Skip to main content

Advertisement

SpringerLink
Log in

Dysbiosis of the rhizosphere microbiome caused by γ-irradiation alters the composition of root exudates and reduces phosphorus uptake by rice in flooded soils

  • Research Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Purpose

The response of rice (Oryza sativa L.) plants to phosphorus (P) deficiency and to alterations in the rhizosphere microbiome in flooded soils remains unexplored. We aimed to identify the association between alterations in bacterial diversity and underground metabolic and chemical reactions in the rhizosphere in P-deficient and γ-irradiated conditions.

Methods

Two rice varieties were grown in a split-root box under flooded conditions and filled with either P-applied or non-P-applied soils with or without γ-irradiation. At 41–42 days after transplanting, we determined plant biomass, P uptake, exudation rates of total carbon and low-molecular-weight organic acids (LMWOAs) from the roots, and bacterial diversity, P fractions, and phosphatase activity in the rhizosphere.

Results

γ-irradiation significantly decreased the P uptake and biomass of both rice varieties and reduced the relative abundance of Alphaproteobacteria and microbiome beta diversity in the rhizosphere. Concurrently, γ-irradiation reduced the uptake of insoluble P from soils. These microbiological and chemical changes in the γ-irradiated rhizosphere occurred irrespective of the P treatments of soils. On the contrary, the proportion of LMWOAs and citric acid exudation, which have a high P-solubilization capacity, increased in the γ-irradiated and P-applied rhizosphere soils at the expense of other carbons. No differences were detected in phosphatase activity in any treatments.

Conclusion

Dysbiosis of the rhizosphere microbiome negatively affected rice growth and the uptake of insoluble P in flooded soils. With a reduction in microbiome diversity, rice plants may have a complementary strategy to increase the proportion of citric acid exudation toward the P-rich soil area.

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

Similar content being viewed by others

Data availability

The sequences generated in this study were deposited in DDBJ under the BioProject PRJDB13616 with DRA accession number DRA014197. The other datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aulakh MS, Wassman R, Bueno C, Rennenberg H (2001) Impact of root exudates of different cultivars and plant development stages of rice (Oryza sativa L.) on methane production in a paddy soil. Plant Soil 230:77–86

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya P, Das S, Adhya TK (2013) Root exudates of rice cultivars affect rhizospheric phosphorus dynamics in soils with different phosphorus statuses. Commun Soil Sci Plant Anal 44:1643–1658

    Article  CAS  Google Scholar 

  • Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46

    Article  CAS  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I, Hengeler C, Marshner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250

    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 

  • Castrillo G, Teixeira PJ, Paredes SH, Law TF, de Lorenzo L, Feltcher ME, Finkel OM, Breakfield NW, Mieczkowski P, Jones CD et al (2017) Root microbiota drive direct integration of phosphate stress and immunity. Nature 543:513–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol Biochem 34:487–499

    Article  CAS  Google Scholar 

  • Chen T, Nomura K, Wang X, Sohrabi R, Xu J, Lingya Y, Paasch BC, Ma L, Kremer J, Cheng Y, Zhang L, Wang N, Wang E, Xin XF, He SY (2020) A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580:653–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    Article  CAS  PubMed  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  CAS  Google Scholar 

  • Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–E920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903

    Article  CAS  Google Scholar 

  • Hayes JE, Richardson AE, Simpson RJ (2000) Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase. Biol Fertil Soil 32:279–286

    Article  CAS  Google Scholar 

  • He Y, Liao H, Yan X (2003) Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248:247–256

    Article  CAS  Google Scholar 

  • Hedley MJ, Kirk GJR, Santos MB (1994) Phosphorus efficiency and the forms of soil phosphorus utilized by upland rice cultivars. Plant Soil 158:53–62

    Article  CAS  Google Scholar 

  • Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O'Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffland E, Wei C, Wissuwa M (2006) Organic anion exudation by lowland rice (Oryza sativa L.) at zinc and phosphorus deficiency. Plant Soil 283:155–162

    Article  CAS  Google Scholar 

  • Johnson SE, Loeppert RH (2006) Role of organic acids in phosphate mobilization from iron oxide. Soil Sci Soc Am J 70:222–234

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere–a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595

    Article  CAS  Google Scholar 

  • Khan AA, Jilani G, Akhtar MS, Naqvi SMS, Rasheed M (2009) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci 1:48–58

    Google Scholar 

  • Kirk GJD, Santo EE, Santos MB (1999) Phosphate solubilization by organic anionexcretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake. New Phytol 142:185–200

