Research progress on molecular mechanisms of autoregulation of nodulation in legumes
-
摘要:
豆科植物通过与土壤中的根瘤菌共生发育形成根瘤,在根瘤中根瘤菌可以将空气中氮气转化成植物可以直接利用的铵态氮。共生过程中为了平衡氮素的摄取和能量的损耗,豆科植物形成了地上与地下信号交互的结瘤自调控机制(Autoregulation of nodulation,AON),进而调节结瘤的数量。本文综述了AON分子调控机制近些年的研究进展,详述了AON通路中关键基因的功能及环境因素对AON体系的影响,包括地下信号短肽、地上受体激酶、地上长距信号(如细胞分裂素、生长素及miR2111等)及其根部F-box蛋白在AON中的作用,讨论了AON研究中部分仍待解答的问题,为结瘤自调控的相关研究提供信息和参考。
Abstract:Legumes form symbionts with rhizobia leading to the development of nitrogen fixing root nodules, while rhizobium in nodules convert nitrogen gas to ammonia for plant development.To balance nitrogen uptake and energy loss during symbiosis, legumes regulate nodule number through an autoregulation of nodulation (AON) systemic pathways.This paper reviewed the recent research progress on the molecular regulatory mechanism of AON and detailed the functions of key genes in host plants that regulate AON and the effects of environmental factors on the AON system, including the roles of underground peptide signals, aboveground receptor kinase, long distance signaling (Cytokinins, auxin and miR2111) and F-box protein in root.Some questions remained to be answered in the AON were discussed to provide information and reference for studies related to AON.
-
Key words:
- legume /
- nodulation /
- biological nitrogen fixation /
- AON
-
[1] REID D E, FERGUSON B J, HAYASHI S, et al. Molecular mechanisms controlling legume autoregulation of nodulation[J]. Annals of Botany, 2011, 108(5): 789-795. doi: 10.1093/aob/mcr205 [2] UDVARDI M K, PRICE G D, GRESSHOFF P M, et al. A dicarboxylate transporter on the peribacteroid membrane of soybean nodules[J]. FEBS Letters, 1988, 231(1): 36-40. doi: 10.1016/0014-5793(88)80697-5 [3] 吕殿青, 同延安, 孙本华, 等. 氮肥施用对环境污染影响的研究[J]. 植物营养与肥料学报, 1998, 4(1): 8-15. doi: 10.3321/j.issn:1008-505X.1998.01.002LV D Q, TONG Y A, SUN B H, et al. Study on effect of nitrogen fertilizer use on environment pollution[J]. Plant Natrition and Fertilizen Science, 1998, 4(1): 8-15. doi: 10.3321/j.issn:1008-505X.1998.01.002 [4] 黄江南, 余莹. 氮肥生产污染及其清洁生产的探讨[J]. 江西化工, 2006(4): 67-68. doi: 10.3969/j.issn.1008-3103.2006.04.018HUANG J N, YU Y. Cleaner production analysis in nitrogenous fertilizer industry[J]. Jiangxi Chemical Industry, 2006(4): 67-68. doi: 10.3969/j.issn.1008-3103.2006.04.018 [5] 刘兆辉, 薄录吉, 李彦, 等. 氮肥减量施用技术及其对作物产量和生态环境的影响综述[J]. 中国土壤与肥料, 2016(4): 1-8. https://www.cnki.com.cn/Article/CJFDTOTAL-TRFL201604001.htmLIU Z H, BO L J, LI Y, et al. Effect of nitrogen fertilizer reduction on crop yield and ecological environment: a review[J]. Soil and Fertilizer Sciences in China, 2016(4): 1-8. https://www.cnki.com.cn/Article/CJFDTOTAL-TRFL201604001.htm [6] 赵叶舟, 王浩铭, 汪自强. 豆科植物和根瘤菌在生态环境中的地位和作用[J]. 农业环境与发展, 2013, 30(4): 7-12. doi: 10.3969/j.issn.1005-4944.2013.04.002ZHAO Y Z, WANG H M, WANG Z Q. The role of leguminous plants and Rhizobium in ecological environment[J]. Agro-Environment and Development, 2013, 30(4): 7-12. doi: 10.3969/j.issn.1005-4944.2013.04.002 [7] 陈文新, 汪恩涛, 陈文峰. 根瘤菌-豆科植物共生多样性与地理环境的关系[J]. 中国农业科学, 2004, 37(1): 81-86. doi: 10.3321/j.issn:0578-1752.2004.01.013CHEN W X, WANG E T, CHEN W F. The relationship between the symbiotic promiscuity of rhizobia and legumes and their geographical environments[J]. Scientia Agricultura Sinica, 2004, 37(1): 81-86. doi: 10.3321/j.issn:0578-1752.2004.01.013 [8] OLDROYD G E D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants[J]. Nature Reviews Microbiology, 2013, 11(4): 252-263. doi: 10.1038/nrmicro2990 [9] ROY S, LIU W, NANDETY R S, et al. