Abstract
Arbuscular mycorrhizal (AM) fungi form ubiquitous symbioses with terrestrial plants in different ecosystems and provide a variety of benefits including improved drought tolerance of host plants. However, the difference and contribution of colonized and un-colonized root-system parts within mycorrhizal plants against drought stress is uncertain. A split-root system was used and the root compartments were either non-inoculated or inoculated with Rhizophagus irregularis, and were subjected to either well-watered or drought-stressed conditions. The growth, photosynthesis, reactive oxygen species (ROS) scavenging, and relative gene expression of aquaporins and phosphate transporters of hybrid poplar (Populus × canadensis ‘Neva’) were evaluated. Our results indicated that the inoculation by R. irregularis in either one or both compartments of split-root systems increased poplar biomass accumulation, photosynthesis, and ROS regulation under well-watered and drought-stressed conditions. When inoculum was applied in both compartments of split-root systems, the beneficial effect of R. irregularis was greater than that in treatment where only one compartment received inoculum. The effect of R. irregularis may attribute to improved phosphorus uptake via upregulation of relative expressions of PcPT3, PcPT4, PcPT5, and a possible improvement of water uptake via modulation of aquaporins (PcPIP2-3, PcPIP2-5, PcTIP1-1, and PcTIP1-2) in colonized root-system parts. Our results demonstrated that the benefits of the AM symbiosis depend on the extent of root colonization through which AM fungus may modulate plant phosphate and water uptake to improve tolerance of poplar against drought stress.
Similar content being viewed by others
References
Ahmed CB, Rouina BB, Sensoy S, Boukhris M, Abdallah FB (2009) Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exp Bot 67:345–352. https://doi.org/10.1016/j.envexpbot.2009.07.006
Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant Microbe 27:349–363. https://doi.org/10.1094/MPMI-09-13-0268-R
Bárzana G, Aroca R, Ruiz-Lozano JM (2015) Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 38(8):1613–1627. https://doi.org/10.1111/pce.12507
Belmondo S, Calcagno C, Genre A, Puppo A, Pauly N, Lanfranco L (2016) The Medicago truncatula MtRbohE gene is activated in arbusculated cells and is involved in root cortex colonization. Planta 243(1):251–262. https://doi.org/10.1007/s00425-015-2407-0
Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn T (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192. https://doi.org/10.1074/jbc.M603761200
Bitterlich M, Sandmann M, Graefe J (2018) Arbuscular mycorrhiza alleviates restrictions to substrate water flow and delays transpiration limitation to stronger drought in tomato. Front Plant Sci 9:154. https://doi.org/10.3389/fpls.2018.00154
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547
Calvo-Polanco M, Sánchez-Castro I, Cantos M, García JL, Azcón R, Ruiz-Lozano JM, Beuzón CR, Aroca R (2016) Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant Cell Environ 39(11):2498–2514. https://doi.org/10.1111/pce.12807
Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Physiol Plant 122:1025–1034. https://doi.org/10.1104/pp.122.4.1025
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(W1):W486–W494. https://doi.org/10.1093/nar/gky310
Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann Bot 106(5):791–802. https://doi.org/10.1093/aob/mcq170
De Oliveira VH, Ullah I, Dunwell JM, Tibbett M (2020) 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
Gan H, Jiao Y, Jia J, Wang X, Li H, Shi W, Peng C, Polle A, Luo Z (2015) Phosphorus and nitrogen physiology of two contrasting poplar genotypes when exposed to phosphorus and/or nitrogen starvation. Tree Physiol 36(1):22–38. https://doi.org/10.1093/treephys/tpv093
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500
Hacke UG, Plavcová L, Almeida-Rodriguez A, King-Jones S, Zhou W, Cooke JEK (2010) Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiol 30:1016–1025. https://doi.org/10.1093/treephys/tpq058
Hao Z, Fayolle L, Van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. J Exp Bot 63(10):3657–3672. https://doi.org/10.1093/jxb/ers046
He F, Zhang HQ, Tang M (2016) Aquaporin gene expression and physiological responses of Robinia pseudoacacia L. to the mycorrhizal fungus Rhizophagus irregularis and drought stress. Mycorrhiza 26:311–323. https://doi.org/10.1007/s00572-015-0670-3
He F, Sheng M, Tang M (2017) Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front Plant Sci 8:183. https://doi.org/10.3389/fpls.2017.00183
He J, Zou Y, Wu Q, Kuca K (2020) Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Sci Hortic 262:108745. https://doi.org/10.1016/j.scienta.2019.108745
Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Univ Calif Agric Exp Stn (berkeley) Circ 347:1–39
