Skip to main content
SpringerLink
Log in

Plant sexual variation modulates rhizospheric nutrient processes through the soil microbiome response to drought and rewetting in Populus cathayana

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Drought affects the physiological environment of the soil microbiome and plants. However, the ability of drought and rewetting to regulate sex-specific soil nutrient availability with respect to bacterial- and fungal-mediated rhizospheric processes has not been clarified. The impact of drought and rewetting on soil bacterial and fungal communities and rhizospheric processes were examined in dioecious Populus cathayana females and males. Drought and rewetting affected the composition and abundance of the bacterial and fungal communities but not their diversity in the rhizosphere of both sexes. Male had more drought-tolerant fungi and bacteria in the rhizosphere of males than females in response to drought. The changing bacterial and fungal community composition promoted soil ammonification in the rhizosphere of female plants, whereas nitrification by ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) was accelerated in the rhizosphere of male plants. Rewetting reduced the sexual differences in the ratio of nitrate (NO3−) to ammonium (NH4+) in the rhizosphere. In the rhizosphere of females, the changes in fungal community composition were linked more strongly to soil N and P reactions during recovery compared with that in the bacterial community composition. Conversely, the bacterial community rather than fungal components was the main contributor to soil N reactions in the rhizosphere of males. Plant sex influenced the response and recovery of fungal and bacterial communities to drought, and sexual dimorphism was detected in the regulation of rhizospheric nutrient reactions. Our results emphasize the ecological relevance of plant sex in determining the response of soil microbial communities to drought and rewetting effects and their ecological functions in P. cathayana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adhikari TB, Joseph CM, Yang G, Phillips DA, Nelson LM (2001) Evaluation of bacteria isolated from rice for plant growth promotion and biological control of seedling disease of rice. Can J Microbiol 47:916–924

  • Allison SD, Martiny JB (2008) Resistance resilience and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnard R, Barthes L, Le Roux X, Leadley PW (2004) Dynamics of nitrifying activities, denitrifying activities and nitrogen in grassland mesocosms as altered by elevated CO2. New Phytol 162:365–376

  • Beier S, Bertilsson S (2013) Bacterial chitin degradation-mechanisms and ecophysiological strategies. Front Microbiol 4:149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microb Ecol 68:1–13

    Article  CAS  Google Scholar 

  • Bhatti AA, Haq S, Bhat RA (2017) Actinomycetes benefaction role in soil and plant health. Microb Pathogenesis 111:458–467

    Article  CAS  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Boil Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13:581–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canarini A, Schmidt H, Fuchslueger L, Martin V, Herbold CW, Zezula D, Gundler P, Hasibeder R, Jecmenica M, Bahn M, Richter A (2021) Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community. Nat Commun 12:1–14

    Article  Google Scholar 

  • Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Pan G, Li L, Zheng J, Zhang X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. App Soil Ecol 71:33–44

    Article  Google Scholar 

  • Chen LY, Liu LI, Qin SQ, Yang GB, Fang K, Zhu B, Kuzyakov Y, Chen PD, Xu Y, Yang YH (2019) Regulation of priming effect by soil organic matter stability over a broad geographic scale. Nat Commun 10:1–10

    Article  Google Scholar 

  • Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol 13:980–989

    Article  Google Scholar 

  • Crowther TW, Maynard DS, Crowther TR, Peccia J, Smith JR, Bradford MA (2014) Untangling the fungal niche: the trait-based approach. Front Microbiol 5:579

    Article  PubMed  PubMed Central  Google Scholar 

  • De Boer W, Gerards S, Klein Gunnewiek PJA, Modderman R (1999) Response of the chitinolytic microbial community to chitin amendments of dune soils. Biol Fert Soils 29:170–177

    Article  Google Scholar 

  • de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Halli S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Communs 9:3033

    Article  Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Article  Google Scholar 

  • Esmaeil Zade NS, Sadeghi A, Moradi P (2019) Streptomyces strains alleviate water stress and increase peppermint (Mentha piperita) yield and essential oils. Plant Soil 434:441–452

    Article  CAS  Google Scholar 

  • Evans SE, Bell-Dereske LP, Dougherty KM, Kittredge HA (2020) Dispersal alters soil microbial community response to drought. Environ Microbiol 22:905–916

    Article  CAS  PubMed  Google Scholar 

  • Feng F, Ge J, Li Y, Cheng J, Zhong J, Yu X (2017) Isolation, colonization, and chlorpyrifos degradation mediation of the endophytic bacterium Sphingomonas strain HJY in Chinese Chives (Allium tuberosum). J Agr Food Chem 65:1131–1138

    Article  CAS  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    Article  CAS  PubMed  Google Scholar 

