Spatial and developmental reprogramming enables root growth under high salinity
Thu NguyeniD, Jason R GarciaiD, Samadhi S. WimalagunasekaraiD, Richard GarciaiD, Hannah Holliday, Maria IftesumiD, Elif Gediz KocaoglaniD, James V Moroney, Manas Ranjan GartiaiD, Jose Ramon DinnenyiD, Maheshi DassanayakeiD
Abstract
How do plant roots sustain growth under salinity levels that would normally arrest development? The extremophyte Schrenkiella parvula maintains root growth under high salinity through a previously unrecognized spatial reorganization of primary root development. The root elongation zone transitions into two distinct developmental states, the bulged and gap zones, during a transient growth pause that precedes renewed tip growth and localized lateral root emergence. In Arabidopsis, a related salt-sensitive species, the cells in the elongation zone simply burst. Jasmonic acid was found to be necessary to initiate this transition in S. parvula, while spatially coordinated jasmonic acid and auxin accumulation accompanies zone establishment and maintenance. We constructed zone-resolved transcriptomic networks to distinguish developmental from salt-responsive processes and identified their interactions under salinity stress. Salt-induced zone-specific networks revealed distinct regulatory programs coordinating hormone signaling, cell wall remodeling, and water, ion, and reactive oxygen species homeostasis. Cell layer-specific Raman spectroscopy, UHPLC-MS/MS metabolite profiling, and cellular imaging provide independent support for the transcriptomic networks, linking spatially organized cellular responses with salt stress mitigation, suppression of cell death, and continued growth. We also identified orthologous genes potentially recruited into novel regulatory roles that support growth under stress. Together, these findings establish spatial developmental reprogramming as a strategy for sustaining root growth under salinity and identify candidate mechanisms for improving crop salt tolerance.
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