Natural variation in salt-induced changes in root:shoot ratio reveals SR3G as a negative regulator of root suberization and salt resilience in Arabidopsis

Authors: ISHKA, MARYAM RAHMATI - Boyce Thompson Institute; SUSSAN, HAYLEY - Boyce Thompson Institute; HU, YUNFEI - Lanzhou University; DAGHASH, ALQAHTANI - King Abdullah University Of Science And Technology; Craft, Eric; SICAT, RONELL - King Abdullah University Of Science And Technology; WANG, MINMIM - University Of California, Davis; YU, LIANG - Boyce Thompson Institute; AITHADDOU, RASHID - King Abdullah University Of Science And Technology; LI, BO - Lanzhou University; DRAKAKAKI, GEORGIA - University Of California, Davis; NELSON, ANDREW - Boyce Thompson Institute; Pineros, Miguel; KORTE, ARTHUR - University Of Wurzburg; JAREMKO, LUKASZ - King Abdullah University Of Science And Technology; TESTERINK, CHRISTA - Wageningen University And Research Center; TESTER, MARK - King Abdullah University Of Science And Technology; JULKOWSKA, MAGDALENA - Boyce Thompson Institute

Submitted to: eLife
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/25/2024
Publication Date: 7/25/2024
Citation: Ishka, M., Sussan, H., Hu, Y., Daghash, A., Craft, E.J., Sicat, R., Wang, M., Yu, L., Aithaddou, R., Li, B., Drakakaki, G., Nelson, A., Pineros, M., Korte, A., Jaremko, L., Testerink, C., Tester, M., Julkowska, M. 2024. Natural variation in salt-induced changes in root:shoot ratio reveals SR3G as a negative regulator of root suberization and salt resilience in Arabidopsis. eLife. v1. https://doi.org/10.7554/eLife.98896.1.
DOI: https://doi.org/10.7554/eLife.98896.1

Interpretive Summary: We have used a cellular, developmental, and physiological analysis to identify a gene that regulates the growth of roots and shoots under salt-stress conditions. Using novel plant architectural features together with association mapping allowed us to discover a novel salt stress resilience gene. Functional characterization indicates this gene contributes to the salt tolerance response overall by regulating shoot growth, root suberization, and sodium accumulation. The innovative approach used and the findings contribute to our understanding of plant stress tolerance mechanisms. Furthermore, this study opens new avenues and a novel set of tools for genetic and agronomic strategies to enhance crop environmental resilience.

Technical Abstract: Soil salinity is one of the major threats to agricultural productivity worldwide. Salt stress exposure alters root and shoot growth rates, thereby affecting overall plant performance. While past studies have extensively documented the effect of salt stress on root elongation and shoot development separately, here we take an innovative approach by examining the coordination of root and shoot growth under salt stress conditions. Utilizing a newly developed tool for quantifying the root:shoot ratio in agar-grown Arabidopsis seedlings, we found that salt stress results in a loss of coordination between root and shoot growth rates. We identify a specific gene cluster encoding domain-of-unknown-function 247 (DUF247), and characterize one of these genes as Salt Root:shoot Ratio Regulator Gene (SR3G). Further analysis elucidates the role of SR3G as a negative regulator of salt stress tolerance, revealing its function in regulating shoot growth, root suberization, and sodium accumulation. We further characterize that SR3G expression is modulated by WRKY75 transcription factor, known as a positive regulator of salt stress tolerance. Finally, we show that the salt stress sensitivity of wrky75 mutant is completely diminished when it is combined with sr3g mutation. Together, our results demonstrate that utilizing root:shoot ratio as an architectural feature leads to the discovery of new stress resilience gene. The study’s innovative approach and findings not only contribute to our understanding of plant stress tolerance mechanisms but also open new avenues for genetic and agronomic strategies to enhance crop environmental resilience.