  • Frankenberger WT Jr, Tabatabai MA (1991) L-Glutaminase activity of soils. Soil Biol Biochem 23:869–874

    Article  CAS  Google Scholar 

  • Frey B, Rieder SR (2013) Response of forest soil bacterial communities to mercury chloride application. Soil Biol Biochem 65:329–337

    Article  CAS  Google Scholar 

  • Fu Z, Wu F, Mo C, Deng Q, Meng W, Giesy JP (2016) Comparison of arsenic and antimony biogeochemical behavior in water, soil and tailings from Xikuangshan, China. Sci Total Environ 539:97–104

    Article  CAS  PubMed  Google Scholar 

  • Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927

    Article  CAS  PubMed  Google Scholar 

  • Gargallo-Garriga A, Preece C, Sardans J, Oravec M, Urban O, Peñuelas J (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep 8:1–15

    Article  CAS  Google Scholar 

  • Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127

    Article  CAS  PubMed  Google Scholar 

  • Hu E, Yuan Z, Zhang H, Zhang W, Wang X, Jones SB, Wang N (2018) Impact of elevated tropospheric ozone on soil C, N and microbial dynamics of winter wheat. Agric Ecosyst Environ 253:166–176

    Article  CAS  Google Scholar 

  • Huang H, Zhou L, Chen J, Wei T (2020) ggcor: Extended tools for correlation analysis and visualization. R Package Version 0.9:7, Shenzhen, China. https://github.com/houyunhuang/ggcor

  • Hultine KR, Grady KC, Wood TE, Shuster SM, Stella JC, Whitham TG (2016) Climate change perils for dioecious plant species. Nat Plants 2:16109

    Article  PubMed  Google Scholar 

  • Huygens D, Díaz S, Urcelay C, Boeckx P (2016) Microbial recycling of dissolved organic matter confines plant nitrogen uptake to inorganic forms in a semi-arid ecosystem. Soil Biol Biochem 101:142–151

    Article  CAS  Google Scholar 

  • Jia Z, Hu X, Xia W, Fornara D, Nannipieri P, Tiedje J (2019) Community shift of microbial ammonia oxidizers in air-dried rice soils after 22 years of nitrogen fertilization. Biol Fertil Soils 55:419–424

    Article  CAS  Google Scholar 

  • Jin J, Krohn C, Franks AE, Wang X, Wood JL, Petrovski S, McCaskill M, Batinovic S, Xie ZH, Tang C (2022) Elevated atmospheric CO2 alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat. Microbiome 10:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joergensen RG, Anderson TH, Wolters V (1995) Carbon and nitrogen relationships in the microbial biomass of soils in beech (Fagus sylvatica L) forests. Biol Fertil Soils 19:141–147

    Article  Google Scholar 

  • Jog R, Nareshkumar G, Rajkumar S (2012) Plant growth promoting potential and soil enzyme production of the most abundant Streptomyces spp from wheat rhizosphere. J Microbiol 113:1154–1164

    CAS  Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480

    Article  CAS  PubMed  Google Scholar 

  • Juvany M, Munné-Bosch S (2015) Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. J Exp Bot 66:6083–6092

    Article  CAS  PubMed  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Kandeler E, Poll C, Frankenberger WT Jr, Ali Tabatabai M (2011) Nitrogen cycle enzymes. Meth Soil Enzymol 9:211–245

    CAS  Google Scholar 

  • Kannenberg SA, Phillips RP (2020) Non-structural carbohydrate pools not linked to hydraulic strategies or carbon supply in tree saplings during severe drought and subsequent recovery. Tree Physiol 40:259–271

    Article  CAS  PubMed  Google Scholar 

  • Khatoon H, Solanki P, Narayan M, Tewari L, Rai JPN, Hina Khatoon C (2017) Role of microbes in organic carbon decomposition and maintenance of soil ecosystem. Int J Chem Stud 5:1648–1656

    CAS  Google Scholar 

  • Kitsopoulos KP (1999) Cation-exchange capacity (CEC) of zeolitic volcaniclastic materials: applicability of the ammonium acetate saturation (AMAS) method. Clay Clay Miner 47:688–696

    Article  CAS  Google Scholar 

  • Krishna RR, Mannar MR, Gnanam A, Bose S (1988) Inhibition of nitrate and nitrite reductase induction in wheat by sandoz 9785. Phytochemistry 27:685–688

  • Kronzucker HJ, Siddiqi MY, Glass AD (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61

    Article  CAS  Google Scholar 

  • Ladd JN, Butler JHA (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4:19–30

