Chinese Bulletin of Botany ›› 2020, Vol. 55 ›› Issue (5): 623-633.DOI: 10.11983/CBB20034
• SPECIAL TOPICS • Previous Articles Next Articles
Weiqin Zhang1, Hang Zou2,3, Nina Zhang1, Xueyuan Lin1, Juan Chen1,2,*()
Received:
2020-03-03
Accepted:
2020-06-05
Online:
2020-09-01
Published:
2020-09-03
Contact:
Juan Chen
Weiqin Zhang, Hang Zou, Nina Zhang, Xueyuan Lin, Juan Chen. Influence Mechanisms of Nitric Oxide on Nodulation and Nitrogen Fixation in Legumes[J]. Chinese Bulletin of Botany, 2020, 55(5): 623-633.
Figure 1 The schematic diagram of NO production and degradation in the symbiotic system (modified from Hichri et al., 2016a) The figure contains the upper and lower parts, which correspond to the production and degradation of NO from plants and symbiotes, respectively. The seven horns star diagrams refer to the oxidation pathway and the oval diagrams refer to the reduction pathway. The lines indicate that studies have been confirmed, and the dashed lines indicate that it is yet to be studied. ETC: Mitochondrial electron transport chain; GSNOR: S-nitrosoglutathione reductase; Hmp: Flavin hemoglobin; Lb: Leghemoglobin; NnrS: Haem- and copper-con- taining membrane protein; Nor: NO reductase; NOS: NO synthase; ns-Hb: Nonsymbiotic hemoglobin; NR: Nitrate reductase; PAOX: Polyamine oxidase; sd-Hb: Single domain hemoglobin; Tr-Hb: Truncated hemoglobin; TrxR: Thioredoxin reduction enzymes; XOR: Xanthine oxidoreductase
Figure 2 Schematic diagram of the role of NO in symbiotic nitrogen fixation (modified from Boscari et al., 2013; Hichri et al., 2015, 2016b) On the one hand, NO inhibits nitrogen fixation and carbon and nitrogen metabolism; on the other hand, it regulates cellular redox status and maintains the energy state under low oxygen levels. A thin line with + indicate the activation, induction, and retention effects of NO; a thin line with - indicate the inhibition of NO. The oval thick line arrows indicate the main metabolic pathways of NO. Explosive type diagrams refer to enzymes from plants and bacterial symbionts, and lightning type diagram represents genes within rhizobium. ACO: Aconitic acid; CS: Citrate synthase; Gln: Glutamine; Glu: Glutamic acid; GS: Glutamine synthetase; GSH: Glutathione; GSHS: Glutathione synthetase; GSNO: S-nitrosoglu- tathione; Hb: Hemoglobin; IDH: Isocitrate dehydrogenase; MDH: Malate dehydrogenase; NH4+: Ammonium ion; Nif: Nitrogenase; SDH: Succinate dehydrogenase; γ-EC: γ-glu- tamylcysteine; γ-ECS: γ-glutamyl cysteine synthetase
[1] | 何恒斌, 贾桂霞 ( 2013). 豆科植物早期共生信号转导的研究进展. 植物学报 48, 665-675. |
[2] | 李欣欣, 许锐能, 廖红 ( 2016). 大豆共生固氮在农业减肥增效中的贡献及应用潜力. 大豆科学 35, 531-535. |
[3] | 尚玉婷, 张妮娜, 上官周平, 陈娟 ( 2018). 硫化氢在植物中的生理功能及作用机制. 植物学报 53, 565-574. |
[4] | 张绪成, 上官周平, 高世铭 ( 2005). NO对植物生长发育的调控机制. 西北植物学报 25, 812-818. |
[5] |
Arjona D, Wikström M, Ädelroth P ( 2015). Nitric oxide is a potent inhibitor of the cbb3-type heme-copper oxidases. FEBS Lett 589, 1214-1218.
DOI URL PMID |
[6] |
Bartnikas TB, Wang YS, Bobo T, Veselo A, Scholes CP, Shapleigh JP ( 2002). Characterization of a member of the NnrR regulon in Rhodobacter sphaeroides 2.4.3 encoding a haem-copper protein: the GenBank accession number for nnrS is U62403. Microbiology 148, 825-833.
