Skip to main content

Advertisement

Log in

The contribution of plant traits and soil microbes to phosphorus uptake from low-phosphorus soil in upland rice varieties

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

Abstract

Aims

Popular African upland rice variety Nerica4 performs poorly under phosphorus (P) deficiency; the objective was to identify plant and soil traits likely to improve its P efficiency.

Methods

Field and glasshouse experiments compared P uptake and root parameters between the popular rice genotype Nerica4, and a known P-efficient genotype, DJ123. Glasshouse experiments used fresh field soil, sterilized soil and sterilized soil resupplied with 15% fresh field soil to assess microbial effects.

Results

DJ123 had faster crown root development and higher proportions of fine roots, leading to larger root surface area (RSA). Additionally, it acquired more P per RSA, thus had more efficient roots. Higher root efficiency of DJ123 compared to Nerica4 was detected in fresh field soil, sterile soil, and sterile+resupplied soil, indicating that plant-specific factors rather than soil microbiome effects explained higher root efficiency in DJ123. In non-sterile soils both genotypes were colonized by arbuscular mycorrhizal fungi (AMF), and high expression of an AMF-induced rice P transporter gene (OsPT11) indicated the symbiosis was functional.

Conclusions

We identified plant traits present in DJ123 such as rapid crown root development, higher proportions of fine lateral roots, as well as superior overall root efficiency that make it a promising donor to improve the performance of Nerica4 in P-deficient environments. In addition, Nerica4 appears more susceptible to growth-inhibitory effects of the soil microbiome.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AMF:

Arbuscular mycorrhizal fungi

DAE:

Days after emergence

DAS:

Days after sowing

RE:

Root efficiency

RSA:

Root surface area

References

  • Ashizawa T, Takahashi M, Moriwaki J, Hirayae K (2010) Quantification of the rice false smut pathogen Ustilaginoidea virens from soil in Japan using real-time PCR. Eur J Plant Pathol 128:221–232

    Article  CAS  Google Scholar 

  • Atakora WK, Fosu M, Abebrese SO, Asanta M, Wissuwa M (2015) Evaluation of low phosphorus tolerance of rice varieties in northern Ghana. Sust Agric Res 4:109–114. https://doi.org/10.5539/sar.v4n4p109

    Article  Google Scholar 

  • Balasubramanian V, Sie M, Hijmans RJ, Otsuka K (2007) Increasing Rice production in sub-Saharan Africa: challenges and opportunities. Adv Agron 94:55–133

    Article  CAS  Google Scholar 

  • Chen XW, Wu FY, Li H, Chan WF, Wu C, Wu SC, Wong MH (2013) Phosphate transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenate stress. J Exp Bot 87:92-99. doi.org/https://doi.org/10.1016/j.envexpbot.2012.08.002

  • Cruz-Paredes C, Svenningsen NB, Nybroe O, Kjøller R, Frøslev TG, Jakobsen I (2019) Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiol Ecol 95. https://doi.org/10.1093/femsec/fiz020

  • Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant Soil 198:147–152

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B, (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500

  • Grønlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I (2013) The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plantarum 149:234–248

    Article  CAS  Google Scholar 

  • Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza–specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20. https://doi.org/10.1105/tpc.108.062414

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

    Article  CAS  Google Scholar 

  • Inukai Y, Miwa M, Nagato Y, Kitano H, Yamauchi A (2001) Characterization of rice mutants deficient in the formation of crown roots. Breeding Sci 51:123–129

    Article  CAS  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    Article  CAS  Google Scholar 

  • Kirk GJD, George T, Courtois B, Senadhira D (1998) Opportunities to improve phosphorus efficiency and soil fertility in rainfed lowland and upland rice ecosystems. Field Crop Res 56:73–92

    Article  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 211:11–18

    Article  CAS  Google Scholar 

  • Koide Y, Pariasca Tanaka J, Rose T, Fukuo A, Konisho K, Yanagihara S, Fukuta Y, Wissuwa M (2013) QTLs for phosphorus-deficiency tolerance detected in upland NERICA varieties. Plant Breed. https://doi.org/10.1111/pbr.12052

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    Article  CAS  Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56

    Article  CAS  Google Scholar 

  • Maiti D, Variar M, Singh RK (2011) Optimizing tillage schedule for maintaining activity of the arbuscular mycorrhizal fungal population in a rainfed upland rice (Oryza sativa L.) agro-ecosystem. Mycorrhiza 21(3):167–171

  • Mbodj D, Effa-Effa B, Kane A, Manneh B, Gantet P, Laplaze L, Diedhiou AG, Grondin A (2018) Arbuscular mycorrhizal symbiosis in rice: establishment, environmental control and impact on plant growth and resistance to abiotic stresses. Rhizosphere 8:12–26

    Article  Google Scholar 

  • Mori A, Fukuda T, Vejchasarn P, Nestler J, Pariasca-Tanaka J, Wissuwa M (2016a) The role of root size versus root efficiency in phosphorus (P) acquisition of rice. J Exp Bot. https://doi.org/10.1093/jxb/erv557

  • Mori A, Kirk GJD, Lee JS, Morete MJ, Nanda AK, Johnson-Beebout SE, Wissuwa M (2016b) Rice genotype differences in tolerance of zinc-deficient soils: evidence for the importance of root-induced changes in the rhizosphere. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.01160

