Abstract
Symbiotic nitrogen fixation between legumes and rhizobia bacteria occurs in a microaerobic environment within a specialized organ, the root nodule. The fixation of dinitrogen requires a considerable energy input and a high respiratory rate, but the fundamental nitrogen fixation enzyme, nitrogenase, is inactivated by free oxygen. Because of this apparent conundrum, the diffusion of oxygen into the nodule infection zone is exquisitely regulated in response to multiple environmental cues, and becomes sensitive to alterations in the external rhizosphere oxygen tension. As a result, most legumes are sensitive to waterlogging, showing reductions in nodulation and productivity in flooded soils. Nevertheless, certain legumes have evolved developmental strategies to modulate the pathway of oxygen diffusion to the nodule, the patterns of nodule formation on roots and stems, and altered pathways of bacterial invasion to adapt to flooding conditions. In the present chapter, the regulation of oxygen diffusion and adaptations to waterlogged conditions by nitrogen fixing nodules of flooding-sensitive and flooding-tolerant legumes are discussed.
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Abbreviations
- ACC:
-
1-Aminocyclopropane-1-carboxylate
- GA:
-
Gibberellic acid
- IT:
-
Infection thread
- K m :
-
Michaelis constant
- kPa:
-
kilopascal
- LRB:
-
Lateral root boundary
- Oi :
-
Free oxygen concentration within the infected cells
- PIP:
-
Plasma membrane intrinsic protein
- P f :
-
Osmotic water permeability
- RHC:
-
Root hair curling
- ROS:
-
Reactive oxygen species
- TIP:
-
Tonoplast intrinsic protein
References
Alazard D (1985) Stem and root nodulation in Aeschynomene spp. Appl Environ Microbiol 50:732–734
Allen ON, Allen EK (1981) The Leguminosae: a source book of characteristics, uses, and nodulation. The University of Wisconsin Press, Madison, WI, USA
Arrese-Igor C, Royuela M, de Lorenzo C, de Felipe MR, Aparicio-Tejo PM (1993) Effect of low rhizosphere oxygen on growth, nitrogen fixation and nodule morphology in lucerne. Physiol Plant 89:55–63
Atkins CA, Hunt S, Layzell DB (1993) Gaseous diffusive properties of soybean nodules cultured with non-ambient pO2. Physiol Plant 87:89–95
Bacanamwo M, Purcell LC (1999a) Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. J Exp Bot 50:689–696
Bacanamwo M, Purcell LC (1999b) Soybean root morphological and anatomical traits associated with acclimation to flooding. Crop Sci 39:143–149
Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Batzli JM, Dawson JO (1999) Development of flood-induced nodule lenticels on red alder during the restoration of nitrogenase activity. Can J Bot 77:1373–1377
Becker M, Ladha JK, Ali M (1995) Green manure technology: potential, usage, and limitations. A case study for lowland rice. Plant Soil 174:181–194
Bergersen FJ (1982) Root nodules of legumes: structure and functions. Wiley, New York
Bergersen FJ (1997) Regulation of nitrogen fixation in infected cells of leguminous root nodules in relation to O2 supply. Plant Soil 191:189–203
Bergersen FJ, Turner GL (1993) Effects of concentrations of substrates supplied to N2-fixing soybean bacteroids in flow chamber reactions. Proc R Soc Lond B 245:59–64
Boivin C, Ndoye I, Molouba F, Lajudie P, Dupuy N, Dreyfus B (1997) Stem nodulation in legumes: diversity, mechanisms, and unusual characteristics. Crit Rev Plant Sci 16:1–30
Bradley DJ, Wood EA, Larkins AP, Galfre G, Butcher GW, Brewin NJ (1988) Isolation of monoclonal antibodies reacting with peribacteroid membranes and other components of pea root nodules containing Rhizobium leguminosarum. Planta 173:149–160
Buttery BR (1987) Some effects of waterlogging and supply of combined nitrogen on soybean growth. Can J Plant Sci 67:69–77
