NAI2 and TSA1 Drive Differentiation of Constitutive and Inducible ER Body Formation in Brassicaceae

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  • Natalia Stefanik
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Jakub Bizan
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Alwine Wilkens
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Katarzyna Tarnawska-Glatt
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Shino Goto-Yamada
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Kazimierz Strzałka
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland
  • Mikio Nishimura
    Department of Cell Biology, National Institute for Basic Biology, Okazaki, 444-8585 Japan
  • Ikuko Hara-Nishimura
    Faculty of Science and Engineering, Konan University, Kobe, 658-8501 Japan
  • Kenji Yamada
    Malopolska Centre of Biotechnology, Jagiellonian University, Krakow 30-387, Poland

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<jats:title>Abstract</jats:title> <jats:p>Brassicaceae and closely related species develop unique endoplasmic reticulum (ER)-derived structures called ER bodies, which accumulate β-glucosidases/myrosinases that are involved in chemical defense. There are two different types of ER bodies: ER bodies constitutively present in seedlings (cER bodies) and ER bodies in rosette leaves induced by treatment with the wounding hormone jasmonate (JA) (iER bodies). Here, we show that At-α whole-genome duplication (WGD) generated the paralogous genes NAI2 and TSA1, which consequently drive differentiation of cER bodies and iER bodies in Brassicaceae plants. In Arabidopsis, NAI2 is expressed in seedlings where cER bodies are formed, whereas TSA1 is expressed in JA-treated leaves where iER bodies are formed. We found that the expression of NAI2 in seedlings and the JA inducibility of TSA1 are conserved across other Brassicaceae plants. The accumulation of NAI2 transcripts in Arabidopsis seedlings is dependent on the transcription factor NAI1, whereas the JA induction of TSA1 in rosette leaves is dependent on MYC2, MYC3 and MYC4. We discovered regions of microsynteny, including the NAI2/TSA1 genes, but the promoter regions are differentiated between TSA1 and NAI2 genes in Brassicaceae. This suggests that the divergence of function between NAI2 and TSA1 occurred immediately after WGD in ancestral Brassicaceae plants to differentiate the formation of iER and cER bodies. Our findings indicate that At-α WGD enabled diversification of defense strategies, which may have contributed to the massive diversification of Brassicaceae plants.</jats:p>

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