The type III effector NopL interacts with GmREM1a and GmNFR5 to promote symbiosis in soybean.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
12 Jul 2024
12 Jul 2024
Historique:
received:
25
10
2023
accepted:
03
07
2024
medline:
12
7
2024
pubmed:
12
7
2024
entrez:
11
7
2024
Statut:
epublish
Résumé
The establishment of symbiotic interactions between leguminous plants and rhizobia requires complex cellular programming activated by Rhizobium Nod factors (NFs) as well as type III effector (T3E)-mediated symbiotic signaling. However, the mechanisms by which different signals jointly affect symbiosis are still unclear. Here we describe the mechanisms mediating the cross-talk between the broad host range rhizobia Sinorhizobium fredii HH103 T3E Nodulation Outer Protein L (NopL) effector and NF signaling in soybean. NopL physically interacts with the Glycine max Remorin 1a (GmREM1a) and the NFs receptor NFR5 (GmNFR5) and promotes GmNFR5 recruitment by GmREM1a. Furthermore, NopL and NF influence the expression of GmRINRK1, a receptor-like kinase (LRR-RLK) ortholog of the Lotus RINRK1, that mediates NF signaling. Taken together, our work indicates that S. fredii NopL can interact with the NF signaling cascade components to promote the symbiotic interaction in soybean.
Identifiants
pubmed: 38992018
doi: 10.1038/s41467-024-50228-w
pii: 10.1038/s41467-024-50228-w
doi:
Substances chimiques
Plant Proteins
0
Bacterial Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5852Informations de copyright
© 2024. The Author(s).
Références
Liang, Q. et al. Natural variation of Dt2 determines branching in soybean. Nat. Commun. 13, 6429 (2022).
pubmed: 36307423
pmcid: 9616897
doi: 10.1038/s41467-022-34153-4
Zhang, H. et al. Modeling the impact of climatological factors and technological revolution on soybean yield: evidence from 13-major provinces of China. Int. J. Environ. Res. Public Health 19, 5708 (2022).
pubmed: 35565101
pmcid: 9103772
doi: 10.3390/ijerph19095708
Hou, S. et al. Targeting high nutrient efficiency to reduce fertilizer input in wheat production of China. Field Crops Res. 292, 108809 (2023).
Cooper, J.E. Multiple Responses of Rhizobia to Flavonoids During Legume Root Infection. In Advances in Botanical Research, Vol. 41 1–62 (Academic Press, 2004).
Oldroyd, G. E. D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013).
pubmed: 23493145
doi: 10.1038/nrmicro2990
Giraud, E. et al. Legumes symbioses: Absence of Nod genes in photosynthetic bradyrhizobia. Science 316, 1307–1312 (2007).
pubmed: 17540897
doi: 10.1126/science.1139548
Broghammer, A. et al. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl Acad. Sci. USA 109, 13859–13864 (2012).
pubmed: 22859506
pmcid: 3427107
doi: 10.1073/pnas.1205171109
Limpens, E. et al. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630–633 (2003).
pubmed: 12947035
doi: 10.1126/science.1090074
Liang, Y. et al. Nonlegumes respond to rhizobial nod factors by suppressing the innate immune response. Science 341, 1384–1387 (2013).
pubmed: 24009356
doi: 10.1126/science.1242736
Roche, P. et al. The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc. Natl Acad. Sci. USA 93, 15305–15310 (1996).
pubmed: 8986807
pmcid: 26400
doi: 10.1073/pnas.93.26.15305
Mergaert, P., Van Montagu, M. & Holsters, M. Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25, 811–817 (1997).
pubmed: 9364907
doi: 10.1111/j.1365-2958.1997.mmi526.x
Rubsam, H. et al. Nanobody-driven signaling reveals the core receptor complex in root nodule symbiosis. Science 379, 272–277 (2023).
pubmed: 36656954
doi: 10.1126/science.ade9204
Smit, P. et al. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789–1791 (2005).
pubmed: 15961669
doi: 10.1126/science.1111025
Crespi, M. & Frugier, F. De novo organ formation from differentiated cells: root nodule organogenesis. Sci. Signal. 1, re11 (2008).
