Abstract
Arbuscular mycorrhizal fungi (AMF) have been reported to improve the resistance to drought stress in some plant species. The aim of this study was to evaluate the effects of Rhizophagus irregularis inoculation on the growth, photosynthetic capacity, nutrient uptake, and nutrient distribution of poplar cuttings under drought stress. The experiment was performed with a randomized block design with two factors: (i) AMF treatment, inoculated with R. irregularis (AM) or not (NM); (ii) drought treatment, well-watered (WW, 70–75% of field capacity), mild stressed (MS, 50–55% of field capacity), or severe stressed (SS, 30–35% of field capacity). The results showed that R. irregularis colonized more than 70% of the roots of poplar cuttings. Drought stress limited the plant growth and photosynthetic capacity of poplar, while inoculation increased the plant height, stem diameter, stem dry weight, root dry weight, net photosynthetic rate (PN), stomatal conductance (gs), and intrinsic water use efficiency (WUEi) regardless of the drought stress treatment. Drought stress decreased the absorption of nutrients and affected their distribution in plant tissues. Regardless of drought stress treatment, inoculation increased the concentrations of Ca and Mn in leaves and the concentration of Cu in roots. Under mild drought stress conditions, the contents of P, Ca, Cu, Fe, and Zn increased significantly in the leaves of inoculated plants, while the contents of P, Ca, Fe, and Mn increased significantly in the roots. Under severe drought stress, inoculation decreased the distribution of N, P, K, and Mg in the leaves; the distribution of K, Ca, Mn, and Zn in roots; and the distribution of Cu in roots. Moreover, a principal components analysis showed that under well-watered and severe drought stress conditions, the inoculation of poplars with R. irregularis could significantly increase the absorption of nutrients. The results of a correlation analysis indicated that the growth parameters and gas exchange parameters positively correlated with the concentrations of leaf P, K, Ca, Fe, Mn, Cu, and Zn. Photosynthetic capacity, nutrient absorption, and a change in nutrient distribution were enhanced in the mycorrhizal poplar cuttings, which resulted in enhanced growth and a limited loss of biomass during drought stress compared with the non-mycorrhizal cuttings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bahraminia M, Zarei M, Ronaghi A, Sepehri M, Etesami H (2020) Ionomic and biochemical responses of maize plant (Zea mays L.) inoculated with Funneliformis mosseae to water-deficit stress. Rhizosphere 16:100269. https://doi.org/10.1016/j.rhisph.2020.100269
Bredow M, Monaghan J (2019) Regulation of plant immune signaling by calcium-dependent protein kinases. Mol Plant Microbe in 32:6–19. https://doi.org/10.1094/MPMI-09-18-0267-FI
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
Cao P, Su XD, Pan XW, Liu ZF, Chang WR, Li M (2018) Structure, assembly and energy transfer of plant photosystem II supercomplex. BBA-Biomembranes 1859:633–644. https://doi.org/10.1016/j.bbabio.2018.03.007
Chen H, Dong Y, Xu T, Wang YP, Wang HT, Duan BL (2017) Root order-dependent seasonal dynamics in the carbon and nitrogen chemistry of poplar fine roots. New for 48:587–607. https://doi.org/10.1007/s11056-017-9587-3
Chong J, Soufan O, Li C, Caraus I, Li SZ, Bourque G, Wishart DS, Xia JG (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46:486–494. https://doi.org/10.1093/nar/gky310
Costa DM, Rech TD, Primieri S, Pigozzi BG, Werner SS, Sturmer SL (2021) Inoculation with isolates of arbuscular mycorrhizal fungi influences growth, nutrient use efficiency and gas exchange traits in micropropagated apple rootstock ‘Marubakaido.’ Plant Cell Tiss Org 145:1–11. https://doi.org/10.1007/s11240-020-01994-0
