Abstract
Aims
The interaction between nitrogen (N) availability in the soil, rhizobia nodule formation and leaf physiological traits of Robinia pseudoacacia L. was explored at initial nodule development.
Methods
We selected two Robinia provenances, one from Northwest (GS) and one from Northeast China (DB), and cultivated seedlings in the greenhouse with and without rhizobia inoculation at normal and high N supply in the soil. After ca. 2.5 months growth, nodule formation, plant biomass, CO2 and H2O gas exchange of the leaves, and foliar N contents and partitioning were analyzed.
Results
Rhizobia inoculation strongly promoted the formation of root nodules independent of N availability in the soil, but this effect was more pronounced in the DB than for GS provenance. It reduced biomass accumulation of the GS provenance, but not for DB provenance at both, normal and high soil N availability. High N supply did not affect biomass accumulation independent of rhizobia inoculation. Leaf photosynthesis of both Robinia origins was enhanced by high N supply, but this effect was counteracted by rhizobia inoculation only in leaves of DB plants. In GS but not in DB plants, high N supply reduced not only nodule formation, but also stomatal conductance, but still enhanced transpiration without modifying the foliar water content. In addition, high N supply plus inoculation enhanced the organic N content in GS plants rather than DB plants.
Conclusion
These results indicate that excess N availability in the soil interacts with the performance of Robinia provenances, as previously reported for drought and phosphorus (P) depletion.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Allito BB, Ewusi-Mensah N, Logah V et al (2021) Legume-rhizobium specificity effect on nodulation, biomass production and partitioning of faba bean (Vicia faba L.). Sci Rep 11:3678. https://doi.org/10.1038/s41598-021-83235-8
Azuchi F, Kinose Y, Matsumura T, Kanomata T, Uehara Y, Kobayashi A, Yamaguchi M, Izuta T (2014) Modeling stomatal conductance and ozone uptake of Fagus crenata grown under different nitrogen loads. Environ Pollut 184:481–487
Bai Y, Wu J, Clark CM et al (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Glob Chang Biol 16:358–372
Bailey-Serres J, Parker JE, Ainsworth EA et al (2019) Genetic strategies for improving crop yields. Nature 575:109–118
Batterman SA, Hedin LO, Michiel VB, Ransijn J, Craven DJ, Hall JS (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227
Batzli J, Graves WR, Van Berkum P (1992) Diversity among rhizobia effective with Robinia pseudoacacia L. Appl Environ Microbiol 58:2137–2143
Bi Y, Zou H, Zhu C (2014) Dynamic monitoring of soil bulk density and infiltration rate during coal mining in sandy land with different vegetation. Int J Coal Sci Technol 1:198–206
Bissonnette C, Fahlman B, Peru KM, Khasa DP, Greer CW, Headley JV, Roy S (2014) Symbiosis with Frankia sp. benefits the establishment of Alnus viridis ssp. crispa and Alnus incana ssp. rugosa in tailings sand from the Canadian oil sands industry. Ecol Eng 68:167–175
Bote AD, Zana Z, Ocho FL, Vos J (2018) Analysis of coffee (Coffea arabica L.) performance in relation to radiation level and rate of nitrogen supply II. Uptake and distribution of nitrogen, leaf photosynthesis and first bean yields. Eur J Agron 92:107–114
Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080
Cao Y, Chen Y (2017) Coupling of plant and soil C:N:P stoichiometry in black locust (Robinia pseudoacacia) plantations on the Loess Plateau, China. Trees 31:1559–1570
Cechin I, Fumis TD (2004) Effect of nitrogen supply on growth and photosynthesis of sunflower plants grown in the greenhouse. Plant Sci 166:1379–1385
Craine J (2009) Resource strategies of wild plants. Princeton University Press, Princeton, NJ
Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868
Cuervo-Alarcon L, Arend M, Muller M, Sperisen C, Finkeldey R, Krutovsky KV (2018) Genetic variation and signatures of natural selection in populations of European beech (Fagus sylvatica L.) along precipitation gradients. Tree Genet Genom 14:84. https://doi.org/10.1007/s11295-018-1297-2
