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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Fundamental parenchyma cells are involved in Na+ and Cl removal ability in rice leaf sheath

Sarin Neang A , Marjorie de Ocampo B , James A. Egdane B , John D. Platten B , Abdelbagi M. Ismail B , Nicola S. Skoulding A , Mana Kano-Nakata C , Akira Yamauchi A and Shiro Mitsuya https://orcid.org/0000-0003-2961-0454 A D
+ Author Affiliations
- Author Affiliations

A Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601, Japan.

B International Rice Research Institute, Los Baños, Laguna 4031, Philippines.

C Institute for Advanced Research, Nagoya University, Furo-cho, Chikusa-ku, 464-8601, Japan.

D Corresponding author. Email: mitsuya@agr.nagoya-u.ac.jp

Functional Plant Biology 46(8) 743-755 https://doi.org/10.1071/FP18318
Submitted: 10 December 2018  Accepted: 24 March 2019   Published: 3 May 2019

Abstract

Salt sensitivity in rice plants is associated with the accumulated amount of Na+ and Cl in shoots and, more significantly, in photosynthetic tissues. Therefore, salt removal ability at the leaf sheath level is an important mechanism of salt tolerance. In the present study we attempted to determine whether rice leaf sheaths excluded Cl as well as Na+, and to identify the tissues that were involved in the removal ability of both ions. In two rice genotypes, salt-tolerant FL478 and -sensitive IR29, leaf sheaths excluded Na+ and Cl under NaCl treatment as estimated using their sheath : blade ratios. The sheath : blade ratio of Na+ but not of Cl, was increased by NaCl treatment. Under NaCl treatment, Na+ concentration was higher in the basal leaf sheath, whereas Cl concentration was higher in the middle and tip parts. At the tissue level, fundamental parenchyma cells of leaf sheaths retained the highest amounts of Na and Cl when treated with high amount of NaCl. These results imply that the leaf sheath potentially functions to remove excess Na+ and Cl from xylem vessels in different locations along the axis, with the fundamental parenchyma cells of leaf sheaths being involved in over-accumulation of both Na+ and Cl.

Additional keywords: energy dispersive X-ray spectroscopy, Oryza sativa, salt stress, salt tolerance.


References

Bonilla P, Dvorak J, Mackill D, Deal K, Gregorio G (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philippine Agricultural Scientist 85, 68–76.

Boursier P, Lynch J, Läuchli A, Epstein E (1987) Chloride partitioning in leaves of salt-stressed sorghum, maize, wheat and barley. Australian Journal of Plant Physiology 14, 463–473.

Chen ZC, Yamaji N, Fujii-Kashino M, Ma JF (2016) A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice. Plant Physiology 171, 494–507.
A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice.Crossref | GoogleScholarGoogle Scholar | 26983995PubMed |

Chonan N, Kawahara H, Matsuda T (1974) Morphology on vascular bundles of leaves in gramineous crops. Nihon Sakumotsu Gakkai Kiji 43, 425–432.
Morphology on vascular bundles of leaves in gramineous crops.Crossref | GoogleScholarGoogle Scholar |

Cotsaftis O, Plett D, Shirley N, Tester M, Hrmova M (2012) A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS One 7, e39865
A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing.Crossref | GoogleScholarGoogle Scholar | 22808069PubMed |

Davenport R, James RA, Zakrisson-plogander A, Tester M, Munns R (2005) Control of sodium transport in durum wheat. Plant Physiology 137, 807–818.
Control of sodium transport in durum wheat.Crossref | GoogleScholarGoogle Scholar | 15734907PubMed |

Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar | 17635215PubMed |

Fahn A (1990) Parenchyma. In ‘Plant anatomy’. 4th edn. (Ed. A Fahn) pp. 80–84. (Pergamon Press: Oxford)

Francois LE, Maas EV (1994) Crop response and management on salt-affected soils. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakli) pp. 149–181. (Marcel Dekker: New York)

Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant & Cell Physiology 45, 146–159.
Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice.Crossref | GoogleScholarGoogle Scholar |

Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233, 175–188.
Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes.Crossref | GoogleScholarGoogle Scholar | 20963607PubMed |

Gregorio GB (1997) Tagging salinity tolerance genes in rice using amplified fragment length polymorphism (AFLP). PhD thesis, University of the Philippines, Los Baños.

Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. International Journal of Genomics 2014, 1–18.
Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization.Crossref | GoogleScholarGoogle Scholar |

Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annual Review of Plant Biology 68, 405–434.
Genomics, physiology, and molecular breeding approaches for improving salt tolerance.Crossref | GoogleScholarGoogle Scholar | 28226230PubMed |

Ismail AM, Heuer S, Thomson MJ, Wissuwa M (2007) Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Molecular Biology 65, 547–570.
Genetic and genomic approaches to develop rice germplasm for problem soils.Crossref | GoogleScholarGoogle Scholar | 17703278PubMed |

Ismail AM, Singh US, Singh S, Dar MH, Mackill DJ (2013) The contribution of submergence-tolerant (sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. Field Crops Research 152, 83–93.
The contribution of submergence-tolerant (sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia.Crossref | GoogleScholarGoogle Scholar |

James RA, Davenport RJ, Munns R (2006) Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiology 142, 1537–1547.
Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2.Crossref | GoogleScholarGoogle Scholar | 17028150PubMed |

James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. Journal of Experimental Botany 62, 2939–2947.
Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions.Crossref | GoogleScholarGoogle Scholar | 21357768PubMed |

Khush GS, Virk PS (2005) IR29. In ‘IR varieties and their impact’. (Eds GS Khush, PS Virk) pp. 56–59. (International Rice Research Institute: Los Baños, Philippines)

Klagges S, Bhatti AS, Sarwar G, Hilpert A, Jeschke WD (1993) Ion distribution in relation to leaf age in Leptochloa fusca (L.) Kunth (Kallar Grass). II. Anions. New Phytologist 125, 521–528.
Ion distribution in relation to leaf age in Leptochloa fusca (L.) Kunth (Kallar Grass). II. Anions.Crossref | GoogleScholarGoogle Scholar |

Kobayashi NI, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T, Nayef MA, Shabala S, An G, Ma JF, Horie T (2017) OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. The Plant Journal 91, 657–670.
OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice.Crossref | GoogleScholarGoogle Scholar | 28488420PubMed |

Kong X-Q, Gao X-H, Sun W, An J, Zhao Y-X, Zhang H (2011) Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1. Plant Molecular Biology 75, 567–578.
Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1.Crossref | GoogleScholarGoogle Scholar | 21369877PubMed |

Läuchli A, James RA, Huang CX, McCully M, Munns R (2008) Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion. Plant, Cell & Environment 31, 1565–1574.
Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion.Crossref | GoogleScholarGoogle Scholar |

Li B, Byrt C, Qiu J, Baumann U, Hrmova M, Evrard A, Johnson AAT, Birnbaum KD, Mayo GM, Jha D, Henderson SW, Tester M, Gilliham M, Roy SJ (2016) Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiology 170, 1014–1029.
Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26662602PubMed |

Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Functional Plant Biology 31, 1105–1114.
A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat.Crossref | GoogleScholarGoogle Scholar |

Matoh T, Watanabe J, Takahashi E (1987) Sodium, potassium, chloride, and betaine concentrations in isolated vacuoles from salt-grown Atriplex gmelini leaves. Plant Physiology 84, 173–177.
Sodium, potassium, chloride, and betaine concentrations in isolated vacuoles from salt-grown Atriplex gmelini leaves.Crossref | GoogleScholarGoogle Scholar | 16665393PubMed |

Mitsuya S, Yano K, Kawasaki M, Taniguchi M, Miyake H (2002) Relationship between the distribution of Na and the damages caused by salinity in the leaves of rice seedlings grown under a saline condition. Plant Production Science 5, 269–274.
Relationship between the distribution of Na and the damages caused by salinity in the leaves of rice seedlings grown under a saline condition.Crossref | GoogleScholarGoogle Scholar |

Moradi F, Ismail AM, Gregorio G, Egdane JA (2003) Salinity tolerance of rice during reproductive development and association with tolerance at seedling stage. Indian Journal of Plant Physiology / Official Publication of the Indian Society for Plant Physiology 8, 105–116.

