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Multiple analysis of root exudates and microbiome in rice (Oryza sativa) under low P conditions

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Abstract

Plants release various metabolites from roots and root exudates contribute to differences in stress tolerance among plant species. Plant and soil microbes have complex interactions that are affected by biotic and abiotic factors. The purpose of this study was to examine the differences in metabolites in root exudates of rice (Oryza sativa) cultivars and their correlation with bacterial populations in the rhizosphere. Two rice cultivars (O. sativa cv. Akamai and O. sativa cv. Koshihikari) were grown in soils fertilized with 0 g P kg−1 (− P) or 4.8 g P kg−1 (+ P). Root exudates and root-attached soil were collected at 13 and 20 days after transplanting (DAT) and their metabolites and bacterial community structure were determined. The exudation of proline, serine, threonine, valine and 4-coumarate were increased under low P conditions in both cultivars. There was a positive correlation between the concentration of pantothenate in root exudates and the representation of members of the genera Clostridium and Sporosarcina, which were negatively correlated with root dry weight. Gracilibacter, Opitutus, Pelotomaculum, Phenylobacterium and Oxobacter were positively correlated with root dry weight and presence of allantoin, 2-aminobtyrate and GlcNac. This study provides new information about the response of plants and rhizosphere soil bacteria to low P conditions.

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References

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Ankati S, Podile AR (2019) Metabolites in the root exudates of groundnut change during interaction with plant growth promoting rhizobacteria in a strain-specific manner. J Plant Physiol. https://doi.org/10.1016/j.jplph.2019.153057

    Article  PubMed  Google Scholar 

  • Annan FJ, Al-Sinawi B, Humphreys CM, Norman R, Winzer K, Kopke M, Simpson SD, Minton NP, Henstra AM (2019) Engineering of vitamin prototrophy in Clostridium ljungdahlii and Clostridium autoethanogenum. Appl Microbiol Biotechnol 103:4633–4648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, Bengtsson-Palme J, Anslan S, Coelho LP, Harend H, Huerta-Cepas J, Medema MH, Maltz MR, Mundra S, Olsson PA, Pent M, Polme S, Sunagawa S, Ryberg M, Tedersoo L, Bork P (2018) Structure and function of the global topsoil microbiome. Nature 560(7717):233–237

    Article  CAS  PubMed  Google Scholar 

  • Bargaz A, Lyamlouli K, Chtouki M, Zeroual Y, Dhiba D (2018) Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front Microbiol 9:1606

    Article  PubMed  PubMed Central  Google Scholar 

  • Barthelmebs L, Divies C, Cavin JF (2000) Knockout of the p-coumarate decarboxylase gene from Lactobacillus plantarum reveals the existence of two other inducible enzymatic activities involved in phenolic acid metabolism. Appl Environ Microbiol 66:3368–3375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bisanz JE (2018) qiime2R: importing QIIME2 artifacts and associated data into R sessions. https://github.com/jbisanz/qiime2R.

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wiren N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, P, potassium, and iron deficiency. J Plant Nutr Soil Sci 174:3–11

    Article  CAS  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of P: global food security and food for thought. Global Environ Change 19:292–305

    Article  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  • Devendran S, Shrestha R, Alves JMP, Wolf PG, Ly L, Hernandez AG, Mendez-Garcia C, Inboden A, Wiley J, Paul O, Allen A, Springer E, Wright CL, Fields CJ, Daniel SL, Ridlon JM (2019) Clostridium scindens ATCC 35704: integration of nutritional requirements, the complete genome sequence, and global transcriptional responses to bile acids. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00052-19

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding LJ, Su JQ, Xu HJ, Jia ZJ, Zhu YG (2015) Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-C-13-acetate probing coupled with pyrosequencing. Isme J 9:721–734

