Specificity in legume nodule symbiosis

doi:10.1126/science.abd3857

GSTDTAP > 气候变化

DOI	10.1126/science.abd3857
	Specificity in legume nodule symbiosis
	Ton Bisseling; Rene Geurts
	2020-08-07
发表期刊	Science
出版年	2020
英文摘要	Some plant species establish mutualistic cooperation with nitrogen-fixing bacteria to overcome nitrogen shortage. The interaction between legume plants and rhizobial bacteria is the canonical example of such mutualism. It leads to the formation of root nodules, which provide the environment for the bacteria to convert atmospheric dinitrogen into ammonia. Nodule formation is initiated by rhizobium-secreted compounds called nodulation (Nod) factors. Perception of Nod factors by receptors in the plant root cells initiates nodule organogenesis and is essential for bacterial infection ([ 1 ][1]). Several legumes evolved a narrow host range such that only one or a few rhizobium species can initiate nodulation ([ 2 ][2]). This specificity is largely determined by the Nod factor receptors. On page 663 of this issue, Bozsoki et al. ([ 3 ][3]) provide structural characterization of the binding site of a Nod factor receptor in legumes. The structural basis of rhizobial Nod factor recognition is a key to understanding the evolution of specificity in symbioses. Rhizobial Nod factors are structural variants of acylated chitin oligomers. Chitin oligomers (COs), as well as acylated COs, also function as important symbiotic signals when released by nutrient-scavenging mutualistic arbuscular mycorrhizal (AM) fungi ([ 4 ][4], [ 5 ][5]). Perception of COs and/or acylated COs by the root enables the fungus to establish intracellular infection in roots of a wide range of plant species. In addition to rhizobia and AM fungi, acylated COs are also produced by other mutualistic microbes, such as some nutrient-scavenging mutualistic ectomycorrhizal fungi that colonize roots of some tree species and probably some nodulating nitrogen-fixing Frankia bacteria ([ 6 ][6]–[ 8 ][7]). COs can also trigger innate immune responses in plants as a defense response to pathogenic fungi. The lysine motif (LysM)–type chitin receptor kinase CHITIN ELICITOR RECEPTOR KINASE (CERK) was found to be essential for AM symbiosis as well as innate immunity ([ 1 ][1]). Genetic and biochemical studies in the model legumes Lotus japonicus (lotus) and Medicago truncatula (medicago) uncovered a heterodimer of LysM-type receptor kinases that function as specific high-affinity rhizobium Nod factor receptors. This receptor pair is called NOD FACTOR RECEPTOR 1 (LjNFR1) and LjNFR5 in lotus and LYSM DOMAIN–CONTAINING RECEPTOR-LIKE KINASE 3 (Mt-LYK3) and NOD FACTOR PERCEPTION (MtNFP) in medicago ([ 1 ][1]). The medicago receptor pair recognizes sulfated Nod factors, whereas the lotus receptor pair binds to fucosylated Nod factors ([ 1 ][1]). LjNFR1 and MtLYK3 are close homologs of the CERK-type receptors LjCERK6 and MtCERK1. They evolved through a series of duplications in a legume ancestor and lost the ability to recognize COs but gained specificity toward Nod factors ([ 9 ][8]–[ 13 ][9]). This raises questions about which structural changes in the receptor had to occur to make it Nod factor specific. ![Figure][10] The nodulation recognition system in legumes Medicago plant (left) is shown with nitrogen-fixing root nodules and rhizobium bacteria that produce nodulation (Nod) factors. On the right is the heterodimeric complex of two lysine motif (LysM)–type receptors [NOD FACTOR PERCEPTION (NFP) and LYSM DOMAIN–CONTAINING RECEPTOR-LIKE KINASE 3 (LYK3)] binding a Nod factor. GRAPHIC: C. BICKEL/ SCIENCE Bozsoki et al. show how the structural adaptations in LjNFR1 and MtLYK3 make them specific for Nod factors. The crystal structures of the ligand-binding sites of LjNFR1, MtLYK3, and the CERK receptors are highly similar. The