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Excess sterols disrupt plant cellular activity by inducing stress-responsive gene expression

  • Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
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Abstract

Sterols are important lipid constituents of cellular membranes in plants and other organisms. Sterol homeostasis is under strict regulation in plants because excess sterols negatively impact plant growth. HIGH STEROL ESTER 1 (HISE1) functions as a negative regulator of sterol accumulation. If sterol production exceeds a certain threshold, excess sterols are detoxified via conversion to sterol esters by PHOSPHOLIPID STEROL ACYL TRANSFERASE 1 (PSAT1). We previously reported that the Arabidopsis thaliana double mutant hise1-3 psat1-2 shows 1.5-fold higher sterol content than the wild type and consequently a severe growth defect. However, the specific defects caused by excess sterol accumulation in plants remain unknown. In this study, we investigated the effects of excess sterols on plants by analyzing the phenotypes and transcriptomes of the hise1-3 psat1-2 double mutant. Transcriptomic analysis revealed that 435 genes were up-regulated in hise1-3 psat1-2 leaves compared with wild-type leaves. Gene ontology (GO) enrichment analysis revealed that abiotic and biotic stress-responsive genes including RESPONSIVE TO DESICCATION 29B/LOW-TEMPERATURE-INDUCED 65 (RD29B/LTI65) and COLD-REGULATED 15A (COR15A) were up-regulated in hise1-3 psat1-2 leaves compared with wild-type leaves. Expression levels of senescence-related genes were also much higher in hise1-3 psat1-2 leaves than in wild-type leaves. hise1-3 psat1-2 leaves showed early senescence, suggesting that excess sterols induce senescence of leaves. In the absence of sucrose, hise1-3 psat1-2 exhibited defects in seedling growth and root elongation. Together, our data suggest that excess sterol accumulation disrupts cellular activities of vegetative organs including leaves and roots, resulting in multiple damages to plants.

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Acknowledgements

This work was supported by Grants-in-Aid for Scientific Research (JP15H05776 and JP22000014 to I.H.-N.; JP16K18834 and JP19K05809 to T.L.S.; JP18H03330 to H.T.) from the Japan Society for the Promotion of Science (JSPS); Leading Initiative for Excellent Young Researchers (LEADER; J16HJ00026 to T.L.S.) and a Grant-in-Aid for Scientific Research on Innovative Areas (KAKENHI, JP17H05659 to H.T.) from the Ministry of Education, Culture, Sports, Science and Technology in Japan (MEXT); Kato Memorial Bioscience Foundation to T.L.S.; SUNBOR GRANT of Suntory Foundation for life science to T.L.S.; Phytochemical Plant Molecular Science of Strategic Priority Research Promotion Program from Chiba University to T.L.S.; the NIBB Collaborative Research Program (17-301, 17-453, 18-301, 18-412, 19-302 to T.L.S.), and the Hirao Taro Foundation of KONAN GAKUEN for Academic Research to I.H.-N. We thank Miwako Matsumoto (NIBB), Asaka Akita (NIBB), Kazuo Ebine (NIBB), and Mitsumasa Hanaoka (Chiba University) for technical assistance.

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Authors and Affiliations

  1. Graduate School of Horticulture, Chiba University, Matsudo648, Matsudo, Chiba, 271-8510, Japan

    Takashi L. Shimada & Hiro Takahashi

  2. Plant Molecular Science Center, Chiba University, Chiba, Chiba, 260-8675, Japan

    Takashi L. Shimada

  3. NIBB Core Research Facilities, National Institute for Basic Biology, Okazaki, Aichi, 444-8585, Japan

    Katsushi Yamaguchi & Shuji Shigenobu

  4. Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, 920-1192, Japan

    Hiro Takahashi & Masataka Murase

  5. Institute of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Ishikawa, 920-1192, Japan

    Shuichi Fukuyoshi

  6. Faculty of Science and Engineering, Konan University, Kobe, Hyogo, 658-8501, Japan

    Ikuko Hara-Nishimura

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  1. Takashi L. Shimada
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  2. Katsushi Yamaguchi
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  3. Shuji Shigenobu
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  4. Hiro Takahashi
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  6. Shuichi Fukuyoshi
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  7. Ikuko Hara-Nishimura
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Correspondence to Takashi L. Shimada.

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Shimada, T.L., Yamaguchi, K., Shigenobu, S. et al. Excess sterols disrupt plant cellular activity by inducing stress-responsive gene expression. J Plant Res 133, 383–392 (2020). https://doi.org/10.1007/s10265-020-01181-4

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  • DOI: https://doi.org/10.1007/s10265-020-01181-4

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