DOI URL PMID |
[7] |
Baudouin E, Pieuchot L, Engler G, Pauly N, Puppo A ( 2006). Nitric oxide is formed in Medicago truncatula-Sinorhizobium meliloti functional nodules. Mol Plant Microbe Interact 19, 970-975.
DOI URL PMID |
[8] | Berger A, Brouquisse R, Pathak PK, Hichri I, Singh I, Bhatia S, Boscari A, Igamberdiev AU, Gupta KJ ( 2018). Pathways of nitric oxide metabolism and operation of phytoglobins in legume nodules: missing links and future directions. Plant Cell Environ 41, 2057-2068. |
[9] |
Bethke PC, Badger MR, Jones RL ( 2004). Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16, 332-341.
DOI URL PMID |
[10] |
Blanquet P, Silva L, Catrice O, Bruand C, Carvalho H, Meilhoc E ( 2015). Sinorhizobium meliloti controls nitric oxide-mediated post-translational modification of a Medicago truncatula nodule protein. Mol Plant Microbe Interact 28, 1353-1363.
DOI URL PMID |
[11] |
Boscari A, del Giudice J, Ferrarini A, Venturini L, Zaffini AL, Delledonne M, Puppo A ( 2013). Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol 161, 425-439.
DOI URL PMID |
[12] |
Breakspear A, Liu CW, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen JQ, Oldroyd GED, Downie JA, Murray JD ( 2014). The root hair "infectome" of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26, 4680-4701.
DOI URL PMID |
[13] |
Calvo-Begueria L, Rubio MC, Martínez JI, Pérez-Ron- tomé C, Delgado MJ, Bedmar EJ, Becana M ( 2018). Redefining nitric oxide production in legume nodules through complementary insights from electron paramagnetic resonance spectroscopy and specific fluorescent probes. J Exp Bot 69, 3703-3714.
DOI URL PMID |
[14] |
Cam Y, Pierre O, Boncompagni E, Hérouart D, Meilhoc E, Bruand C ( 2012). Nitric oxide (NO): a key player in the senescence of Medicago truncatula root nodules. New Phytol 196, 548-560.
DOI URL PMID |
[15] |
Castillo MC, Lozano-Juste J, González-Guzmán M, Rodriguez L, Rodriguez PL, León J ( 2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8, ra89.
DOI URL PMID |
[16] |
Chadha N, Mishra M, Rajpal K, Bajaj R, Choudhary DK, Varma A ( 2015). An ecological role of fungal endophytes to ameliorate plants under biotic stress. Arch Microbiol 197, 869-881.
DOI URL PMID |
[17] |
Chaki M, Kovacs I, Spannagl M, Lindermayr C ( 2014). Computational prediction of candidate proteins for S-nitrosylation in Arabidopsis thaliana. PLoS One 9, e110232.
DOI URL PMID |
[18] |
Cueto M, Hernández-Perera O, Martín R, Bentura ML, Rodrigo J, Lamas S, Golvano MP ( 1996). Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Lett 398, 159-164.
DOI URL PMID |
[19] |
De Bruijn FJ, Rossbach S, Bruan C, Parrish JR ( 2006). A highly conserved Sinorhizobium meliloti operon is induced microaerobically via the FixLJ system and by nitric oxide (NO) via NnrR. Environ Microbiol 8, 1371-1381.
DOI URL PMID |
[20] |
Dean JV, Harper JE ( 1988). The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol 88, 389-395.
DOI URL PMID |
[21] |
del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A ( 2011). Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191, 405-417.
DOI URL PMID |
[22] |
Desalvo MK, Sunagawa S, Voolstra CR, Medina M ( 2010). Transcriptomic responses to heat stress and bleaching in the Elkhorn coral Acropora palmata. Mar Ecol Prog Ser 402, 97-113.
DOI URL |
[23] |
Ding YL, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GED ( 2008). Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20, 2681-2695.
DOI URL PMID |
[24] |
Escuredo PR, Minchin FR, Gogorcena Y, Iturbe-Or- maetxe I, Klucas RV, Becana M ( 1996). Involvement of activated oxygen in nitrate-induced senescence of pea root nodules. Plant Physiol 110, 1187-1195.
