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Root hydrotropism is controlled via a cortex-specific growth mechanism

Nature Plants volume 3, Article number: 17057 (2017) Cite this article

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Abstract

Plants can acclimate by using tropisms to link the direction of growth to environmental conditions. Hydrotropism allows roots to forage for water, a process known to depend on abscisic acid (ABA) but whose molecular and cellular basis remains unclear. Here we show that hydrotropism still occurs in roots after laser ablation removed the meristem and root cap. Additionally, targeted expression studies reveal that hydrotropism depends on the ABA signalling kinase SnRK2.2 and the hydrotropism-specific MIZ1, both acting specifically in elongation zone cortical cells. Conversely, hydrotropism, but not gravitropism, is inhibited by preventing differential cell-length increases in the cortex, but not in other cell types. We conclude that root tropic responses to gravity and water are driven by distinct tissue-based mechanisms. In addition, unlike its role in root gravitropism, the elongation zone performs a dual function during a hydrotropic response, both sensing a water potential gradient and subsequently undergoing differential growth.

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Figure 1: Laser ablation of columella cells affects the gravitropic but not the hydrotropic response of roots.
Figure 2: ABA signalling in the cortex is crucial for root hydrotropism.
Figure 3: Root growth and cortical endoreplication are induced by low levels of ABA.
Figure 4: Inhibition of differential cell elongation in the cortex prevents hydrotropism but not gravitropism.
Figure 5: Conceptual model for root hydrotropism.

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Acknowledgements

The authors thank C. Howells, K. Swarup and M. Whitworth for technical assistance, J.-K. Zhu for providing snrk2.2 snrk2.3 seeds, W. Grunewald for pDONR-L1-GAL4-VP16-R2 and S. Tsukinoki for generating WER:MIZ1-GFP(HSPter) and PIN2:MIZ1-GFP(HSPter) transgenic plants and acknowledge the following funding agencies for financial support: D.D., J.F., R.A., T.N., D.W., S.T., C.S., S.M., M.R.O., L.R.B., R.D., O.J., J.K., J.R., T.B. and M.J.B. thank the Biological and Biotechnology Science Research Council (BBSRC) for responsive mode and CISB awards to the Centre for Plant Integrative Biology; D.W., C.S., S.M., M.R.O., J.K., T.P. and M.J.B. thank the European Research Council (ERC) for FUTUREROOTS project funding; L.R.B. thanks the Leverhulme Trust for an Early Career Fellowship; V.B., R.B. and L.D.V. are supported by grants of the Research Foundation Flanders (G.002911N). R.B. and M.J.B. thank the Royal Society for Newton and Wolfson Research Fellowship awards; R.A., T.I.B. and M.J.B. thank the FP7 Marie Curie Fellowship Scheme; R.D. thanks the Engineering and Physical Sciences Research Council, J.D. and M.J.B. thank the GII scheme; and V.B., R.B., L.D.V. and M.J.B. thank the Interuniversity Attraction Poles Programme (IUAP P7/29 “MARS”), initiated by the Belgian Science Policy Office. R.B.P. was funded by grants from the Knut and Alice Wallenberg Foundation. This work was also supported by a Grant-in-Aid for Scientific Research on Innovative Areas (No. 22120004) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to H.T., a Grant-in-Aid for Young Scientists (B) (No. 26870057) from the Japan Society for the Promotion of Science (JSPS) to A.K., a Grant-in-Aid for Scientific Research on Innovative Areas (No. 22120002) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan to A.N., a Grant-in-Aid for Scientific Research on Innovative Areas (No. 22120010) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan to Y.H. and the Funding Program for Next-Generation World-Leading Researchers (GS002) to Y.M. L.P. was financially supported by a scholarship from the Japanese government. T.-W.B. was financially supported by the Funding Program for Next-Generation World-Leading Researchers (GS002) and the Grant-in-Aid for Scientific Research on Innovative Areas (No. 22120004).

