Salt-induced hyperplastic growth and functional diversification in the root system of a salt-tolerant poplar species

Salinity stress is a growing global challenge. We investigated how Populus euphratica, a salinity-adapted tree, acclimates to NaCl from cellular to whole-plant levels. Photosynthesis and aboveground growth declined, but root length and biomass remained stable under salinity. Unlike lateral roots (LRs), main roots (MRs) displayed hyperplastic growth, with a twofold increase in tip diameter due to additional cortical cell layers but without changes in cell volume. This root thickening was Na⁺-specific and absent under KCl exposure. MRs accumulated high Na⁺ levels, while LRs did not, consistent with strong Na⁺ extrusion capacity and elevated expression of Na⁺ transporters in LRs, indicating specialized ion management within the root system. Transcriptomic analysis revealed stronger salinity responses in LRs, with enrichment of transcripts involved in stress defense, transport, and transcriptional regulation. In contrast, MRs upregulated genes related to mitotic cell division, steroid biosynthesis, and cell wall organization, supporting hyperplasia. Root phytohormones showed increased ABA and JA, especially in MRs, while auxin declined. Long-term salinity led to downregulation of stress responses in MRs, suggesting acclimation, whereas LRs maintained active defense pathways. GO enrichment highlighted distinct developmental programs: MRs prioritized cell proliferation and structural remodeling, while LRs focused on stress tolerance and salt extrusion. These results suggest that P. euphratica employs a dual salt-coping strategy: MRs undergo hyperplastic growth for structural resilience and ion buffering, while LRs dynamically exclude Na⁺ and transmit stress signals. This opens new perspectives on mechanisms of salt tolerance in plants, supporting that root-level specialization enables efficient salinity adaptation in halophytes.