Cullin 3 substrate-adaptor protein 1 (MtCSP1) modulates nodulation through interaction with the GTPase ARFA1

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Cullin 3 substrate-adaptor protein 1 (MtCSP1) modulates nodulation through interaction with the GTPase ARFA1

References

  1. Bailey-Serres, J., Sorenson, R. & Juntawong, P. Getting the message across: Cytoplasmic ribonucleoprotein complexes. Trends Plant Sci. 14, 443–453. https://doi.org/10.1016/j.tplants.2009.05.004 (2009).

    Google Scholar 

  2. Ban, Z. & Estelle, M. CUL3 E3 ligases in plant development and environmental response. Nat. Plants 7, 6–16. https://doi.org/10.1038/s41477-020-00833-6 (2021).

    Google Scholar 

  3. Chen, L. & Hellmann, H. Plant E3 ligases: Flexible enzymes in a sessile world. Mol. Plant 6, 1388–1404. https://doi.org/10.1093/mp/sst005 (2013).

    Google Scholar 

  4. Ferguson, B. J. & Reid, J. B. Cochleata: Getting to the root of legume nodules. Plant Cell Physiol. 46, 1583–1589. https://doi.org/10.1093/pcp/pci171 (2005).

    Google Scholar 

  5. Liu, S. et al. The transcriptional co-regulators NBCL1 and NBCL2 redundantly coordinate aerial organ development and root nodule identity in legumes. J. Exp. Bot. 74, 194–213. https://doi.org/10.1093/jxb/erac389 (2023).

    Google Scholar 

  6. Shen, D. et al. The Medicago truncatula nodule identity gene MtNOOT1 is required for coordinated apical-basal development of the root. BMC Plant Biol. 19, 571. https://doi.org/10.1186/s12870-019-2194-z (2019).

    Google Scholar 

  7. Robertson, G. P. & Vitousek, P. M. Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. Environ. Resour. 34, 97–125. https://doi.org/10.1146/annurev.environ.032108.105046 (2009).

    Google Scholar 

  8. Oldroyd, G. E., Murray, J. D., Poole, P. S. & Downie, J. A. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119–144. https://doi.org/10.1146/annurev-genet-110410-132549 (2011).

    Google Scholar 

  9. Murray, J. D. Invasion by invitation: Rhizobial infection in legumes. Mol. Plant-Microbe Interact. 24, 631–639. https://doi.org/10.1094/mpmi-08-10-0181 (2011).

    Google Scholar 

  10. Xiao, T. T. et al. Fate map of Medicago truncatula root nodules. Development 141, 3517–3528. https://doi.org/10.1242/dev.110775 (2014).

    Google Scholar 

  11. Zhang, X., Wu, J. & Kong, Z. Cellular basis of legume–rhizobium symbiosis. Plant Commun. 5, 101045. https://doi.org/10.1016/j.xplc.2024.101045 (2024).

    Google Scholar 

  12. Rutherford, S. & Moore, I. The Arabidopsis Rab GTPase family: another enigma variation. Curr. Opin. Plant Biol. 5, 518–528 (2002).

    Google Scholar 

  13. Rivero, C., Traubenik, S., Zanetti, M. E. & Blanco, F. A. Small GTPases in plant biotic interactions. Small GTPases https://doi.org/10.1080/21541248.2017.1333557 (2017).

    Google Scholar 

  14. Limpens, E. et al. Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21, 2811–2828. https://doi.org/10.1105/tpc.108.064410 (2009).

    Google Scholar 

  15. Cheon, C. I., Lee, N. G., Siddique, A. B., Bal, A. K. & Verma, D. P. Roles of plant homologs of Rab1p and Rab7p in the biogenesis of the peribacteroid membrane, a subcellular compartment formed de novo during root nodule symbiosis. EMBO J 12, 4125–4135 (1993).

    Google Scholar 

  16. Ke, D. et al. 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 (2012).

    Google Scholar 

  17. Ke, D. et al. ROP6 is involved in root hair deformation induced by Nod factors in Lotus japonicus. Plant Physiol. Biochem. 108, 488–498. https://doi.org/10.1016/j.plaphy.2016.08.015 (2016).

    Google Scholar 

  18. Kiirika, L. M. et al. Silencing of the Rac1 GTPase MtROP9 in Medicago truncatula stimulates early mycorrhizal and oomycete root colonizations but negatively affects rhizobial infection. Plant Physiol. 159, 501–516. https://doi.org/10.1104/pp.112.193706 (2012).

    Google Scholar 

  19. Lei, M.-J. et al. The small GTPase ROP10 of Medicago truncatula is required for both tip growth of root hairs and Nod factor-induced root hair deformation. Plant Cell 27, 806–822. https://doi.org/10.1105/tpc.114.135210 (2015).

    Google Scholar 

  20. Peltzer Meschini, E. et al. Host genes involved in nodulation preference in common bean (Phaseolus vulgaris)-rhizobium etli symbiosis revealed by suppressive subtractive hybridization. Mol. Plant-Microbe Interact. 21, 459–468. https://doi.org/10.1094/MPMI-21-4-0459 (2008).