pubmed: 19066400
doi: 10.1126/scisignal.149re11
Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592 (2003).
pubmed: 14534578
doi: 10.1038/nature02039
Gourion, B., Berrabah, F., Ratet, P. & Stacey, G. Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci. 20, 186–194 (2015).
pubmed: 25543258
doi: 10.1016/j.tplants.2014.11.008
Antolin-Llovera, M., Ried, M. K. & Parniske, M. Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with nod factor receptor 5. Curr. Biol. 24, 422–427 (2014).
pubmed: 24508172
doi: 10.1016/j.cub.2013.12.053
Madsen, E. B. et al. Autophosphorylation is essential for the in vivo function of the Lotus japonicu Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65, 404–417 (2011).
pubmed: 21265894
doi: 10.1111/j.1365-313X.2010.04431.x
He, J. et al. A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Mol. Plant 12, 1561–1576 (2019).
pubmed: 31706032
doi: 10.1016/j.molp.2019.10.015
Gutjahr, C. et al. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20, 2989–3005 (2008).
pubmed: 19033527
pmcid: 2613669
doi: 10.1105/tpc.108.062414
Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775 (2008).
pubmed: 18794914
doi: 10.1038/nrmicro1987
Yu, Y. Remorins: essential regulators in plant-microbe interaction and cell death induction. Plant Physiol. 183, 435–436 (2020).
pubmed: 32493806
pmcid: 7271777
doi: 10.1104/pp.20.00490
Lefebvre, B. et al. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl Acad. Sci. USA 107, 2343–2348 (2010).
pubmed: 20133878
pmcid: 2836688
doi: 10.1073/pnas.0913320107
Su, C. et al. Stabilization of membrane topologies by proteinaceous remorin scaffolds. Nat. Commun. 14, 323 (2023).
pubmed: 36658193
pmcid: 9852587
doi: 10.1038/s41467-023-35976-5
Chiu, C. H. & Paszkowski, U. Receptor-like kinases sustain symbiotic scrutiny. Plant Physiol. 182, 1597–1612 (2020).
pubmed: 32054781
pmcid: 7140970
doi: 10.1104/pp.19.01341
Liang, P. et al. Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains. Proc. Natl Acad. Sci. USA 115, 5289–5294 (2018).
pubmed: 29712849
pmcid: 5960310
doi: 10.1073/pnas.1721868115
Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105 (2021).
pubmed: 33692546
pmcid: 8016741
doi: 10.1038/s41586-021-03316-6
Feng, F. & Zhou, J.-M. Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15, 469–476 (2012).
pubmed: 22465133
doi: 10.1016/j.pbi.2012.03.004
Raffeiner, M. et al. The Xanthomonas type-III effector XopS stabilizes CaWRKY40a to regulate defense responses and stomatal immunity in pepper (Capsicum annuum). Plant Cell 34, 1684–1708 (2022).
pubmed: 35134217
pmcid: 9048924
doi: 10.1093/plcell/koac032
Desaki, Y., Miyata, K., Suzuki, M., Shibuya, N. & Kaku, H. Plant immunity and symbiosis signaling mediated by LysM receptors. Innate Immun. 24, 92–100 (2018).
pubmed: 29105533
doi: 10.1177/1753425917738885
Teulet, A., Camuel, A., Perret, X. & Giraud, E. The versatile roles of type III secretion systems in rhizobium-legume symbioses. Annu. Rev. Microbiol. 76, 45–65 (2022).
pubmed: 35395168
doi: 10.1146/annurev-micro-041020-032624
Teulet, A. et al. The rhizobial type III effector ErnA confers the ability to form nodules in legumes. Proc. Natl Acad. Sci. USA 116, 21758–21768 (2019).
pubmed: 31591240
pmcid: 6815186
doi: 10.1073/pnas.1904456116
Xin, D.-W. et al. Functional analysis of NopM, a Novel E3 ubiquitin ligase (NEL) domain effector of Rhizobium sp strain NGR234. Plos Pathog. 8, e1002707 (2012).
