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Involvement of autoregulation in the interaction between rhizobial nodulation and AM fungal colonization in soybean roots

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An Erratum to this article was published on 18 January 2014

Abstract

Soybean plants autoregulate to suppress excessive nodulation. It has been revealed recently that the autoregulation of various legumes controls both nodulation and arbuscular mycorrhizal (AM) fungal colonization. We investigated the involvement of autoregulation in the interaction between rhizobial nodulation and AM fungal colonization. We used a wild-type soybean cv. Enrei and its hypernodulating mutant Kanto100, defective in the autoregulation. We included four different treatments: an uninoculated control, inoculation with rhizobium Bradyrhizobium japonicum alone, inoculation with AM fungus Gigaspora rosea alone, and dual inoculation with rhizobium and AM fungus. In both Enrei and Kanto100, AM fungal colonization enhanced the weight and N2 fixation of nodules, suggesting that autoregulation of host plant is not involved in the stimulatory effect of AM fungal colonization on rhizobial nodulation. In plants with the AM fungus alone, the AM fungal colonization of Enrei was comparable to that of Kanto100. In plants with dual inoculation, however, this was significantly (P < 0.05) lower than in Kanto100. To confirm the control of AM fungal colonization by the autoregulation of host plant, a reciprocal grafting experiment was performed between Enrei and Kanto100. In plants with the AM fungus alone, AM fungal colonization was comparable among Enrei (shoot)/Enrei (root), Enrei/Kanto100, Kanto100/Enrei, and Kanto100/Kanto100 grafts. In plants with dual inoculation, however, AM fungal colonization of Enrei/Enrei and Enrei/Kanto100 grafts was significantly (P < 0.05) lower than that of Kanto100/Enrei and Kanto100/Kanto100. These results indicate that rhizobial nodulation suppresses AM fungal colonization, and the autoregulation of host plant, initiated by nodulation, is involved in this phenomenon.

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References

  • Akao S, Kouchi H (1992) A supernodulating mutant isolated from soybean cultivar Enrei. Soil Sci Plant Nutr 38:183–187

    Article  Google Scholar 

  • Antunes PM, Rajcan I, Goss MJ (2006a) Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max (L.) Merr.). Soil Biol Biochem 38:533–543

    Article  CAS  Google Scholar 

  • Antunes PM, de Varennes A, Rajcan I, Goss MJ (2006b) Accumulation of specific flavonoids in soybean (Glycine max (L.) Merr.) as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum (Kirchner) Jordan. Soil Biol Biochem 38:1234–1242

    Article  CAS  Google Scholar 

  • Antunes PM, de Varennes A, Zhang T, Goss MJ (2006c) The tripartite symbiosis formed by indigenous arbuscular mycorrhizal fungi, Bradyrhizobium japonicum and soya bean under field conditions. J Agron Crop Sci 192:373–378

    Article  Google Scholar 

  • Arai M, Hayashi M, Takahashi M, Shimada S, Harada K (2005) Expression and sequence analysis of systemic regulation gene for symbiosis, NTS1/GmNARK in supernodulating soybean cultivar, Sakukei 4. Breed Sci 55:147–152

    Article  CAS  Google Scholar 

  • Asai T (1944) Über die Mykorrhizenbildung der leguminosen Pflanzen. Jpn J Bot 13:463–485

    Google Scholar 

  • Badr El-Din SMS, Moawad H (1988) Enhancement of nitrogen fixation in lentil, faba bean, and soybean by dual inoculation with rhizobia and mycorrhizae. Plant Soil 108:117–124

    Article  Google Scholar 

  • Bagyaraj DJ, Manjunath A, Patil RB (1979) Interaction between a vesicular–arbuscular mycorrhiza and Rhizobium and their effects on soybean in the field. New Phytol 82:141–145

    Article  CAS  Google Scholar 

  • Barea JM, Azcón-Aguilar C (1983) Mycorrhizas and their significance in nodulating nitrogen-fixing plants. Adv Agron 36:1–54