Dang YA, Li SQ, Wang GD, Shao MA (2007) Distribution characteristics of soil total nitrogen and soil microbial biomass nitrogen for the typical types of soils on the Loess Plateau. Plant Nutr Fertil Sci 13:1020–1027
Du B, Pang J, Hu B, Allen DE, Bell TL, Pfautsch S, Netzer F, Dannenmann M, Zhang S, Rennenberg H (2019) N2-fixing black locust intercropping improves ecosystem nutrition at the vulnerable semi-arid Loess Plateau region, China. Sci Total Environ 688:333–345
Duan X, Xie Y, Liu G, Gao X, Lu H (2010) Field capacity in black soil region, Northeast China. Chin Geogr Sci 20:406–413
Fang YJ, Xiong LZ (2014) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689
Ferguson BJ, Mens C, Hastwell AH et al (2018) Legume nodulation: the host controls the party. Plant Cell Environ 42:1–11
Finér L, Helmisaari H-S, Lõhmus K, Majdi H, Brunner I, Børja I et al (2007) Variation in fine root biomass of three European tree species: beech (Fagus sylvatica L.), Norway spruce (Picea abies L. Karst.), and Scots pine (Pinus sylvestris L.). Plant Biosyst 141:394–405
Flemetakis E, Efrose RC, Ott T, Stedel C, Aivalakis G, Udvardi MK, Katinakis P (2006) Spatial and temporal organization of sucrose metabolism in Lotus japonicus nitrogen-fixing nodules suggests a role for the elusive alkaline/neutral invertase. Plant Mol Biol 62:53–69
Fowells HA (1965) Silvics of the forest trees of the United States. Agriculture Handbook No. 271. Washington DC, USA: USDA, Forest Service
Franzini VI, Azcón R, Méndes FL, Aroca R (2013) Different interaction among Glomus and Rhizobium species on phaseolus vulgaris and z ea mays plant growth, physiology and symbiotic development under moderate drought stress conditions. Plant Growth Regul 70:265–273
Galloway JN, Townsend AR, Erisman GW et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Gandour M, Khouja ML, Toumi L et al (2007) Morphological evaluation of cork oak (Quercus suber), Mediterranean provenance variability in Tunisia. Ann For Sci 64:549–555
Gao S, Cai Z, Yang C, Luo J, Zhang S (2021) Provenance-specific ecophysiological responses to drought in Cunninghamia lanceolata. J Plant Ecol 14:1060–1072
Ge T (2020) The Research on Soil Repair Effect Under Different Vegetation Types in Fushun West Open-pit. Diploma thesis
Gicharu G, Gitonga N, Boga H, Cheruiyot R, Maingi J (2013) Effect of inoculating selected climbing bean cultivars with different rhizobia strains on nitrogen fixation. Int J Microbiol Res 1:25–31
Göttlein A (2015) Ranges of threshold values for the nutritional assessment of the main tree species spruce, pine, oak and beech. Allgemeine Forst- und Jagdzeitung 186:110–116
Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M, Marmagne A, Lothier J, Masclaux-Daubresse C (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol 199:683–694
Guo Y, Yu N, Jianguo H (2010) Effects of rhizobium, arbuscular mycorrhiza and lime on nodulation, growth and nutrient uptake of lucerne in acid purplish soil in China. Trop Grasslands 44:109–114
Heju H (2005) Spring nursery soil disinfection. Northern Horticulture 45:21–34
Hertel D, Strecker T, Müller-Haubold H, Leuschner C (2013) Fine root biomass and dynamics in beech forests across a precipitation gradient - is optimal resource partitioning theory applicable to water-limited mature trees? J Ecol 101:1183–1200
Hu B, Simon J, Kuster TM, Arend M, Siegwolf R, Rennenberg H (2013) Nitrogen partitioning in oak leaves depends on species, provenance, climate conditions and soil type. Plant Biol 15:198–209
Hu B, Zhou M, Dannenmann M, Saiz G, Simon J, Bilela S, Liu XG, Hou L, Chen H, Zhang D, Butterbach-Bahl K, Rennenberg H (2017) Comparison of nitrogen nutrition and soil carbon status of afforested stands established in degraded soil of the Loess Plateau, China. For Ecol Manag 389:46–58
Jin X, Shi C, Yu CY, Yamada T, Sacks EJ (2017) Determination of leaf water content by visible and near-infrared spectrometry and multivariate calibration in miscanthus. Front Plant Sci 8:721. https://doi.org/10.3389/fpls.2017.00721