DOI URL PMID |
[25] |
Ferrarini A, De Stefano M, Baudouin E, Pucciariello C, Polverari A, Puppo A, Delledonne M ( 2008). Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol Plant Microbe Interact 21, 781-790.
URL PMID |
[26] | Garg N, Geetanjali , (2007). Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C, eds. Sustainable Agriculture. Dordrecht: Springer. pp. 519-531. |
[27] |
Gonzalez-Rizzo S, Crespi M, Frugier F ( 2006). The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18, 2680-2693.
DOI URL PMID |
[28] |
Gupta KJ, Hebelstrup KH, Mur LAJ, Igamberdiev AU ( 2011). Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett 585, 3843-3849.
DOI URL PMID |
[29] |
Hawkins TD, Krueger T, Becker S, Fisher PL, Davy SK ( 2014). Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals. Coral Reefs 33, 141-153.
DOI URL |
[30] |
Herold S, Puppo A ( 2005). Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules? J Biol Inorg Chem 10, 935-945.
DOI URL PMID |
[31] |
Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R ( 2015). Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66, 2877-2887.
DOI URL PMID |
[32] | Hichri I, Boscari A, Meilhoc E, Catalá M, Barreno E, Bruand C, Lanfranco L, Brouquisse R (2016a). Nitric oxide: a multitask player in plant-microorganism symbioses. In: Lamattina L, García-Mata C, eds. Gasotransmitters in Plants: The Rise of a New Paradigm in Cell Signaling. Cham: Springer. pp. 239-268. |
[33] | Hichri I, Meilhoc E, Boscari A, Bruand C, Frendo P, Brouquisse R ( 2016b). Nitric oxide: jack-of-all-trades of the nitrogen-fixing symbiosis? Adv Bot Res 77, 193-218. |
[34] |
Hill RD ( 2012). Non-symbiotic haemoglobins-what's happening beyond nitric oxide scavenging? AoB Plants 2012, pls004.
DOI URL PMID |
[35] | Horchani F, Prévot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi- Smiti S, Puppo A, Brouquisse R ( 2011). Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 15, 1023-1036. |
[36] |
Hu JL, Huang XH, Chen LC, Sun XW, Lu CM, Zhang LX, Wang YC, Zuo JR ( 2015). Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167, 1731-1746.
DOI URL PMID |
[37] |
Iarullina DR, Asafova EV, Kartunova IE, Ziiatdinova GK, Il'inskaia ON ( 2014). Probiotics for plants: NO-producing lactobacilli protect plants from drought. Prikl Biokhim Mikrobiol 50, 189-192.
URL PMID |
[38] |
Igamberdiev AU, Hill RD ( 2004). Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55, 2473-2482.
URL PMID |
[39] |
Igamberdiev AU, Hill RD ( 2009). Plant mitochondrial function during anaerobiosis. Ann Bot 103, 259-268.
DOI URL PMID |
[40] |
Igamberdiev AU, Ratcliffe RG, Gupta KJ ( 2014). Plant mitochondria: source and target for nitric oxide. Mitochondrion 19, 329-333.
DOI URL PMID |
[41] |
Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P ( 2007). Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225, 1597-1602.
URL PMID |
[42] |
Kato K, Kanahama K, Kanayama Y ( 2010). Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules. J Plant Physiol 167, 238-241.
DOI URL PMID |
[43] |
Kearns EV, Assmann SM ( 1993). The guard cell-environment connection. Plant Physiol 102, 711-715.
DOI URL PMID |
[44] |
Lee HW, Hitchcoc TM, Park SH, Mi R, Kraft JD, Luo J, Cao WG ( 2010). Involvement of thioredoxin domain-containing 5 in resistance to nitrosative stress. Free Radic Biol Med 49, 872-880.
DOI URL PMID |
[45] |
Li BH, Li GJ, Kronzucker HJ, Baluška F, Shi WM ( 2014). Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends Plant Sci 19, 107-114.
DOI URL PMID |
[46] |
Lin AH, Wang YQ, Tang JY, Xue P, Li CL, Liu LC, Hu B, Yang FQ, Loake GJ, Chu CC ( 2012). Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158, 451-464.