Author information

Author notes

  1. John A. Fozard

    Present address: Computational and Systems Biology, John Innes Centre, Norwich, NR4 7UH, UK

  2. Regina Antoni

    Present address: Centre Nacional d'Anàlisi Genòmica (CNAG-CRG), 08028, Barcelona, Spain

  3. Saoirse R. Tracy

    Present address: School of Agriculture and Food Science, University College Dublin, Belfield Campus, Dublin, 4, Ireland

  4. Jeremy A. Roberts

    Present address: School of Biological and Marine Sciences, University of Plymouth, Plymouth, PL4 8AA, UK

  5. Daniela Dietrich, Lei Pang and Akie Kobayashi: These authors contributed equally to this work

  6. Hideyuki Takahashi and Malcolm J. Bennett: Denotes co-corresponding authorship.

Authors and Affiliations

  1. Centre for Plant Integrative Biology, University of Nottingham, Nottingham, LE12 5RD, UK

    Daniela Dietrich, John A. Fozard, Rahul Bhosale, Regina Antoni, Tuan Nguyen, Darren M. Wells, Markus R. Owen, Leah R. Band, Oliver E. Jensen, John R. King, Saoirse R. Tracy, Craig J. Sturrock, Sacha J. Mooney, Jeremy A. Roberts, Tobias I. Baskin, Tony P. Pridmore & Malcolm J. Bennett

  2. Plant & Crop Sciences, School of Biosciences, University of Nottingham, Nottingham, LE12 5RD, UK

    Daniela Dietrich, Rahul Bhosale, Darren M. Wells, Jeremy A. Roberts & Malcolm J. Bennett

  3. Graduate School of Life Sciences, Tohoku University, Sendai, 980-8577, Japan

    Lei Pang, Akie Kobayashi, Sotaro Hiratsuka, Nobuharu Fujii, Tae-Woong Bae & Hideyuki Takahashi

  4. Department of Plant Biotechnology and Bioinformatics, Ghent University, (Technologiepark 927), 9052 Ghent, Belgium

    Véronique Boudolf, Rahul Bhosale & Lieven De Veylder

  5. VIB Center for Plant Systems Biology, (Technologiepark 927), 9052 Ghent, Belgium

    Véronique Boudolf, Rahul Bhosale & Lieven De Veylder

  6. School of Computer Science, University of Nottingham, Nottingham, NG8 1BB, UK

    Tuan Nguyen & Tony P. Pridmore

  7. Faculty of Science, Yamagata University, Yamagata, 990-8560, Japan

    Yutaka Miyazawa

  8. Centre for Mathematical Medicine & Biology, University of Nottingham, Nottingham, NG7 2RD, UK

    Markus R. Owen, Leah R. Band & John R. King

  9. School of Mathematics, University of Birmingham, Birmingham, B15 2TT, UK

    Rosemary J. Dyson

  10. School of Mathematics, University of Manchester, Oxford Road, Manchester, M13 9PL, UK

    Oliver E. Jensen

  11. Agricultural and Environmental Sciences, School of Biosciences, University of Nottingham, Nottingham, LE12 5RD, UK

    Saoirse R. Tracy, Craig J. Sturrock & Sacha J. Mooney

  12. Department of Forest Genetics and Plant Physiology, SLU, S-901 83 Umea, Sweden

    Rishikesh P. Bhalerao

  13. College of Science, KSU, Riyadh, Saudi Arabia

    Rishikesh P. Bhalerao

  14. Department of Plant Biology, Carnegie Institution for Science, 260 Panama Street, Stanford, 94305, California, USA

    José R. Dinneny

  15. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Cientificas-Universidad Politecnica de Valencia, ES-46022 Valencia, Spain

    Pedro L. Rodriguez

  16. Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Akira Nagatani

  17. Graduate School of Materials Science, Nara Institute of Science & Technology, Ikoma, 630-0101, Japan

    Yoichiroh Hosokawa

  18. Biology Department, University of Massachusetts, Amherst, 01003-9297, Massachusetts, USA

    Tobias I. Baskin

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  1. Daniela Dietrich
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Contributions

D.D., L.P., A.K., J.F., V.B., R.B., R.A., T.N., S.H., T.-W.B., Y.M., D.M.W., S.T. and C.J.S. performed experimental work and data analysis and mathematical modelling. D.M.W., M.R.O., L.R.B., R.D., O.J., J.R.K., S.J.M., J.R., R.B., J.D., P.L.R., T.I.B., T.P., L.D.V., N.F., Y.M., A.N., Y.H., H.T. and M.J.B. oversaw project planning and discussed experimental results and modelling simulations. D.D., L.P., A.K., N.F., Y.M., T.I.B., H.T. and M.J.B. wrote the paper.

Corresponding authors

Correspondence to Hideyuki Takahashi or Malcolm J. Bennett.

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The authors declare no competing financial interests.

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Supplementary Figures 1–8, Supplementary Methods, Supplementary References, Supplementary Table 1, Supplementary Notes 1 and 2. (PDF 6852 kb)

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Dietrich, D., Pang, L., Kobayashi, A. et al. Root hydrotropism is controlled via a cortex-specific growth mechanism. Nature Plants 3, 17057 (2017). https://doi.org/10.1038/nplants.2017.57

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