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

  • Nanda AK, Wissuwa M (2016) Rapid crown root development confers tolerance to zinc deficiency in rice. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00428

  • Nanda AK, Puyol V, Wissuwa M (2017) Patterns of stress response and tolerance based on transcriptome profiling of rice crown tissue under Zn deficiency. J Exp Bot. https://doi.org/10.1093/jxb/erx039

  • Nestler J, Wissuwa M (2016) Superior root hair formation confers root efficiency in some, but not all, rice (Oryza sativa) genotypes upon P deficiency. Front Plant Sci 7:1935. https://doi.org/10.3389/fpls.2016.01935

    Article  PubMed  PubMed Central  Google Scholar 

  • Nestler J, Keyes SD, Wissuwa M (2016) Artificial growth conditions alter root hair formation on rice (Oryza sativa L.) root types. J Exp Bot 67:3699–3708. https://doi.org/10.1093/jxb/erw115

    Article  PubMed  CAS  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 99:13324–13329

    Article  CAS  Google Scholar 

  • Rakotoson T (2014) Overcoming phosphate deficiency in flooded rice in Madagascar. Ph.D. dissertation, KU Leuven

  • Rebouillat A, Dievart A, Verdeil JL, Escoute J, Giese G, Breitler JC, Gantet P, Espeout S, Guiderdoni E, Périn C (2009) Molecular genetic of rice root development. Rice 2:15–34

    Article  Google Scholar 

  • Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869

    Article  CAS  Google Scholar 

  • Ruíz-Sánchez M, Armada E, Muñoz Y, García de Salamone IE, Aroca R, Ruíz-Lozano JM, Azcón R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168:1031–1037

    Article  CAS  Google Scholar 

  • Saito K, Asai H, Zhao D, Laborte AG, Greiner C (2018) Progress in varietal improvement for increasing upland rice productivity in the tropics. Plant Prod Sci 21:145–158

    Article  Google Scholar 

  • Saito K, Vandamme E, Johnson JM et al (2019) Yield-limiting macronutrients for rice in sub-Saharan Africa. Geoderma 338:546–554

    Article  CAS  Google Scholar 

  • Sesma A, Osbourn AE (2004) The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431:582–586

    Article  CAS  Google Scholar 

  • Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:130

    Article  Google Scholar 

  • Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I (2018) Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J 12:1296–1307. https://doi.org/10.1038/s41396-018-0059-3

  • 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 phosphorus deficiency. J Plant Nutr 36:1138–1159

    Article  CAS  Google Scholar 

  • Vandamme E, Wissuwa M, Rose TJ, Dieng I, Drame KN, Fofana M, Senthilkumar K, Venuprasad R, Jallow D, Segda Z, Suriyagoda L, Sirisena D, Kato Y, Saito K (2016) Genotypic variation in grain P loading across diverse rice growing environments and implications for field P balances. Front Plant Sci 7:1435. https://doi.org/10.3389/fpls.2016.01435

    Article  PubMed  PubMed Central  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and Vinegar, a Simple Staining Technique for Arbuscular-Mycorrhizal Fungi. ‎Appl Environ Microbiol 64(12):5004–5007

  • Watts-Williams SJ, Jakobsen I, Cavagnaro TR, Grønlund M (2015) Local and distal effects of arbuscular mycorrhizal colonization on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot 66:4061–4073

  • Wissuwa M (2003) How do plants achieve tolerance to phosphorus deficiency - small causes with big effects. Plant Physiol 133:1947–1958

    Article  CAS  Google Scholar 

  • Wissuwa M, Ae N (2001) Genotypic variation for tolerance to phosphorus deficiency in Rice and the potential for its exploitation in Rice improvement. Plant Breed 120:43–48

    Article  CAS  Google Scholar 

  • Wissuwa M, Kretzschmar T, Rose TJ (2016) From promise to application: root traits for enhanced nutrient capture in rice breeding. J Exp Bot 67:3605–3615

    Article  CAS  Google Scholar 

  • Yamauchi A, Kono Y, Tatsumi J (1987) Quantitative analysis on root system structures of upland rice and maize. JPN J Crop Sci 56:608–617

    Article  Google Scholar 

  • Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24:4236–4251

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Authors acknowledge the excellent technical assistance of Taro Matsuda in the qPCR analysis. Scans of root images used for the measurements of root properties shown in Table 3 were provided by James DM King. Financial support in the form of a CONACYT – I2T2 scholarship to DG is acknowledged. SJWW acknowledges the University of Adelaide Ramsay Fellowship for support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthias Wissuwa.

Additional information

Responsible Editor: Andrea Schnepf.

Publisher’s note

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

Highlight

Efficient P uptake by rice is explained by genotypic differences in root traits and rhizosphere effects, even in the presence of an active mycorrhizal symbiosis

Electronic supplementary material

ESM 1

(DOCX 14 kb)

ESM 2

(PDF 138 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wissuwa, M., Gonzalez, D. & Watts-Williams, S.J. The contribution of plant traits and soil microbes to phosphorus uptake from low-phosphorus soil in upland rice varieties. Plant Soil 448, 523–537 (2020). https://doi.org/10.1007/s11104-020-04453-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04453-z

Keywords

Navigation