De Oliveira VH, Ullah I, Dunwell JM, Tibbett M (2019) Mycorrhizal symbiosis induces divergent patterns of transport and partitioning of Cd and Zn in Populus trichocarpa. Environ Exp Bot 171:103925. https://doi.org/10.1016/j.envexpbot.2019.103925
Feodorova TA, Alexandrov OS (2020) Comparative studying of leaf trichomes, teeth and glands in Populus nigra L., Populus deltoides W. Bartram ex Marshall and their hybrids. Forests 11:1267. https://doi.org/10.3390/f11121267
Geng GT, Cakmak I, Ren T, Lu ZF, Lu JW (2021) Effect of magnesium fertilization on seed yield, seed quality, carbon assimilation and nutrient uptake of rapeseed plants. Field Crop Res 264:108082. https://doi.org/10.1016/j.fcr.2021.108082
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Goehing J, Henkel-Johnson D, Macdonald SE, Bork EW, Thomas BR (2019) Spatial partitioning of competitive effects from neighbouring herbaceous vegetation on establishing hybrid poplars in plantations. Can J Forest Res 49:595–605. https://doi.org/10.1139/cjfr-2018-0410
Goll DS, Joetzjer E, Huang M, Ciais P (2018) Low phosphorus availability decreases susceptibility of tropical primary productivity to droughts. Geophys Res Lett 45:8231–8240. https://doi.org/10.1029/2018GL077736
Hu WT, Zhang HQ, Zhang XY, Chen H, Tang M (2017) Characterization of six PHT1 members in Lycium barbarum and their response to arbuscular mycorrhiza and water stress. Tree Physiol 37:351–366. https://doi.org/10.1093/treephys/tpw125
Hussain HA, Men S, Hussain S, Chen Y, Ali S, Zhang S, Zhang KP, Li Y, Xu QW, Liao CQ, Wang LC (2019) Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci Rep 9:3890. https://doi.org/10.1038/s41598-019-40362-7
Ishka MR, Vatamaniuk OK (2020) Copper deficiency alters shoot architecture and reduces fertility of both gynoecium and androecium in Arabidopsis thaliana. Plant Direct 4:e00288. https://doi.org/10.1002/pld3.288
Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175. https://doi.org/10.1126/science.aam9970
Keller M (2020) Water relations and nutrient uptake. In: Keller M (ed) The science of grapevines, 3rd edn. Academic Press, New York, pp 105–127. https://doi.org/10.1016/B978-0-12-816365-8.00003-8
Khan A, Anwar Y, Hasan M, Iqbal A, Ali M, Alharby H, Hakeem KR, Hasanuzzaman M (2017) Attenuation of drought stress in Brassica seedlings with exogenous application of Ca2+ and H2O2. Plants 6:20. https://doi.org/10.3390/plants6020020
Kong Z, Glick BR, Duan J, Ding S, Tian J, McConkey BJ, Wei G (2015) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 39:383–398. https://doi.org/10.1007/s11104-015-2434-4
Li X, Mao XH, Xu YJ, Li Y, Zhao N, Yao JX, Dong YF, Tigabu M, Zhao XY, Li SW (2021) Comparative transcriptomic analysis reveals the coordinated mechanisms of Populus × canadensis ‘Neva’ leaves in response to cadmium stress. Ecotox Environ Safe 216:112179. https://doi.org/10.1016/j.ecoenv.2021.112179
Liu L, Li D, Ma YL, Shen HT, Zhao SM, Wang YF (2020) Combined application of arbuscular mycorrhizal fungi and exogenous melatonin alleviates drought stress and improves plant growth in tobacco seedlings. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10165-6
Liu T, Sheng M, Wang CY, Chen H, Li Z, Tang M (2015) Impact of arbuscular mycorrhizal fungi on the growth, water status and photosynthesis of hybrid poplar under drought stress and recovery. Photosynthetica 5:250–258. https://doi.org/10.1007/s11099-015-0100-y
Lopes JI, Arrobas M, Brito C, Goncalves A, Silva E, Martins S, Raimundo S, Rodrigues MA, Correia CM (2020) Mycorrhizal fungi were more effective than zeolites in increasing the growth of non-irrigated young olive trees. Sustainability 12:10630. https://doi.org/10.3390/su122410630
Lubitz W, Chrysina M, Cox N (2019) Water oxidation in photosystem II. Photosynth Res 142:105–125. https://doi.org/10.1007/s11120-019-00648-3
Mbengue MD, Hervé C, Debellé F (2020) Nod factor signaling in symbiotic nodulation. Adv Bot Res 94:1–39. https://doi.org/10.1016/bs.abr.2019.10.002