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation[J]. The Plant Cell, 2019, 32(1): 15-41. [10] GEURTS R, BISSELING T. Rhizobium nod factor perception and signalling[J]. The Plant Cell, 2002, 14(S1): S239-S249. [11] RADUTOIU S, MADSEN L H, MADSEN E B, et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases[J]. Nature, 2003, 425(6958): 585-592. doi: 10.1038/nature02039 [12] MADSEN E B, MADSEN L H, RADUTOIU S, et al. A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals[J]. Nature, 2003, 425(6958): 637-640. doi: 10.1038/nature02045 [13] KAWAHARADA Y, KELLY S, NIELSEN M W, et al. Receptor-mediated exopolysaccharide perception controls bacterial infection[J]. Nature, 2015, 523(7560): 308-312. doi: 10.1038/nature14611 [14] WONG J E M M, NADZIEJA M, MADSEN L H, et al. A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(28): 14339-14348. doi: 10.1073/pnas.1815425116 [15] CHARPENTIER M, BREDEMEIER R, WANNER G, et al. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis[J]. The Plant Cell, 2008, 20(12): 3467-3479. [16] STRACKE S, KISTNER C, YOSHIDA S, et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis[J]. Nature, 2002, 417(6892): 959-962. doi: 10.1038/nature00841 [17] LEVY J, BRES C, GEURTS R, et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses[J]. Science, 2004, 303(5662): 1361-1364. doi: 10.1126/science.1093038 [18] HIRSCH S, KIM J, MUNOZ A, et al. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula[J]. The Plant Cell, 2009, 21(2): 545-557. doi: 10.1105/tpc.108.064501 [19] SCHAUSER L, ROUSSIS A, STILLER J, et al. A plant regulator controlling development of symbiotic root nodules[J]. Nature, 1999, 402(6758): 191-195. doi: 10.1038/46058 [20] VERNIE T, KIM J, FRANCES L, et al. The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root[J]. The Plant Cell, 2015, 27(12): 3410-3424. doi: 10.1105/tpc.15.00461 [21] MARSH J F, RAKOCEVIC A, MITRA R M, et al. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase[J]. Plant Physiology, 2007, 144(1): 324-335. doi: 10.1104/pp.106.093021 [22] DELVES A C, MATHEWS A, DAY D A, et al. Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors[J]. Plant Physiology, 1986, 82(2): 588-590. doi: 10.1104/pp.82.2.588 [23] CLARK S E, JACOBSEN S E, LEVIN J Z, et al. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis[J]. Development, 1996, 122(5): 1567-1575. doi: 10.1242/dev.122.5.1567 [24] NONTACHAIYAPOOM S, SCOTT P T, MEN A E, et al. Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants[J]. Molecular Plant-Microbe Interactions, 2007, 20(7): 769-780. doi: 10.1094/MPMI-20-7-0769 [25] KRUSELL L, MADSEN L H, SATO S, et al. Shoot control of root development and nodulation is mediated by a receptor-like kinase[J]. Nature, 2002, 420(6914): 422-426. doi: 10.1038/nature01207 [26] SEARLE I R, MEN A E, LANIYA T S, et al. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase[J]. Science, 2003, 299(5603): 109-112. doi: 10.1126/science.1077937 [27] SCHNABEL E, JOURNET E P, DE CARVALHO-NIEBEL F, et al. The Medicago truncatula SUNN gene encodes a CLV1 -like leucine-rich repeat receptor kinase that regulates nodule number and root length[J]. Plant Molecular Biology, 2005, 58(6): 809-822. doi: 10.1007/s11103-005-8102-y [28] FERGUSON B J, LI D X, HASTWELL A H, et al. The soybean(Glycine max)nodulation-suppressive CLE peptide, GmRIC1, functions interspecifically in common white bean(Phaseolus vulgaris), but not in a supernodulating line mutated in the receptor PvNARK[J]. Plant Biotechnology Journal, 2014, 12(8): 1085-1097. doi: 10.1111/pbi.12216 [29] CROOK A D, SCHNABEL E L, FRUGOLI J A. The systemic nodule number regulation kinase SUNN in Medicago truncatula interacts with MtCLV2 and MtCRN[J]. The Plant Journal, 2016, 88(1): 108-119. doi: 10.1111/tpj.13234 [30] OKA-KIRA E, TATENO K, MIURA K I, et al. Klavier(klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction[J]. The Plant Journal, 2005, 44(3): 505-515. doi: 10.1111/j.1365-313X.2005.02543.x [31] MIYAZAWA H, OKA-KIRA E, SATO N, et al. The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus[J]. Development, 2010, 137(24): 4317-4325. doi: 10.1242/dev.058891 [32] OGAWA M, SHINOHARA H, SAKAGAMI Y, et al. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain[J]. Science, 2008, 319(5861): 294. doi: 10.1126/science.1150083 [33] OKAMOTO S, OHNISHI E, SATO S, et al. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation[J]. Plant and Cell Physiology, 2009, 50(1): 67-77. doi: 10.1093/pcp/pcn194 [34] MORTIER V, DEN HERDER G, WHITFORD R, et al. CLE peptides control Medicago truncatula nodulation locally and systemically[J]. Plant Physiology, 2010, 153(1): 222-237. doi: 10.1104/pp.110.153718 [35] REID D E, FERGUSON B J, GRESSHOFF P M. Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation[J]. Molecular Plant-Microbe Interactions, 2011, 24(5): 606-618. doi: 10.1094/MPMI-09-10-0207 [36] HASTWELL A H, GRESSHOFF P M, FERGUSON B J. The structure and activity of nodulation-suppressing CLE peptide hormones of legumes[J]. Functional Plant Biology, 2015, 42(3): 229-238. doi: 10.1071/FP14222 [37] REID D E, LI D X, FERGUSON B J, et al. Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean[J]. Journal of Experimental Botany, 2013, 64(6): 1575-1585. doi: 10.1093/jxb/ert008 [38] HASTWELL A H, GRESSHOFF P M, FERGUSON B J. Genome-wide annotation and characterization of CLAVATA/ESR(CLE)peptide hormones of soybean(Glycine max) and common bean(Phaseolus vulgaris), and their orthologues of Arabidopsis thaliana[J]. Journal of Experimental Botany, 2015, 66(17): 5271-5287. doi: 10.1093/jxb/erv351 [39] OKAMOTO S, SHINOHARA H, MORI T, et al. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase[J]. Nature Communications, 2013, 4: 2191. doi: 10.1038/ncomms3191 [40] HASTWELL A H, CORCILIUS L, WILLIAMS J T, et al. Triarabinosylation is required for nodulation-suppressive CLE peptides to systemically inhibit nodulation in Pisum sativum[J]. Plant, Cell and Environment, 2019, 42(1): 188-197. doi: 10.1111/pce.13325 [41] SCHNABEL E L, KASSAW T K, SMITH L S, et al. The ROOT DETERMINED NODULATION1 gene regulates nodule number in roots of Medicago truncatula and defines a highly conserved, uncharacterized plant gene family[J]. Plant Physiology, 2011, 157(1): 328-340. doi: 10.1104/pp.111.178756 [42] KASSAW T, NOWAK S, SCHNABEL E, et al. ROOT DETERMINED NODULATION1 is required for M. truncatula CLE12, but not CLE13, peptide signaling through the SUNN receptor kinase[J]. Plant Physiology, 2017, 174(4): 2445-2456. doi: 10.1104/pp.17.00278 [43] WANG Y N, WANG L X, ZOU Y M, et al. Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation[J]. The Plant Cell, 2014, 26(12): 4782-4801. [44] WANG L X, SUN Z X, SU C, et al. A GmNINa-miR172c-NNC1 regulatory network coordinates the nodulation and autoregulation of nodulation pathways in soybean[J]. Molecular Plant, 2019, 12(9): 1211-1226. doi: 10.1016/j.molp.2019.06.002 [45] MAGORI S, OKA-KIRA E, SHIBATA S, et al. TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus[J]. Molecular Plant-Microbe Interactions, 2009, 22(3): 259-268. doi: 10.1094/MPMI-22-3-0259 [46] TAKAHARA M, MAGORI S, SOYANO T, et al. TOO MUCH LOVE, a novel kelch repeat-containing F-box protein, functions in the long-distance regulation of the legume-Rhizobium symbiosis[J]. Plant and Cell Physiology, 2013, 54(4): 433-447. doi: 10.1093/pcp/pct022 [47] LIN Y H, FERGUSON B J, KERESZT A, et al. Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction[J]. The New Phytologist, 2010, 185(4): 1074-1086. doi: 10.1111/j.1469-8137.2009.03163.x [48] JIN J, WATT M, MATHESIUS U. The autoregulation gene SUNN mediates changes in root organ formation in response to nitrogen through alteration of shoot-to-root auxin transport[J]. Plant Physiology, 2012, 159(1): 489-500. doi: 10.1104/pp.112.194993 [49] VAN NOORDEN G E, ROSS J J, REID J B, et al. Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant[J]. Plant Physiology, 2006, 140(4): 1494-1506. doi: 10.1104/pp.105.075879 [50] SASAKI T, SUZAKI T, SOYANO T, et al. Shoot-derived cytokinins systemically regulate root nodulation[J]. Nature Communications, 2014, 5: 4983. doi: 10.1038/ncomms5983 [51] TSIKOU D, YAN Z, HOLT D B, et al. Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA[J]. Science, 2018, 362(6411): 233-236. doi: 10.1126/science.aat6907 [52] BARBULOVA A, ROGATO A, D'APUZZO E, et al. Differential effects of combined N sources on early steps of the Nod factor-dependent transduction pathway in Lotus japonicus[J]. Molecular Plant-Microbe Interactions, 2007, 20(8): 994-1003. doi: 10.1094/MPMI-20-8-0994 [53] MENS C, HASTWELL A H, SU H N, et al. Characterisation of Medicago truncatula CLE34 and CLE35 in nitrate and rhizobia regulation of nodulation[J]. The New Phytologist, 2021, 229(5): 2525-2534. doi: 10.1111/nph.17010 [54] MOREAU C, GAUTRAT P, FRUGIER F. Nitrate-induced CLE35 signaling peptides inhibit nodulation through the SUNN receptor and miR2111 repression[J]. Plant Physiology, 2021, 185(3): 1216-1228. doi: 10.1093/plphys/kiaa094 [55] NISHIDA H, TANAKA S, HANDA Y, et al. A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus[J]. Nature Communications, 2018, 9(1): 499. doi: 10.1038/s41467-018-02831-x [56] LIN J S, LI X L, LUO Z P, et al. NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula[J]. Nature Plants, 2018, 4(11): 942-952. doi: 10.1038/s41477-018-0261-3 [57] HUAULT E, LAFFONT C, WEN J Q, et al. Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase[J]. PLoS Genetics, 2014, 10(12): e1004891. doi: 10.1371/journal.pgen.1004891 [58] IMIN N, MOHD-RADZMAN N A, OGILVIE H A, et al. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula[J]. Journal of Experimental Botany, 2013, 64(17): 5395-5409. doi: 10.1093/jxb/ert369 [59] TABATA R, SUMIDA K, YOSHⅡ T, et al. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling[J]. Science, 2014, 346(6207): 343-346. doi: 10.1126/science.1257800 [60] MOHD-RADZMAN N A, LAFFONT C, IVANOVICI A, et al. Different pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development[J]. Plant Physiology, 2016, 171(4): 2536-2548. doi: 10.1104/pp.16.00113 [61] GAUTRAT P, LAFFONT C, FRUGIER F. Compact root architecture 2 promotes root competence for nodulation through the miR2111 systemic effector[J]. Current Biology, 2020, 30(7): 1339-1345. e3. doi: 10.1016/j.cub.2020.01.084 [62] BAI M Y, YUAN J H, KUANG H Q, et al. Generation of a multiplex mutagenesis population via pooled CRISPR-Cas9 in soya bean[J]. Plant Biotechnology Journal, 2020, 18(3): 721-731. doi: 10.1111/pbi.13239 [63] LEBEDEVA M A, YASHENKOVA Y A S, DODUEVA I E, et al. Molecular dialog between root and shoot via regulatory peptides and its role in systemic control of plant development[J]. Russian Journal of Plant Physiology, 2020, 67(6): 985-1002. doi: 10.1134/S1021443720060114 [64] MURRAY J D, KARAS B J, SATO S, et al. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis[J]. Science, 2007, 315(5808): 101-104. doi: 10.1126/science.1132514