pubmed: 22615567
pmcid: 3355095
doi: 10.1371/journal.ppat.1002707
Camuel, A. et al. Widespread Bradyrhizobium distribution of diverse Type III effectors that trigger legume nodulation in the absence of Nod factor. Isme J. 17, 1416–1429 (2023).
pubmed: 37355742
pmcid: 10432411
doi: 10.1038/s41396-023-01458-1
Acosta-Jurado, S. et al. Sinorhizobium fredii HH103 syrM inactivation affects the expression of a large number of genes, impairs nodulation with soybean and extends the host-range to Lotus japonicus. Environ. Microbiol. 22, 1104–1124 (2020).
pubmed: 31845498
doi: 10.1111/1462-2920.14897
Margaret, I. et al. Symbiotic properties and first analyses of the genomic sequence of the fast growing model strain Sinorhizobium fredii HH103 nodulating soybean. J. Biotechnol. 155, 11–19 (2011).
pubmed: 21458507
doi: 10.1016/j.jbiotec.2011.03.016
Pueppke, S. G. & Broughton, W. J. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant Microbe Interact. 12, 293–318 (1999).
pubmed: 10188270
doi: 10.1094/MPMI.1999.12.4.293
Krysciak, D. et al. RNA sequencing analysis of the broad-host-range strain Sinorhizobium fredii NGR234 Identifies a Large Set of Genes Linked to Quorum Sensing-Dependent Regulation in the Background of a traI and ngrI deletion mutant. Appl. Environ. Microbiol. 80, 5655–5671 (2014).
pubmed: 25002423
pmcid: 4178615
doi: 10.1128/AEM.01835-14
Bartsev, A. V. et al. NopL, an effector protein of Rhizobium sp NGR234, thwarts activation of plant defense reactions. Plant Physiol. 134, 871–879 (2004).
pubmed: 14966249
pmcid: 344561
doi: 10.1104/pp.103.031740
Zhang, L., Chen, X.-J., Lu, H.-B., Xie, Z.-P. & Staehelin, C. Functional analysis of the type 3 effector nodulation outer protein L (NopL) from Rhizobium sp NGR234 symbiotic effects, phosphorylation, and interference with mitogen-activated protein kinase signaling. J. Biol. Chem. 286, 32178–32187 (2011).
pubmed: 21775427
pmcid: 3173237
doi: 10.1074/jbc.M111.265942
Ge, Y.-Y. et al. The type 3 effector NopL of Sinorhizobium sp strain NGR234 is a mitogen-activated protein kinase substrate. J. Exp. Bot. 67, 2483–2494 (2016).
pubmed: 26931172
doi: 10.1093/jxb/erw065
Okazaki, S., Kaneko, T., Sato, S. & Saeki, K. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc. Natl Acad. Sci. USA 110, 17131–17136 (2013).
pubmed: 24082124
pmcid: 3801068
doi: 10.1073/pnas.1302360110
Ratu, S. T. N. et al. Rhizobia use a pathogenic-like effector to hijack leguminous nodulation signalling. Sci. Rep. 11, 2034 (2021).
pubmed: 33479414
pmcid: 7820406
doi: 10.1038/s41598-021-81598-6
Liu, Y. et al. Pan-genome of wild and cultivated soybeans. Cell 182, 162 (2020).
pubmed: 32553274
doi: 10.1016/j.cell.2020.05.023
Schwedock, J. & Long, S. R. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348, 644–647 (1990).
pubmed: 2250719
doi: 10.1038/348644a0
Fan, W. et al. Rhizobial infection of 4C cells triggers their endoreduplication during symbiotic nodule development in soybean. N. Phytologist 234, 1018–1030 (2022).
doi: 10.1111/nph.18036
Stagljar, I., Korostensky, C., Johnsson, N. & te Heesen, S. A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc. Natl Acad. Sci. USA 95, 5187–5192 (1998).
pubmed: 9560251
pmcid: 20236
doi: 10.1073/pnas.95.9.5187
Branon, T. C. et al. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36, 880 (2018).