    Article  Google Scholar 

  • Bethenfalvay GJ, Brown M, Stafford AE (1985) Glycine–Glomus–Rhizobium symbiosis: II. antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiol 79:1054–1058

    Article  Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Ann Rev Microbiol 45:345–382

    Article  Google Scholar 

  • Carling DE, Riehle WG, Brown MF, Johnson DR (1978) Effect of a vesicular–arbuscular mycorrhizal fungus on nitrate reductase and nitrogenase activities in nodulating and non-nodulating soybeans. Phytopathol 68:1590–1596

    Article  CAS  Google Scholar 

  • Carroll BJ, McNeil DL, Gresshoff PM (1985a) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82:4162–4166

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carroll BJ, McNeil DL, Gresshoff PM (1985b) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78:34–40

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Catford J-G, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54:1481–1487

    Article  CAS  PubMed  Google Scholar 

  • Catford J-G, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266

    Article  CAS  Google Scholar 

  • Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149

    Article  CAS  Google Scholar 

  • Chalk PM, RdeF S, Urquiqga S, Alves BJR, Boddy RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  • Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean–Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82:588–590

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132

    Google Scholar 

  • Francisco PB Jr, Akao S (1993) Autoregulation and nitrate inhibition of nodule formation in soybean cv. Enrei and its nodulation mutants. J Exp Bot 44:547–553

    Article  CAS  Google Scholar 

  • Goss MJ, de Varennes A (2002) Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol Biochem 34:1167–1173

    Article  CAS  Google Scholar 

  • Gremaud MF, Harper JE (1989) Selection and initial characterization of partially nitrate tolerant nodulation mutants of soybean. Plant Physiol 89:169–173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hamaguchi H, Kokubun M, Akao S (1992) Shoot control of nodulation is modified by the root in the supernodulating soybean mutant En6500 and its wild-type parent cultivar Enrei. Soil Sci Plant Nutr 38:771–774

    Article  Google Scholar 

  • Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean–Rhizobium–Glomus associations. New Phytol 101:427–440

    Article  CAS  Google Scholar 

  • Hayman DS (1986) Mycorrhizae of nitrogen-fixing legumes (review). MIRCEN J 2:121–145

    Article  Google Scholar 

  • Isoi T (1997) Comparison of arbuscular mycorrhizal fungal flora under different cropping systems in a light-colored Andosol of Japan. Soil Microorganisms 50:61–64

    Google Scholar 

  • Jalaluddin M (2005) Effect of inoculation with VAM-fungi and Bradyrhizobium on growth and yield of soybean in Sindh. Pak J Bot 37:169–173

    Google Scholar 

  • Jia Y, Gray VM, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann Bot 94:251–258

    Article  CAS  PubMed  Google Scholar 

  • Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbiosis? Soil Biol Biochem 41:1233–1244

    Article  CAS  Google Scholar 

  • Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127

    Article  CAS  Google Scholar 

  • Kawai Y, Yamamoto Y (1986) Increase in the formation and nitrogen fixation of soybean nodules by vesicular–arbuscular mycorrhiza. Plant Cell Physiol 27:399–405

    CAS  Google Scholar 

  • Khalil S, Loynachan TE, McNabb HS Jr (1992) Colonization of soybean by mycorrhizal fungi and spore populations in Iowa soils. Agron J 84:832–836

    Article  Google Scholar 

  • Khan MK, Sakamoto K, Yoshida T (1995) Dual inoculation of peanut with Glomus sp. and Bradyrhizobium sp. enhanced the symbiotic nitrogen fixation as assessed by 15N-technique. Soil Sci Plant Nutr 41:769–779

    Article  CAS  Google Scholar 

  • Kinkema M, Scott PT, Gresshoff PM (2006) Legume nodulation: successful symbiosis through short- and long-distance signaling. Funct Plant Biol 33:707–721

    Article  CAS  Google Scholar 

  • Kosslak RM, Bohlool BB (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol 75:125–130