Jung-Tai L, Sung-Ming T (2018) The nitrogen-fixing Frankia significantly increases growth, uprooting resistance and root tensile strength of Alnus formosana. Afr J Biotechnol 17:213–225
Kalloniati C, Krompas P, Karalias G, Udvardi MK, Rennenberg H, Herschbach C, Flemetakis E (2015) Nitrogen-fixing nodules are an important source of reduced sulfur, which triggers global changes in sulfur metabolism in lotus japonicus. Plant Cell 27:2384–2400
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 54:707–714
Kohl DH, Reynolds SPH, Shearer G (1989) Distibution of 15N within pea, lupin and soybean nodules. Plant Physiol 90:420–426
Kong X, Cao J, Tang R, Zhang S, Dong F (2014) Pollution of intensively managed greenhouse soils by nutrients and heavy metals in the Yellow River irrigation region, Northwest China. Environ Monit Assess 186:7719–7731
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Koppen-Geiger climate classification updated. Meteorol Z 15:259–263
Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R et al (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15:378–392
Kruse J, Turnbull T, Rennenberg H, Adams MA (2020) Plasticity of leaf respiratory and photosynthetic traits in eucalyptus grandis and e. regnans grown under variable light and nitrogen availability. Frontiers in Forests and Global Change 3. https://doi.org/10.3389/ffgc.2020.00005
Laliberté E, Turner B, Costes T et al (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the South-Western Australia biodiversity hotspot. J Ecol 100:631–642
Lambers H, Atkin OK, Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkaki U (eds) Plant roots: the hidden half. Marcel Dekker, Inc., New York, NY, pp 521–552
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Li J, Zhang S, Shi S, Du J, Huo P (2020) Effect of phosphate solubilizing rhizobium strains on alfalfa seedlings growth under nitrogen free and phosphorus deficient conditions. J Biobased Mater Bioenergy 14:133–137
Lin Y, Feng Z, Wu W, Yang Y, Zhou Y, Xu C (2017) Potential impacts of climate change and adaptation on maize in Northeast China. Agron J 109:1476–1490
Liu X, Fan Y, Long J, Wei R, Kjelgren R, Gong C, Zhao J (2013) Effects of soil water and nitrogen availability on photosynthesis and water use efficiency of Robinia pseudoacacia seedlings. J Environ Sci 25:585–595. https://doi.org/10.1016/s1001-0742(12)60081-3
Liu Z, Chen W, Jiao S, Wang X, Fan M, Wang E, Wei G (2019) New insight into the evolution of symbiotic genes in black locust-associated rhizobia. Genome Biol Evol 11:1736–1750
Liu Z, Hu B, Bell TL, Flemetakis E, Rennenberg H (2020) Significance of mycorrhizal associations for the performance of N2-fixing black locust (Robinia pseudoacacia L.). Soil Biol Biochem 145:107776
Lorite MJ, Estrella MJ, Escaray FJ, Sannazzaro A, de Castro IMV, Monza J, Sanjuan J, Leon-Barrios M (2018) The rhizobia-lotus symbioses: deeply specific and widely diverse. Front Microbiol 9:2055
Luo J, Zhou J, Li H, Shi W, Polle A, Lu M, Sun X, Luo Z (2015a) Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess. Tree Physiol 35:1283–1302
Luo J, Zhou J, Li H, Shi W, Polle A, Lu M, Sun X, Luo Z (2015b) Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess. Tree Physiol 35:1283–1302
Luo C, Zhang B, Liu J, Wang X, Han F, Zhou J (2020) Effects of different ages of Robinia pseudoacacia plantations on soil physiochemical properties and microbial communities. Sustainability 12:9161–9179
Mantovani D, Veste M, Boldt-Burisch K, Fritsch S, Koning LA, Freese D (2015) Carbon allocation, nodulation, and biological nitrogen fixation of black locust (Robinia pseudoacacia L.) under soil water limitation. Ann For Res 58:259–274
Mariangela NF, Daniela T, Anna K, Georgios A, Panagiotis K, Michael KU, Rennenberg H, Emmanouil F (2011) Nodulation enhances dark CO2 fixation and recycling in the model legume Lotus japonicus. J Exp Bot 62:2959–2971
Matamaoros MA, Moran JF, Iturbe-ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol (Bethesda) 121:879–888
McKenzie R, Middleton A, Solberg E, DeMulder J, Flore N, Clayton G, Bremer E (2001) Response of pea to rhizobia inoculation and starter nitrogen in Alberta. Can J Plant Sci 81:637–643. https://doi.org/10.4141/P01-006