    Article  CAS  Google Scholar 

  • Kochian LV (2012) Rooting for more phosphorus. Nature 488:466–467

    Article  CAS  PubMed  Google Scholar 

  • Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biolo Biochem 27:1353–1357

    Article  CAS  Google Scholar 

  • Kpomblekou-A K, Tabatabai MA (2003) Effect of low-molecular weight organic acids on phosphorus release and phytoavailabilty of phosphorus in phosphate rocks added to soils. Agric Ecosyst Environ 100:275–284

    Article  CAS  Google Scholar 

  • Lee SM, Kong HG, Song GC, Ryu CM (2021) Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME J 15:330–347

    Article  CAS  PubMed  Google Scholar 

  • Lidbury IDEA, Murphy ARJ, Scanlan DJ, Bending GD, Jones AME, Moore JD, Goodal MA, Hammond JP, Wellington EM (2016) Comparative genomic, proteomic and exoproteomic analyses of three Pseudomonas strains reveals novel insights into the phosphorus scavenging capabilities of soil bacteria. Environ Microbiol 18:3535–3549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Ma W, Kou D, Niu X, Wang T, Chen Y, Chen D, Zhu X, Zhao M, Hao B, Zhang J, Yang Y, Hu H (2020) A comparison of patterns of microbial C: N: P stoichiometry between topsoil and subsoil along an aridity gradient. Biogeosciences 17:2009–2019

    Article  CAS  Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237

    Article  CAS  Google Scholar 

  • Mackill DJ, Khush GS (2018) IR64: A high-quality and high-yielding mega variety. Rice 11:1–11

    Article  Google Scholar 

  • Mažylytė R, Kaziūnienė J, Orola L, Valkovska V, Lastauskienė E, Gegeckas A (2022) Phosphate solubilizing microorganism bacillus sp. MVY-004 and its significance for biomineral fertilizers’ development in agrobiotechnology. Biology 11:254

    Article  PubMed  PubMed Central  Google Scholar 

  • McKeague JA, Brydon JE, Miles NM (1971) Differentiation of forms of extractable iron and aluminum in soils. Soil Sci Soc Am J 35:33–38

    Article  CAS  Google Scholar 

  • McNamara NP, Black HIJ, Beresford NA, Parekh NR (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24:117–132

    Article  Google Scholar 

  • Mitra D, Mondal R, Khoshru B, Senapati A, Radha TK, Mahakur B, Uniyal N, MyoEM BH, Guerra Sierra BE et al (2022) Actinobacteria-enhanced plant growth, nutrient acquisition, and crop protection: advances in soil, plant, and microbial multifactorial interactions. Pedosphere 32:149–170

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chem Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nestler J, Wissuwa M (2016) Superior root hair formation confers root efficiency in some, but not all, rice genotypes upon P deficiency. Front Plant Sci 7:1–13

    Article  Google Scholar 

  • Oburger E, Jones DL, Wenzel WW (2011) Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant Soil 341:363–382

    Article  CAS  Google Scholar 

  • Oo AZ, Tsujimoto Y, Mukai M, Nishigaki T, Takai T, Uga Y (2021) Synergy between a shallow root system with a DRO1 homologue and localized P application improves P uptake of lowland rice. Sci Rep 11:1–10

    Article  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian H, Zhu Y, Chen S, Jin Y, Lavoie M, Ke M, Fu Z (2018) Interacting effect of diclofop-methyl on the rice rhizosphere microbiome and denitrification. Pestic Biochem Physiol 146:90–96

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rakotoson T, Tsujimoto Y, Nishigaki T (2022) Phosphorus management strategies to increase lowland rice yields in sub-Saharan Africa: A review. Field Crop Res 275:108370

    Article  Google Scholar 

  • Richardson AE (2009) Regulating the phosphorus nutrition of plants: molecular biology meeting agronomic needs. Plant Soil 322:17–24

    Article  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  Google Scholar 

  • Rose TJ, Impa SM, Rose MT, Pariasca-Tanaka J, Mori A, Heuer S, Johnson-Beebout SE, Wissuwa (2013) Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding. Ann Bot 112: 331–345

  • Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mBio 7:e01395–e01315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross GJ, Wang C (1993) Extractable Al, Fe, Mn, and Si. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, Boca Raton, pp 239–246

    Google Scholar 

  • Seeling B, Zasoski RJ (1993) Microbial effects in maintaining organic and inorganic solution phosphorus concentrations in a grassland topsoil. Plant Soil 148:277–284

    Article  CAS  Google Scholar 

  • Singh G, Mukerji KG (2006) Root exudates as determinant of rhizospheric microbial biodiversity. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizoshere, Soil Biol, vol 7. Springer, Berlin, pp 39–53

    Chapter  Google Scholar 

  • Song Y, Wilson AJ, Zhang XC et al (2021) FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat Plant 7:644–654