main structural difference is in a small region of the first LysM domain of the Nod factor receptors, which determines ligand specificity (see the figure). In Nod factor receptors of different legume species, this region is variable, suggesting adaptations to recognize specific Nod factor structures. By contrast, in CERK receptors, this region is highly conserved. Using these molecular fingerprints, Bozsoki et al. constructed ligand recognition motifs specific for fucosylated or sulfated Nod factors, which allows engineering of rhizobium specificity. The structural characterization of rhizobium Nod factor–binding motifs in receptors is an essential advance in understanding their evolution. Furthermore, it may provide a basis for engineering specific Nod factor receptors that can be used to improve the nodulation trait, or even to transfer it to nonlegume crops, which would allow these crops to grow without addition of nitrogen fertilizer. Nevertheless, the study of Bozsoki et al. also raises several questions. Additional regions contribute to the functionality of LjNFR1 and MtLYK3 in symbiotic signaling. This suggests that lineage-specific adaptations have occurred in these Nod factor receptors that go beyond ligand specificity. This divergence could be the result of coevolution with the interacting LysM-type receptor with which they form a heterodimer, but data are currently lacking. Lotus and medicago have a narrow rhizobial host range, which, at least in part, can be explained by the occurrence of specific ligand recognition motifs in LjNFR1 and MtLYK3. However, several legumes are more promiscuous and can establish root nodules with a wide range of rhizobium species that produce Nod factors with different structures. It should be feasible to model the corresponding Nod factor receptors and identify the structural characteristics of such promiscuity. An important issue is the evolutionary origin of Nod factor perception in nodulation. Nodulation is not specific to legumes, but occurs in 10 plant lineages in four taxonomic orders. It has been proposed that nodulation has a single evolutionary origin (∼110 million years ago), driven by an acylated CO-producing, nitrogen-fixing Frankia bacterium ([ 14 ][11]). Among nodulating nonlegumes, Parasponia (Cannabaceae) is the only lineage that is nodulated by Nod factor–producing rhizobia, and the corresponding receptors have recently been identified ([ 13 ][9]). Notably, Parasponia did not experience a duplication of the CERK gene. Instead, a single LysM-type receptor fulfills multiple functions, including CO-induced innate immunity, AM symbiosis, and rhizobium Nod factor–induced nodulation ([ 13 ][9]). These observations suggest that the ancestral gene from which the legume Nod factor receptors evolved already encoded a LysM-type receptor that could perceive COs as well as acylated COs. In legumes, the duplication of this gene may have allowed the evolution of highly specific Nod factor receptors. Subsequent coevolution of Nod factor structure and the receptor ligand–binding site could have resulted in host specificity through a key-lock system, which is considered an important driver in the evolution of efficient symbiotic systems ([ 2 ][2]). 1. [↵][12]1. C. Zipfel, 2. G. E. D. Oldroyd , Nature 543, 328 (2017). [OpenUrl][13][CrossRef][14][PubMed][15] 2. [↵][16]1. P. Remigi, 2. J. Zhu, 3. J. P. W. Young, 4. C. Masson-Boivin , Trends Microbiol. 24, 63 (2016). [OpenUrl][17][CrossRef][18] 3. [↵][19]1. Z. Bozsoki et al ., Science 369, 663 (2020). [OpenUrl][20][Abstract/FREE Full Text][21] 4. [↵][22]1. F. Maillet et al ., Nature 469, 58 (2011). [OpenUrl][23][CrossRef][24][PubMed][25][Web of Science][26] 5. [↵][27]1. A. Genre et al ., New Phytol. 