    Article  CAS  PubMed  Google Scholar 

  • Dinkelaker B, Romheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292

    Article  CAS  Google Scholar 

  • Dissanayaka D, Maruyama H, Nishida S, Tawaraya K, Wasaki J (2017) Landrace of japonica rice, Akamai exhibits enhanced root growth and efficient leaf P remobilization in response to limited P availability. Plant Soil 414:327–338

    Article  CAS  Google Scholar 

  • Feigel BJ, Knackmuss HJ (1988) Bacterial catabolism of sulfanilic acid via catechol-4-sulfonic acid. Fems Microbiol Lett 55:113–117

    Article  CAS  Google Scholar 

  • Fuchs G (2008) Anaerobic metabolism of aromatic compounds incredible anaerobes. Ann NY Acad Sci 1125:82–99

    Article  CAS  PubMed  Google Scholar 

  • Gilbert N (2009) Environment: the disappearing nutrient. Nature 461:716–718

    Article  CAS  PubMed  Google Scholar 

  • Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153

    Article  CAS  Google Scholar 

  • Hocking PJ (2001) Organic acid exuded from roots in phosphorus uptake and aluminium tolerance of plants in acid soils. Adv Agron 74(74):63–97

    Article  CAS  Google Scholar 

  • Hoffland E, Gunter R, Findenegg R, Nelemans JA (1989) Solubilization of rock phosphate by rape II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113:161–165

    Article  CAS  Google Scholar 

  • Hoffland E, Wei CZ, Wissuwa M (2006) Organic anion exudation by lowland rice (Oryza sativa L.) at zinc and phosphorus deficiency. Plant Soil 283(1–2):155–162

    Article  CAS  Google Scholar 

  • Johnson JF, Vance CP, Allan DL (1996) P deficiency in Lupinus albus—altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol 112:31–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk GJD, Santos EE, Findenegg GR (1999) Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211(1):11–18

    Article  CAS  Google Scholar 

  • Lahti L, Shetty S (2019) microbiome R package. http://microbiome.github.io

  • Lovley DR, Phillips EJP (1988) Novel mode of microbial energy-metabolism—organic-carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49(49):219–286

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5(2):169–172

    Article  PubMed  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient-uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    Article  CAS  Google Scholar 

  • McMurdie P, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohwaki Y, Hirata H (1992) Differences in carboxylic-acid exudation among p-starved leguminous crops in relation to carboxylic-acid contents in plant-tissues and phospholipid level in roots. Soil Sci Plant Nutr 38:235–243

    Article  CAS  Google Scholar 

  • Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36(5):841–848

    Article  CAS  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of rhizobium-meliloti nodulation genes. Science 233:977–980

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving P acquisition efficiency of crop plants. Field Crops Res 117:169–176

    Article  Google Scholar 

  • Reuter DJ, Edwards DG, Wilhelm NS (1997) Temperate and tropical crops. In: Reuter DJ, Robinson JB (eds) Plant analysis: an interpretation manual. CSIRO Publishing, Collingwood, pp 81–284

    Chapter  Google Scholar 

  • RStudio Team (2020) RStudio: Integrated development for R. RStudio, PBC, Boston, MA. http://www.rstudio.com/

  • Schachtman DP, Reid RJ, Ayling SM (1998) P uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segura D, Mahadevan R, Juarez K, Lovley DR (2008) Computational and experimental analysis of redundancy in the central metabolism of Geobacter sulfurreducens. Plos Comput Biol 4:e36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen JB, Yuan LX, Zhang JL, Li HG, Bai ZH, Chen XP, Zhang WF, Zhang FS (2011) P dynamics: from soil to plant. Plant Physiol 156:997–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic P mineralization can be stimulated by root exudates—a P-33 isotopic dilution study. Soil Biol Biochem 65:254–263

    Article  CAS  Google Scholar 

  • Tadano T, Sakai H (1991) Secretion of acid-phosphatase by the roots of several crop species under p-deficient conditions. Soil Sci Plant Nutr 37:129–140