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tinker PBH, Nye PH (2000) Solute transport in the rhizosphere. Oxford University Press, Oxford

    Google Scholar 

  • Tsujimoto Y, Sakata M, Raharinivo V, Tanaka JP, Takai T (2021) AZ-97 (Oryza sativa ssp. Indica) exhibits superior biomass production by maintaining the tiller numbers, leaf width, and leaf elongation rate under phosphorus deficiency. Plan Prod Sci 24:41–51

    Article  CAS  Google Scholar 

  • Uren NC (2000) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil plant interface. Marcel Dekker, Inc, New York, pp 19–40

    Google Scholar 

  • Utami YD, Kuwahara H, Igai K, Murakami T, Sugaya K et al (2019) Genome analyses of uncultured TG2/ZB3 bacteria in ‘Margulisbacteria’ specifically attached to ectosymbiotic spirochetes of protists in the termite gut. ISME J 13:455–467

    Article  CAS  PubMed  Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  CAS  Google Scholar 

  • Wehr JB, Kirchhof G (2021) Gamma irradiation with 50 kGy has a limited effect on agronomic properties of air-dry soil. Soil Syst 5:28

    Article  CAS  Google Scholar 

  • Wissuwa M (2005) Combining a modelling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake. Plant Soil 269:57–68

    Article  CAS  Google Scholar 

  • Wissuwa M, Ae N (2001) Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant Soil 237:275–286

    Article  CAS  Google Scholar 

  • Xiong J, Lu J, Li X, Qiu Q, Chen J, Yan C (2021) Effect of rice (Oryza sativa L.) genotype on yield: evidence from recruiting spatially consistent rhizosphere microbiome. Soil Biol Biochem 161:108395

    Article  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Routine procedure for growing rice plants in culture solution. In: Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Los Baños pp. 61–66

  • Zhang FS, Ma J, Cao YP (1997) Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raghanus satiuvs L.) and rape (Brassica napus L.) plants. Plant Soil 196:261–264

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Takuma Ishizaki and Dr. Hiroki Saito, for supporting the experimental soil collection and Dr. Matthias Wissuwa for providing us with valuable comments and suggestions to improve the draft of this manuscript. We are grateful to Dr. Tetsuro Kikuchi and Ms. Mayumi Yonemura who helped during soil and plant chemical analysis. We are also grateful to Dr. Chika Tateda and Ms. Akemi Uchiyama for technical assistance with the microbial experiments.

Funding

This work was supported by the Japan Society for Promotion of Science (JSPS) KAKENHI (Grant Numbers [19KK0154], [21H05150] and [20H02986]), the CGIAR Research Program on Rice Agri-Food Systems (RICE), and Science and Technology Research Partnership for Sustainable Development (SATREPS), Japan Science and Technology Agency (JST)/Japan International Cooperation Agency (JICA) (grant number [JPMJSA1608]).

Author information

Authors and Affiliations

  1. Japan International Research Center for Agricultural Sciences, 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan

    Mana Mukai, Tomohiro Nishigaki, Junnosuke Otaka, Tadashi Yoshihashi, Papa Saliou Sarr, Aung Zaw Oo, Toshiyuki Takai & Yasuhiro Tujimoto

  2. Faculty of Life and Environmental Sciences, University of Yamanashi, 4-4-37 Takeda, Kofu, 400-8510, Japan

    Mana Mukai

  3. Department of Life Science, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902, Japan

    Kei Hiruma & Yuniar Devi Utami

Authors
  1. Mana Mukai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kei Hiruma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomohiro Nishigaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuniar Devi Utami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junnosuke Otaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tadashi Yoshihashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Papa Saliou Sarr
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Aung Zaw Oo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toshiyuki Takai
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yasuhiro Tujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YT, MM, TN, TT designed the study and MM, YT, AZO, and TN performed field sampling. Data collections and analysis in the laboratories were performed by MM, YDU, JO, TY, PSS. The first draft of the manuscript was written by MM, YT, KH and all authors reviewed, revised and approved the articles.

Corresponding authors

Correspondence to Kei Hiruma or Yasuhiro Tujimoto.

Ethics declarations

Competing interests

The authors have no conflicts of interest to declare.

Additional information

Responsible Editor: Amandine Erktan.

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 3625 kb)

Rights and permissions

Springer Nature or its licensor 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

Mukai, M., Hiruma, K., Nishigaki, T. et al. Dysbiosis of the rhizosphere microbiome caused by γ-irradiation alters the composition of root exudates and reduces phosphorus uptake by rice in flooded soils. Plant Soil (2022). https://doi.org/10.1007/s11104-022-05726-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11104-022-05726-5

Keywords

Search

Navigation