Skip to main content
SpringerLink
Log in

Cadmium uptake via apoplastic bypass flow in Oryza sativa

  • Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

It is known that rice roots take up cadmium (Cd) via the symplastic route mediated by membrane-bound mineral transporters. Here we provide evidence that apoplastic bypass flow is another Cd uptake route in rice. High concentrations of Cd rendered apoplastic bypass flow rate increased in rice seedlings. These concentrations of Cd compromised membrane integrity in the root meristem and transition zone. Polyethleneglycol and proline inhibited the Cd-induced apoplastic bypass flow and Cd transfer to the shoots. Loss-of-function mutant of the Cd uptake transporter, nramp5, showed Cd transport to the shoot comparable to the wild type. At a low Cd concentration, increased apoplastic bypass flow rate by NaCl stress resulted in an elevation of Cd transport to shoots both in the wildtype and nramp5. These observations indicate that apoplastic bypass flow in roots carries Cd transport leading to xylem loading of Cd in addition to the symplastic pathway mediated by mineral transporters under stressed conditions.

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

Similar content being viewed by others

References

  • Bertin G, Averbeck D (2006) Cadmium: Cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88:1549–1559

    Article  CAS  Google Scholar 

  • Brundrett MC, Enstone DE, Peterson CA (1988) A berberine-aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146:133–142

    Article  Google Scholar 

  • Clemens S, Aarts MGM, Thomie S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: Staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280

    Article  CAS  Google Scholar 

  • Faiyue B, Vijayalakshmi C, Nawaz S, Nagato Y, Taketa S, Ichii M, Al-Azzawi MJ, Flowers TJ (2010a) Studies on sodium bypass flow in lateral rootless mutants lrt1 and lrt2, and crown rootless mutant crl1 of rice (Oryza sativa L.). Plant Cell Environ 33:687–701

    CAS  PubMed  Google Scholar 

  • Faiyue B, Al-Azzawi MJ, Flowers TJ (2010b) The role of lateral roots in bypass flow in rice (Oryza sativa L.). Plant Cell Environ 33:702–716

    CAS  PubMed  Google Scholar 

  • Flam-Shepherd R, Huynh WQ, Coskun D, Hamam AM, Britto DT, Kronzucker HJ (2018) Membrane fluxes, bypass flows, and sodium stress in rice: the influence of silicon. J Exp Bot 69:1679–1692

    Article  CAS  Google Scholar 

  • Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian J Plant Physiol 22:875–884

    Google Scholar 

  • Fritz M, Ehwald R (2013) Radial transport of salt and water in roots of the common reed (Phragmites australis Trin. ex Steudel). Plant Cell Environ 36:1860–1870

    Article  CAS  Google Scholar 

  • Garcia A, Rizzo CA, Ud-Din J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR (1997) Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium: potassium selectivity differs between rice and wheat. Plant Cell Environ 20:1167–1174

    Article  CAS  Google Scholar 

  • Greger M, Johansson M (1992) Cadmium effects on leaf transpiration of sugar beet (Beta vulgaris). Physiol Plant 86:465–473

    Article  CAS  Google Scholar 

  • Hirayama T, Lei GJ, Yamaji N, Nakagawa N, Ma JF (2018) The putative peptide gene FEP1 regulates iron deficiency response in Arabidopsis. Plant Cell Physiol 59:1739–1752

    Article  CAS  Google Scholar 

  • Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346

    Article  CAS  Google Scholar 

  • Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Screiber L, Mathew MK (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230:119–134

    Article  CAS  Google Scholar 

  • Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228

    Article  CAS  Google Scholar 

  • Li J, Zhu S, Song X, Shen Y, Chen H, Yu J, Yi K, Liu Y, Karplus VJ, Wu P, Deng XW (2006) A rice glutamate receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–349

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:951–981

    Article  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru U, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469

    Article  CAS  Google Scholar 

  • Nawrot T, Plusquin M, Hogevorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7:119–126

    Article  CAS  Google Scholar 

  • Ochiai K, Matoh T (2002) Characterization of the Na+ delivery from roots to shoots in rice under saline stress: excessive salt enhances apoplastic transport in rice plants. Soil Sci Plant Nutr 43:371–337

