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Dynamic cytokinin signaling and function of auxin in cytokinin responsive domains during rice crown root development

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We reveal the onset and dynamic tissue-specific cytokinin signaling domains and functional importance of auxin in the auxin–cytokinin interaction domains in shaping root architecture in the economically important rice plant.

Abstract

Plant hormones such as auxin and cytokinin are central regulators of root organogenesis. Typical in the grass species, the root system in rice is primarily composed of post-embryonic adventitious/crown roots (ARs/CRs). Antagonistic auxin–cytokinin activities mutually balance each other to ensure proper root development. Cytokinin has been shown to inhibit crown root initiation in rice; albeit, the responsive domains remain elusive during the initiation and outgrowth of crown root primordia (CRP). Here, we show the cytokinin response domains during various stages of CRP development. RNA–RNA in situ hybridization and protein immunohistochemistry studies of the reporter gene expressed under the cytokinin responsive synthetic promoter revealed detailed spatio-temporal cytokinin signaling domains in the developing CRP. Furthermore, rice lines genetically depleted for endogenous auxin in the cytokinin responsive domains provided insight into the functional importance of auxin signaling during crown root development. Thus, our study demonstrates the onset and dynamic tissue-specific cytokinin response and functional significance of auxin–cytokinin interaction during root architecture formation in rice, a model grass species.

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Acknowledgements

We are grateful to Dr. Bruno Müller at the University of Zürich, Switzerland for kindly sharing TCSn-min35S::GFP-ER plasmid, and Prof. Usha Vijayraghavan, Indian Institute of Science, Bangalore, India, for sharing pRSET-TCSn-min35S::ER-GFP and pCAMBIA1380 OsM1::OsMGH3 plasmids.

Funding

This work was supported by Department of Biotechnology, Ministry of Science and Technology (DBT-IYBA), Government of India. Infrastructural facilities were provided by the Indian Institute of Technology, Roorkee. University Grant Commission (UGC), India is acknowledged to provide fellowships to A.N. and Indian Institute of Technology, Roorkee to Z.S. and K.K.K.M.

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Authors and Affiliations

  1. Department of Biotechnology, Indian Institute of Technology, Roorkee, Roorkee, Uttarakhand, 247667, India

    Ananya Neogy, Zeenu Singh, Khrang Khrang Khunggur Mushahary & Shri Ram Yadav

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  1. Ananya Neogy
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  2. Zeenu Singh
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  3. Khrang Khrang Khunggur Mushahary
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  4. Shri Ram Yadav
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Contributions

A.N. designed and performed most of the experiments. Z.S. contributed in performing RNA in situ hybridization experiment with A.N., and K.K.K.M. contributed in generating and maintaining transgenic rice lines with A.N.. S.R.Y. conceived the project, designed all the experiments, analyzed data and wrote the manuscript together with AN.

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Correspondence to Shri Ram Yadav.

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Communicated by Neal Stewart.

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299_2020_2618_MOESM1_ESM.pdf

Supplementary file1 Supplementary Fig. 1: Immuno-histochemistry using the anti-GFP antibody in TCSn::GFP-ER lines (a and b) and wild-type (c). Supplementary Fig. 2: Effect of exogenous IAA treatment on wild-type rice seedlings. (a–d) Rice wild-type plants were grown in ½ MS medium supplemented with no IAA (a), with 10nM IAA (b), with 25nM IAA (c), and with 75nM IAA (d). Scale bar: 1 cm (a–d). Supplementary Fig. 3: Effect of exogenous IAA treatment on TCSn::OsMGH3 L#1. The number of CRs of TCSn::OsMGH3 L#1 (n=3) on the seventh day after germination is plotted as compared to wild-type (n=3). Two-tailed Student’s t-test determines significance, ns, not significant, * p-value <0.05 (PDF 408 kb)

Supplementary file2 Supplementary Table 1: The list of primers used in the study (PDF 260 kb)

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Neogy, A., Singh, Z., Mushahary, K.K.K. et al. Dynamic cytokinin signaling and function of auxin in cytokinin responsive domains during rice crown root development. Plant Cell Rep 40, 1367–1375 (2021). https://doi.org/10.1007/s00299-020-02618-9

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