2011. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119-144.

Panchy, N., Lehti-Shiu, M., Shiu, S.H., 2016. Evolution of gene duplication in plants. Plant Physiol. 171, 2294-2316.

Pankievicz, V.C.S., Irving, T.B., Maia, L.G.S., Ane, J.M., 2019. Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops. BMC Biol. 17, 99.

Pereira, W.J., Knaack, S., Chakraborty, S., Conde, D., Folk, R.A., Triozzi, P.M., Balmant, K.M., Dervinis, C., Schmidt, H.W., Ane, J.M., 2022. Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen-fixing clade. New Phytol. 234, 634-649.

Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., et al., 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592.

Remigi, P., Zhu, J., Young, J.P.W., Masson-Boivin, C., 2016. Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol. 24, 63-75.

Roodt, D., Li, Z., Van de Peer, Y., Mizrachi, E., 2019. Loss of wood formation genes in monocot genomes. Genome Biol. Evol. 11, 1986-1996.

Roy, S., Liu, W., Nandety, R.S., Crook, A., Mysore, K.S., Pislariu, C.I., Frugoli, J., Dickstein, R., Udvardi, M.K., 2020. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32, 15-41.

Schauser, L., Roussis, A., Stiller, J., Stougaard, J., 1999. A plant regulator controlling development of symbiotic root nodules. Nature 402, 191-195.

Schiessl, K., Lilley, J.L.S., Lee, T., Tamvakis, I., Kohlen, W., Bailey, P.C., Thomas, A., Luptak, J., Ramakrishnan, K., Carpenter, M.D., et al., 2019. NODULE INCEPTION recruits the lateral root developmental program for symbiotic nodule organogenesis in Medicago truncatula. Curr. Biol. 29, 3657-3668.

Shen, D., Xiao, T.T., van Velzen, R., Kulikova, O., Gong, X., Geurts, R., Pawlowski, K., Bisseling, T., 2020a. A homeotic mutation changes legume nodule ontogeny into actinorhizal-type ontogeny. Plant Cell 32, 1868-1885.

Shen, F., Qin, Y., Wang, R., Huang, X., Wang, Y., Gao, T., He, J., Zhou, Y., Jiao, Y., Wei, J., et al., 2023. Comparative genomics reveals a unique nitrogen-carbon balance system in Asteraceae. Nat. Commun. 14, 4334.

Shen, G., Liu, N., Zhang, J., Xu, Y., Baldwin, I.T., Wu, J., 2020b. Cuscuta australis (dodder) parasite eavesdrops on the host plants' FT signals to flower. Proc. Natl. Acad. Sci. USA 117, 23125-23130.

Shen, L., Feng, J., 2024. NIN-at the heart of NItrogen-fixing Nodule symbiosis. Front. Plant Sci. 14, 1284720.

Shimoda, Y., Han, L., Yamazaki, T., Suzuki, R., Hayashi, M., Imaizumi-Anraku, H., 2012. Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus. Plant Cell 24, 304-321.

Sieberer, B.J., Chabaud, M., Fournier, J., Timmers, A.C.J., Barker, D.G., 2012. A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J. 69, 822-830.

Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S., et al., 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050.

Singh, S., Katzer, K., Lambert, J., Cerri, M., Parniske, M., 2014. CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe. 15, 139-152.

Soltis, D.E., Soltis, P.S., Morgan, D.R., Swensen, S.M., Mullin, B.C., Dowd, J.M., Martin, P.G., 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. U. S. A. 92, 2647-2651.

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.

Soyano, T., Shimoda, Y., Kawaguchi, M., Hayashi, M., 2019. A shared gene drives lateral root development and root nodule symbiosis pathways in Lotus. Science 366, 1021-1023.

Stokstad, E., 2016. The nitrogen fix. Science 353, 1225-1227.

Swensen, S.M., 1996. The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. Am. J. Bot. 83, 1503-1512.

Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., Murakami, Y., Madsen, L.H., Miwa, H., Nakagawa, T., Sandal, N., Albrektsen, A.S., Kawaguchi, M., et al., 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153-1156.

Trizzino, M., Park, Y., Holsbach-Beltrame, M., Aracena, K., Mika, K., Caliskan, M., Perry, G.H., Lynch, V.J., Brown, C.D., 2017. Transposable elements are the primary source of novelty in primate gene regulation. Genome Res. 27, 1623-1633.

Van de Peer, Y., Maere, S., Meyer, A., 2009. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725-732.

van Velzen, R., Holmer, R., Bu, F., Rutten, L., van Zeijl, A., Liu, W., Santuari, L., Cao, Q., Sharma, T., Shen, D., et al., 2018. Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. Proc. Natl. Acad. Sci. U. S. A. 115, E4700-E4709.

Vernie, T., Kim, J., Frances, L., Ding, Y., Sun, J., Guan, D., Niebel, A., Gifford, M.L., de Carvalho-Niebel, F., Oldroyd, G.E.D., 2015. The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root. Plant Cell 27, 3410-3424.

Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D., Gough, C., Denarie, J., Long, S.R., 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl. Acad. Sci. U. S. A. 97, 13407-13412.

Wang, C., Yu, H., Luo, L., Duan, L., Cai, L., He, X., Wen, J., Mysore, K.S., Li, G., Xiao, A., et al., 2016. NODULES WITH ACTIVATED DEFENSE 1 is required for maintenance of rhizobial endosymbiosis in Medicago truncatula. New Phytol. 212, 176-191.

Wen, Z.Y., Kang, Y.J., Ke, L., Yang, D.C., Gao, G., 2023. Genome-wide identification of gene loss events suggests loss relics as a potential source of functional lncRNAs in humans. Mol. Biol. Evol. 40, msad103.

Werner, G.D., Cornwell, W.K., Sprent, J.I., Kattge, J., Kiers, E.T., 2014. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat. Commun. 5, 4087.

Yano, K., Yoshida, S., Muller, J., Singh, S., Banba, M., Vickers, K., Markmann, K., White, C., Schuller, B., Sato, S., et al., 2008. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. U. S. A. 105, 20540-20545.

Yu, H., Xiao, A., Zou, Z., Wu, Q., Chen, L., Zhang, D., Sun, Y., Wang, C., Cao, J., Zhu, H., et al., 2024. Conserved cis-elements enable NODULES WITH ACTIVATED DEFENSE1 regulation by NODULE INCEPTION during nodulation. Plant Cell 36, 4622-4636.

Zhang, Y., Fu, Y., Xian, W., Li, X., Feng, Y., Bu, F., Shi, Y., Chen, S., van Velzen, R., Battenberg, K., et al., 2024. Comparative phylogenomics and phylotranscriptomics provide insights into the genetic complexity of nitrogen-fixing root-nodule symbiosis. Plant Commun. 5, 100671.

Zhi, X.Y., Jiang, Z., Yang, L.L., Huang, Y., 2017. The underlying mechanisms of genetic innovation and speciation in the family Corynebacteriaceae: A phylogenomics approach. Mol. Phylogen. Evol. 107, 246-255.

Zhu, H., Chen, T., Zhu, M., Fang, Q., Kang, H., Hong, Z., Zhang, Z., 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.

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