Capoen W, Den Herder J, Rombauts S, De Gussem J, De Keyser A, Holsters M, Goormachtig S (2007) Comparative transcriptome analysis reveals common and specific tags for root hair and crack-entry invasion in Sesbania rostrata. Plant Physiol 144:1878–1889
Capoen W, Den Herder J, Sun J, Verplancke C, De Keyser A, De Rycke R, Goormachtig S, Oldroyd G, Holsters M (2009) Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell 21:1526–1540
Criswell JG, Havelka UD, Quebedeaux B, Hardy RWF (1976) Adaptation of nitrogen fixation by intact soybean nodules to altered rhizosphere pO2. Plant Physiol 58:622–625
D'Haeze W, Gao M, De Rycke R, Van Montagu M, Engler G, Holsters M (1998) Roles for azorhizobial nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol Plant-Microbe Interact 11:999–1008
D'Haeze W, Mergaert P, Promé JC, Holsters M (2000) Nod factor requirements for efficient stem and root nodulation of the tropical legume Sesbania rostrata. J Biol Chem 275:15676–15684
D'Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79–105
D'Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S, Verplancke C, Capoen W, Holsters M (2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Proc Natl Acad Sci USA 100:11789–11794
Dakora FD, Atkins CA (1990a) Morphological and structural adaptation of nodules of cowpea to functioning under sub- and supra-ambient oxygen pressure. Planta 182:572–582
Dakora FD, Atkins CA (1990b) Effect of pO2 on growth and nodule functioning of symbiotic cowpea (Vigna unguiculata L. Walp.). Plant Physiol 93:948–955
Dakora FD, Atkins CA (1990c) Effect of pO2 during growth on the gaseous diffusional properties of nodules of cowpea (Vigna unguiculata L. Walp.). Plant Physiol 93:956–961
Dakora FD, Atkins CA (1991) Adaptation of nodulated soybean (Glycine max L. Merr.) to growth in rhizospheres containing nonambient pO2. Plant Physiol 96:728–736
de Lorenzo C, Iannetta PPM, Fernandez-Pascual M, James EK, Lucas MM, Sprent JI, Witty JF, Minchin FR, de Felipe MR (1993) Oxygen diffusion in lupin nodules II. Mechanisms of diffusion barrier operation. J Exp Bot 44:1469–1474
Den Herder J, Schroeyers K, Holsters M, Goormachtig S (2006) Signaling and gene expression for water-tolerant legume nodulation. Crit Rev Plant Sci 25:367–380
Denison RF, Kinraide TB (1995) Oxygen-induced membrane depolarizations in legume root nodules (Possible evidence for an osmoelectrical mechanism controlling nodule gas permeability). Plant Physiol 108:235–240
Denison RF, Layzell DB (1991) Measurement of legume nodule respiration and photometry of leghemoglobin. Plant Physiol 96:137–143
Denison RF, Hunt S, Layzell DB (1992) Nitrogenase activity, nodule respiration, and O(2) permeability following detopping of Alfalfa and Birdsfoot trefoil. Plant Physiol 98:894–900
Drevon JJ, Gaudillère JP, Bernoud JP, Jardinet F, Evrard M (1991) Influence of photon flux density and fluctuation on the nitrogen fixing Glycine max (L Merr)-Bradyrhizobium japonicum symbiosis in a controlled environment. Agronomie 11:193–199
Dreyfus BM, Dommergues YR (1981) Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbiol Lett 10:313–317
Evans WR, Fleischman DE, Calvert HE, Pyati PV, Alter GM, Subba Rao NS (1990) Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium Strain BTAi 1. Appl Environ Microbiol 56:3445–3449
Fernandez-Lopez M, Goormachtig S, Gao M, D'Haeze W, Van Montagu M, Holsters M (1998) Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata. Proc Natl Acad Sci USA 95:12724–12728
Ferrell RT, Himmelblau DM (1967) Diffusion coefficients of nitrogen and oxygen in water. J Chem Eng Data 12:111–115
Fleurat-Lessard P, Michonneau P, Maeshima M, Drevon JJ, Serraj R (2005) The distribution of aquaporin subtypes (PIP1, PIP2 and gamma-TIP) is tissue dependent in soybean (Glycine max) root nodules. Ann Bot 96:457–460
