Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (3): 553-562    DOI: 10.1016/S2095-3119(18)61992-6
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
GmNMH7, a MADS-box transcription factor, inhibits root development and nodulation of soybean (Glycine max [L.] Merr.)
MA Wen-ya1*, LIU Wei1*, HOU Wen-sheng1, SUN Shi1, JIANG Bing-jun1, HAN Tian-fu1, FENG Yong-jun2, WU Cun-xiang1 
1 Key Laboratory of Soybean Biology (Beijing), Ministry of Agriculture/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 School of Life Science, Beijing Institute of Technology, Beijing 100081, P.R.China
Download:  PDF (1031KB) ( )  
Export:  BibTeX | EndNote (RIS)      
Abstract  As an important food crop and oil crop, soybean (Glycine max [L.] Merr.) is capable of nitrogen-fixing by root nodule.  Previous studies showed that GmNMH7, a transcription factor of MADS-box family, is associated with nodule development, but its specific function remained unknown.  In this study, we found that GmNMH7 was specifically expressed in root and nodule and the expression pattern of GmNMH7 was similar to several genes involved in early development of nodule (GmENOD40-1, GmENOD40-2, GmNFR1a, GmNFR5a, and GmNIN) after rhizobia inoculation.  The earlier expression peak of GmNMH7 compared to the other genes (GmENOD40-1, GmENOD40-2, GmNFR1a, GmNFR5a, and GmNIN) indicated that the gene is related to the nod factor (NF) signaling pathway and functions at the early development of nodule.  Over-expression of GmNMH7 in hairy roots significantly reduced the nodule number and the root length.  In the transgenic hairy roots, over-expression of GmNMH7 significantly down-regulated the expression levels of GmENOD40-1, GmENOD40-2, and GmNFR5α.  Moreover, the expression of GmNMH7 could respond to abscisic acid (ABA) and gibberellin (GA3) treatment in the root of Zigongdongdou seedlings.  Over-expressing GmNMH7 gene reduced the content of ABA, and increased the content of GA3 in the positive transgenic hairy roots.  Therefore, we concluded that GmNMH7 might participate in the NF signaling pathway and negatively regulate nodulation probably through regulating the content of GA3.
 
Keywords:  soybean        GmNMH7        MADS-box gene        nodulation        ABA       GA3  
Received: 28 December 2017   Accepted: 07 March 2019
Fund: This work was supported by the National Natural Science Foundation of China (31271636) and the earmarked fund for China Agriculture Research System (CARS-04).
Corresponding Authors:  Correspondence FENG Yong-jun, Tel: +86-10-68914495-804, Fax: +86-10-68915956, E-mail: fengyj@bit.edu.cn; WU Cun-xiang, Tel: +86-10-82105865, Fax: +86-10-82108784, E-mail: wucunxiang@caas.cn    
About author:  * These authors contributed equally to this study.

Cite this article: 

MA Wen-ya, LIU Wei, HOU Wen-sheng, SUN Shi, JIANG Bing-jun, HAN Tian-fu, FENG Yong-jun, WU Cun-xiang. 2019. GmNMH7, a MADS-box transcription factor, inhibits root development and nodulation of soybean (Glycine max [L.] Merr.). Journal of Integrative Agriculture, 18(3): 553-562.

Amor B B, Shaw S L, Oldroyd G E, Maillet F, Penmetsa R V, Cook D, Long S R, Dénarié J, Gough C. 2003. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. The Plant Journal, 34, 495–506.
Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan J T, Maolanon N, Vinther M, Lorentzen A, Madsen E B, Jensen K J, Roepstorff P, Thirup S, Ronson C W, Thygesen M B, Stougaard J. 2012. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proceedings of the National Academy of Sciences of the United States of America, 109, 13859–13864.
Cao D, Hou W S, Liu W, Yao W W, Wu C X, Liu X B, Han T F. 2011. Overexpression of TaNHX2, enhances salt tolerance of ‘composite’ and whole transgenic soybean plants. Plant Cell Tissue & Organ Culture, 107, 541–552.
Charon C, Sousa C, Crespi M, Kondorosi A. 1999. Alteration of ENOD40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti. The Plant Cell, 11, 1953–1965.
Compaan B, Yang W C, Bisseling T, Franssen H. 2001. ENOD40 expression in the pericycle precedes cortical cell division in rhizobium-legume interaction and the highly conserved internal region of the gene does not encode a peptide. Plant and Soil, 230, 1–8.
Crespi M D, Jurkevitch E, Poiret M, D’Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A. 1994. ENOD40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. The EMBO Journal, 13, 5099–5112.
Fåhraeus G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. Journal of General Microbiology, 16, 374–381.
Feng Z, Bo P, Smith D L. 1997. Application of gibberellic acid to the surface of soybean seed (Glycine max L. Merr.) and symbiotic nodulation, plant development, final grain and protein yield under short season conditions. Plant and Soil, 188, 329–335.