Nakandalage N, Seneweera S (2018) Micronutrients use efficiency of crop-plants under changing climate. In: Hossain MA, Kamiya T, Burritt DJ, Tran L-S P, Fujiwara T (Eds) Plant micronutrient use efficiency. Academic Press, New York, pp 209–214. https://doi.org/10.1016/B978-0-12-812104-7.00015-0
Nejad RAH, Kafi M, Jari SK, Mozafari H, Motesharezadeh B (2021) Arbuscular mycorrhizal fungi improve growth, physiological status and nutrients accumulation of Ailanthus altissima seedlings under cadmium pollution and salinity. Russ J Plant Physi 68:266–273. https://doi.org/10.1134/S102144372102014X
Nisha N, Rao PB (2017) Atomic absorption spectrophotometer (AAS) analysis for evaluation of variation in mineral content in different varieties of Trigonella foenumgraecum L. Legume Res 41:132–134. https://doi.org/10.18805/lr.v0i0.8396
Ortuño MF, Lorente B, Hernández JA, Sánchez-Blanco MJ (2018) Mycorrhizal inoculation on compost substrate affects nutritional balance, water uptake and photosynthetic efficiency in Cistus albidus plants submitted to water stress. Braz J Bot 41:299–310. https://doi.org/10.1007/s40415-018-0457-9
Phillips J, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Püschel D, Bitterlich M, Rydlová J, Jansa J (2021) Drought accentuates the role of mycorrhiza in phosphorus uptake. Soil Biol Biochem 157:108243. https://doi.org/10.1016/j.soilbio.2021.108243
Qi JG, Sun SM, Yang L, Li MJ, Ma FW, Zou YJ (2019) Potassium uptake and transport in apple roots under drought stress. Hortic Plant J 5:10–16. CNKI:SUN:YYZW.0.2019–01–002
Ramos-Artuso F, Galatro A, Lima A, Batthyány C, Simontacchi M (2019) Early events following phosphorus restriction involve changes in proteome and affects nitric oxide metabolism in soybean leaves. Environ Exp Bot 161:203–217. https://doi.org/10.1016/j.envexpbot.2019.01.002
Rodrigues VA, Crusciol CAC, Bossolani JW, Moretti LG, Portugal JR, Mundt TT, De Oliveira SL, Garcia A, Calonego JC, Lollato RP (2021) Magnesium foliar supplementation increases grain yield of soybean and maize by improving photosynthetic carbon metabolism and antioxidant metabolism. Plants, 10:797. https://doi.org/10.3390/plants10040797
Ruytinx J, Kafle A, Usman M, Coninx L, Zimmermann S, Garcia K (2019) Micronutrient transport in mycorrhizal symbiosis; zinc steals the show. Fungal Biol Rev 34:1–9. https://doi.org/10.1016/j.fbr.2019.09.001
Sterckeman T, Moyne C, Le TD (2021) A modelling study to evaluate the mechanisms of root iron uptake by Noccaea caerulescens. Plant Soil. https://doi.org/10.1007/s11104-021-04873-5
Sujkowska-Rybkowska M, Znojek E (2018) Localization of calreticulin and calcium ions in mycorrhizal roots of Medicago truncatula in response to aluminum stress. J Plant Physiol 229:22–31. https://doi.org/10.1016/j.jplph.2018.05.014
Sun H, Zheng YL, Xie YX, Lin YL, Yang FY (2019) Varied responses of growth and mineral elements concentrations in Pennisetum ericanum and Festuca arundinacea under Cd/Cu addition. Pol J Environ Stud 28:1385–1396. https://doi.org/10.15244/pjoes/81562
Sun YM, Wang M, Mur LAJ, Shen QR, Guo SW (2020) The cros-kingdom roles of mineral nutrient transporters in plant-microbe relations. Physiol Plantarum 171:771–784. https://doi.org/10.1111/ppl.13318
Symanczik S, Lehmann MF, Wiemken A, Boller T, Courty PE (2018) Effects of two contrasted arbuscular mycorrhizal fungal isolates on nutrient uptake by Sorghum bicolor under drought. Mycorrhiza 28:779–785. https://doi.org/10.1007/s00572-018-0853-9
Tripathi AM, Klem K, Fischer M, Orság M, Trnka M, Marek MV (2018) Water availability influences accumulation and allocation of nutrients and metals in short-rotation poplar plantation. Biomass Bioenerg 116:151–160. https://doi.org/10.1016/j.biombioe.2018.06.010
Upadhayay VK, Singh J, Khan A, Lohani S, Singh AV (2019) Mycorrhizal mediated micronutrients transportation in food based plants: a biofortification strategy. In: Varma A, Choudhary D (eds) Mycorrhizosphere and pedogenesis. Springer, Singapore, pp 1–24. https://doi.org/10.1007/978-981-13-6480-8-1