Goormachtig S, Capoen W, James EK, Holsters M (2004a) Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proc Natl Acad Sci USA 101:6303–6308
Goormachtig S, Capoen W, Holsters M (2004b) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci 9:518–522
Geurts R, Bisseling T (2002) Rhizobium nod factor perception and signalling. Plant Cell 14:239–249
Guinel FC, Sloetjes LL (2000) Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16), a pleiotropic mutant that nodulates poorly and has pale green leaves. J Exp Bot 51:885–894
Holsters H, Capoen W, Den Herder J, Goormachtig S (2005) Signaling for nodulation in a water-tolerant legume. In: Wang Y-P, Lin M, Tian ZX, Elmerich C, Newton WE (eds) Biological nitrogen fixation, sustainable agriculture, and the environment. Proceedings of the 14th International Nitrogen Fixation Congress, Springer, The Netherlands, pp 161–164
Hunt S, King BJ, Canvin DT, Layzell DB (1987) Steady and nonsteady state gas exchange characteristics of soybean nodules in relation to the oxygen diffusion barrier. Plant Physiol 84:164–172
Hunt S, King BJ, Layzell DB (1989) Effects of gradual increases in O2 concentration on nodule activity in soybean. Plant Physiol 91:315–321
Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511
Ianetta PPM, De Lorenzo C, Iannetta PPM, James EK, Fernandez-Pascual M, Sprent JI, Lucas MM, Witty JF, De Felipe MR, Minchin FR (1993) Oxygen diffusion in lupin nodules I. Visualization of diffusion barrier operation. J Exp Bot 44:1461–1467
Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287
James EK, Sprent JI, Minchin FR, Brewin NJ (1991) Intercellular location of glycoprotein in soybean nodules: effect of altered rhizosphere oxygen concentration. Plant Cell Environ 14:467–476
James EK, Sprent JI, Sutherland JM, McInroy SG, Minchin FR (1992a) The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena. Ann Bot 69:173–180
James EK, Minchin FR, Sprent JI (1992b) The physiology and nitrogen-fixing capability of aquatically and terrestrially grown Neptunia plena: the importance of nodule oxygen supply. Ann Bot 69:181–187
James EK, Crawford RMM (1998) Effect of oxygen availability on nitrogen fixation by two Lotus species under flooded conditions. J Exp Bot 49:599–609
James EK, Minchin FR, Oxborough K, Cookson A, Baker NR, Witty JF, Crawford RMM, Sprent JI (1998) Photosynthetic oxygen evolution within Sesbania rostrata stem nodules. Plant J 13:29–38
James EK, Sprent JI (1999) Development of N2-fixing nodules on the wetland legume Lotus uliginosus exposed to conditions of flooding. New Phytol 142:219–231
James EK, Iannetta PPM, Deeks L, Sprent JI, Minchin FR (2000) Detopping causes production of intercellular space occlusions in both the cortex and infected region of soybean nodules. Plant Cell Environ 23:377–386
James EK, Loureiro MF, Pott A, Pott VIJ, Martins CM, Franco AA, Sprent JI (2001) Flooding-tolerant legume symbioses from the Brazilian Pantanal. New Phytol 150:723–738
Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495
King BJ, Hunt S, Weagle GE, Walsh KB, Pottier RH, Canvin DT, Layzell DB (1988) Regulation of O2 concentration in soybean nodules observed by in situ spectroscopic measurement of leghemoglobin oxygenation. Plant Physiol 87:296–299
King BJ, Layzell DB (1991) Effect of increases in oxygen concentration during the argon-induced decline in nitrogenase activity in root nodules of soybean. Plant Physiol 96:376–381
Koponen P, Nygren P, Domenach AM, Le Roux C, Saur E, Roggy JC (2003) Nodulation and dinitrogen fixation of legume trees in a tropical freshwater swamp forest in French Guiana. J Trop Ecol 19:655–666
Kuzma MM, Winter H, Storer P, Oresnik I, Atkins CA, Layzell DB (1999) The site of oxygen limitation in soybean nodules. Plant Physiol 119:399–408