    Google Scholar 

  21. Blanco, F. A., Meschini, E. P., Zanetti, M. E. & Aguilar, O. M. A small GTPase of the Rab family is required for root hair formation and preinfection stages of the common bean-Rhizobium symbiotic association. Plant Cell 21, 2797–2810. https://doi.org/10.1105/tpc.108.063420 (2009).

    Google Scholar 

  22. Dalla Via, V. et al. The monomeric GTPase RabA2 is required for progression and maintenance of membrane integrity of infection threads during root nodule symbiosis. Plant Mol. Biol. https://doi.org/10.1007/s11103-016-0581-5 (2017).

    Google Scholar 

  23. Takeuchi, M., Ueda, T., Yahara, N. & Nakano, A. Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 31, 499–515. https://doi.org/10.1046/j.1365-313X.2002.01372.x (2002).

    Google Scholar 

  24. Xu, J. & Scheres, B. Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17, 525–536. https://doi.org/10.1105/tpc.104.028449 (2005).

    Google Scholar 

  25. Stefano, G. et al. In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J. 46, 95–110. https://doi.org/10.1111/j.1365-313X.2006.02675.x (2006).

    Google Scholar 

  26. Robinson, D. G., Scheuring, D., Naramoto, S. & Friml, J. ARF1 localizes to the Golgi and the Trans-Golgi network. Plant Cell 23, 846–849. https://doi.org/10.1105/tpc.110.082099 (2011).

    Google Scholar 

  27. Battaglia, M. et al. A Nuclear Factor Y interacting protein of the GRAS family is required for nodule organogenesis, infection thread progression, and lateral root growth. Plant Physiol. 164, 1430–1442. https://doi.org/10.1104/pp.113.230896 (2014).

    Google Scholar 

  28. Banno, H. & Chua, N.-H. Characterization of the Arabidopsis formin-like protein AFH1 and its interacting protein. Plant Cell Physiol. 41, 617–626. https://doi.org/10.1093/pcp/41.5.617 (2000).

    Google Scholar 

  29. Pimpl, P. et al. In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 12, 2219–2235. https://doi.org/10.1105/tpc.12.11.2219 (2000).

    Google Scholar 

  30. Estrada-Navarrete, G. et al. Agrobacterium rhizogenes transformation of the Phaseolus spp.: A tool for functional genomics. Mol. Plant-Microbe Interact. 19, 1385–1393. https://doi.org/10.1094/MPMI-19-1385 (2006).

    Google Scholar 

  31. Karimi, M., Inze, D. & Depicker, A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002).

    Google Scholar 

  32. Steklov, M. et al. Mutations in LZTR1 drive human disease by dysregulating RAS ubiquitination. Science 362, 1177–1182. https://doi.org/10.1126/science.aap7607 (2018).

    Google Scholar 

  33. Bigenzahn, J. W. et al. LZTR1 is a regulator of RAS ubiquitination and signaling. Science 362, 1171–1177. https://doi.org/10.1126/science.aap8210 (2018).

    Google Scholar 

  34. Castel, P. et al. RIT1 oncoproteins escape LZTR1-mediated proteolysis. Science 363, 1226–1230. https://doi.org/10.1126/science.aav1444 (2019).

    Google Scholar 

  35. Zhang, H. et al. BIG enhances Arg/N-degron pathway-mediated protein degradation to regulate Arabidopsis hypoxia responses and suberin deposition. Plant Cell 36, 3177–3200. https://doi.org/10.1093/plcell/koae117 (2024).

    Google Scholar 

  36. Pucciariello, C., Boscari, A., Tagliani, A., Brouquisse, R. & Perata, P. Exploring legume-rhizobia symbiotic models for waterlogging tolerance. Front. Plant Sci. 10, 578. https://doi.org/10.3389/fpls.2019.00578 (2019).

    Google Scholar 

  37. Hervé, C., Lefebvre, B. & Cullimore, J. How many E3 ubiquitin ligase are involved in the regulation of nodulation?. Plant Signal. Behav. 6, 660–664. https://doi.org/10.4161/psb.6.5.15024 (2011).

    Google Scholar 

  38. Yuan, S. et al. A ubiquitin ligase of symbiosis receptor kinase involved in nodule organogenesis. Plant Physiol. 160, 106–117. https://doi.org/10.1104/pp.112.199000 (2012).

    Google Scholar 

  39. Mbengue, M. et al. 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 (2010).

    Google Scholar 

  40. Li, H. et al. Dynamic modulation of nodulation factor receptor levels by phosphorylation-mediated functional switch of a RING-type E3 ligase during legume nodulation. Mol. Plant 17, 1090–1109. https://doi.org/10.1016/j.molp.2024.05.010 (2024).

    Google Scholar 

  41. Tsikou, D. et al. A Lotus japonicus E3 ligase interacts with the Nod Factor Receptor 5 and positively regulates nodulation. BMC Plant Biol. 18, 217. https://doi.org/10.1186/s12870-018-1425-z (2018).