    Article  CAS  Google Scholar 

  • Leizeaga A, Meisner A, Rousk J, Bååth E (2022) Repeated drying and rewetting cycles accelerate bacterial growth recovery after rewetting. Biol Fertil Soils 58:365–374

    Article  CAS  Google Scholar 

  • Liu H, Wu Y, Xu H, Ai Z, Zhang J, Liu G, Xue S (2021a) N enrichment affects the arbuscular mycorrhizal fungi-mediated relationship between a C4 grass and a legume. Plant Physiol 187:1519–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Korpelainen H, Li C (2021b) Sexual differences and sex ratios of dioecious plants under stressful environments. J Plant Ecol 14:920–933

    Article  Google Scholar 

  • Liu M, Liu X, Kang J, Korpelainen H, Li C (2020) Are males and females of Populus cathayana differentially sensitive to Cd stress. J Haz Mat 393:122411

    Article  CAS  Google Scholar 

  • Liu M, Liu X, Zhao Y, Korpelainen H, Li C (2022b) Sex-specific nitrogen allocation tradeoffs in the leaves of Populus cathayana cuttings under salt and drought stress. Plant Physiol Bioch 172:101–110

    Article  CAS  Google Scholar 

  • Liu M, Zhao Y, Wang Y, Korpelainen H, Li C (2022a) Stem xylem traits and wood formation affect sex-specific responses to drought and rewetting in Populus cathayana. Tree Physiol 10:1093

    CAS  Google Scholar 

  • Martens HW, Berube PM, Urakawa H, de La Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying. Archaea Bact Nat. 461:976–979

    Google Scholar 

  • McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meisner A, Jacquiod S, Snoek BL, Ten Hooven FC, Van der Putten WH (2018) Drought legacy effects on the composition of soil fungal and prokaryote communities. Front Microbiol 9:294

    Article  PubMed  PubMed Central  Google Scholar 

  • Meisner A, Snoek BL, Nesme J, Dent E, Jacquiod S, Classen AT, Priemé A (2021) Soil microbial legacies differ following drying-rewetting and freezing-thawing cycles. ISME J 15:1207–1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata Y, Fujiyama A, Tsuda M, Kurokawa K (2014) Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res 21:217–227

    Article  CAS  PubMed  Google Scholar 

  • Najera F, Dippold MA, Boy J, Seguel O, Koester M, Stock S, Merino C, Kuzyakov Y, Matus F (2020) Effects of drying/rewetting on soil aggregate dynamics and implications for organic matter turnover. Biol Fertil Soils 56:893–905

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher-Jenull J, Ceccherini MT, Pietramellara G, Renella G, Schloter M (2020) Beyond microbial diversity for predicting soil functions: a mini review. Pedosphere 30:5–17

    Article  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Oberson S, Frossard E (eds) Phosphorus in action. Springer, Berlin, Heidelberg, pp 215–243

    Chapter  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic mater. Methods of Soil Analysis, eds Page AL, Miller RH, Keeney DR (American Society ofAgronomy, Madison, WI), Part II, 2nd Ed, pp 539–576

  • Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glockner FO, Tedersoo L (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:259–264

    Article  Google Scholar 

  • Nowak J, Kaklewski K, Klódka D (2002) Influence of various concentrations of selenic acid (IV) on the activity of soil enzymes. Sci Total Environ 291:105–110

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J (2011) Vegan: Community Ecology Package-R package version 1.17-8. http://CRAN.R-project.org/package= vegan.

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests MASS (2007) The vegan package. Comm Ecol Pack 10:631–637

  • Olsen SR, Watanabe FS, Cosper HR, Larson WE, Nelson LB (1954) Residual phosphorus availability in long-time rotations on calcareous soils. Soil Sci 78:141–152

    Article  CAS  Google Scholar 

  • Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Microbiol 117:766–773

    CAS  Google Scholar 

  • Preece C, Peñuelas J (2016) Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil 409:1–17

    Article  CAS  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Raheem A, Shaposhnikov A, Belimov AA, Dodd IC, Ali B (2018) Auxin production by rhizobacteria was associated with improved yield of wheat (Triticum aestivum L.) under drought stress. Arch Agron Soil 64:574–587

    Article  CAS  Google Scholar 

  • Sahrawat KL, Prasad R (1975) A rapid method for determination of nitrate, nitrite, and ammoniacal nitrogen in soils. Plant Soil 42:305–308

    Article  CAS  Google Scholar 

  • Shoun H, Fushinobu S, Jiang L, Kim SW, Wakagi T (2012) Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philos T R Soc B 367:1186–1194

    Article  CAS  Google Scholar 

  • Sims JR, Jackson GD (1971) Field measurement of pan evaporation 1. Agron J 63:339–340

