GmNMH7, a MADS-box transcription factor, inhibits root development and nodulation of soybean(Glycine max [L.] Merr.)
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摘要
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 GmN MH7 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, GmNFR1 a, GmNFR5 a, and GmNIN) after rhizobia inoculation. The earlier expression peak of GmNMH7 compared to the other genes(GmENOD40-1, GmENOD40-2, GmNFR1 a, GmNFR5 a, 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, overexpression of GmN MH7 significantly down-regulated the expression levels of GmE NOD40-1, GmE NOD40-2, and GmN FR5α. Moreover, the expression of GmNMH7 could respond to abscisic acid(ABA) and gibberellin(GA_3) treatment in the root of Zigongdongdou seedlings. Over-expressing GmNMH7 gene reduced the content of ABA, and increased the content of GA_3 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 GA_3.
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 GmN MH7 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, GmNFR1 a, GmNFR5 a, and GmNIN) after rhizobia inoculation. The earlier expression peak of GmNMH7 compared to the other genes(GmENOD40-1, GmENOD40-2, GmNFR1 a, GmNFR5 a, 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, overexpression of GmN MH7 significantly down-regulated the expression levels of GmE NOD40-1, GmE NOD40-2, and GmN FR5α. Moreover, the expression of GmNMH7 could respond to abscisic acid(ABA) and gibberellin(GA_3) treatment in the root of Zigongdongdou seedlings. Over-expressing GmNMH7 gene reduced the content of ABA, and increased the content of GA_3 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 GA_3.
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 GmN MH7 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, GmNFR1 a, GmNFR5 a, and GmNIN) after rhizobia inoculation. The earlier expression peak of GmNMH7 compared to the other genes(GmENOD40-1, GmENOD40-2, GmNFR1 a, GmNFR5 a, 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, overexpression of GmN MH7 significantly down-regulated the expression levels of GmE NOD40-1, GmE NOD40-2, and GmN FR5α. Moreover, the expression of GmNMH7 could respond to abscisic acid(ABA) and gibberellin(GA_3) treatment in the root of Zigongdongdou seedlings. Over-expressing GmNMH7 gene reduced the content of ABA, and increased the content of GA_3 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 GA_3.
引文
Amor B B,Shaw S L,Oldroyd G E,Maillet F,Penmetsa R V,Cook D,Long S R,DénariéJ,Gough C.2003.The NFPlocus 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 Ta NHX2,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 EMBOJournal,13,5099-5112.
F?hraeus 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 KA,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 AV,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 CD,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 BJ,Gresshoff P M.2011.Nodulation factor receptor kinase1αcontrols 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,ImaizumiAnraku 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 MADSdomain 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 MADSdomain 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,Gr?nlund 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.Amolecular view on nodule senescence in Medicago truncatula.Plant Physiology,141,711-720.
Wan X,Franssen H.2007.Medicago truncatulaENOD40-1and 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 GmNMH7gene 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 Gm ENOD40,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 MADSbox gene expressed in alfalfa root nodules.Molecular PlantMicrobe Interactions,14,1463-1467.
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 Ta NHX2,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 EMBOJournal,13,5099-5112.
F?hraeus 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 KA,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 AV,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 CD,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 BJ,Gresshoff P M.2011.Nodulation factor receptor kinase1αcontrols 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,ImaizumiAnraku 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 MADSdomain 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 MADSdomain 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,Gr?nlund 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.Amolecular view on nodule senescence in Medicago truncatula.Plant Physiology,141,711-720.
Wan X,Franssen H.2007.Medicago truncatulaENOD40-1and 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 GmNMH7gene 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 Gm ENOD40,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 MADSbox gene expressed in alfalfa root nodules.Molecular PlantMicrobe Interactions,14,1463-1467.