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A possible involvement of autophagy in amyloplast degradation in columella cells during hydrotropic response of Arabidopsis roots

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Abstract

Seedling roots display not only gravitropism but also hydrotropism, and the two tropisms interfere with one another. In Arabidopsis (Arabidopsis thaliana) roots, amyloplasts in columella cells are rapidly degraded during the hydrotropic response. Degradation of amyloplasts involved in gravisensing enhances the hydrotropic response by reducing the gravitropic response. However, the mechanism by which amyloplasts are degraded in hydrotropically responding roots remains unknown. In this study, the mechanistic aspects of the degradation of amyloplasts in columella cells during hydrotropic response were investigated by analyzing organellar morphology, cell polarity and changes in gene expression. The results showed that hydrotropic stimulation or systemic water stress caused dramatic changes in organellar form and positioning in columella cells. Specifically, the columella cells of hydrotropically responding or water-stressed roots lost polarity in the distribution of the endoplasmic reticulum (ER), and showed accelerated vacuolization and nuclear movement. Analysis of ER-localized GFP showed that ER redistributed around the developed vacuoles. Cells often showed decomposing amyloplasts in autophagosome-like structures. Both hydrotropic stimulation and water stress upregulated the expression of AtATG18a, which is required for autophagosome formation. Furthermore, analysis with GFP-AtATG8a revealed that both hydrotropic stimulation and water stress induced the formation of autophagosomes in the columella cells. In addition, expression of plastid marker, pt-GFP, in the columella cells dramatically decreased in response to both hydrotropic stimulation and water stress, but its decrease was much less in the autophagy mutant atg5. These results suggest that hydrotropic stimulation confers water stress in the roots, which triggers an autophagic response responsible for the degradation of amyloplasts in columella cells of Arabidopsis roots.

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Abbreviations

ER:

Endoplasmic reticulum

GFP:

Green fluorescent protein

DAPI:

4′,6-diamidino-2-phenylindole

DIC:

Differential interference contrast microscope

TEM:

Transmission electron microscope

RT-PCR:

Reverse transcription-polymerase chain reaction

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Acknowledgments

We thank Dr. Maureen R. Hanson of Cornell University for providing us with the seeds of pt-GFP transgenic plants. We are grateful to Dr. Atsushi Higashitani of the Graduate School of Life Sciences, Tohoku University for his helpful suggestions and critical reading of this manuscript. This work was supported by a Grant-in-Aid for Scientific Research B (No. 20370017) from the Japan Society for the Promotion of Science (JSPS) and a Grant-in-Aid for Scientific Research on Innovative Areas (No. 22120004) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to H.T., a Research Fellowship for Young Scientists from the JSPS to M.N., and the Funding Program for Next-Generation World-Leading Researchers (GS002) to Y.M. This work was also carried out as a part of the Global COE Program J03 (Ecosystem Management Adapting to Global Change).

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Authors and Affiliations

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

    Mayumi Nakayama, Yutaka Miyazawa, Nobuharu Fujii, Nahoko Higashitani & Hideyuki Takahashi

  2. Faculty of Education, Saitama University, Saitama, 338-8570, Japan

    Yasuko Kaneko

  3. Graduate School of Agriculture, Tohoku University, Sendai, 981-8555, Japan

    Shinya Wada & Hiroyuki Ishida

  4. Plant Science Center, RIKEN, Yokohama, 230-0045, Japan

    Kohki Yoshimoto & Ken Shirasu

  5. National Institute for Basic Biology, Okazaki, 444-8585, Japan

    Kenji Yamada & Mikio Nishimura

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  1. Mayumi Nakayama
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  2. Yasuko Kaneko
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  3. Yutaka Miyazawa
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  4. Nobuharu Fujii
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Correspondence to Hideyuki Takahashi.

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Nakayama, M., Kaneko, Y., Miyazawa, Y. et al. A possible involvement of autophagy in amyloplast degradation in columella cells during hydrotropic response of Arabidopsis roots. Planta 236, 999–1012 (2012). https://doi.org/10.1007/s00425-012-1655-5

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  • DOI: https://doi.org/10.1007/s00425-012-1655-5

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