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Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess

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Abstract

Plants are routinely subjected to multiple environmental stresses that constrain growth. Zinc (Zn) deficiency and high bicarbonate are two examples that co-occur in many soils used for rice production. Here, the utility of metabolomics in diagnosing the effect of each stress alone and in combination on rice root function is demonstrated, with potential stress tolerance indicators identified through the use of contrasting genotypes. Responses to the dual stress of combined Zn deficiency and bicarbonate excess included greater root solute leakage, reduced dry matter production, lower monosaccharide accumulation and increased concentrations of hydrogen peroxide, phenolics, peroxidase and N-rich metabolites in roots. Both hydrogen peroxide concentration and root solute leakage were correlated with higher levels of citrate, allantoin and stigmasterol. Zn stress resulted in lower levels of the tricarboxylic acid (TCA) cycle intermediate succinate and the aromatic amino acid tyrosine. Bicarbonate stress reduced shoot iron (Fe) concentrations, which was reflected by lower Fe-dependent ascorbate peroxidase activity. Bicarbonate stress also favoured the accumulation of the TCA cycle intermediates malate, fumarate and succinate, along with the non-polar amino acid tyrosine. Genotypic differentiation revealed constitutively higher levels of d-gluconate, 2-oxoglutarate and two unidentified compounds in the Zn-efficient line RIL46 than the Zn-inefficient cultivar IR74, suggesting a possible role for these metabolites in overcoming oxidative stress or improving metal re-distribution.

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Abbreviations

ADH:

Alcohol dehydrogenase

ANOVA:

Analysis of variance

APX:

Ascorbate peroxidase

DI:

De-ionised

DMA:

Deoxymugineic acid

EDTA:

Ethylenediaminetetraacetic acid

GC–MS:

Gas chromatography–mass spectrometry

NAD:

Nicotinamide adenine dinucleotide

NBT:

Nitroblue tetrazolium

PLS-DA:

Partial least-squares discriminant analysis

POX:

Peroxidase

QTL:

Quantitative trait loci

RI:

Retention index

RIL:

Recombinant inbred line

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TCA:

Tricarboxylic acid

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Acknowledgments

We thank Eiko Yoshiba, Taro Matsuda and Mitsuko Matsumoto for their technical support and two anonymous reviewers for their contribution to improving this manuscript. The contribution of the Japan Society for the Promotion of Science (JSPS) in the form of Postdoctoral Fellowships for MTR and TJR is gratefully acknowledged.

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Author notes

  1. Michael T. Rose

    Present address: School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia

  2. Terry J. Rose

    Present address: Southern Cross Plant Science, Southern Cross University, PO Box 57, Lismore, NSW, 2480, Australia

Authors and Affiliations

  1. Crop Production and Environment Division, Japan International Research Centre for Agricultural Science, 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan

    Michael T. Rose, Terry J. Rose, Juan Pariasca-Tanaka & Matthias Wissuwa

  2. Postharvest Science and Technology Division, Japan International Research Centre for Agricultural Science, 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan

    Tadashi Yoshihashi

  3. Bioinformatics Resource Facility, Universität Bielefeld, 33594, Bielefeld, Germany

    Heiko Neuweger & Alexander Goesmann

  4. INRES-Institut für Nutzpflanzenwissenschaften und Ressourcenschutz, Universität Bonn, 53115, Bonn, Germany

    Michael Frei

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Rose, M.T., Rose, T.J., Pariasca-Tanaka, J. et al. Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236, 959–973 (2012). https://doi.org/10.1007/s00425-012-1648-4

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