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 18444910PubMed |

Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology 30, 360–364.
Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene.Crossref | GoogleScholarGoogle Scholar | 22407351PubMed |

Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant & Cell Physiology 47, 32–42.
Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Oda Y, Kobayashi NI, Tanoi K, Ma JF, Itou Y, Katsuhara M, Itou T, Horie T (2018) T-DNA tagging-based gain-of-function of OsHKT1;4 reinforces Na exclusion from leaves and stems but triggers Na toxicity in roots of rice under salt stress. International Journal of Molecular Sciences 19, 235
T-DNA tagging-based gain-of-function of OsHKT1;4 reinforces Na exclusion from leaves and stems but triggers Na toxicity in roots of rice under salt stress.Crossref | GoogleScholarGoogle Scholar |

Oomen RJFJ, Benito B, Sentenac H, Rodriguez-Navarro A, Talon M, Very A-A, Domingo C (2012) HKT2;2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. The Plant Journal 71, 750–762.
HKT2;2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism.Crossref | GoogleScholarGoogle Scholar |

Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism? BMC Plant Biology 13, 32
Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism?Crossref | GoogleScholarGoogle Scholar | 23445750PubMed |

Qiu J, Henderson SW, Tester M, Roy SJ, Gilliham M (2016) SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl– accumulation and salt tolerance in Arabidopsis thaliana. Journal of Experimental Botany 67, 4495–4505.
SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl accumulation and salt tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27340232PubMed |

Rahman MA, Thomson MJ, Shah-E-Alam M, de Ocampo M, Egdane J, Ismail AM (2016) Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization. Annals of Botany 117, 1083–1097.
Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization.Crossref | GoogleScholarGoogle Scholar | 27063367PubMed |

Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics 37, 1141–1146.
A rice quantitative trait locus for salt tolerance encodes a sodium transporter.Crossref | GoogleScholarGoogle Scholar | 16155566PubMed |

Shi Y, Wang Y, Flowers TJ, Gong H (2013) Silicon decreases chloride transport in rice (Oryza sativa L.) in saline conditions. Journal of Plant Physiology 170, 847–853.
Silicon decreases chloride transport in rice (Oryza sativa L.) in saline conditions.Crossref | GoogleScholarGoogle Scholar | 23523465PubMed |

Singh RK, Redoña ED, Refuerzo L (2010) Varietal improvement for abiotic stress tolerance in crop plants: special reference to salinity in rice. In ‘Abiotic stress adaptation in plants: physiological, molecular, and genomic foundation’. (Eds A Pareek, SK Sopory, HJ Bohnert, Govindjee) pp. 387–415. (Springer: Dordrecht, The Netherlands)

Suzuki K, Yamaji N, Costa A, Okuma E, Kobayashi NI, Kashiwagi T, Katsuhara M, Wang C, Tanoi K, Murata Y, Schroeder JI, Ma JF, Horie T (2016) OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biology 16, 22
OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress.Crossref | GoogleScholarGoogle Scholar | 26786707PubMed |

Thomson MJ, de Ocampo M, Egdane J, Rahman MA, Sajise AG, Adorada DL, Tumimbang-Raiz A, Blumwald E, Seraj ZI, Singh RK, Gregorio GB (2010) Ismail AM characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3, 148–160.
Ismail AM characterizing the Saltol quantitative trait locus for salinity tolerance in rice.Crossref | GoogleScholarGoogle Scholar |

Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiology 139, 822–835.
Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage.Crossref | GoogleScholarGoogle Scholar | 16183841PubMed |

Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theoretical and Applied Genetics 79, 377–384.
Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance.Crossref | GoogleScholarGoogle Scholar | 24226357PubMed |

Yoshida S, Forno DA, Cook JH, Gomes KA (1976) Routine procedure for growing rice plants in culture solution. In ‘Laboratory manual for physiological studies of rice’. (Eds S Yoshida, DA Forno, JH Cook, KA Gomez) pp. 61–66. (International Rice Research Institute: Los Baños, Philippines)

Zeng L, Shannon MC, Grieve CM (2002) Evaluation of salt tolerance in rice genotypes by multiple agronomic parameters. Euphytica 127, 235–245.
Evaluation of salt tolerance in rice genotypes by multiple agronomic parameters.Crossref | GoogleScholarGoogle Scholar |