    Article  Google Scholar 

  • Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: Identification and characterization of the metal ion transporter HIRT1. Plant Physiol 148:455–466

    Article  CAS  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Envir Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Qi X, Tam NF, WC L, Ye Z (2020) The role of root apoplastic barriers in cadmium translocation and accumulation in cultivars of rice (Oryza sativa L.) with different Cd-accumulating characteristics. Environ Pollut 254:1147736

    Google Scholar 

  • Ranathunge K, Steudle E, Laritte R (2005) Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. Plant Cell Environ 28:121–133

    Article  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  Google Scholar 

  • Shah K, Dubey RS (1997) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enxyme protectant. Biol Plant 40:121–130

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2006) The significance of amino acid and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  Google Scholar 

  • Sobahan MA, Arias CR, Okuma E, Shimoishi Y, Nakamura Y, Hirai Y, Mori IC, Murata Y (2009) Exogenous proline and glycinebetaine suppress apoplastic flow to reduce Na+ uptake in rice seedlings. Biosci Biotechnol Biochem 73:2037–2042

    Article  CAS  Google Scholar 

  • Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182:644–653

    Article  CAS  Google Scholar 

  • Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107:16500–16505

    Article  CAS  Google Scholar 

  • UNEP (United Nations Environmental Programme) (2008) Draft final review of scientific information on cadmium. http://www.chem.unep.ch/Pb_and_Cd/SR/Draft_final_reviews/Cd_Review/Final_UNEP_Cadmium_review_Nov_2008.pdf. Accessed 30 Sept 2018

  • Van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947

    Article  Google Scholar 

  • Yadav R, Flowers TJ, Yeo AR (1996) The involvement of the transpirational bypass flow in sodium uptake by high- and low-sodium-transporting lines of rice developed through intravarietal selection. Plant Cell Environ 19:329–336

    Article  CAS  Google Scholar 

  • Yan GC, Fan XP, Tan L, Yin C, Li TQ, Liang YC (2021) Root silicon deposition and its resultant reduction of sodium bypass flow is modulated by OsLsi1 and OsLsi2 in rice. Plant Physiol Biochem 158:219–227

    Article  CAS  Google Scholar 

  • Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an apoplastic pathway to sodium uptake by rice roots in saline condition. J Exp Bot 38:1141–1153

    Article  CAS  Google Scholar 

  • Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ 22:559–565

    Article  CAS  Google Scholar 

  • Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34:D745–D748

    Article  CAS  Google Scholar 

Download references

Acknowledgements

ICP analysis and histochemical analysis were helped by Ms. Sanae Rikiishi and Ms. Chiemi Hasegawa (Institute of Plant Science and Resource, Okayama University). The authors thank Dr. Jian Feng Ma and Rice Mutant Database for providing the mutant seeds. This study was funded by The Japan Society for the Promotion of Science KAKENHI (17078006 to Y.M. and I.C.M).

Author information

Authors and Affiliations

  1. Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, Kurashiki, 710-0046, Japan

    Izumi C. Mori, Carlos Raul Arias-Barreiro & Lia Ooi

  2. Department of Life Sciences, Faculty of Science and Engineering, Sorbonne University, 4 place Jussieu, 75005, Paris, France

    Nam-Hee Lee

  3. Graduate School of Environmental and Life Science, Okayama University, 1-1-1 Tsushima-naka, Kita-ku, Okayama, 700-8530, Japan

    Muhammad Abdus Sobahan, Yoshimasa Nakamura, Yoshihiko Hirai & Yoshiyuki Murata

Authors
  1. Izumi C. Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos Raul Arias-Barreiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lia Ooi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nam-Hee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Abdus Sobahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshimasa Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yoshihiko Hirai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yoshiyuki Murata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Izumi C. Mori.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 9776 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mori, I.C., Arias-Barreiro, C.R., Ooi, L. et al. Cadmium uptake via apoplastic bypass flow in Oryza sativa. J Plant Res 134, 1139–1148 (2021). https://doi.org/10.1007/s10265-021-01319-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-021-01319-y

Keywords

Search

Navigation