198, 190 (2013). [OpenUrl][28][CrossRef][29][PubMed][30][Web of Science][31] 6. [↵][32]1. P. Lerouge et al ., Nature 344, 781 (1990). [OpenUrl][33][CrossRef][34][PubMed][35][Web of Science][36] 7. 1. T. V. Nguyen et al ., BMC Genomics 17, 796 (2016). [OpenUrl][37][CrossRef][38] 8. [↵][39]1. K. R. Cope et al ., Plant Cell 31, 2386 (2019). [OpenUrl][40][Abstract/FREE Full Text][41] 9. [↵][42]1. S. De Mita, 2. A. Streng, 3. T. Bisseling, 4. R. Geurts , New Phytol. 201, 961 (2014). [OpenUrl][43][CrossRef][44][PubMed][45][Web of Science][46] 10. 1. Z. Bozsoki et al ., Proc. Natl. Acad. Sci. U.S.A. 114, E8118 (2017). [OpenUrl][47][Abstract/FREE Full Text][48] 11. 1. C. Gibelin-Viala et al ., New Phytol. 223, 1516 (2019). [OpenUrl][49] 12. 1. F. Feng et al ., Nat. Commun. 10, 5047 (2019). [OpenUrl][50][CrossRef][51][PubMed][52] 13. [↵][53]1. L. Rutten et al ., Plant Physiol. 10.1104/pp.19.01420 (2020), 14. [↵][54]1. R. van Velzen, 2. J. J. Doyle, 3. R. Geurts , Trends Plant Sci. 24, 49 (2019). [OpenUrl][55][CrossRef][56] [1]: #ref-1 [2]: #ref-2 [3]: #ref-3 [4]: #ref-4 [5]: #ref-5 [6]: #ref-6 [7]: #ref-8 [8]: #ref-9 [9]: #ref-13 [10]: pending:yes [11]: #ref-14 [12]: #xref-ref-1-1 "View reference 1 in text" [13]: {openurl}?query=rft.jtitle%253DNature%26rft.volume%253D543%26rft.spage%253D328%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fnature22009%26rft_id%253Dinfo%253Apmid%252F28300100%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [14]: /lookup/external-ref?access_num=10.1038/nature22009&link_type=DOI [15]: /lookup/external-ref?access_num=28300100&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [16]: #xref-ref-2-1 "View reference 2 in text" [17]: {openurl}?query=rft.jtitle%253DTrends%2BMicrobiol.%26rft.volume%253D24%26rft.spage%253D63%26rft_id%253Dinfo%253Adoi%252F10.1016%252Fj.tim.2015.10.007%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [18]: /lookup/external-ref?access_num=10.1016/j.tim.2015.10.007&link_type=DOI [19]: #xref-ref-3-1 "View reference 3 in text" [20]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DBozsoki%26rft.auinit1%253DZ.%26rft.volume%253D369%26rft.issue%253D6504%26rft.spage%253D663%26rft.epage%253D670%26rft.atitle%253DLigand-recognizing%2Bmotifs%2Bin%2Bplant%2BLysM%2Breceptors%2Bare%2Bmajor%2Bdeterminants%2Bof%2Bspecificity%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.abb3377%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [21]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEyOiIzNjkvNjUwNC82NjMiO3M6NDoiYXRvbSI7czoyMjoiL3NjaS8zNjkvNjUwNC82MjAuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9 [22]: #xref-ref-4-1 "View reference 4 in text" [23]: {openurl}?query=rft.jtitle%253DNature%26rft.stitle%253DNature%26rft.aulast%253DMaillet%26rft.auinit1%253DF.%26rft.volume%253D469%26rft.issue%253D7328%26rft.spage%253D58%26rft.epage%253D63%26rft.atitle%253DFungal%2Blipochitooligosaccharide%2Bsymbiotic%2Bsignals%2Bin%2Barbuscular%2Bmycorrhiza.%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fnature09622%26rft_id%253Dinfo%253Apmid%252F21209659%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [24]: /lookup/external-ref?access_num=10.1038/nature09622&link_type=DOI [25]: /lookup/external-ref?access_num=21209659&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [26]: /lookup/external-ref?access_num=000285921600030&link_type=ISI [27]: #xref-ref-5-1 "View reference 5 in text" [28]: {openurl}?query=rft.jtitle%253DNew%2BPhytol.%26rft.volume%253D198%26rft.spage%253D190%26rft_id%253Dinfo%253Adoi%252F10.1111%252Fnph.12146%26rft_id%253Dinfo%253Apmid%252F23384011%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [29]: /lookup/external-ref?access_num=10.1111/nph.12146&link_type=DOI [30]: /lookup/external-ref?access_num=23384011&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [31]: /lookup/external-ref?access_num=000315440400019&link_type=ISI [32]: #xref-ref-6-1 "View reference 6 in text" [33]: {openurl}?query=rft.jtitle%253DNature%26rft.stitle%253DNature%26rft.aulast%253DLerouge%26rft.auinit1%253DP.