Meller S, Frossard E, Spohn M, Luster J (2020) Plant nutritional status explains the modifying effect of provenance on the response of beech sapling root traits to differences in soil nutrient supply. Front For Glob Change 3:535117. https://doi.org/10.3389/ffgc.2020.535117
Mellert KH, Göttlein A (2012) Comparison of new foliar nutrient thresholds derived from van den Burg’s literature compilation with established central European references. Eur J For Res 131:1461–1472
Mierzwa B, Wdowiak-Wrobel S, Kalita M, Gnat S, Malek W (2010) Insight into the evolutionary history of symbiotic genes of Robinia pseudoacacia rhizobia deriving from Poland and Japan. Arch Microbiol 192:341–350
Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095
Miller AJ, Fan XR, Orsel M et al (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306
Minotta G, Pinzauti S (1996) Effects of light and soil fertility on growth, leaf chlorophyll content and nutrient use efficiency of beech (Fagus sylvatica L.) seedlings. For Ecol Manag 86:61–71
Moshki A, Lamersdorf NP (2011) Symbiotic nitrogen fixation in black locust (Robinia pseudoacacia L.) seedlings from four seed sources. J For Res (Harbin) 22:689–692
Mothapo NV, Grossman JM, Sooksa-nguan T, Maul J, Bräuer SL, Shi W (2013) Cropping history affects nodulation and symbiotic efficiency of distinct hairy vetch (Vicia villosa Roth.) genotypes with resident soil rhizobia. Biol Fertil Soils 49(7):871–879. https://doi.org/10.1007/s00374-013-0781-y
Ni J, Su S, Li H, Geng Y, Zhou H, Feng Y, Xu X (2020a) Distinct physiological and transcriptional responses of leaves of paper mulberry (Broussonetia kazinoki x B. papyrifera) under different nitrogen supply levels. Tree Physiol 40:667–682
Ni J, Su S, Li H, Geng Y, Zhou H, Feng Y, Xu X (2020b) Distinct physiological and transcriptional responses of leaves of paper mulberry (Broussonetia kazinoki × B. papyrifera) under different nitrogen supply levels. Tree Physiol 40:667–682
Oberson A, Frossard E, Bühlmann C, Mayer J, Mäder P, Lüscher A (2013) Nitrogen fixation and transfer in grass-clover leys under organic and conventional cropping systems. Plant Soil 371:237–255
Ohyama T, Kumazawa K (1980) Nitrogen assimilation in soybena nodules. II 15N2 assimilation in bacteriods and cytosol fractions of soybean nodules. Soil Sci Plant Nutr 26:205–213
Olesniewicz SK, Thomas BR (1999) Effects of mycorrhizal colonization on biomass production and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide. New Phytol 142:133–140
Parker MA, Wurtz AK, Paynter Q (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biol Invasions 9:127–138
Pereyra G, Hartmann H, Michalzik B, Ziegler W, Trumbore S (2015) Influence of rhizobia inoculation on biomass gain and tissue nitrogen content of leucaena leucocephala seedlings under drought. Forests 6:3686–3703
Pitcairn CER, Fowler D, Grace J (1995) Deposition of fixed atmospheric nitrogen and foliar nitrogen content of bryophytes and Calluna vulgaris (L.) Hull. Environ Pollut 88:193–205
Quinkenstein A, Pape DA, Freese D, Schneider BU, Hüttl RF (2012) Biomass, carbon and nitrogen distribution in living woody plant parts of Robinia pseudoacacia L. Growing on reclamation sites in the mining region of Lower Lusatia (Northeast Germany). Int J For Res 2012:1–10
Ramírez-Valiente JA, Valladares F, Sánchez-Gómez D et al (2014) Population variation and natural selection on leaf traits in cork oak throughout its distribution range. Acta Oecologia 58:49–56
Raven JA, Andrews M (2010) Evolution of tree nutrition. Tree Physiol 30:1050–1071
Ren ZG, Lin CL, Li Y, Song CS, Wang XZ, Piao CG, Tian GZ (2014a) Comparative molecular analyses of phytoplasmas infecting Sophora japonica cv. golden and Robinia pseudoacacia. J Phytopathol 162:98–106
Ren ZG, Lin CL, Li Y, Song CS, Wang XZ, Piao CG, Tian GZ (2014b) Comparative molecular analyses of phytoplasmas infecting Sophora japonica cv. golden and Robinia pseudoacacia. J Phytopathol 162:98–106