Walker C, Harper CJ, Brundrett MC, Krings M (2018) Looking for arbuscular mycorrhizal fungi in the fossil record: an illustrated guide. In: Krings M, Harper CJ, Cuneo NR, Rothwell GW (eds) Transformative paleobotany: papers to commemorate the life and legacy of Thomas N. Taylor. Academic Press, London, pp 481–517. https://doi.org/10.1016/B978-0-12-813012-4.00020-6
Wang WX, Zhang F, Chen ZL, Liu J, Guo C, He JD, Zou YN, Wu QS (2017) Responses of phytohormones and gas exchange to mycorrhizal colonization in trifoliate orange subjected to drought stress. Arch Agron Soil Sci 63:14–23. https://doi.org/10.1080/03650340.2016.1175556
Watts-Williams SJ, Nguyen TD, Kabiri S, Losic D, McLaughlin MJ (2019) Potential of zinc-loaded graphene oxide and arbuscular mycorrhizal fungi to improve the growth and zinc nutrition of Hordeum vulgare and Medicago truncatula. Appl Soil Ecol 150:103464. https://doi.org/10.1016/j.apsoil.2019.103464
Wu F, Zhang HQ, Fang FR, Liu HG, Tang M (2017a) Arbuscular mycorrhizal fungi alter nitrogen allocation in the leaves of Populus × canadensis ‘Neva.’ Plant Soil 421:477–491. https://doi.org/10.1007/s11104-017-3461-0
Wu F, Zhang HQ, Fang FR, Wu N, Zhang YX, Tang M (2017b) Effects of nitrogen and exogenous Rhizophagus irregularis on the nutrient status, photosynthesis and leaf anatomy of Populus × canadensis ‘Neva.’ J Plant Growth Regul 36:824–835. https://doi.org/10.1007/s00344-017-9686-6
Wu F, Zhang HQ, Fang FR, Tang M (2018) Nutrient allocation and photochemical responses of Populus × canadensis ‘Neva’ to nitrogen fertilization and exogenous Rhizophagus irregularis inoculation. Acta Physiol Plant 40:152. https://doi.org/10.1007/s11738-018-2728-2
Wu F, Fang FR, Wu N, Li L, Tang M (2020) Nitrate transporter gene expression and kinetics of nitrate uptake by Populus × canadensis ‘Neva’ in relation to arbuscular mycorrhizal fungi and nitrogen availability. Front Microbiol 11:176. https://doi.org/10.3389/fmicb.2020.00176
Yi L, Li B, Korpelainen H, Yu F, Wu L, Tong L, Liu M (2020) Mechanisms of drought response in Populus. South Forests 82:359–366. https://doi.org/10.2989/20702620.2020.1733755
Zai XM, Fan JJ, Hao ZP, Li XM, Zhang WX (2021) Effect of co-inoculation with arbuscular mycorrhizal fungi and phosphate solubilizing fungi on nutrient uptake and photosynthesis of beach palm under salt stress environment. Sci Rep 11:5761. https://doi.org/10.1038/s41598-021-84284-9
Zhang HZ, Zhao SH, Li DD, Xu XM, Li CH (2017) Genome-wide analysis of the ZRT, IRT-Like protein (ZIP) family and their responses to metal stress in Populus trichocarpa. Plant Mol Biol Rep 35:534–549. https://doi.org/10.1007/s11105-017-1042-2
Zhang BB, Zhang H, Wang H, Wang P, Wu YX, Wang MM (2018a) Effect of phosphorus additions and arbuscular mycorrhizal fungal inoculation on the growth, physiology, and phosphorus uptake of wheat under two water regimes. Commun Soil Sci Plan 49:862–874. https://doi.org/10.1080/00103624.2018.1435798
Zhang JS, Zhang H, Srivastava AK, Pan YJ, Bai JJ, Fang JJ, Shi HZ, Zhu JK (2018b) Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol 176:2082–2094. https://doi.org/10.1104/pp.17.01432
Funding
This research was funded by the National Natural Science Foundation of China (32071639 and 31700530), the National Key Research and Development Program of China (2018YFD0600203-3), the China Postdoctoral Science Foundation (2016M592849), and the Postdoctoral Foundation of Shaanxi Province (2016BSHYDZZ19). The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding authors
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
Li, L., Zhang, H., Tang, M. et al. Nutrient Uptake and Distribution in Mycorrhizal Cuttings of Populus × canadensis ‘Neva’ Under Drought Stress. J Soil Sci Plant Nutr 21, 2310–2324 (2021). https://doi.org/10.1007/s42729-021-00523-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-021-00523-y