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51:1381–1397

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426

    Article  CAS  PubMed  Google Scholar 

  • Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148

    Article  Google Scholar 

  • Larose G, Chenevert R, Moutoglis P, Gagné S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339

    Article  CAS  Google Scholar 

  • Meghvansi MK, Prasad K, Harwani D, Mahna SK (2008) Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi and Bradyrhizobium japonicum in the alluvial soil. Eur J Soil Biol 44:316–323

    Article  CAS  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    Article  CAS  PubMed  Google Scholar 

  • Meixner C, Vegvari G, Ludwig-Müller J, Gagnon H, Steinkellner S, Staehelin C, Gresshoff P, Vierheilig H (2007) Two defined alleles of the LRR receptor kinase GmNARK in supernodulating soybean govern differing autoregulation of mycorrhization. Physiol Plant 130:261–270

    Article  CAS  Google Scholar 

  • Minchin FR, Summerfield RJ, Hadley P, Roberts EH, Rawsthorne S (1981) Carbon and nitrogen nutrition of nodulated roots of grain legumes. Plant Cell Environ 4:5–26

    Article  CAS  Google Scholar 

  • Morandi D (1996) Occurrence of phytoalexins and phenolic compounds on endomycorrhizal interactions, and their potential role in biological control. Plant Soil 185:241–225

    Article  CAS  Google Scholar 

  • Morandi D, Sagan M, Prado-Vivant E, Duc G (2000) Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza 10:37–42

    Article  CAS  Google Scholar 

  • Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D'haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153:222–237

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Niranjan R, Mohan V, Rao VM (2007) Effect of indole acetic acid on the synergistic interactions of Bradyrhizobium and Glomus fasciculatum on growth, nodulation, and nitrogen fixation of Dalbergia sissoo Roxb. Arid Land Res Manag 21:329–342

    Article  CAS  Google Scholar 

  • Nishimura R, Hayashi M, Wu G-J, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signaling. Curr Opin Plant Biol 9:351–357

    Article  CAS  PubMed  Google Scholar 

  • Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310

    Article  CAS  Google Scholar 

  • Osunde AO, Gwan S, Bala A, Sanginga N (2003) Responses to rhizobial inoculation by two promiscuous soybean cultivars in soils of the Southern Guinea savanna zone of Nigeria. Biol Fertil Soils 37:274–279

    Google Scholar 

  • Pacovsky RS, Fuller G, Stafford AE (1986a) Nutrient and growth interactions in soybeans colonized with Glomus fasciculatum and Rhizobium japonicum. Plant Soil 92:37–45

    Article  Google Scholar 

  • Pacovsky RS, Paul EA, Bethlenfalvay GJ (1986b) Response of mycorrhizal and P-fertilized soybeans to nodulation by Bradyrhizobium or ammonium nitrate. Crop Sci 26:145–150

    Article  Google Scholar 

  • Pacovsky RS, Fuller G (1988) Mineral and lipid composition of Glycine–Glomus–Bradyrhizobium symbioses. Physiol Plant 72:733–746

    Article  CAS  Google Scholar 

  • Pierce M, Bauer WD (1983) A rapid regulatory response governing nodulation in soybean. Plant Physiol 73:286–290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rajapakse S, Miller JC (1994) Methods for studying vesicular–arbuscular mycorrhizal root colonization and related root physical properties. In: Norris JR, Read D, Varma AK (eds) Techniques for mycorrhizal research. Academic, London, pp 761–776

    Google Scholar 

  • Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant-Microbe Interact 24:606–618

    Article  CAS  PubMed  Google Scholar 

  • Sanginga N, Carsky RJ, Dashiell K (1999) Arbuscular mycorrhizal fungi respond to rhizobial inoculation and cropping systems in farmers' fields in the Guinea savanna. Biol Fertil Soils 30:179–186

    Article  Google Scholar 

  • Sakamoto K, Iijima T, Higuchi R (2004) Use of specific phospholipid fatty acids for identifying and quantifying the external hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea. Soil Biol Biochem 36:1827–1834