Rennenberg H, Dannenmann M (2015) Nitrogen nutrition of trees in temperate forests—the significance of nitrogen availability in the pedosphere and atmosphere. Forests 6:2820–2835
Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol (Stuttg) 12:275–291
Rizwan M, Mostofa MG, Ahmad MZ, Zhou Y, Adeel M, Mehmood S, Ahmad MA, Javed R, Imtiaz M, Aziz O, Ikram M, Tu S, Liu Y (2019) Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel. Plant Physiol Biochem 138:100–111
Saikia SP, Jain V (2007) Biological nitrogen fixation with non-legumes: an achievable target or a dogma. Curr Sci 92:317–322
Saito A, Tanabata S, Tanabata T et al (2014) Effect of nitrate on nodule and root growth of soybean (Glycine max (L.) Merr.). Int J Mol Sci 15:4464–4480
Sala OE et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Savidov NA, Lips SH (1997) Regulation ofMo-cofactor, NAHD- and NAD(P)H-specific nitrate reductase activities in the wild type and two nar- mutant lines ofbarley (Hordeum vul-gare L.). J Exp Bot 48:847–855
Sharaya LS, Novik SN, Pariiskaya AN, Kalakutskii LV (1987) Specific deformation of Alder root hairs upon interaction with infectious Frankia culture. Microbiology 56:110–114
Shi H, Ye T, Song B et al (2015) Comparative physiological and metabolomic responses of four Brachypodium distachyon varieties contrasting in drought stress resistance. Physiol Plant 37:122
Simon J, Dannenmann M, Pena R, Gessler A, Rennenberg H (2017) Nitrogen nutrition of beech forests in a changing climate: importance of plant-soil-microbe water, carbon, and nitrogen interactions. Plant Soil 418:89–114
Song J, Wang Y, Pan Y, Pang J, Zhang X, Fan J, Zhang Y (2019) The influence of nitrogen availability on anatomical and physiological responses of Populus alba x P. glandulosa to drought stress. BMC Plant Biol 19:63
Sprent JI (2008) 60Ma of legume nodulation. What's new? What's changing? Comp Biochem Physiol Part A Mol Integr Physiol 59:S215–S216
Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 215:40–56
Streeter J, Wong PP (1998) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23
Talaat NB, Abdallah AM (2008) Response of faba bean (Vicia faba L.) to dual inoculation with Rhizobium and VA mycorrhiza under different levels of N and P fertilization. J Appl Sci Res 4:1092–1102
Tardieu F, Simonneau T, Muller B (2018) The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu Rev Plant Biol 69:733–759. https://doi.org/10.1146/annurev-arplant-042817-040218
Ulrich A, Zaspel I (2000) Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology 146:2997–3005
Ulzen J (2018) Optimizing legume-rhizobia symbiosis to enhance legume grain yield in smallholder farming system in Ghana. A thesis submitted to the Department of Crop and Soil Sciences, Faculty of Agriculture, Kwame Nkrumah University Science and Technology, Kumasi, in partial fulfillment of the requirements of the degree of doctor of philosophy in soil science
Vallano MD, Sparks PJ (2013) Foliar δ15N is affected by foliar nitrogen uptake, soil nitrogen, and mycorrhizae along a nitrogen deposition gradient. Oecologia 1:47–58
Vincent JM (1970) A manual for the practical study of root-nodule bacteria
Vitousek PM, Aber JD, Howarth RW, Likens GE, Tilman DG (1997) Human alteration of the global nigrogen cycle: sources and consequences. Ecol Appl 7:737–750
Voisin A-S, Salon C, Munier-Jolain NG, Ney B (2002) Quantitative effects of soil nitrate, growth potential and phenology on symbiotic nitrogen fixation of pea (Pisum sativum L.). Plant Soil 243:31–42
Wang G, Liu F (2014) Carbon allocation of Chinese pine seedlings along a nitrogen addition gradient. For Ecol Manag 334:114–121
Wang X, Li X, Zhang S, Korpelainen H, Li C (2016) Physiological and transcriptional responses of two contrasting Populus clones to nitrogen stress. Tree Physiol 36:628–642
Wang X, Guo X, Yu Y, Cui H, Wang R, Guo W (2018) Increased nitrogen supply promoted the growth of non-N-fixing woody legume species but not the growth of N-fixing Robinia pseudoacacia. Sci Rep 8:17896. https://doi.org/10.1038/s41598-018-35972-6