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162(1):9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hu W, Zhang H, Zhang X, Chen H, Tang M (2016) Characterization of six PHT1 members in Lycium barbarum and their response to arbuscular mycorrhiza and water stress. Tree Physiol 37(3):351–366. https://doi.org/10.1093/treephys/tpw125
Huang D, Ma M, Wang Q, Zhang M, Jing G, Li C, Ma F (2020) Arbuscular mycorrhizal fungi enhanced drought resistance in apple by regulating genes in the MAPK pathway. Plant Physiol Biochem 149:245–255. https://doi.org/10.1016/j.plaphy.2020.02.020
Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D et al (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175. https://doi.org/10.1126/science.aam9970
Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T (2016) Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211(4):1202–1208. https://doi.org/10.1111/nph.14016
Kilpeläinen J, Aphalo PJ, Barbero-López A, Adamczyk B, Nipu SA, Lehto T (2020) Are arbuscular-mycorrhizal Alnus incana seedlings more resistant to drought than ectomycorrhizal and nonmycorrhizal ones? Tree Physiol 40(6):782–795. https://doi.org/10.1093/treephys/tpaa035
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25(2):275–294
Leyva-Morales R, Gavito ME, Carrillo-Saucedo SM (2019) Morphological and physiological responses of the external mycelium of Rhizophagus intraradices to water stress. Mycorrhiza 29:141–147. https://doi.org/10.1007/s00572-019-00880-8
Li Z, Wu N, Liu T, Chen H, Tang M (2015) Effect of arbuscular mycorrhizal inoculation on water status and photosynthesis of Populu cathayana males and females under water stress. Physiol Plant 155(2):192–204. https://doi.org/10.1111/ppl.12336
Li T, Sun Y, Ruan Y, Xu L, Hu Y, Hao Z, Zhang X, Li H, Wang Y, Yang L, Chen B (2016) Potential role of D-myo-inositol-3-phosphate synthase and 14-3-3 genes in the crosstalk between Zea mays and Rhizophagus intraradices under drought stress. Mycorrhiza 26:879–893. https://doi.org/10.1007/s00572-016-0723-2
Li L, Zhang H, Tang M, Chen H (2021) Nutrient uptake of distribution in mycorrhizal cuttings of Populus × canadensis ’Neva’ under drought stress. J Soil Sci Plant Nut 21:2310–2324. https://doi.org/10.1007/s42729-021-00523-y
Liu T, Sheng M, Wang C, 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 53(2):250–258. https://doi.org/10.1007/s11099-015-0100-y
Liu T, Li Z, Hui C, Tang M, Zhang H (2016) Effect of Rhizophagus irregularis on osmotic adjustment, antioxidation and aquaporin PIP genes expression of Populus× canadensis ‘Neva’ under drought stress. Acta Physiol Plant 38(8):191. https://doi.org/10.1007/s11738-016-2207-6
Liu B, Li L, Rengel Z, Tian J, Li H, Lu M (2019a) Roots and arbuscular mycorrhizal fungi are independent in nutrient foraging across subtropical tree species. Plant Soil 442:97–112. https://doi.org/10.1007/s11104-019-04161-3
Liu JJ, Liu JL, Liu JH, Cui MM, Huang YJ, Tian Y, Chen A, Xu GH (2019b) The potassium transporter SIHAK10 is involved in mycorrhizal potassium uptake. Plant Physiol 180(1):465–479. https://doi.org/10.1104/pp.18.01533
López-Ráez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis. Planta 243:1375–1385. https://doi.org/10.1007/s00425-015-2435-9
Loth-Pereda V, Orsini E, Courty P, Lota F, Kohler A, Diss L, Blaudez D, Chalot M, Nehls U, Bucher M, Martin F (2011) Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiol 156(4):2141–2154. https://doi.org/10.1104/pp.111.180646
Luo ZB, Polle A (2009) Wood composition and energy content in a poplar short rotation plantation on fertilized agricultural land in a future CO2 atmosphere. Glob Change Biol 15:38–47. https://doi.org/10.1111/j.1365-2486.2008.01768.x
Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17(1):9–15. https://doi.org/10.1016/j.tplants.2011.10.001
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624. https://doi.org/10.1146/annurev.arplant.59.032607.092734
Meixner C, Ludwig-Muller 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. https://doi.org/10.1007/s00425-005-0003-4
Neumann E, Schmid B, Romheld V, George E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20(1):13–23. https://doi.org/10.1007/s00572-009-0259-9
Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi TM, Thibaud M (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83. https://doi.org/10.3389/fpls.2011.00083
Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhizal. Plant Physiol 120:587–598
Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM (2017) Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci 8:1056. https://doi.org/10.3389/fpls.2017.01056
Quiroga G, Erice G, Araca R, Delgado-Huertas A, Ruiz-Lozano JM (2020) Elucidating the possible involvement of maize aquaporins and arbuscular mycorrhizal symbiosis in the plant ammonium and urea transport under drought stress conditions. Plants 9:148. https://doi.org/10.3390/plants9020148
