Hydrogen sulfide promotes lateral root formation in peach through persulfidation of SnRK1α kinase.

Abstract

Root development is crucial for the growth and yield of horticultural crops. Hydrogen sulfide (H₂S), an important gasotransmitter, has been shown to regulate lateral root (LR) formation in plants, including peach (Prunus persica). However, its specific regulatory mechanism remains largely unclear. Here, we show that the energy/metabolic sensor SUCROSE NON-FERMENTING RELATED KINASE 1 (SnRK1) mediates the control of peach LR growth by H₂S. PpSnRK1 activity in peach roots is enhanced with H₂S to promote LR generation. Cys419, Cys430 and Cys505 residues in the catalytic α-subunit of PpSnRK1 are modified by H₂S persulfidation. Reduced persulfidation inhibits the H₂S-induced PpSnRK1 activity. Mutating Cys419 and Cys430 of PpSnRK1α severely impedes H₂S-promoted LR formation. LATERAL ORGAN BOUNDARIES DOMAIN 16 (LBD16) is a transcription factor essential for LR initiation. Further evidence shows that PpSnRK1α interacts with PpLBD16 in the nucleus, thereby enhancing the transcription of LR development-related genes PpCNGC1 (CYCLIC NUCLEOTIDE-GATED ION CHANNEL 1) and PpEXPB2 (EXPANSIN-B2). In peach roots, transcription of these two genes is markedly up-regulated by H₂S-induced PpSnRK1 activity. Silencing of PpLBD16, PpEXPB2 or PpCNGC1 significantly reduces exogenous H₂S-induced LR formation. In situ hybridization analysis shows that they are strongly expressed in peach LR primordia along with PpSnRK1α. Our data reveal an interaction between H₂S signal and SnRK1 kinase, providing mechanistic insights into the shaping of agronomically important root systems.