4.7 Article

Cytokinin signaling promotes salt tolerance by modulating shoot chloride exclusion in maize

Journal

MOLECULAR PLANT
Volume 16, Issue 6, Pages 1031-1047

Publisher

CELL PRESS
DOI: 10.1016/j.molp.2023.04.011

Keywords

cytokinin signaling; salt tolerance; high-Cl- tolerance; Cl-transporter; maize

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This study investigates the molecular mechanisms underlying the exclusion of chloride (Cl-) from shoots and natural variation of salt tolerance in maize. It finds that a type A response regulator (ZmRR1) negatively regulates cytokinin signaling and salt tolerance by inhibiting His phosphotransfer proteins. The study also reveals that ZmRR1 undergoes degradation under saline conditions, leading to the release of ZmHP2 and subsequent improvement of salt tolerance through promoting Cl- exclusion from shoots. Additionally, the study shows that ZmHP2-mediated signaling upregulates ZmMATE29 and its tonoplast-located Cl- transporter function, facilitating Cl- exclusion from shoots. These findings provide important insights into the molecular mechanisms of salt tolerance and offer promising strategies for developing salt-tolerant maize.
Excessive accumulation of chloride (Cl-) in the aboveground tissues under saline conditions is harmful to crops. Increasing the exclusion of Cl- from shoots promotes salt tolerance in various crops. However, the underlying molecular mechanisms remain largely unknown. In this study, we demonstrated that a type A response regulator (ZmRR1) modulates Cl- exclusion from shoots and underlies natural variation of salt tolerance in maize. ZmRR1 negatively regulates cytokinin signaling and salt tolerance, likely by interacting with and inhibiting His phosphotransfer (HP) proteins that are key mediators of cytokinin signaling. A naturally occurring non-synonymous SNP variant enhances the interaction between ZmRR1 and ZmHP2, conferring maize plants with a salt-hypersensitive phenotype. We found that ZmRR1 undergoes degradation under saline conditions, leading to the release of ZmHP2 from ZmRR1 inhibition, and subsequently ZmHP2-mediated signaling improves salt tolerance primarily by promoting Cl- exclusion from shoots. Furthermore, we showed that ZmMATE29 is transcriptionally upregulated by ZmHP2-mediated signaling under highly saline conditions and encodes a tonoplast-located Cl- transporter that promotes Cl- exclusion from shoots by compartmentalizing Cl- into the vacuoles of root cortex cells. Collectively, our study provides an important mechanistic understanding of the cytokinin signaling-mediated promotion of Clexclusion from shoots and salt tolerance and suggests that genetic modification to promote Cl- exclusion from shoots is a promising route for developing salt-tolerant maize.

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