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Soil salinity and mechanical obstruction differentially affects embryonic root architecture in different rice genotypes from West Bengal

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Abstract

Making the first contact with the soil environment, roots are the first responders of soil borne stress including nutrient and water scarcity, hyper salinity and soil compactness. Embryonic root responds by bending, twisting, foraging and regulation of lateral root initiation. Traditional rice cultivars adapted to diverse topography harbour novel stress tolerance traits. We established a quantitative measurement coefficient termed stress adaptation coefficient (SAC) dependent on root responses to stress and applied it to study the effect of mechanical stress and salinity on roots of rice genotypes collected all across West Bengal, India. The responses of root to mechanical and salinity stress are overlapping. Analysis of the response of roots by means of SAC in 28 rice cultivars including high-yield salt tolerant varieties as well as geographically isolated native rice genotypes shows that many of the salt tolerant varieties also perform better in mechanical stress while the opposite is not always true. Transcriptome analysis through cDNA microarray of stress sensitive variety IR64 shows about 6000 common transcripts to be differentially regulated among the two stresses. Quantitative real time expression analyses of salt sensitive and known salt tolerant varieties reveal the involvement of identified genes in salinity and mechanical stress. Overall, our study indicates that there is an important commonality in the molecular basis of salt and mechanical stress and presents an easy-to-perform early establishment stress screen for rice genotypes.

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References

  • Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., & Ecker, J. R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science, 284(5423), 2148–2152.

    Article  CAS  PubMed  Google Scholar 

  • Ampudia, C. S. G., Julkowska, M. M., Darwish, E., Gandullo, J., Korver, R. A., Brunoud, G., et al. (2013). Halotropism is a response of plant roots to avoid a saline environment. Current Biology, 23, 2044–2050.

    Article  CAS  Google Scholar 

  • Babicki, S., Arndt, D., Marcu, A., Liang, Y., Grant, J. R., Maciejewski, A., et al. (2016). Heatmapper: Web-enabled heat mapping for all. Nucleic Acids Research, 44, W147–W153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai, H., & Wolverton, C. (2011). Gravitropism in lateral roots of Arabidopsis pgm-1 mutants is indistinguishable from that of wild-type. Plant Signaling and Behavior, 6(10), 1423–1424.

    Article  CAS  PubMed  Google Scholar 

  • Baldwin, K. L., Strohm, A. K., & Masson, P. H. (2013). Gravity sensing and signal transduction in vascular plant primary roots. American Journal of Botany, 100(1), 126–142.

    Article  CAS  PubMed  Google Scholar 

  • Baluška, F., & Mancuso, S. (2009). Plant neurobiology: From stimulus perception to adaptive behavior of plants, via integrated chemical and electrical signaling. Plant Signaling and Behavior, 4(9), 475–476.

    Article  PubMed  Google Scholar 

  • Bao, Y., Aggarwal, P., Robbins, I. I. N. E., Sturrock, C. J., Thompson, M. C., Tan, H. Q., et al. (2014). Plant roots use a patterning mechanism to position lateral root branches toward available water. Proceedings of the National Academy of Sciences of the United States of America, 111(25), 9319–9324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardou, P., Mariette, J., Escudié, F., Djemiel, C., & Klopp, C. (2014). jvenn: An interactive Venn diagram viewer. BMC Bioinformatics, 15, 293.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bariola, P. A., Retelska, D., Stasiak, A., Kammerer, R. A., Fleming, A., Hijri, M., et al. (2004). Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants. Plant Molecular Biology, 55(4), 579–594.

    Article  CAS  PubMed  Google Scholar 

  • Bengough, A. G., Bransby, M. F., Hans, J., McKenna, S. J., Roberts, T. J., & Valentine, T. A. (2006). Root responses to soil physical conditions; growth dynamics from field to cell. Journal of Experimental Botany, 57(2), 437–447.

    Article  CAS  PubMed  Google Scholar 

  • Bengough, A. G., McKenzie, B. M., Hallett, P. D., & Valentine, T. A. (2011). Root elongation, water stress, and mechanical impedance: A review of limiting stresses and beneficial root tip traits. Journal of Experimental Botany, 62(1), 59–68.