%26rft.volume%253D344%26rft.issue%253D6268%26rft.spage%253D781%26rft.epage%253D784%26rft.atitle%253DSymbiotic%2Bhost-specificity%2Bof%2BRhizobium%2Bmeliloti%2Bis%2Bdetermined%2Bby%2Ba%2Bsulphated%2Band%2Bacylated%2Bglucosamine%2Boligosaccharide%2Bsignal.%26rft_id%253Dinfo%253Adoi%252F10.1038%252F344781a0%26rft_id%253Dinfo%253Apmid%252F2330031%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [34]: /lookup/external-ref?access_num=10.1038/344781a0&link_type=DOI [35]: /lookup/external-ref?access_num=2330031&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [36]: /lookup/external-ref?access_num=A1990CZ67800060&link_type=ISI [37]: {openurl}?query=rft.jtitle%253DBMC%2BGenomics%26rft.volume%253D17%26rft.spage%253D796%26rft_id%253Dinfo%253Adoi%252F10.1186%252Fs12864-016-3140-1%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [38]: /lookup/external-ref?access_num=10.1186/s12864-016-3140-1&link_type=DOI [39]: #xref-ref-8-1 "View reference 8 in text" [40]: {openurl}?query=rft.jtitle%253DPlant%2BCell%26rft_id%253Dinfo%253Adoi%252F10.1105%252Ftpc.18.00676%26rft_id%253Dinfo%253Apmid%252F31416823%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [41]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6OToicGxhbnRjZWxsIjtzOjU6InJlc2lkIjtzOjEwOiIzMS8xMC8yMzg2IjtzOjQ6ImF0b20iO3M6MjI6Ii9zY2kvMzY5LzY1MDQvNjIwLmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ== [42]: #xref-ref-9-1 "View reference 9 in text" [43]: {openurl}?query=rft.jtitle%253DNew%2BPhytol.%26rft.volume%253D201%26rft.spage%253D961%26rft_id%253Dinfo%253Adoi%252F10.1111%252Fnph.12549%26rft_id%253Dinfo%253Apmid%252F24400903%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [44]: /lookup/external-ref?access_num=10.1111/nph.12549&link_type=DOI [45]: /lookup/external-ref?access_num=24400903&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [46]: /lookup/external-ref?access_num=000337082000023&link_type=ISI [47]: {openurl}?query=rft.jtitle%253DProc.%2BNatl.%2BAcad.%2BSci.%2BU.S.A.%26rft_id%253Dinfo%253Adoi%252F10.1073%252Fpnas.1706795114%26rft_id%253Dinfo%253Apmid%252F28874587%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [48]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6NDoicG5hcyI7czo1OiJyZXNpZCI7czoxMjoiMTE0LzM4L0U4MTE4IjtzOjQ6ImF0b20iO3M6MjI6Ii9zY2kvMzY5LzY1MDQvNjIwLmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ== [49]: {openurl}?query=rft.jtitle%253DNew%2BPhytol.%26rft.volume%253D223%26rft.spage%253D1516%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [50]: {openurl}?query=rft.jtitle%253DNat.%2BCommun.%26rft.volume%253D10%26rft.spage%253D5047%26rft_id%253Dinfo%253Adoi%252F10.1038%252Fs41467-019-12999-5%26rft_id%253Dinfo%253Apmid%252F31695035%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [51]: /lookup/external-ref?access_num=10.1038/s41467-019-12999-5&link_type=DOI [52]: /lookup/external-ref?access_num=31695035&link_type=MED&atom=%2Fsci%2F369%2F6504%2F620.atom [53]: #xref-ref-13-1 "View reference 13 in text" [54]: #xref-ref-14-1 "View reference 14 in text" [55]: {openurl}?query=rft.jtitle%253DTrends%2BPlant%2BSci.%26rft.volume%253D24%26rft.spage%253D49%26rft_id%253Dinfo%253Adoi%252F10.1016%252Fj.tplants.2018.10.005%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [56]: /lookup/external-ref?access_num=10.1016/j.tplants.2018.10.005&link_type=DOI
领域	气候变化 ; 资源环境
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引用统计
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/287987
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Ton Bisseling,Rene Geurts. Specificity in legume nodule symbiosis[J]. Science,2020.
APA	Ton Bisseling,&Rene Geurts.(2020).Specificity in legume nodule symbiosis.Science.
MLA	Ton Bisseling,et al."Specificity in legume nodule symbiosis".Science (2020).