Wang X, Guo X, Du N, Guo W, Pang J (2021) Rapid nitrogen fixation contributes to a similar growth and photosynthetic rate of Robinia pseudoacacia supplied with different levels of nitrogen. Tree Physiol 41:177–189
Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ et al (2017a) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169
Weemstra M, Sterck FJ, Visser EJW, Kuyper TW, Goudzwaard L, Mommer L (2017b) Fine-root trait plasticity of beech (Fagus sylvatica) and spruce (Picea abies) forests on two contrasting soils. Plant Soil 415:175–188. https://doi.org/10.1007/s11104-016-3148-y
Wei G, Chen W, Zhu W, Chen C, Young JPW, Bontemps C (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol Ecol 68:320–328
Weir BS, Turner SJ, Silvester WB, Park DC, Young JM (2004) Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl Environ Microbiol 70:5980–5987
Yang N, Zavišić A, Pena R, Polle A (2016) Phenology, photosynthesis, and phosphorus in European beech (Fagus sylvatica L.) in two forest soils with contrasting P contents. J Plant Nutr Soil Sci 179:151–158. https://doi.org/10.1002/jpln.201500539
Yuan H, Hu B, Zhsh L, Sun HG, Zhou M, Rennenberg H (2022) Physiological responses of black locust-rhizobia symbiosis to water stress. Physiol Plantarium 174:e13641. https://doi.org/10.1111/ppl.13641
Zavišić A, Yang N, Marhan S, Kandeler E, Polle A (2018) Forest soil phosphorus resources and fertilization affect ectomycorrhizal community composition, beech P uptake, and photosynthesis. Front Plant Sci 9:463. https://doi.org/10.3389/fpls.2018.00463
Zhang S, Jiang H, Zhao H, Korpelainen H, Li C (2014) Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol 34:343–354
Zhang Y et al (2016) Nitrogen enrichment weakens ecosystem stability through decreased species asynchrony and population stability in a temperate grassland. Glob Chang Biol 22:1445–1455
Zhang P, Dumroese RK, Pinto JR (2019a) Organic or inorganic nitrogen and rhizobia inoculation provide synergistic growth response of a leguminous forb and tree. Front Plant Sci 10:1308
Zhang P, Dumroese RK, Pinto JR (2019b) Organic or inorganic nitrogen and rhizobia inoculation provide synergistic growth response of a leguminous forb and tree. Front Plant Sci 10:1308
Zhang F, Liu Y, Shi C, Zhao Y, Xiao J, Wang X (2021a) Soil carbon, nitrogen, phosphorus content and their ecological stoichiometric characteristics in different plantation ages. Ecol Environ Sci 30:485–491
Zhang M, Nazieh S, Nkrumah T, Wang X (2021b) Simulating grassland carbon dynamics in Gansu for the past fifty (50) years (1968–2018) using the century model. Sustainability 13(16):9434. https://doi.org/10.3390/su13169434
Zhou M, Zhsh L, Yuan H, Sun HG, Hu B, Rennenberg H (2022) Physiological sensitivity of Robinia pseudoacacia L.-rhizobia association to low phosphorus availability. Environ Exp Bot 199:104893
Acknowledgements
The authors extend them thanks to the graduate-fellow team of Center of Molecular Ecophysiology (CMEP), College of Resources and Environment, Southwest University for their excellent assistance in the greenhouse planting and sampling work. The financial supports of the “Double-First Class” Initiative Program for Foreign Talents of Southwest University and the “Prominent Scientist Program” of Chongqing Talents (cstc2021ycjh-bgzxm0002 & cstc2021ycjh-bgzxm0020), China are gratefully acknowledged.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Hongguang Sun, Rui Liu, Zhenshan Liu, Mi Zhou and Hui Yuan. The first draft of the manuscript was written by Hongguang Sun and Bin Hu. Heinz Rennenberg and Bin Hu contributed to the finalization and revision of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interests.
Additional information
Responsible Editor: Katharina Pawlowski.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 112 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sun, H., Liu, R., Yuan, H. et al. Interaction of nitrogen availability in the soil with leaf physiological traits and nodule formation of Robinia pseudoacacia-rhizobia symbiosis depends on provenance. Plant Soil 490, 239–259 (2023). https://doi.org/10.1007/s11104-023-06069-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06069-5