Abstract
Flowering Sesbania sericea (Willd.) Link sampled from seasonally-flooded soils in the field displayed a 3-fold greater aerial biomass and root nodulation than individuals grown in nearby dry soils. Flooded plants (FP) showed high N2-fixation rates as apparent from their active leaf ureide catabolism and the high ureide content in nodules surrounded by an aerenchymatous phellem. Field-grown FP also exhibited high leaf Mn, P and chlorophyll but low carotenoid contents, suggesting non-stressful mineral nutrition and photosynthetic conditions. However, sufficient P in growing FP was not ascribed to an effective arbuscular mycorrhiza (AM) symbiosis. This was indicated by the age-related progressive decrease of root AM fungal colonization, and by the absence of AM arbuscules from the juvenile stages of growth. Aeration of flooded soils under greenhouse controlled conditions hindered growth, nodulation, leaf P content, and N2-fixation in rhizobia (Rh) and AM co-inoculated (Rh + AM) FP ruling out anoxia as the key factor underlying the inefficiency of the AM symbiosis in FP. Negative effects of aeration on FP were not counteracted by the addition of 2 mM KNO3 that inhibited nodulation, nor by the presence of the aerenchymatous phellem in the aerated roots. On the other hand, addition of 2 mM P enhanced the aerial mass of aerated and non-aerated FP, while inhibiting the colonization of root by AM. Analyses of rhizospheric fluorescein diacetate hydrolysis, urease, alkaline phosphatase and dehydrogenase enzymatic activities did not reveal marked differences in the soil microbial status between aerated and non-aerated FP, neither Rh + AM inoculated nor when fertilized by N and P. Overall results suggest a key role of AM only in seedling and juveniles providing sufficient P for the onset of N2-fixation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- FP:
-
Flooded plants
- Rh + AM:
-
Rhizobia and arbuscular mycorrhiza fungal co-inoculation
- +P and + N:
-
Supplied with P and N
- -P:
-
Non P supplied
References
Aziz MA, Hazra F, Salma S, Nursyamsi D (2019) Soil enzyme activities and their relationship to total soil bacteria, soil microbial biomass and soil chemical characteristics of organic and conventional farming. J Trop Soils 23:133–141. https://doi.org/10.5400/jts.2018.v23i3.133-141
Baral B, da Silva JAT, Izaguirre-Mayoral ML (2016) Early signaling, synthesis, transport and metabolism of ureides. J Plant Physiol 193:97–109. https://doi.org/10.1016/j.jplph.2016.01.013
Bashar KK, Tareq MZ, Islam MDS (2020) Unlocking the mystery of plants’ survival capability under flooding stress. Plant Sci Today 7:142–153. https://doi.org/10.14719/pst.2020.7.2.663
Brunner MI, Sikorska AE, Seibert J (2018) Bivariate analysis of floods in climate impact assessments. Sci Total Environ 616:1392–1403. https://doi.org/10.1016/j.scitotenv.2017.10.176
Bunma S, Balslev H (2019) A review of the economic botany of Sesbania (Leguminosae). Bot Rev 85:185–251. https://doi.org/10.1007/s12229-019-09205-y
Cornwell WK, Bedford BL, Chapin CT (2001) Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am J Bot 88:1824–1829. https://doi.org/10.2307/3558359
Cummings SP, Gyaneshwar P, Vinuesa P, Farruggia FT, Andrews M, Humphry D, Elliott GN, Nelson A, Orr C, Pettitt D, Shah GR, Santos SR, Krishnan HB, Odee D, Moreira FMS, Sprent JI, Young JPW, James EK (2009) Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environ Microbiol 11:2510–2525. https://doi.org/10.1111/j.1462-2920.2009.01975.x
