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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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

    • Daniela Dietrich
    • , Lei Pang
    •  & Akie Kobayashi

    These authors contributed equally to this work

    • John A. Fozard
    • , Regina Antoni
    • , Saoirse R. Tracy
    •  & Jeremy A. Roberts

    Present address: Computational and Systems Biology, John Innes Centre, Norwich NR4 7UH, UK (J.A.F.). Centre Nacional d'Anàlisi Genòmica (CNAG-CRG), 08028 Barcelona, Spain (R.A.). School of Agriculture and Food Science, University College Dublin, Belfield Campus, Dublin 4, Ireland (S.R.T.). School of Biological and Marine Sciences, University of Plymouth, Plymouth PL4 8AA, UK (J.A.R.)

    • Hideyuki Takahashi
    •  & Malcolm J. Bennett

    Denotes co-corresponding authorship.

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, California 94305, 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, Massachusetts 01003-9297, USA

    • Tobias I. Baskin

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Hideyuki Takahashi or Malcolm J. Bennett.

Supplementary information

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    Supplementary Information

    Supplementary Figures 1–8, Supplementary Methods, Supplementary References, Supplementary Table 1, Supplementary Notes 1 and 2.