DOI URL PMID |
[47] |
Loscos J, Matamoros MA, Becana M ( 2008). Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146, 1282-1292.
DOI URL PMID |
[48] |
Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M ( 1999). Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121, 879-888.
DOI URL PMID |
[49] |
Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz KJ, Becana M ( 2015). Function of glutathione peroxidases in legume root nodules. J Exp Bot 66, 2979-2990.
DOI URL PMID |
[50] |
Meakin GE, Bueno E, Jepson B, Bedmar EJ, Richardson DJ, Delgado MJ ( 2007). The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules. Microbiology 153, 411-419.
DOI URL PMID |
[51] |
Meilhoc E, Blanquet P, Cam Y, Bruand C ( 2013). Control of NO level in rhizobium-legume root nodules: not only a plant globin story. Plant Signal Behav 8, e25923.
DOI URL |
[52] |
Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R ( 2011). Nitric oxide in legume-rhizobium symbiosis. Plant Sci 181, 573-581.
DOI URL PMID |
[53] |
Melo PM, Silva LS, Ribeiro I, Seabra AR, Carvalho HG ( 2011). Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiol 157, 1505-1517.
DOI URL PMID |
[54] |
Moreau M, Lindermayr C, Durner J, Klessig DF ( 2010). NO synthesis and signaling in plants-where do we stand?. Physiol Plant 138, 372-383.
DOI URL PMID |
[55] |
Mur LAJ, Prats E, Pierre S, Hall MA, Hebelstrup KH ( 2013). Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Front Plant Sci 4, 215.
DOI URL PMID |
[56] |
Murakami EI, Nagata M, Shimoda Y, Kucho KI, Higashi S, Abe M, Hashimoto M, Uchiumi T ( 2011). Nitric oxide production induced in roots of Lotus japonicus by lipopolysaccharide from Mesorhizobium loti. Plant Cell Physiol 52, 610-617.
DOI URL PMID |
[57] |
Nagata M, Murakami EI, Shimoda Y, Shimoda-Sasakura F, Kucho KI, Suzuki A, Abe M, Higashi S, Uchiumi T ( 2008). Expression of a class 1 hemoglobin gene and production of nitric oxide in response to symbiotic and pathogenic bacteria in Lotus japonicus. Mol Plant Microbe Interact 21, 1175-1183.
DOI URL PMID |
[58] |
Navascués J, Pérez-Rontomé C, Gay M, Marcos M, Yang F, Walker FA, Desbois A, Abián J, Becana M ( 2012). Leghemoglobin green derivatives with nitrated hemes evidence production of highly reactive nitrogen species during aging of legume nodules. Proc Natl Acad Sci USA 109, 2660-2665.
URL PMID |
[59] |
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I ( 2008). Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59, 165-176.
DOI URL PMID |
[60] |
Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C ( 2008). Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59, 177-186.
DOI URL PMID |
[61] |
Pérez-Chaca MV, Rodríguez-Serrano M, Molina AS, Pedranzani HE, Zirulnik F, Sandalio LM, Romero- Puertas MC ( 2014). Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant Cell Environ 37, 1672-1687.
DOI URL PMID |
[62] |
Pérez Guerra JC, Coussens G, De Keyser A, De Rycke R, De Bodt S, Van De Velde W, Goormachtig S, Holsters M ( 2010). Comparison of developmental and stress-indu- ced nodule senescence in Medicago truncatula. Plant Physiol 152, 1574-1584.
DOI URL PMID |
[63] |
Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T ( 2007). Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7, 21.
URL PMID |
[64] |
Procházková D, Wilhelmová N ( 2011). Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. Nitric Oxide 24, 61-65.
DOI URL PMID |
[65] |
Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R ( 2013). Hydrogen peroxide and nitric oxide: key regulators of the legume- Rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18, 2202-2219.
URL PMID |
[66] |
Radi R ( 2004). Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci USA 101, 4003-4008.
DOI URL PMID |
[67] |
Romanov VI, Fedulova NG, Tchermenskaya IE, Shramko VI, Molchanov MI, Kretovich WL ( 1980). Metabolism of poly-hydroxybutyric acid in bacteroids of Rhizobium lupini in connection with nitrogen fixation and photosynthesis. Plant Soil 56, 379-390.