Geurts R, Heidstra R, Hadri A E, Downie J A, Franssen H, Van K A, Bisseling T. 1997. Sym2 of pea is involved in a nodulation factor-perception mechanism that controls the infection process in the epidermis. Plant Physiology, 115, 351–359.
Heidstra R, Geurts R, Franssen H, Spaink H P, Kammen A V, Bisseling T. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiology, 105, 787–797.
Indrasumunar A, Kereszt A, Searle I, Miyagi M, Li D, Nguyen C D, Men A, Carroll B J, Gresshoff P M. 2010. 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 Physiology, 51, 201–214.
Indrasumunar A, Searle I, Lin M H, Kereszt A, Men A, Carroll B J, Gresshoff P M. 2011. Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr.). The Plant Journal, 65, 39–50.
Kumagai H, Kinoshita E, Ridge R W, Kouchi H. 2006. RNAi knock-down of ENOD40s leads to significant suppression of nodule formation in Lotus japonicus. Plant & Cell Physiology, 47, 1102–1111.
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.
Madsen E B, Madsen L H, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. 2003. A receptor kinase gene of the lysm type is involved in legume perception of rhizobial signals.Nature, 425, 637–640.
Maekawa T, Maekawa-Yoshikawa M, Takeda N, Imaizumi-Anraku H, Murooka Y, Hayashi M. 2009. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. The Plant Journal, 58, 183–194.
Mathesius U, Charon C, Rolfe B G, Kondorosi A, Crespi M. 2000. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Molecular Plant-Microbe Interactions, 13, 617–628.
Páez-Valencia J, Sánchez-Gómez C, Valencia-Mayoral P, Contreras-Ramos A, Hernández-Lucas I, Orozco-Segovia A, Gamboa-deBuen A. 2008a. Localization of the MADS domain transcriptional factor NMH7 during seed, seedling and nodule development of Medicago sativa. Plant Science, 175, 596–603.
Páez-Valencia J, Valencia-Mayoral P, Sánchez-Gómez C, Contreras-Ramos A, Hernández-Lucas I, Martínez-Barajas E, Gamboa-deBuen A. 2008b. Identification of fructose-1,6-bisphosphate aldolase cytosolic class I as an NMH7 MADS domain associated protein. Biochemical & Biophysical Research Communications, 376, 700–705.
Patel D, Thaker V S. 2007. Estimation of endogenous contents of phytohormones during internode development in Merremia emarginata. Biologia Plantarum, 51, 75–79.
Radutoiu S, Madsen L H, Madsen E B, Felle H H, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. 2003. Plant recognition of symbiotic bacteria requires two lysm receptor-like kinases. Nature, 425, 585–592.
Sanjuan J, Carlson R W, Spaink H P, Bhat U R, Barbour W M, Glushka J, Stacey G. 1992. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proceedings of the National Academy of Sciences of the United States of America, 89, 8789–8793.
Schauser L, Roussis A, Stiller J, Stougaard J. 1999. A plant regulator controlling development of symbiotic root nodules. Nature, 402, 191–195.
Velde W V D, Guerra J C P, Keyser A D, Rycke R D, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S. 2006. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology, 141, 711–720.
Wan X, Franssen H. 2007. Medicago truncatulaENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. Journal of Experimental Botany, 58, 2033–2041.
Wang M, Heimovaara-Dijkstra S, Duijn B V. 1995. Modulation of germination of embryos isolated from dormant and nondormant barley grains by manipulation of endogenous abscisic acid. Planta, 195, 586–592.
Williams P M, Mallorca M S D. 1984. Effect of gibberellins and the growth retardant CCC on the nodulation of soya. Plant and Soil, 77, 53–60.
Wu C X, Ma Q B, Yam K M, Cheung M Y, Xu Y Y, Han T F, Lam H M, Chong K. 2006. In situ expression of the GmNMH7 gene is photoperiod-dependent in a unique soybean (Glycine max [L.] Merr.) flowering reversion system. Planta, 223, 725–735.
Yang W C, Katinakis P, Hendriks P, Smolders A, De V F, Spee J, Van A K, Bisseling T, Franssen H. 1993. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. The Plant Journal, 3, 573–585.
Zucchero J C, Caspi M, Dunn K. 2001. NGL9: A third MADS box gene expressed in alfalfa root nodules. Molecular Plant-Microbe Interactions, 14, 1463–1467.
[1] Muhammad Ahsan ASGHAR, JIANG Heng-ke, SHUI Zhao-wei, CAO Xi-yu, HUANG Xi-yu, Shakeel IMRAN, Bushra AHMAD, ZHANG Hao, YANG Yue-ning, SHANG Jing, YANG Hui, YU Liang, LIU Chun-yan, YANG Wen-yu, SUN Xin, DU Jun-bo. Interactive effect of shade and PEG-induced osmotic stress on physiological responses of soybean seedlings[J]. >Journal of Integrative Agriculture, 2021, 20(9): 2382-2394.