Della Mónica IF, Godeas AM, Scervino JM (2020) In vivo modulation of arbuscular mycorrhizal symbiosis and soil quality by fungal P solubilizers. Microb Ecol 79:21–29. https://doi.org/10.1007/s00248-019-01396-6
Dharmakeerthi RS, Kumaragamage D, Goltz D, Indraratne SP (2019) Phosphorus release from unamended and gypsum-or biochar-amended soils under simulated snowmelt and summer flooding conditions. J Environ Qual 48:822–830. https://doi.org/10.2134/jeq2019.02.0091
Dotaniya ML, Aparna K, Dotaniya CK, Singh M, Regar KL (2019) Role of soil enzymes in sustainable crop production. In: Kuddus M (ed) Enzymes in food biotechnology. Academic Press, pp 569–589. https://doi.org/10.1016/B978-0-12-813280-7.00023-2
Engler RM, Patrick WH (1974) Nitrate removal from floodwater overlying flooded soils and sediments. J Environ Qual 3:409–413. https://doi.org/10.2134/jeq1974.00472425000300040025x
Farruggia FT, Lavin M, Wojciechowski MF (2018) Phylogenetic systematics and biogeography of the pantropical genus Sesbania (Leguminosae). Syst Bot 43:414–429. https://doi.org/10.1600/036364418X697175
Fougnies L, Renciot S, Muller F, Plenchette C, Prin Y, De Faria SM, Bouvet JM, Sylla SN, Dreyfus B, Bâ AM (2007) Arbuscular mycorrhizal colonization and nodulation improve flooding tolerance in Pterocarpus officinalis Jacq. Seedlings. Mycorrhiza 17:159–166. https://doi.org/10.1007/s00572-006-0085-2
Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and flooding stress in plants: a review highlighting research opportunities and understudied aspects. Front Plant Sci 10:340. https://doi.org/10.3389/FPls.2019.00340
Fusconi A, Mucciarelli M (2018) How important is arbuscular mycorrhizal colonization in wetland and aquatic habitats? Environ Exp Bot 155:128–141. https://doi.org/10.1016/j.envexpbot.2018.06.016
Goormachtig S, Capoen W, Holsters M (2004) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci 9:518–522. https://doi.org/10.1016/j.tplants.2004.09.005
Gschwend F, Aregger K, Gramlich A, Walter T, Widmer F (2020) Periodic flooding consistently shapes agricultural soil microbiomes by promoting specific taxa. App Soil Ecol 155:103623. https://doi.org/10.1016/j.apsoil.2020.103623
Gu C, Zhang S, Han P, Hu X, Xie L, Li Y, Brooks M, Liao X, Qin L (2019) Soil enzyme activity in soils subjected to flooding and the effect on nitrogen and phosphorus uptake by oilseed rape. Front Plant Sci 10:368. https://doi.org/10.3389/FPls.2019.00368
Hattori R, Matsumura A, Yamawaki K, Tarui A, Daimon H (2013) Effects of flooding on arbuscular mycorrhizal colonization and root-nodule formation in different roots of soybeans. Agric Sci 4:673–677 http://www.scirp.org/journal/PaperInformation.aspx?PaperID=40845
Havaux M (2014) Carotenoid oxidation products as stress signals in plants. Plant J 79:597–606. https://doi.org/10.1111/tpj.12386
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:332–1334. https://doi.org/10.1139/b79-163
Hu S, Chen Z, Vosátka M, Vymazal J (2020) Arbuscular mycorrhizal fungi colonization and physiological functions toward wetland plants under different water regimes. Sci Total Environ 716:137040. https://doi.org/10.1016/j.scitotenv.2020.137040
Izaguirre-Mayoral ML (2005) Distribución geográfica, nodulación y comportamiento agronómico de tres especies de Sesbania nativas de zonas inundables en Venezuela. Agronomia Trop 55:63–81
Izaguirre-Mayoral ML, Carballo O, Flores S, De Mallorca M, Oropeza T (1992) Quantitative analysis of the symbiotic N2-fixation, non-structural carbohydrates and chlorophyll content in sixteen native legume species collected in different savanna sites. Symbiosis 12:293–312
