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Defects in the rice aconitase-encoding OsACO1 gene alter iron homeostasis

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Rice aconitase gene OsACO1 is involved in the iron deficiency-signaling pathway for the expression of iron deficiency-inducible genes, either thorough enzyme activity or possible specific RNA binding for post-transcriptional regulation.

Abstract

Iron (Fe) is an essential element for virtually all living organisms. When plants are deficient in Fe, Fe acquisition systems are activated to maintain Fe homeostasis, and this regulation is mainly executed at the gene transcription level. Many molecules responsible for Fe uptake, translocation, and storage in plants have been identified and characterized. However, how plants sense Fe status within cells and then induce a transcriptional response is still unclear. In the present study, we found that knockdown of the OsACO1 gene, which encodes an aconitase in rice, leads to the down-regulation of selected Fe deficiency-inducible genes involved in Fe uptake and translocation in roots, and a decrease in Fe concentration in leaves, even when grown under Fe-sufficient conditions. OsACO1 knockdown plants showed a delayed transcriptional response to Fe deficiency compared to wild-type plants. In contrast, overexpression of OsACO1 resulted in the opposite effects. These results suggest that OsACO1 is situated upstream of the Fe deficiency-signaling pathway. Furthermore, we found that the OsACO1 protein potentially has RNA-binding activity. In vitro screening of RNA interactions with OsACO1 revealed that RNA potentially forms a unique stem-loop structure that interacts with OsACO1 via a conserved GGUGG motif within the loop structure. These results suggest that OsACO1 regulate Fe deficiency response either thorough enzyme activity catalyzing isomerization of citrate, or specific RNA binding for post-transcriptional regulation.

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Acknowledgements

We thank Dr. Yoshiaki Nagamura and Ms. Rituko Motoyama (National Institute of Agrobiological Sciences, Japan) for the rice microarray analysis, Ms. Akane Konishi, Ms. May Linn Aung, Ms. Hiroko Hori, and Ms. Mariko Sakashita (Ishikawa Prefectural University, Japan) for assistance with the rice culture and analysis. This research was supported by Advanced Low Carbon Technology Research and Development Program (ALCA) from Japan Science and Technology Agency (JST) (to N. K. N), and the Japan Society for the Promotion of Sciences (JSPS) KAKENHI Grant Numbers 16H04891 (to N. K. N) and 18H02115 (to T. K.).

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Authors and Affiliations

  1. Research Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, 1-308 Suematsu, Nonoichi, Ishikawa, 921-8836, Japan

    Takeshi Senoura, Takanori Kobayashi & Naoko K. Nishizawa

  2. Crop Biotech Institute and Graduate School of Biotechnology, Kyung Hee University, Yongin, 17104, Korea

    Gynheung An

  3. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Hiromi Nakanishi

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  1. Takeshi Senoura
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  2. Takanori Kobayashi
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  3. Gynheung An
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  4. Hiromi Nakanishi
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  5. Naoko K. Nishizawa
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Contributions

TS designed the research, carried out most of the experiments, and wrote the manuscript with discussion from all the co-authors. TK carried out data analysis and manuscript revision. GA provided the aco1(+ /−) T-DNA lines. HN and NKN supervised the research.

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Correspondence to Takanori Kobayashi or Naoko K. Nishizawa.

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Senoura, T., Kobayashi, T., An, G. et al. Defects in the rice aconitase-encoding OsACO1 gene alter iron homeostasis. Plant Mol Biol 104, 629–645 (2020). https://doi.org/10.1007/s11103-020-01065-0

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  • DOI: https://doi.org/10.1007/s11103-020-01065-0

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