    Article  CAS  Google Scholar 

  • Tawaraya K, Horie R, Saito A, Shinano T, Wagatsuma T, Saito K, Oikawa A (2013) Metabolite profiling of shoot extracts, root extracts, and root exudates of rice plant under p deficiency. J Plant Nutr 36:1138–1159

    Article  CAS  Google Scholar 

  • Tawaraya K, Horie R, Shinano T, Wagatsuma T, Saito K, Oikawa A (2014) Metabolite profiling of soybean root exudates under P deficiency. Soil Sci Plant Nutr 60:679–694

    Article  CAS  Google Scholar 

  • Tawaraya K, Honda S, Cheng W, Chuba M, Okazaki Y, Saito K, Oikawa A, Maruyama H, Wasaki J, Wagatsuma T (2018) Ancient rice cultivar extensively replaces phospholipids with non-P glycolipid under P deficiency. Physiol Plant 163:297–305

    Article  CAS  Google Scholar 

  • Wang P, Kong CH, Hu F, Xu XH (2007) Allantoin involved in species interactions with rice and other organisms in paddy soil. Plant Soil 296:43–51

    Article  CAS  Google Scholar 

  • Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008) Physiological roles of the beta-substituted alanine synthase gene family in arabidopsis. Plant Physiol 146(1):310–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang XF, Li L, Xu Y, Kong CH (2018) Kin recognition in rice (Oryza sativa) lines. New Phytol 220(2):567–578

    Article  CAS  PubMed  Google Scholar 

  • Yuwono T (2005) Metabolism of betaine as a carbon source by an osmotolerant bacterium isolated from the weed rhizosphere. World J Microbiol Biotechnol 21:69–73

    Article  CAS  Google Scholar 

  • Zhu XF, Wang ZW, Wan JX, Sun Y, Wu YR, Li GX, Shen RF, Zheng SJ (2015) Pectin enhances rice (Oryza sativa) root P remobilization. J Exp Bot 66:1017–1024

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Zhu CQ, Zhao XS, Zheng SJ, Shen RF (2016) Ethylene is involved in root P remobilization in rice (Oryza sativa) by regulating cell-wall pectin and enhancing phosphate translocation to shoots. Ann Bot 118:645–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was partly supported by a Grant-in-Aid for Scientific Research (No. 15H04466) from the Japan Society for the Promotion of Science (JSPS), the research project “Development of mitigation and adaptation techniques to global warming in the sectors of agriculture, forestry, and fisheries” funded by the Ministry of Agriculture, Forestry and Fisheries (MAFF), and Japan Advanced Plant Science Network, Japan.

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Author notes

  1. Matthew Shenton

    Present address: Institute of Crop Science, National Agriculture and Food Research Organization (NARO), Tsukuba, 305-8518, Japan

  2. Chisato Matsushima and Matthew Shenton have contributed equally to this research.

Authors and Affiliations

  1. Faculty of Agriculture, Yamagata University, Tsuruoka, 997-8555, Japan

    Chisato Matsushima, Ayaka Kitahara, Akira Oikawa, Weiguo Cheng & Keitaro Tawaraya

  2. Plant Genetics Laboratory, National Institute of Genetics, Mishima, 411-8540, Japan

    Matthew Shenton

  3. Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi, Hiroshima, 739-8521, Japan

    Jun Wasaki

  4. DNA Data Analysis Laboratory, National Institute of Genetics, Mishima, 411-8540, Japan

    Kazuho Ikeo

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Contributions

All authors contributed to the study conception and design. CM and MS contributed equally to this research. Material preparation, data collection, and analysis were performed by CM, MS, and AK. The first draft of the manuscript was written by CM, MS, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Keitaro Tawaraya.

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Communicated by Yusuf Akhter.

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Matsushima, C., Shenton, M., Kitahara, A. et al. Multiple analysis of root exudates and microbiome in rice (Oryza sativa) under low P conditions. Arch Microbiol 203, 5599–5611 (2021). https://doi.org/10.1007/s00203-021-02539-5

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