Ranganathan K, Cooke JE, El Kayal W, Equiza MA, Vaziriyeganeh M, Zwiazek JJ (2017) Over-expression of PIP2;5 aquaporin alleviates gas exchange and growth inhibition in poplars exposed to mild osmotic stress with polyethylene glycol. Acta Physiol Plant 39:187. https://doi.org/10.1007/s11738-017-2486-6
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New Perspecti Mol Stud Mycorrhiza 13:309–317. https://doi.org/10.1007/s00572-003-0237-6
Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39:441–452. https://doi.org/10.1111/pce.12631
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156(3):1050–1057. https://doi.org/10.1104/pp.111.174581
Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176. https://doi.org/10.1139/B04-015
Wang X, Wang Y, Pineros MA, Wang Z, Wang W, Li C, Wu Z, Kochian LV, Wu P (2014) Phosphate transporters OsPHT1,9 and OsPHT1,10 are involved in phosphate uptake in rice. Plant Cell Environ 37(5):1159–1170. https://doi.org/10.1111/pce.12224
Wang C, Reid JB, Foo E (2018) The art of self-control—autoregulation of plant–microbe symbioses. Front Plant Sci 9:998. https://doi.org/10.3389/fpls.2018.00988
Wang SS, Chen AQ, Xie K, Yang XF, Luo ZZ, Chen JD et al (2020) Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.2000926117
Wu QS, Xia RX, Zou YN (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163(11):1101–1110. https://doi.org/10.1016/j.jplph.2005.09.001
Wu QS, Cao MQ, Zou YN, Wu C, He XH (2016) Mycorrhizal colonization represents functional equilibrium on root morphology and carbon distribution of trifoliate orange grown in a split-root system. Sci Hortic 199:95–102. https://doi.org/10.1016/j.scienta.2015.12.039
Wu F, Zhang H, Fang F, Wu N, Zhang Y, Tang M (2017) Effects of nitrogen and exogenous Rhizophagus irregularis on the nutrient status, photosynthesis and leaf anatomy of Populus × canadensis ‘Neva.’ J Plant Growth Regul 36(4):824–835. https://doi.org/10.1007/s00344-017-9686-6
Yan M, Wang L, Ren H, Zhang X (2017) Biomass production and carbon sequestration of a short-rotation forest with different poplar clones in northwest China. Sci Total Environ 586:1135–1140. https://doi.org/10.1016/j.scitotenv.2017.02.103
Zhang H, Franken P (2014) Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza 24(6):419–430. https://doi.org/10.1007/s00572-013-0553-4
Zhang H, Liu Z, Chen H, Tang M (2016) Symbiosis of arbuscular mycorrhizal fungi and Robinia pseudoacacia L. improves root tensile strength and soil aggregate stability. PLoS ONE 11(4):e0153378. https://doi.org/10.1371/journal.pone.0153378
Zhang F, Zou Y, Wu Q (2018) Quantitative estimation of water uptake by mycorrhizal extraradical hyphae in citrus under drought stress. Sci Hortic 229:132–136. https://doi.org/10.1016/j.scienta.2017.10.038
Zhang J, Bi YL, Song ZH, Xiao L, Christie P (2021) Arbuscular mycorrhizal fungi alter root and foliar responses to fissure-induced root damage. Ecol Indic 127:107800. https://doi.org/10.1016/j.ecolind.2021.107800
Zheng FL, Liang SM, Chu XN, Yang YL, Wu QS (2020) Mycorrhizal fungi enhance flooding tolerance of peace through inducing proline accumulation and improving root architecture. Plant Soil Environ 66(12):624–631. https://doi.org/10.17221/520/2020-PSE
Acknowledgements
This research was funded by the National Natural Science Foundation of China (31700530, 32071639), the National Key Research and Development Program of China (2018YFD0600203), and the State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources (SKLCUSA-b202007). We also thank the anonymous reviewers for reviewing the manuscript and offering helpful suggestions.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by M. J. Reigosa.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
11738_2022_3393_MOESM1_ESM.tif
Supplementary file1 Figure S1 Circular tree of the 4 full-length phosphate transporters sequences from Populus × canadensis ‘Neva’, along with the NCBI PHT1 protein sequences from Populus trichocarpa, Populus euphratica, Glycine max, Oryza sativa L., Zea mays L., Lycium barbarum, Arabidopsis thaliana, Nicotiana tabacum, Solanum melongena, Medicago truncatula, Lycopersicon esculentum, and Solanum tuberosum (TIF 13981 KB)
11738_2022_3393_MOESM2_ESM.tif
Supplementary file2 Figure S2 Circular tree of the 10 full-length aquaporin sequences from Populus × canadensis ‘Neva’, along with the NCBI aquaporin sequences from Populus trichocarpa, Populus euphratica, Glycine max, Oryza sativa L., Zea mays L., Lycium barbarum, Arabidopsis thaliana, Nicotiana tabacum, Solanum melongena, Medicago truncatula, Lycopersicon esculentum, and Solanum tuberosum (TIF 76573 KB)
Rights and permissions
About this article
Cite this article
Zhang, H., Li, L., Ren, W. et al. Arbuscular mycorrhizal fungal colonization improves growth, photosynthesis, and ROS regulation of split-root poplar under drought stress. Acta Physiol Plant 44, 62 (2022). https://doi.org/10.1007/s11738-022-03393-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03393-8