    Article  CAS  Google Scholar 

  • Sakamoto K, Nohara Y (2009) Soybean (Glycine max [L.] Merr.) shoots systemically control arbuscule formation in mycorrhizal symbiosis. Soil Sci Plant Nutr 55:252–257

    Article  Google Scholar 

  • Schenck NC, Kinloch RA (1980) Incidence of mycorrhizal fungi on six field crops in monoculture on a newly cleared woodland site. Mycologia 72:445–456

    Article  Google Scholar 

  • Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112

    Article  CAS  PubMed  Google Scholar 

  • Shrihari PC, Sakamoto K, Inubushi K, Akao S (2000) Interaction between supernodulating or non-nodulating mutants of soybean and two mycorrhizal fungi. Mycorrhiza 10:101–106

    Article  Google Scholar 

  • Singh HP, Singh TA (1993) The interaction of rockphosphate, Bradyrhizobium, vesicular–arbuscular mycorrhizae and phosphate-solubilizing microbes on soybean grown in a sub-Himalayan mollisol. Mycorrhiza 4:37–43

    Article  Google Scholar 

  • Solaiman MZ, Senoo K, Kawaguchi M, Imaizumi-Anraku H, Akao S, Tanaka A, Obata H (2000) Characterization of mycorrhizas formed by Glomus sp. on roots of hypernodulating mutants of Lotus japonicus. J Plant Res 113:443–448

    Article  Google Scholar 

  • Stougaard J (2001) Genetic and genomics of root symbiosis. Curr Opin Plant Biol 4:328–335

    Article  CAS  PubMed  Google Scholar 

  • Takahashi M, Shimada S, Nakayama N, Arihara J (2005) Characteristics of nodulation and nitrogen fixation in the improved supernodulating soybean (Glycine max (L.) Merr.) cultivar ‘Sakukei 4’. Plant Prod Sci 8:405–411

    Article  Google Scholar 

  • Thiagarajan TR, Ahmad MH (1993) Influence of a vesicular–arbuscular mycorrhizal fungus on the competitive ability of Bradyrhizobium spp. for nodulation of cowpea Vigna unguiculata (L.) Walp in non-sterilized soil. Biol Fertil Soils 15:294–296

    Article  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d`un systéme radiculaire. Recherche de méthodes d`estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • Vejsadová H, Siblíková D, Hršelová H, Vančura V (1992) Effect of the VAM fungus Glomus sp. on the growth and yield of soybean inoculated with Bradyrhizobium japonicum. Plant Soil 140:121–125

    Article  Google Scholar 

  • Vierheilig H, Bago B, Albrecht C, Poulin MJ, Piché Y (1998) Flavonoids and arbuscular–mycorrhizal fungi. In: Manthey J, Buslig B (eds) Flavonoids in the living system. Plenum, New York, pp 9–33

    Chapter  Google Scholar 

  • Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y (2000) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595

    Article  CAS  Google Scholar 

  • Vierheilig H (2004a) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 161:339–341

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H (2004b) Regulatory mechanisms during the plant–arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    Article  CAS  Google Scholar 

  • Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181

    Article  PubMed  Google Scholar 

  • Xie Z-P, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vögeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Ryo Yamamoto, NARO Institute of Crop Science, Tsukuba, Japan, for providing soybean seeds. We thank Professor Kazuyuki Inubushi and Dr. Miwa Matsushima-Yashima, Chiba University, for their valuable suggestions. This work was supported by the Japan Society for the Promotion of Science KAKENHI grant numbers 18380047 and 23380042.

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  1. Department of Horticulture, Chiba University, Matsudo, Chiba, 271-8510, Japan

    Kazunori Sakamoto, Natsuko Ogiwara & Tomomitsu Kaji

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Sakamoto, K., Ogiwara, N. & Kaji, T. Involvement of autoregulation in the interaction between rhizobial nodulation and AM fungal colonization in soybean roots. Biol Fertil Soils 49, 1141–1152 (2013). https://doi.org/10.1007/s00374-013-0804-8

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