Layzell DB (1998) Oxygen and the control of nodule metabolism and N2 fixation. In: Emerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer Academic, Dordrecht, The Netherlands, pp 435–440
Layzell DB, Hunt S, Palmer GR (1990) Mechanism of nitrogenase inhibition in soybean nodules: Pulse-modulated spectroscopy indicates that nitrogenase activity Is limited by O2. Plant Physiol 92:1101–1107
Lievens S, Goormachtig S, Den Herder J, Capoen W, Mathis R, Hedden P, Holsters M (2005) Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol 139:1366–1379
Linkemer G, Board JE, Musgrave ME (1998) Waterlogging effects on growth and yield components in late-planted soybean. Crop Sci 38:1576–1584
Loureiro MF, de Faria SM, James EK, Pott A, Franco AA (1994) Nitrogen-fixing stem nodules of the legume Discolobium pulchellum Benth. New Phytologist 128:283–295
Loureiro MF, James EK, Sprent JI, Franco AA (1995) Stem and root nodules on the tropical wetland legume Aeshynomene fluminensis. New Phytol 130:531–544
Loureiro MF, James EK, Franco AA (1998) Nitrogen fixation by legumes in flooded regions. In: Scarano FR, Franco AC (eds) Oecologia Brasiliensis, vol IV. PPGE-UFRJ, Rio de Janeiro, Brazil, pp 195–233
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Minchin FR, Pate JS (1975) Effects of water, aeration, and salt regime on nitrogen fixation in a nodulated legume. Definition of an optimum root environment. J Exp Bot 26:60–69
Minchin FR, Summerfield RJ (1976) Symbiotic nitrogen fixation and vegetative growth of cowpea (Vigna unguiculata (L.) walp.) in waterlogged conditions. Plant Soil 45:113–127
Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29:881–888
Minchin FR, James EK, Becana M (2008) Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, The Netherlands, pp 321–362
Ndoye I, de Billy F, Vasse J, Dreyfus B, Truchet G (1994) Root nodulation of Sesbania rostrata. J Bacteriol 176:1060–1068
Ober ES, Sharp RE (1996) A microsensor for direct measurement of O2 partial pressure within plant tissues. J Exp Bot 44:447–454
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Pankhurst CE, Sprent JI (1975a) Effects of water stress on the respiratory and nitrogen-fixing activity of soybean root nodules. J Exp Bot 26:287–304
Pankhurst CE, Sprent JI (1975b) Surface features of soybean root nodules. Protoplasma 85:85–98
Parsons R, Day DA (1990) Mechanism of soybean nodule adaptation to different oxygen pressures. Plant Cell Environ 13:501–512
Patriarca E, Tate R, Ferraioli S, Iaccarrino M (2004) Organogenesis of legume root nodules. Int Rev Cytol 234:201–263
Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275:527–530
Perata P, Voesenek LA (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci 12:43–46
Purcell LC, Sinclair TR (1994) An osmotic hypothesis for the regulation of oxygen permeability in soybean nodules. Plant Cell Environ 17:837–843
Pugh R, Witty JF, Mytton LR, Minchin FR (1995) The effect of waterlogging on nitrogen fixation and nodule morphology in soil-grown white clover (Trifolium repens L.). J Exp Bot 46:285–290
Ralston EJ, Imsande J (1982) Entry of oxygen and nitrogen into intact soybean nodules. J Exp Bot 33:208–214
Saur E, Carcelle S, Guezennec S, Rousteau A (2000) Nodulation of legume species in wetlands of Guadeloupe (Lesser Antilles). Wetlands 20:730–734
Scott HD, DeAngulo J, Daniels MB, Wood LS (1989) Flood duration effects on soybean growth and yield. Agron J 81:631–636
Schaede R (1940) Die Knöllchen der adventiven Wasserwurzeln Von Neptunia oleracea und ihre Bakteriensymbiose. Planta 31:1–21
Schroeyers K, Chaparro C, Goormachtig S, Holsters M (2004) Nodulation-enhanced sequences from the water stress-tolerant tropical legume Sesbania rostrata. Plant Sci 167:207–216