    Google Scholar 

  42. Feng, Y. et al. A LjBAK1-associated E3 ubiquitin ligase, LjPUB7, negatively regulates early symbiosis by targeting NFRs. BMC Plant Biol. 25, 1334. https://doi.org/10.1186/s12870-025-07265-4 (2025).

    Google Scholar 

  43. Piper, R. C. & Lehner, P. J. Endosomal transport via ubiquitination. Trends Cell Biol. 21, 647–655. https://doi.org/10.1016/j.tcb.2011.08.007 (2011).

    Google Scholar 

  44. Hellmann, H. & Estelle, M. Plant development: Regulation by protein degradation. Science 297, 793–797. https://doi.org/10.1126/science.1072831 (2002).

    Google Scholar 

  45. Quandt, H. J., Pühler, A., and Broer, I. Transgenic root nodules of Vicia hirsuta: A fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol Plant-Microbe Interact, 699–706 (1993).

  46. Meade, H. M. & Signer, E. R. Genetic mapping of Rhizobium meliloti. Proc. Natl. Acad. Sci. U. S. A. 74, 2076–2078 (1977).

    Google Scholar 

  47. Tian, C. F., Garnerone, A. M., Mathieu-Demazière, C., Masson-Boivin, C. & Batut, J. Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti–Medicago symbiosis. Proc. Natl. Acad. Sci. U. S. A. 109, 6751–6756. https://doi.org/10.1073/pnas.1120260109 (2012).

    Google Scholar 

  48. Kirolinko, C. et al. A lateral organ boundaries domain transcription factor acts downstream of the auxin response factor 2 to control nodulation and root architecture in Medicago truncatula. New Phytol. 242, 2746–2762. https://doi.org/10.1111/nph.19766 (2024).

    Google Scholar 

  49. Mustroph, A. et al. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 106, 18843–18848. https://doi.org/10.1073/pnas.0906131106 (2009).

    Google Scholar 

  50. Hirsch, S. et al. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21, 545–557. https://doi.org/10.1105/tpc.108.064501 (2009).

    Google Scholar 

  51. Clúa, J. et al. NIPK, a protein pseudokinase that interacts with the C subunit of the transcription factor NF-Y, is involved in rhizobial infection and nodule organogenesis. Front. Plant Sci. https://doi.org/10.3389/fpls.2022.992543 (2022).

    Google Scholar 

  52. Rípodas, C. et al. The PvNF-YA1 and PvNF-YB7 subunits of the heterotrimeric NF-Y transcription factor influence strain preference in the Phaseolus vulgaris–Rhizobium etli symbiosis. Front. Plant Sci. https://doi.org/10.3389/fpls.2019.00221 (2019).

    Google Scholar 

  53. Fahraeus, G. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16, 374–381 (1957).

    Google Scholar 

  54. Hobecker, K. V. et al. The microRNA390/TAS3 pathway mediates in symbiotic nodulation and lateral root growth. Plant Physiol https://doi.org/10.1104/pp.17.00464 (2017).

    Google Scholar 

  55. Kirolinko, C. et al. Auxin response factor 2 (ARF2), ARF3, and ARF4 mediate both lateral root and nitrogen fixing nodule development in Medicago truncatula. Front. Plant Sci. https://doi.org/10.3389/fpls.2021.659061 (2021).

    Google Scholar 

  56. Risseeuw, E. P. et al. Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J. 34, 753–767. https://doi.org/10.1046/j.1365-313x.2003.01768.x (2003).

    Google Scholar 

  57. Gray, W. M., Hellmann, H., Dharmasiri, S. & Estelle, M. Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. Plant Cell 14, 2137–2144. https://doi.org/10.1105/tpc.003178 (2002).

    Google Scholar 

  58. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539. https://doi.org/10.1038/msb.2011.75 (2011).

    Google Scholar 

  59. Lemoine, F. et al. NGPhylogeny.fr: New generation phylogenetic services for non-specialists. Nucleic Acids Res. 47, W260-w265. https://doi.org/10.1093/nar/gkz303 (2019).

    Google Scholar 

  60. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650. https://doi.org/10.1093/molbev/msp077 (2009).

    Google Scholar 

  61. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – Approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490. https://doi.org/10.1371/journal.pone.0009490 (2010).

    Google Scholar 

  62. Le, S. Q. & Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320. https://doi.org/10.1093/molbev/msn067 (2008).

    Google Scholar 

  63. Letunic, I. & Bork, P. Interactive tree of life (iTOL) v6: Recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, W78-w82. https://doi.org/10.1093/nar/gkae268 (2024).

    Google Scholar 

  64. Schiessl, K. et al. Nodule inception recruits the lateral root developmental program for symbiotic nodule organogenesis in Medicago truncatula. Curr. Biol. 29, 3657-3668.e3655. https://doi.org/10.1016/j.cub.2019.09.005 (2019).

    Google Scholar 

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