pubmed: 30125270
pmcid: 6126969
doi: 10.1038/nbt.4201
Zhang, Y. et al. TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity. Nat. Commun. 10, 3252 (2019).
pubmed: 31324801
pmcid: 6642208
doi: 10.1038/s41467-019-11202-z
Li, X. et al. Atypical Receptor Kinase RINRK1 Required for Rhizobial Infection But Not Nodule Development in Lotus japonicus. Plant Physiol. 181, 804–816 (2019).
pubmed: 31409696
pmcid: 6776872
doi: 10.1104/pp.19.00509
Wang, L. et al. A GmNINa-miR172c-NNC1 regulatory network coordinates the nodulation and autoregulation of nodulation pathways in soybean. Mol. Plant 12, 1211–1226 (2019).
pubmed: 31201867
doi: 10.1016/j.molp.2019.06.002
Wang, Y. et al. Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation. Plant Cell 26, 4782–4801 (2014).
pubmed: 25549672
pmcid: 4311200
doi: 10.1105/tpc.114.131607
Franssen, H. J. et al. Root developmental programs shape the Medicago truncatula nodule meristem. Development 142, 2941–294 (2015).
pubmed: 26253408
Ghantasala, S. & Choudhury, S. R. Nod factor perception: an integrative view of molecular communication during legume symbiosis. Plant Mol. Biol. 110, 485–509 (2022).
pubmed: 36040570
doi: 10.1007/s11103-022-01307-3
Libourel, C. et al. Comparative phylotranscriptomics reveals ancestral and derived root nodule symbiosis programmes. Nat. Plants 9, 1067 (2023).
pubmed: 37322127
pmcid: 10356618
doi: 10.1038/s41477-023-01441-w
Deakin, W. J. & Broughton, W. J. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7, 312–320 (2009).
pubmed: 19270720
doi: 10.1038/nrmicro2091
Okazaki, S. et al. Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS. ISME J. 10, 64–74 (2016).
pubmed: 26161635
doi: 10.1038/ismej.2015.103
Nguyen, H. P., Ratu, S. T. N., Yasuda, M., Teaumroong, N. & Okazaki, S. Identification of Bradyrhizobium elkanii USDA61 Type III effectors determining symbiosis with Vigna mungo. Genes 11, 474 (2020).
pubmed: 32349348
pmcid: 7291247
doi: 10.3390/genes11050474
Reeve, W. et al. Complete genome sequence of the Medicago microsymbiont Ensifer (Sinorhizobium) medicae strain WSM419. Stand. Genom. Sci. 2, 77–86 (2010).
doi: 10.4056/sigs.43526
Martinez-Abarca, F., Martinez-Rodriguez, L., Lopez-Contreras, J. A., Jimenez-Zurdo, J. I. & Toro, N. Complete genome sequence of the alfalfa symbiont Sinorhizobium/Ensifer meliloti strain GR4. Genome Announc. 1, e00174–12 (2013).
pubmed: 23409262
pmcid: 3569321
doi: 10.1128/genomeA.00174-12
Toth, K. et al. Functional domain analysis of the remorin protein LjSYMREM1 in Lotus japonicus. PLoS ONE 7, e30817 (2012).
pubmed: 22292047
pmcid: 3264624
doi: 10.1371/journal.pone.0030817
Gronnier, J. et al. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. Elife 6, e26404 (2017).
pubmed: 28758890
pmcid: 5536944
doi: 10.7554/eLife.26404
Huang, D. et al. Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization. Proc. Natl Acad. Sci. USA 116, 21274–21284 (2019).
pubmed: 31575745
pmcid: 6800329
doi: 10.1073/pnas.1911892116
Raffaele, S. et al. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21, 1541–1555 (2009).
pubmed: 19470590
pmcid: 2700541
doi: 10.1105/tpc.108.064279
Marin, M., Thallmair, V. & Ott, T. The intrinsically disordered N-terminal region of AtREM1.3 remorin protein mediates protein-protein interactions. J. Biol. Chem. 287, 39982–39991 (2012).
pubmed: 23027878
pmcid: 3501056
doi: 10.1074/jbc.M112.414292
Martinez, D. et al. Coiled-coil oligomerization controls localization of the plasma membrane REMORINs. J. Struct. Biol. 206, 12–19 (2019).
