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Manganese and iron both influence the shoot transcriptome of Typha angustifolia despite distinct preference towards manganese accumulation

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Abstract

Typha angustifolia is a metal hypertolerant grass that predominates the wetlands of uranium tailings in Jaduguda, India, contaminated with extreme levels of iron (Fe) and manganese (Mn). In the paper investigations were carried out to understand the molecular mechanism of metal tolerance in this tolerant macrophyte. Metal analysis was coupled with fluorescent differential display (FDD) and reverse northern to compare the metal profile and transcriptome between Typha plants growing in the tailings versus a control wetland. The expressions of the validated transcripts in Mn and Fe stress were confirmed using reverse northern and semiquantitaive RT-PCR. Typha selectively accumulated and stored Mn in shoots but excluded/restricted Fe both in the field and in vitro. Differential expressions of 23 ESTs were validated among 118 FDD genes. Although Typha behaved as a Mn accumulator, these transcripts were found to be regulated in a complex fashion not only by Mn accumulated in the shoots but also by Fe excluded from the shoots. Our results provide the first report in the molecular understanding of metal tolerance in Typha angustifolia and indicate a complex regulation of genes in response to metals in a contaminated habitat.

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Abbreviations

FDD:

Fluorescent differential display

FAAS:

Flame atomic absorption spectroscopy

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Acknowledgements

We would like to acknowledge the Board of Research in Nuclear Science, Department of Atomic Energy for funding this work. We sincerely acknowledge Dr. A. Lahiri Majumdar for help in the photosynthetic efficiency measurement and Dr. Debabrata Bose and Dr. Sampa Das for their help in the reverse northern experiments. We thank Dr. M. Dasgupta and Dr. Mahashweta Mitra Ghosh for critically reading the manuscript. Monali Sen and Soumita Das acknowledge Council of Scientific and Industrial research, India (CSIR) and Department of Biotechnology India respectively for their fellowships.

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Authors and Affiliations

  1. B. C. Guha Centre of Genetic Engineering and Department of Biotechnology, University of Calcutta, 35 Ballygunge Circular Road, Kolkata, 700019, India

    D. Chakraborty, S. Das & A. Seal

  2. Department of Biotechnology, West Bengal University of Technology, BF-142, Sector I, Salt Lake, Kolkata, 700064, India

    M. Sen

  3. Analytical Chemistry Division, Bhabha Atomic Research Centre, Trombay, Mumbai, 400085, India

    S. Abhay Kumar & A. V. R. Reddy

  4. Radiochemistry Division, Bhabha Atomic Research Centre, Trombay, Mumbai, 400085, India

    R. Acharya

  5. Molecular and Human Genetics Division, Indian Institute of Chemical Biology, Raja S.C Mullick Road, Kolkata, 700032, India

    T. Das & S. Roychaudhury

  6. Molecular Biology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, 400085, India

    S. K. Apte & H. Rajaram

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  1. D. Chakraborty
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  2. S. Abhay Kumar
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Correspondence to A. Seal.

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Supplementary Table 1

(XLS 40 kb)

Supplementary Fig. 1

Metal analysis of DCB treated roots of T. angustifolia. Roots of T. angustifolia collected from tailings and control wetland were treated with DCB as described in materials and methods. DCB treated roots were dried, digested with acid and used for FAAS analysis. Mn and Fe were measured both in DCB treated and untreated root. (GIF 5 kb)

High Resolution. (TIFF 2344 kb)

Supplementary Fig. 2

Restriction digestion based ribotyping of Typha. 18SrDNA was amplified from the genomic DNA isolated from the shoot tissue of Typha and the PCR product was digested with Ava I. C1, C2 are two sample plants collected from control wetland and T1, T2 are that collected from tailings ponds. U indicates the uncut 18SrDNA PCR product having an expected size of 1.5Kbp. (GIF 19 kb)

High Resolution. (TIFF 1131 kb)

Supplementary Fig. 3

Fluorescence differential display (FDD) of shoot transcripts of T. angustifolia. Representative FDD poly acrylamide gel. RNA was isolated from shoots of T. angustifolia collected from tailings and control wetland and Fluorescent differential display performed with Red RNA Spectra kit (Genhunter). The PCR products were run on 6% polyacrylamide gel and scanned by Typhoon imager. The abbreviations above the lane explain the template cDNA and primer combination. T and C for cDNA from tailings and control Typha respectively, A,C and G stands for three different oligo dT RT 11-A, RT 11-C, RT 11-G supplied with RNA spectra kit and the numbers 1 to 8 indicate the arbitrary primer number (→) Indicate some of the differentially expressed bands. (GIF 147 kb)

High Resolution. (TIFF 8943 kb)

Supplementary Fig. 4

Chlorophyll measurement in Mn and Fe treated Typha plants vitro. Typha seeds collected from Jaduguda wetlands were treated with Mn and Fe as ‘long term treatment’. Chlorophyll was extracted from 400mg of fresh tissue treated with 8ml of 80% acetone overnight in dark. Florescence was measured at 645nm and 663nm. Total chlorophyll and chlorophyll a and b was calculated according to the following equation (Arnon, D (1949) Plant Physiology 24: 1–15 ). Total chlorophyll (mg/g) = 20.2 (A645) + 8.02 (A663) X V/1000 X 1/W Chlorophyll a (mg/g) = 12.7 (A663) - 2.69 (A645) X V/1000 X 1/W. Chlorophyll b (mg/g) = 22.9 (A645) - 4.68 (A663) X V/1000 X 1/W. V= final volume of 80% acetone chlorophyll extract. W= fresh weight of tissue (GIF 4 kb)

High Resolution. (TIFF 2313 kb)

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Chakraborty, D., Kumar, S.A., Sen, M. et al. Manganese and iron both influence the shoot transcriptome of Typha angustifolia despite distinct preference towards manganese accumulation. Plant Soil 342, 301–317 (2011). https://doi.org/10.1007/s11104-010-0696-4

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