Izaguirre-Mayoral ML, Flores S, Pieters A, Olivares E, Cuenca G (2011) Rhizophagus manihotis promotes the growth of rhizobia-nodulated Vigna luteola L in phosphorus deficient acid montane soils devoid of ground cover vegetation. Symbiosis 5:1–9. https://doi.org/10.1007/s13199-011-0145-z
Izaguirre-Mayoral ML, Vivas AI (1996) Symbiotic N2-fixation in tropical legume species growing at high geographic elevation. Symbiosis 21:49–60
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. https://doi.org/10.1093/jxb/49.320.599
James EK, Loureiro MDF, Pott A, Pott VJ, Martins CM, Franco AA, Sprent JI (2001) Flooding-tolerant legume symbioses from the Brazilian Pantanal. New Phytol 150:723–738 www.jstor.org/stable/1353676
Krishnan HB, Oehrle NW, Alaswad AA, Stevens WG, Maria John KM, Luthria DL, Natarajan SS (2019) Biochemical and anatomical investigation of Sesbania herbacea (mill.) McVaugh nodules grown under flooded and non-flooded conditions. Int J Mol Sci 20:1824. https://doi.org/10.3390/ijms20081824
Marins JFD, Carrenho R (2017) Arbuscular mycorrhizal fungi and dark septate fungi in plants associated with aquatic environments. Acta Bot Bras 31:295–308. https://doi.org/10.1590/0102-33062016abb0296
Mendoza R, Escudero V, García I (2005) Plant growth, nutrient acquisition and mycorrhizal symbioses of a flooding tolerant legume (Lotus glaber mill.) in a saline-sodic soil. Plant Soil 275:305–315. https://doi.org/10.1007/s11104-005-2501-3
Naher UA, Choudhury AT, Biswas JC, Panhwar QA, Kennedy IR (2020) Prospects of using leguminous green manuring crop Sesbania rostrata for supplementing fertilizer nitrogen in rice production and control of environmental pollution. J Plant Nutr 43:285–296. https://doi.org/10.1080/01904167.2019.1672734
Ndoye I, de Billy F, Vasse J, Dreyfus B, Truchet G (1994) Root nodulation of Sesbania rostrata. J Bacteriol 176(4):1060–1068
Pedersen O, Sauter M, Colmer TD, Nakazono M (2020) Regulation of root adaptive anatomical and morphological traits during low soil oxygen. New Phytol 229:42–49. https://doi.org/10.1111/nph.16375
Peng YQ, Zhu J, Li WJ, Gao W, Shen RY, Meng LJ (2020) Effects of grafting on root growth, anaerobic respiration enzyme activity and aerenchyma of bitter melon under flooding stress. Sci Hortic 261:108977. https://doi.org/10.1016/j.scienta.2019.108977
Pucciariello C, Boscari A, Tagliani A, Brouquisse R, Perata P (2019) Exploring legume-rhizobia symbiotic models for flooding tolerance. Front Plant Sci 10:578. https://doi.org/10.3389/FPls.2019.00578
Rautaray SK, Pradhan S, Mohanty S, Dubey R, Raychaudhuri S, Mohanty RK, Mishra A, Ambast SK (2020) Energy efficiency, productivity and profitability of rice farming using Sesbania as green manure-cum-cover crop. Nutr Cycl Agroecosyst 116:83–101. https://doi.org/10.1007/s10705-019-10034-z
Rojas YDCP, Arias RM, Ortiz RM, Aguilar DT, Heredia G, Yon YR (2019) Effects of native arbuscular mycorrhizal and phosphate-solubilizing fungi on coffee plants. Agrofor Syst 93:961–972. https://doi.org/10.1007/s10457-018-0190-1
Sánchez-Rodríguez AR, Hill PW, Chadwick DR, Jones DL (2019) Typology of extreme flood event leads to differential impacts on soil functioning. Soil Biol Biochem 129:153–168. https://doi.org/10.1016/j.soilbio.2018.11.019
Schulze ED, Beck E, Buchmann N, Clemens S, Müller-Hohenstein K, Scherer-Lorenzen M (2019) Oxygen deficiency. In: Plant Ecology. Springer, Berlin. https://doi.org/10.1007/978-3-662-56233-8_5
Schwember AR, Schulze J, del Pozo A, Cabeza RA (2019) Regulation of symbiotic nitrogen fixation in legume root nodules. Plants 8:333. https://doi.org/10.3390/plants8090333