[2] ZHANG Yong-fang, ZHANG Chun-yan, ZHANG Bo, YIN Man, HONG Hui-long, YU Li-li, GAO Hua-wei, GU Yong-zhe, LIU Zhang-xiong, LI Fu-heng, QIU Li-juan. Establishment and application of an accurate identification method for fragrant soybeans[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1193-1203.
[3] Alireza NEHBANDANI, Afshin SOLTANI, Ali RAHEMI-KARIZAKI, Amir DADRASI, Faranak NOURBAKHSH. Determination of soybean yield gap and potential production in Iran using modeling approach and GIS[J]. >Journal of Integrative Agriculture, 2021, 20(2): 395-407.
[4] Hyen Chung CHUN, Sanghun LEE, Young Dae CHOI, Dong Hyeok GONG, Ki Youl JUNG. Effects of drought stress on root morphology and spatial distribution of soybean and adzuki bean[J]. >Journal of Integrative Agriculture, 2021, 20(10): 2639-2651.
[5] YE Wen-wu, ZENG Dan-dan, XU Miao, YANG Jin, MA Jia-xin, WANG Yuan-chao, ZHENG Xiao-bo. A LAMP-assay-based specific microbiota analysis reveals community dynamics and potential interactions of 13 major soybean root pathogens[J]. >Journal of Integrative Agriculture, 2020, 19(8): 2056-2063.
[6] WANG Yi-fan, LIAO Yu-qiu, WANG Ya-peng, YANG Jiang-wei, ZHANG Ning, SI Huai-jun. Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1609-1624.
[7] GUO Bing-fu, HONG Hui-long, HAN Jia-nan, ZHANG Li-juan, LIU Zhang-xiong, GUO Yong, QIU Li-juan. Development and identification of glyphosate-tolerant transgenic soybean via direct selection with glyphosate[J]. >Journal of Integrative Agriculture, 2020, 19(5): 1186-1196.
[8] JIANG Zhen-feng, LIU Dan-dan, WANG Tian-qiong, LIANG Xi-long, CUI Yu-hai, LIU Zhi-hua, LI Wen-bin. Concentration difference of auxin involved in stem development in soybean[J]. >Journal of Integrative Agriculture, 2020, 19(4): 953-964.
[9] ZHANG Li-xin, LIU Wei, Mesfin Tsegaw, XU Xin, QI Yan-ping, Enoch Sapey, LIU Lu-ping, WU Ting-ting, SUN Shi, HAN Tian-fu. Principles and practices of the photo-thermal adaptability improvement in soybean[J]. >Journal of Integrative Agriculture, 2020, 19(2): 295-310.
[10] CHENG Hang-yuan, WANG Xing, FENG Tian-yu, PENG Chuan-xi, WANG Wei, YANG Mu-yu, ZHOU Yu-yi. Giving maize an excited start – Effects of dopamine on maize germination[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2690-2698.
[11] YAN Hao, ZHANG Jing-yong, ZHANG Chun-bao, PENG Bao, ZHANG Wei-long, WANG Peng-nian, DING Xiao-yang, LIU Bao-hui, FENG Xian-zhong, ZHAO Li-mei . Genetic effects and plant architecture influences on outcrossing rate in soybean[J]. >Journal of Integrative Agriculture, 2019, 18(9): 1971-1979.
[12] FU Zhi-dan, ZHOU Li, CHEN Ping, DU Qing, PANG Ting, SONG Chun, WANG Xiao-chun, LIU Wei-guo, YANG Wen-yu, YONG Tai-wen. Effects of maize-soybean relay intercropping on crop nutrient uptake and soil bacterial community[J]. >Journal of Integrative Agriculture, 2019, 18(9): 2006-2018.
[13] LIU Wei-guo, WEN Bing-xiao, ZHOU Tao, WANG Li, GAO Yang, LI Shu-xian, QIN Si-si, LIU Jiang, YANG Wen-yu. iTRAQ protein profile analysis of soybean stems reveals new aspects critical for lodging in intercropping systems[J]. >Journal of Integrative Agriculture, 2019, 18(9): 2029-2040.
[14] XIAO Pei-ying, LIU Yi, CAO Yue-ping.
Overexpression of G10-EPSPS in soybean provides high glyphosate tolerance
[J]. >Journal of Integrative Agriculture, 2019, 18(8): 1851-1858.
[15] XIA Ning, YAN Wen-bing, WANG Xiao-qi, SHAO Yu-peng, YANG Ming-ming, WANG Zhi-kun, ZHAN Yu-hang, TENG Wei-li, HAN Ying-peng, SHI Yan-guo. Genetic dissection of hexanol content in soybean seed through genome-wide association analysis[J]. >Journal of Integrative Agriculture, 2019, 18(6): 1222-1229.
No Suggested Reading articles found!