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SUPPRESSOR OF GAMMA RESPONSE 1 acts as a regulator coordinating crosstalk between DNA damage response and immune response in Arabidopsis thaliana

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Abstract

Plants live in constantly changing and often unfavorable or stressful environments. Environmental changes induce biotic and abiotic stress, which, in turn, may cause genomic DNA damage. Hence, plants simultaneously suffer abiotic/biotic stress and DNA damage. However, little information is available on the signaling crosstalk that occurs between DNA damage and abiotic/biotic stresses. Arabidopsis thaliana SUPPRESSOR OF GAMMA RESPONSE1 (SOG1) is a pivotal transcription factor that regulates thousands of genes in response to DNA double-strand break (DSB), and we recently reported that SOG1 has a role in immune responses. In the present study, the effects of SOG1 overexpression on the DNA damage and immune responses were examined. Results found that SOG1 overexpression enhances the regulation of numerous downstream genes. Relative to the wild type plants, then, DNA damage responses were observed to be strongly induced. SOG1 overexpression also upregulates chitin (a major components of fungal cell walls) responsive genes in the presence of DSBs, implying that pathogen defense response is activated by DNA damage via SOG1. Further, SOG1 overexpression enhances fungal resistance. These results suggest that SOG1 regulates crosstalk between DNA damage response and the immune response and that plants have evolved a sophisticated defense network to contend with environmental stress.

Key message

Overexpression of SOG1 enhances various DNA damage responses and fungal resistance, suggesting that SOG1 regulates the crosstalk between the DNA damage response and immune responses.

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Acknowledgements

The authors thank Drs. Atsushi Higashitani and Shusei Sato for their support in the present study. We also thank Drs. Mika Teranishi and Yasukazu Daigaku for their helpful discussion throughout the study. This work was supported by JSPS KAKENHI (Grant No. 17K07455 to K.O.Y.; Grant No. 19K06708 to N. T.; Grant No. 18H04822 to K. H.; Grant No. 16KT0031 and 18H02467 to Y. S.; Grant No. 15H05945 and 17H01872 to J. H.; Grant No. 17H06470, 17H06477 and 17H03965 to M. U.; Grant No. 16H01472, 16K07408, 18H04787, and 18H04844 to S. K.), by JST (Grant No. JPMJPR16Q7 to K. H.), by the MEXT Supported Program for the Strategic Research Foundation at Private Universities from the Ministry of Education, Culture, Sports, Science & Technology of Japan, (Grant No. S1511023 to S.K.), and by the Sumitomo foundation (Grant No. 181147 to K. O. Y).

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Authors and Affiliations

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

    Kaoru Okamoto Yoshiyama & Jun Hidema

  2. Life Sciences, Kyoto Sangyo University, Kamigamo Motoyama Kitaku, Kyoto, 603-8555, Japan

    Tomoaki Sakamoto & Seisuke Kimura

  3. Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara, 630-0192, Japan

    Naoki Aoshima, Naoki Takahashi, Kei Hiruma, Yusuke Saijo & Masaaki Umeda

  4. Center for Ecological Evolutionary Developmental Biology, Kyoto Sangyo University, Kamigamo Motoyama Kitaku, Kyoto, 603-8555, Japan

    Seisuke Kimura

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  1. Kaoru Okamoto Yoshiyama
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  2. Naoki Aoshima
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  4. Tomoaki Sakamoto
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  5. Kei Hiruma
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Contributions

KOY planned the experiments and performed most of the experiments. TS performed analysis of SOG1-binding sequence. SK performed data RNA-seq data analysis. NA, NT, KH, YS, and MU, performed pathogen inoculating assay. KOY, JH, and SK conceived the project and wrote the manuscript.

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Correspondence to Seisuke Kimura.

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Yoshiyama, K.O., Aoshima, N., Takahashi, N. et al. SUPPRESSOR OF GAMMA RESPONSE 1 acts as a regulator coordinating crosstalk between DNA damage response and immune response in Arabidopsis thaliana. Plant Mol Biol 103, 321–340 (2020). https://doi.org/10.1007/s11103-020-00994-0

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