    Article  CAS  PubMed  Google Scholar 

  • Butt, H. I., Yang, Z., Gong, Q., Chen, E., Wang, X., Zhao, G., et al. (2017). GaMYB85 an R2R3 MYB gene, in transgenic Arabidopsis plays an important role in drought tolerance. BMC Plant Biology, 17(1), 142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, Y., Qi, Y., Zhu, Q., Chen, X., Wang, N., Zhao, X., et al. (2009). New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics, 9(11), 3100–3114.

    Article  CAS  PubMed  Google Scholar 

  • Coutts, M. P. (1983). Root architecture and tree stability. Plant and Soil, 71, 171–188.

    Article  Google Scholar 

  • Czolpinska, M., & Rurek, M. (2018). Plant glycine-rich proteins in stress response: An emerging, still prospective story. Frontiers in Plant Science, 9, 302.

    Article  PubMed  PubMed Central  Google Scholar 

  • Elavumoottil, O. C., Martin, J. P., & Moreno, M. L. (2003). Changes in sugars, sucrose synthase activity and proteins in salinity tolerant callus and cell suspension cultures of Brassica oleracea L. Biologia Plantarum, 46(1), 7–12.

    Article  CAS  Google Scholar 

  • Ferreira, L. J., Azevedo, V., Maroco, J., Oliveira, M. M., & Santos, A. P. (2015). Salt tolerant and sensitive rice varieties display differential methylome flexibility under salt stress. PLoS ONE. https://doi.org/10.1371/journal.pone.0124060.

    Article  PubMed  PubMed Central  Google Scholar 

  • Friml, J. (2010). Subcellular trafficking of PIN auxin efflux carriers in auxin transport. European Journal of Cell Biology, 89, 231–235.

    Article  CAS  PubMed  Google Scholar 

  • Geldner, N., Friml, J., Stierhof, Y. D., Jurgens, G., & Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature, 413, 425–428.

    Article  CAS  PubMed  Google Scholar 

  • Horie, T., Brodsky, D. E., Costa, A., Kaneko, T., Lo Schiavo, F., Katsuhara, M., et al. (2011). K+ transport by the OsHKT2;4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiology, 156, 1493–1507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horie, T., Costa, A., Kim, T. H., Han, M. J., Horie, R., Leung, H. Y., et al. (2007). Rice OsHKT2;1 transporter mediates large Na+ influx component into K+−starved roots for growth. The EMBO Journal, 26(12), 3003–3014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Julkowska, M. M., Koevoets, I. T., Mol, S., Hoefsloot, H., Feron, R., Tester, M. A., et al. (2017). Genetic components of root architecture remodeling in response to salt stress. The Plant Cell, 29, 3198–3213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung, Y. J., Melencion, S. M. B., Lee, E. S., Park, J. H., Alinapon, C. V., Oh, H. T., et al. (2015). Universal stress protein exhibits a redox dependent chaperone function in arabidopsis and enhances plant tolerance to heat shock and oxidative stress. Frontiers in Plant Science, 6, 1141.

    PubMed  PubMed Central  Google Scholar 

  • Kazan, K. (2013). Auxin and the integration of environmental signals into plant root development. Annals of Botany, 112(9), 1655–1665.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koevoets, I. T., Venema, J. H., Elzenga, J. T. M., & Testerink, C. (2016). Roots withstanding their environment: Exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science, 7, 1335.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, J., Xu, H. H., Liu, W. C., Zhang, X., & Lu, Y. T. (2015). Ethylene inhibits root elongation during alkaline stress through AUXIN1 and associated changes in auxin accumulation. Plant Physiology, 168, 1777–1791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Majee, M., Maitra, S., Dastidar, K. G., Pattanaik, S., Chatterjee, A., Hait, N. C., et al. (2004). A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: Molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. The Journal of Biological Chemistry, 279(27), 28539–28552.

    Article  CAS  PubMed  Google Scholar 

  • Malakshah, S. N., Rezaei, M. H., Heidari, M., & Salekdeh, G. H. (2007). Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Bioscience, Biotechnology, and Biochemistry, 71(19), 2144–2154.

    Article  CAS  Google Scholar 

  • Marchant, A., Kargul, J., May, S. T., Muller, P., Delbarre, A., Perrot-Rechenmann, C., et al. (1999). AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. The EMBO Journal, 18(8), 2066–2073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masle, J., & Passioura, J. B. (1987). The effect of soil strength on the growth of young wheat plants. Australian Journal of Plant Physiology, 14, 643–656.