pubmed: 29481850
doi: 10.1016/j.jsb.2018.02.003
Jaillais, Y. & Ott, T. The nanoscale organization of the plasma membrane and its importance in signaling: a proteolipid perspective. Plant Physiol. 182, 1682–1696 (2020).
pubmed: 31857424
doi: 10.1104/pp.19.01349
Yu, H., Bao, H., Zhang, Z. & Cao, Y. Immune signaling pathway during terminal bacteroid differentiation in nodules. Trends Plant Sci. 24, 299–302 (2019).
pubmed: 30772172
doi: 10.1016/j.tplants.2019.01.010
Roy, S. et al. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32, 15–41 (2020).
pubmed: 31649123
doi: 10.1105/tpc.19.00279
Zhang, Y. et al. Mining for genes encoding proteins associated with NopL of Sinorhizobium fredii HH103 using quantitative trait loci in soybean (Glycine max Merr.) recombinant inbred lines. Plant Soil 431, 245–255 (2018).
doi: 10.1007/s11104-018-3745-z
Berrabah, F. et al. Insight into the control of nodule immunity and senescence during Medicago truncatula symbiosis. Plant Physiol. 191, 729–746 (2022).
pmcid: 9806560
doi: 10.1093/plphys/kiac505
Ma, C. et al. GmTNRP1, associated with rhizobial type-III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max). Food Energy Secur. 12, e466 (2023).
Ma, C. et al. QTL mapping of genes related to Nod factor signalling using recombinant inbred lines of soybean (Glycine max). Plant Breed. 140, 1070–1080 (2021).
doi: 10.1111/pbr.12976
Quandt, J. & Hynes, M. F. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127, 15–21 (1993).
pubmed: 8486283
doi: 10.1016/0378-1119(93)90611-6
Figurski, D. H., Meyer, R. J. & Helinski, D. R. Suppression of Co1E1 replication properties by the Inc P-1 plasmid RK2 in hybrid plasmids constructed in vitro. J. Mol. Biol. 133, 295–318 (1979).
pubmed: 395312
doi: 10.1016/0022-2836(79)90395-4
Indrasumunar, A. et al. Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. 51, 201–214 (2010).
pubmed: 20007291
doi: 10.1093/pcp/pcp178
Paciorek, T., Sauer, M., Balla, J., Wisniewska, J. & Friml, J. Immunocytochemical technique for protein localization in sections of plant tissues. Nat. Protoc. 1, 104–107 (2006).
pubmed: 17406219
doi: 10.1038/nprot.2006.16
Dong, W. et al. An SHR-SCR module specifies legume cortical cell fate to enable nodulation. Nature 589, 586 (2021).
pubmed: 33299183
doi: 10.1038/s41586-020-3016-z
Jia, D. et al. A nonstructural protein encoded by a rice reovirus induces an incomplete autophagy to promote viral spread in insect vectors. PLoS Pathog. 18, e1010506 (2022).
pubmed: 35533206
pmcid: 9119444
doi: 10.1371/journal.ppat.1010506
Cheng, Z. et al. Nup96 and HOS1 are mutually stabilized and gate CONSTANS protein level, conferring long-day photoperiodic flowering regulation in Arabidopsis. Plant Cell 32, 374–391 (2020).
pubmed: 31826964
doi: 10.1105/tpc.19.00661
Brueckner, A., Polge, C., Lentze, N., Auerbach, D. & Schlattner, U. Yeast two-hybrid, a powerful tool for systems biology. Int. J. Mol. Sci. 10, 2763–2788 (2009).
doi: 10.3390/ijms10062763
Thaminy, S., Miller, J. & Stagljar, I. The split-ubiquitin membrane-based yeast two-hybrid system. Methods Mol. Biol. 261, 297–312 (2004).
pubmed: 15064465
Toth, K., Batek, J. & Stacey, G. Generation of soybean (Glycine max) transient transgenic roots. Curr. Protoc. Plant Biol. 1, 1–13 (2016).