    Article  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal: bacterial dominance in soils–methods controls and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Tabatabai A (1994) Soil enzymes In: Weaver RW, Angle JS, Bottomley PS (Ed) Methods of soil analyses Part 2 Microbiological and biochemical properties, 2nd ed. Science Society America, Madison, pp 775–833

  • Thomas SC, LaFrankie JV (1993) Sex, size and interyear variation in flowering among dioecious trees of the Malayan rain forest. Ecology 74:1529–1537

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wang R, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA (2021) Carbon allocation to the rhizosphere is affected by drought and nitrogen addition. J Ecol 109:3699–3709

    Article  CAS  Google Scholar 

  • Wang RZ, Dorodnikov M, Yang S, Zhang YY, Filley TR, Turco RF, Zhang YG, Xu ZW, Li H, Jiang Y (2015) Responses of enzymatic activities within soil aggregates to 9-year nitrogen and water addition in a semi-arid grassland. Soil Biol Biochem 81:159–167

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols. Academic Press, Inc, Burlington, MA, pp 315–322

    Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis springer-Verlag, New York URL: http://ggplot2.org

  • Wu HS, Shi X, Li J, Liu YD, Xu Y, Chen SY, Ren QQ, Xiao SH (2016) Soil ecological safety evaluation for bivalent transgenic cotton plants: root exudates versus soil enzyme activities and soil microbial diversity. Appl Ecol Env Res 14:319–336

    Article  Google Scholar 

  • Wu MH, Chen SY, Chen JW, Xue K, Chen SL, Wang XM, Chen T, Kang SC, Rui JP, Thies JE, Bardgett RD, Wang YF (2021) Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation. Proc Natl Acad Sci USA 118:e2025321118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia Z, He Y, Yu L, Li Z, Korpelainen H, Li C (2021) Revealing interactions between root phenolic metabolomes and rhizosphere bacterial communities in Populus euphratica plantations. Biol Fertil Soils 57:421–434

    Article  CAS  Google Scholar 

  • Yang S, Xu Z, Wang R, Zhang Y, Yao F, Zhang Y, Turco RF, Jiang Y, Zou H, Li H (2017) Variations in soil microbial community composition and enzymatic activities in response to increased N deposition and precipitation in Inner Mongolian grassland. Appl Soil Ecol 119:275–285

    Article  Google Scholar 

  • Zhang GL, Gong ZT (2012) Soil survey laboratory methods, vol 38. Science Press, Beijing, pp 47–49

    Google Scholar 

  • Zhang Y, Hao X, Alexander TW, Thomas BW, Shi X, Lupwayi NZ (2018) Long-term and legacy effects of manure application on soil microbial community composition. Biol Fertil Soils 54:269–283

    Article  CAS  Google Scholar 

  • Zhang Z, Yuan Y, Liu Q, Yin H (2019) Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol Biochem 136:107517

    Article  CAS  Google Scholar 

  • Zhang Z, Zhang Q, Cui H, Li Y, Xu N, Lu T, Chen J, Penuelas J, Hu BL, Qian HF (2022) Composition identification and functional verification of bacterial community in disease-suppressive soils by machine learning. Environ Microbiol 10:1462–2920

    Google Scholar 

  • Zhao Y, Liang C, Shao S, Chen J, Qin H, Xu Q (2021) Linkages of litter and soil C: N: P stoichiometry with soil microbial resource limitation and community structure in a subtropical broadleaf forest invaded by Moso bamboo. Plant Soil 465:473–490

    Article  CAS  Google Scholar 

  • Zhou LK (1987) Soil enzymology. Science and Technology Press Beijing China

    Google Scholar 

Download references

Funding

This work was supported by the Natural Science Foundation of China (32171743) and Talent Program of the Hangzhou Normal University (2016QDL020).

Author information

Authors and Affiliations

  1. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 311121, China

    Yang Zhao, Liangliang Chen, Qihang Yang & Miao Liu

  2. Guangdong Solid Waste and Chemicals Environmental Centre, Guangdong, 511356, China

    Yankai Chen

Authors
  1. Yang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liangliang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yankai Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qihang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yang Zhao was mainly responsible for data collection, analysis, and writing; Liangliang Chen, Yankai Chen and Qihang Yang contributed to data collection; and Miao Liu (the corresponding author) was responsible for the experimental design and project management.

Corresponding author

Correspondence to Miao Liu.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Chen, L., Chen, Y. et al. Plant sexual variation modulates rhizospheric nutrient processes through the soil microbiome response to drought and rewetting in Populus cathayana. Biol Fertil Soils 59, 571–587 (2023). https://doi.org/10.1007/s00374-023-01721-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-023-01721-9

Keywords

Search

Navigation