Shiba H, Daimon H (2003) Histological observation of secondary aerenchyma formed immediately after flooding in Sesbania cannabina and S. rostrata. Plant Soil 255:209–215. https://doi.org/10.1023/A:1026147301146
Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. J Exp Bot 68:1851–1872. https://doi.org/10.1093/jxb/erw239
Teng Z, Chen Z, Zhang Q, Yao Y, Song M, Li M (2019) Isolation and characterization of phosphate solubilizing bacteria from rhizosphere soils of the Yeyahu wetland in Beijing, China. Environ Sci Pollut Res 26:33976–33987. https://doi.org/10.1007/s11356-018-2955-5
Torres Rodríguez NA (2017) Cambios en las comunidades de hongos micorrízicos arbusculares asociados a la invasión por Pteridium arachnoideum y sus efectos sobre la repoblación de un árbol nativo micotrófico (Oyedaea verbesinoides) en un bosque nublado. Master Tesis. Instituto Venezolano de Investigaciones Científicas, Caracas
Tuheteru FD, Wu QS (2017) Arbuscular mycorrhizal fungi and tolerance of flooding stress in plants. In: Wu QS (ed) Arbuscular Mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 46–66. https://doi.org/10.1007/978-981-10-4115-0_3
Unger IM, Kennedy AC, Muzika RM (2009) Flooding effects on soil microbial communities. Appl Soil Ecol 42:1–8. https://doi.org/10.1016/j.apsoil.2009.01.007
Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martínez-Romero E (2005) Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst App Microbiol 8:702–716. https://doi.org/10.1016/j.syapm.2005.05.007
Vogels GD, Van der Drift C (1970) Differential analyses of glyoxylate derivatives. Anal Biochem 33:143–157
Wang L, Luo X, Xiong X, Chen W, Hao X, Huang Q (2019) Soil aggregate stratification of ureolytic microbiota affects urease activity in an Inceptisol. J Agricul Food Chem 67:11584–11590. https://doi.org/10.1021/acs.jafc.9b04244
Waring EF, Maricle BR (2013) Stomatal conductance correlates with flooding tolerance in Phragmites australis and Sorghum halepense. Trans Kans Acad Sci 115:161–166. https://doi.org/10.1660/062.115.0310
Zhang M, Huang JC, Sun S, Rehman MMU, He S, Zhou W (2021) Dissimilatory nitrate reduction processes and corresponding nitrogen loss in tidal flow constructed wetlands. J Clean Product 295:126429. https://doi.org/10.1016/j.jclepro.2021.126429
Zhao Z, Ge T, Gunina A, Li Y, Zhu Z, Peng P, Wu J, Kuzyakov Y (2019) Carbon and nitrogen availability in paddy soil affects rice photosynthate allocation, microbial community composition, and priming: combining continuous 13C labeling with PLFA analysis. Plant Soil 445:137–152. https://doi.org/10.1007/s11104-018-3873-5
Acknowledgments
Authors thank Dr. Gisela Cuenca and Lic. Milagros Lovera for their assistances with the mycorrhizal analyses. We also thank Dr. L.H. Allen Jr. (USA) and Prof. José Alió (Ecuador) for their editorial comments on the manuscript. Data is part of the PhD thesis of Carlos Pelaez carried out under the supervision of M.L. Izaguirre-Mayoral.
Funding
Experiments were funded by the laboratory grant given by Instituto Venezolano de Investigaciones Cientìficas.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest/competing interests
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pelaez, C., Izaguirre-Mayoral, M.L. Outstanding adaptation of N2-fixing Sesbania sericea to flooded soils is not mediated by symbiosis with arbuscular mycorrhizal fungi. Symbiosis 84, 49–60 (2021). https://doi.org/10.1007/s13199-021-00769-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-021-00769-1