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The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes

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Abstract

It is known that the polyamine (PA) biosynthetic pathway is modulated at the transcriptional level during abiotic stresses. Here we studied the expression of PA biosynthetic pathway genes upon exposure to heat shock (HS) in Arabidopsis and showed that the spermine (Spm) synthase gene (SPMS) and S-adenosylmethionine decarboxylase 2 gene are induced at the earliest stage, followed by the induction of the arginine decarboxylase 2 gene. Correspondingly, Spm content increased linearly upon HS, and putrescine (Put) and spermidine (Spd) content also increased but not thermospermine (T-Spm) content. Exogenously applied Spm had a potential to protect Arabidopsis plants from HS-induced damage. Such protection was also observed to the same extent with T-Spm and by Spd to a lesser extent but not by Put. Then we tested whether altered endogenous Spm content affects sensitivity to HS using both transgenic plants overexpressing SPMS and a Spm deficient (spms) mutant plant. The result revealed that the higher the Spm content the higher the thermotolerance. Even in the spms plant, representative genes encoding heat shock proteins (HSPs) and heat shock transcription factors were upregulated upon HS, while the expression of such genes was increased in a positively correlated manner with Spm content. Furthermore four kinds of HSPs (HSP101, HSP90, HSP70 and HSP17.6) were detected proportionally with the levels of their respective transcripts upon HS. We propose that Spm increases the HS response at transcriptional and translational levels and protects host plants from HS-induced damage.

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Acknowledgments

We thank Anthony J. Michael for critically reading the manuscript. This work was supported in part by Grant-in-Aids from the Japan Society for the Promotion of Science (JSPS) to TK (21380063) and YT (21780087, 23780345), by the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts to TB and by the grant from The Saito Gratitude Foundation to GHMS. GHMS is a recipient of a MEXT fellowship.

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Authors and Affiliations

  1. Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba, Sendai, Miyagi, 980-8577, Japan

    G. H. M. Sagor, Yoshihiro Takahashi & Tomonobu Kusano

  2. Biodiversity and Climate Research Center (BiK-F), 60323, Frankfurt, Germany

    Thomas Berberich

  3. Faculty of Pharmaceutical Sciences, Josai University, Sakado, Saitama, 350-0295, Japan

    Masaru Niitsu

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  1. G. H. M. Sagor
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  2. Thomas Berberich
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  3. Yoshihiro Takahashi
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  4. Masaru Niitsu
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  5. Tomonobu Kusano
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Correspondence to Tomonobu Kusano.

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Sagor, G.H.M., Berberich, T., Takahashi, Y. et al. The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22, 595–605 (2013). https://doi.org/10.1007/s11248-012-9666-3

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