DOI URL |
[68] |
Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M ( 2015). Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J 81, 723-735.
DOI URL PMID |
[69] |
Sánchez C, Cabrera JJ, Gates AJ, Bedmar EJ, Richardson DJ, Delgado MJ ( 2011). Nitric oxide detoxification in the rhizobia-legume symbiosis. Biochem Soc Trans 39, 184-188.
DOI URL PMID |
[70] |
Sánchez C, Gates AJ, Meakin GE, Uchiumi T, Girard L, Richardson DJ, Bedmar EJ, Delgado MJ ( 2010). Production of nitric oxide and nitrosylleghemoglobin complexes in soybean nodules in response to flooding. Mol Plant Microbe Interact 23, 702-711.
DOI URL PMID |
[71] | She XP, Song XG, He JM ( 2004). Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Bot Sin 46, 1292-1300. |
[72] |
Shimoda Y, Nagata M, Suzuki A, Abe M, Sato S, Kato T, Tabata S, Higashi S, Uchiumi T ( 2005). Symbiotic rhizobium and nitric oxide induce gene expression of non- symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46, 99-107.
DOI URL PMID |
[73] |
Singh VP, Singh S, Kumar J, Prasad SM ( 2015). Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181, 20-29.
URL PMID |
[74] |
Smil V ( 1999). Detonator of the population explosion. Nature 400, 415.
DOI URL |
[75] |
Suzuki A, Akune M, Kogiso M, Imagama Y, Osuk K, Uchiumi T, Higashi S, Han SY, Yoshida S, Asami T, Abe M ( 2004). Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol 45, 914-922.
DOI URL PMID |
[76] | Swaraj K, Sheokand S, Fernandez-Pascual MM, de Felipe MR ( 2001). Dark-induced changes in legume nodule functioning. Aust J Plant Physiol 28, 429-438. |
[77] |
Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho KI, Hashiguchi M, Akashi R, Hirsch A, Arima S, Suzuki A ( 2010). Effect of abscisic acid on symbiotic nitrogen fixation activity in the root nodules of Lotus japonicus. Plant Signal Behav 5, 440-443.
DOI URL PMID |
[78] |
Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ ( 1997). Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci USA 94, 12230-12234.
DOI URL PMID |
[79] |
Van de Velde W, Guerra JCP, De Keyser A, De Rycke R, 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 Physiol 141, 711-720.
DOI URL PMID |
[80] |
Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A, Kondorosi E ( 2003). Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15, 2093-2105.
DOI URL PMID |
[81] |
Wally OSD, Mira MM, Hill RD, Stasolla C ( 2013). Hemoglobin regulation of plant embryogenesis and plant pathogen interaction. Plant Signal Behav 8, e25264.
DOI URL PMID |
[82] |
Wodala B, Deák Z, Vass I, Erdei L, Altorjay I, Horváth F ( 2008). In vivo target sites of nitric oxide in photosynthetic electron transport as studied by chlorophyll fluorescence in pea leaves. Plant Physiol 146, 1920-1927.
DOI URL PMID |
[83] |
Yoshida T, Mogami J, Yamaguchi-Shinozaki K ( 2015). Omics approaches toward defining the comprehensive abscisic acid signaling network in plants. Plant Cell Physiol 56, 1043-1052.
DOI URL PMID |
[84] |
Zeiger E ( 1983). The biology of stomatal guard cells. Annu Rev Plant Physiol 34, 441-474.
DOI URL |
[85] |
Zimmer-Prados LM, Moreira ASFP, Magalhaes JR, França MGC ( 2014). Nitric oxide increases tolerance responses to moderate water deficit in leaves of Phaseolus vulgaris and Vigna unguiculata bean species. Physiol Mol Biol Plants 20, 295-301.