Serraj R, Fleurat-Lessard P, Jaillard B, Drevon JJ (1995) Structural changes in the inner-cortex cells of soybean root-nodules are induced by short-term exposure to high salt or oxygen concentrations. Plant Cell Environ 18:455–462
Serraj R, Frangne N, Maeshima M, Fleurat-Lessard P, Drevon JJ (1998) γ-TIP cross-reacting protein is abundant in the cortex of soybean N2-fixing nodules. Planta 206:681–684
Sheehy JE, Minchin FR, Witty JF (1983) Biological control of the resistance to oxygen flux in nodules. Ann Bot 60:345–351
Shimamura S, Mochizuki T, Nada Y, Fukuyama M (2003) Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean (Glycine max) under flooded conditions. Plant Soil 251:351–359
Sprent JI (1999) Nitrogen fixation and growth of non-crop legume species in diverse environments. Perspect Plant Ecol Evol Syst 2:149–162
Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581
Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Sci 9:110–121
Subba-Rao NS, Mateos PF, Baker D, Pankratz HS, Palma J, Dazzo FB, Sprent JI (1995) The unique root-nodule symbiosis between Rhizobium and the aquatic legume, Neptunia natans (L. f.) Druce. Planta 196:311–320
Sung L, Moloney AH, Hunt S, Layzell DB (1991) The effect of excision on O2 diffusion and metabolism in soybean nodules. Physiol Plant 83:67–74
Sung FJM (1993) Waterlogging effect on nodule nitrogenase and leaf nitrate reductase activities in soybean. Field Crops Res 35:183–189
Thomas AL, Guerreiro SMC, Sodek L (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Ann Bot 96:1191–1198
Tjepkema JD, Yocum CS (1974) Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrodes. Planta 119:351–360
Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10:222–228
van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529–1543
VandenBosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J 8:335–342
Vessey JK, Walsh KB, Layzell DB (1988) Oxygen limitation of N2 fixation in stem-girdled and nitrate-treated soybean. Physiol Plant 73:113–121
Walker BA, Pate JS, Kuo J (1983) Nitrogen fixation by nodulated roots of Viminaria juncea (Schrad. & Wendl.) Hoffmans, (Fabaceae) when submerged in water. Aust J Plant Physiol 10:409–421
Walter CA, Bien A (1989) Aerial root nodules in the tropical legume, Pentaclethra macroloba. Oceologia 80:27–31
Wei H, Layzell DB (2006) Adenylate-coupled ion movement. A mechanism for the control of nodule permeability to O2 diffusion. Plant Physiol 141:280–287
Weisz PR, Sinclair TR (1987a) Regulation of soybean nitrogen fixation in response to rhizosphere oxygen: I. Role of nodule respiration. Plant Physiol 84:900–906
Weisz PR, Sinclair TR (1987b) Regulation of soybean nitrogen fixation in response to rhizosphere oxygen: II. Quantification of nodule gas permeability. Plant Physiol 84:906–910
Witty JF, Minchin FR, Skøt L, Sheehy JE (1986) Nitrogen fixation and oxygen in legume root nodules. Oxford Surv Plant Mol Cell Biol 3:275–314
Witty JF, Skøt L, Revsbech NP (1987) Direct evidence for changes in the resistance of legume root nodules to O2 resistance. J. Exp Bot 38:1129–1140
Wycoff KL, Hunt S, Gonzales MB, VandenBosch KA, Layzell DB, Hirsch AM (1998) Effects of oxygen on nodule physiology and expression of nodulins in alfalfa. Plant Physiol 117:385–395
Young ND, Udvardi M (2009) Translating Medicago truncatula genomics to crop legumes. Curr Opin Plant Biol 12:193–201
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Supported by National Science Foundation grant MCB-0618075 to DMR.
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Roberts, D.M., Choi, W.G., Hwang, J.H. (2010). Strategies for Adaptation to Waterlogging and Hypoxia in Nitrogen Fixing Nodules of Legumes. In: Mancuso, S., Shabala, S. (eds) Waterlogging Signalling and Tolerance in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10305-6_3
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