    Google Scholar 

  • Negi, S., Ivanchenko, M. G., & Muda, G. K. (2008). Ethylene regulates lateral root formation and auxin transport. The Plant Journal, 55(2), 175–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peyronnet, R., Tran, D., Girault, T., & Frachisse, J. M. (2014). Mechanosensitive channels: Feeling tension in a world under pressure. Frontiers in Plant Science, 5, 53.

    Article  Google Scholar 

  • Santisree, P., Nongmaithem, S., Vasuki, H., Sreelakshmi, Y., Ivanchenko, M. G., & Sharma, R. (2011). Tomato root penetration in soil requires a coaction between ethylene and auxin signaling. Plant Physiology, 156, 1424–1438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sengupta, S. (2014). The possible overlap between salinity and mechanical challenges in Porteresia coarctata. Proceedings of the Indian National Science Academy, 80, 1013–1023.

    Article  Google Scholar 

  • Singh, A., Kumar, P., Gautam, V., Rengasamy, B., Adhikari, B., Udayakumar, M., et al. (2016). Root transcriptome of two contrasting indica rice cultivars uncovers regulators of root development and physiological responses. Scientific Reports, 6, 39266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, F., Zhang, W., Hu, H., Li, B., Wang, Y., Zhao, Y., et al. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in arabidopsis. Plant Physiology, 146, 178–188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udawat, P., Jha, R. K., Sinha, D., Mishra, A., & Jha, B. (2016). Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Frontiers in Plant Science, 7, 518.

    Article  PubMed  PubMed Central  Google Scholar 

  • Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., et al. (2013). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097–1102.

    Article  CAS  PubMed  Google Scholar 

  • Valmonte, G. R., Arthur, K., Higgins, C. M., & MacDiarmid, R. M. (2014). Calcium-dependent protein kinases in plants: Evolution, expression and function. Plant and Cell Physiology, 55(3), 551–569.

    Article  CAS  PubMed  Google Scholar 

  • Walker, L., Boddington, C., Jenkins, D., et al. (2017). Changes in gene expression in space and time orchestrate environmentally mediated shaping of root architecture. The Plant Cell, 29, 2393–2412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, H. Z., Yang, K. Z., Zou, J. J., Zhu, L. L., Xie, Z. D., Morita, M. T., et al. (2015). Transcriptional regulation of PIN genes by FOUR LIPS and MYB88 during Arabidopsis root gravitropism. Nature Communications, 6, 8822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whalley, W. R., Leeds-Harrison, P. B., Clark, L. J., & Gowing, D. J. G. (2005). Use of effective stress to predict the penetrometer resistance of unsaturated agricultural soils. Soil and Tilliage Research, 84(1), 18–27.

    Article  Google Scholar 

  • Xi, W., Gong, X., Yang, Q., Yu, H., & Liou, Y. C. (2016). Pin1At regulates PIN1 polar localization and root gravitropism. Nature Communications, 7, 10430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, I. M., Montagu, K., Conroy, J., & Bengough, A. G. (1997). Mechanical impedance of root growth directly reduces leaf elongation rates of cereals. New Phytologist, 135(4), 613–619.

    Article  Google Scholar 

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Acknowledgements

The work is supported by grants from Department of Biotechnology, GOI (BT/AB/05/02/2007-III dt.21/09/2010 and BT/IN/NWO/17/ALM dated 02.09.2015) and Raja Ramanna Fellowship (10/29/2010/RRF-R&D-II/6403 dt.03/06/2011), awarded to ALM, currently an INSA Senior Scientist and by Department of Science and Technology-SERB research Grant (SR/FT/LS-170/2010 dt. 21/08/12) to SSG. SA is funded by Govt. of India University Grants Commission-RGN Fellowship (2011-12/RGNF-SC-WES-13271). Funding for PD, AR and AM were from Department of Science and Technology-SERB research Grant (YSS/2015/001872), fellowship from Bose Institute and DBT Project respectively.

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SSG and ALM generated the concept and designed the experiments. SA performed the major experiments while AR and AM conducted the initial experiments. SA and PD analyzed the data. SA, SSG and PD wrote the draft manuscript. ALM finalized the manuscript.

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Correspondence to Arun Lahiri Majumder.

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Adak, S., Roy, A., Das, P. et al. Soil salinity and mechanical obstruction differentially affects embryonic root architecture in different rice genotypes from West Bengal. Plant Physiol. Rep. 24, 192–209 (2019). https://doi.org/10.1007/s40502-019-00450-2

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