DOI URL PMID |
[1] | Xiaomin Feng, Xiang Gao, Huadong Zang, Yuegao Hu, Changzhong Ren, Zhiping Hao, Huiqing Lü, Zhaohai Zeng. Intercropping Effect and Nitrogen Transfer Characteristics of Oat-Mungbean Intercrop [J]. Chinese Bulletin of Botany, 2023, 58(1): 122-131. |
[2] | LI Qiang, HUANG Ying-Xin, ZHOU Dao-Wei, CONG Shan. Mechanism of the trade-off between biological nitrogen fixation and phosphorus acquisition strategies of herbaceous legumes under nitrogen and phosphorus addition [J]. Chin J Plant Ecol, 2021, 45(3): 286-297. |
[3] | WANG Yin-Liu, GENG Qian-Qian, HUANG Jian-Hui, WANG Chang-Hui, LI Lei, HASI Muqier, NIU Guo-Xiang. Effects of nitrogen addition and planting density on the growth and biological nitrogen fixation of Lespedeza davurica [J]. Chin J Plant Ecol, 2021, 45(1): 13-22. |
[4] | Chengwu Liu, Zhong Zhao. The Legume SHR-SCR Module Predetermines Nodule Founder Cell Identity [J]. Chinese Bulletin of Botany, 2020, 55(6): 661-665. |
[5] | Zeng Yinwei, Cao Yuman, Sha Xuyang, Li Shuxia, Yang Peizhi, Hu Tianming, Liu Jinlong. An Observation Method of Nodule and Root Morphology without Damage in Real-time [J]. Chinese Bulletin of Botany, 2018, 53(5): 661-670. |
[6] | Ai Wenqin, Jiang Hanyuan, Li Xinxin, Liao Hong. An Efficient Nutrient Solution System to Study Symbiotic Nitrogen Fixation in Soybean [J]. Chinese Bulletin of Botany, 2018, 53(4): 519-527. |
[7] | Mei Qiao, Jiawei Sun, Yan Chen, Shengfang Han, Chunyan Hou, Gang Liu, Dongmei Wang. Dynamics and Interaction of Ca2+ and Nitric Oxide in Wheat Suspension Cells in the Hypersensitive Response [J]. Chinese Bulletin of Botany, 2015, 50(1): 1-11. |
[8] | Hengbin He, Guixia Jia. Research Progress in Early Symbiotic Signal Transduction in Legumes [J]. Chinese Bulletin of Botany, 2013, 48(6): 665-675. |
[9] | Yuji Lian, Guangzhe Lin, Xiaomei Zhao. Histology and Development Analysis of Meristematic Nodules from Cultured Pulsatilla koreana [J]. Chinese Bulletin of Botany, 2013, 48(5): 540-549. |
[10] | Yuan Zhong, Fangyun Cheng, Lei Qin. Meristematic Nodule: a Valuable Developmental Pathway for Plant Regeneration [J]. Chinese Bulletin of Botany, 2011, 46(3): 350-360. |
[11] | CHOU Min-Xia, WEI Xin-Yuan. Review of research advancements on the molecular basis and regulation of symbiotic nodulation of legumes [J]. Chin J Plant Ecol, 2010, 34(7): 876-888. |
[12] | ZHANG Can-Juan, WU Dong-Xiu, ZHANG Lin, ZHAN Xiao-Yun, ZHOU Shuang-Xi, YANG Yun-Xia. NODULE CHARACTERISTICS OF THREE-YEAR-OLD CARAGANA MICROPHYLLA AND THEIR RESPONSES TO ENVIRONMENTAL CHANGES IN AN INNER MONGOLIA GRASSLAND [J]. Chin J Plant Ecol, 2009, 33(6): 1165-1176. |
[13] | LI Su-Mei, LONG Chun-Lin, DAO Zhi-Ling. AN EFFECTIVE WAY TO IMPROVE SOIL FERTILITY IN TRADITIONAL AGROFORESTRY: PLANTING ALNUS NEPALENSIS [J]. Chin J Plant Ecol, 2006, 30(5): 878-886. |
[14] | GUO Bao-Sheng;WENG Yue-Jin. Salt Tolerance Mechanism and Molecular Markers of Genes Associated with Salt Tolerance in Soybean [J]. Chinese Bulletin of Botany, 2004, 21(01): 113-120. |
[15] | NIU Shu-Li, JIANG Gao-Ming. Effect of Elevated CO2 on Legume Plants With Nitrogen Fixation [J]. Chin J Plant Ecol, 2003, 27(6): 844-851. |
Viewed | ||||||
Full text |
|
|||||
Abstract |
|
|||||