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Abstract Plant roots navigate the soil ecosystem with each cell type uniquely responding to environmental stimuli. Below ground, the plant's response to its surroundings is orchestrated at the cellular level, including morphological and molecular adaptations that shape root system architecture as well as tissue and organ functionality. Our understanding of the transcriptional responses at cell type resolution has been profoundly enhanced by studies of the model plant Arabidopsis thaliana. However, both a comprehensive view of the transcriptional basis of these cellular responses to single and combinatorial environmental cues in diverse plant species remains elusive. In this review, we highlight the ability of root cell types to undergo specific anatomical or morphological changes in response to abiotic and biotic stresses or cues and how they collectively contribute to the plant's overall physiology. We further explore interconnections between stress and the temporal nature of developmental pathways and discuss examples of how this transcriptional reprogramming influences cell type identity and function. Finally, we highlight the power of single-cell and spatial transcriptomic approaches to refine our understanding of how environmental factors fine tune root spatiotemporal development. These complex root system responses underscore the importance of spatiotemporal transcriptional mapping, with significant implications for enhanced agricultural resilience. 

Abstract Multicellular organisms control environmental interactions through specialized barriers in specific cell types. A conserved barrier in plant roots is the endodermal Casparian strip (CS), a ring-like structure made of polymerized lignin that seals the endodermal apoplastic space. Most angiosperms have another root cell type, the exodermis, that is reported to form a barrier. Our understanding of exodermal developmental and molecular regulation and function is limited as this cell type is absent fromArabidopsis thaliana. We demonstrate that in tomato (Solanum lycopersicum), the exodermis does not form a CS. Instead, it forms a polar lignin cap (PLC) with equivalent barrier function to the endodermal CS but distinct genetic control. Repression of the exodermal PLC in inner cortical layers is conferred by theSlSCZandSlEXO1transcription factors, and these two factors genetically interact to control its polar deposition. Several target genes that act downstream ofSlSCZandSlEXO1in the exodermis are identified. Although the exodermis and endodermis produce barriers that restrict mineral ion uptake, the exodermal PLC is unable to fully compensate for the lack of a CS. The presence of distinct lignin structures acting as apoplastic barriers has exciting implications for a root’s response to abiotic and biotic stimuli. 

Plant roots integrate environmental signals with development using exquisite spatiotemporal control. This is apparent in the deposition of suberin, an apoplastic diffusion barrier, which regulates flow of water, solutes and gases, and is environmentally plastic. Suberin is considered a hallmark of endodermal differentiation but is absent in the tomato endodermis. Instead, suberin is present in the exodermis, a cell type that is absent in the model organismArabidopsis thaliana. Here we demonstrate that the suberin regulatory network has the same parts driving suberin production in the tomato exodermis and theArabidopsisendodermis. Despite this co-option of network components, the network has undergone rewiring to drive distinct spatial expression and with distinct contributions of specific genes. Functional genetic analyses of the tomato MYB92 transcription factor and ASFT enzyme demonstrate the importance of exodermal suberin for a plant water-deficit response and that the exodermal barrier serves an equivalent function to that of the endodermis and can act in its place.