Plants adapt to heterogeneous soil conditions by altering their root architecture. For example, roots branch when in contact with water by using the hydropatterning response. We report that hydropatterning is dependent on auxin response factor ARF7. This transcription factor induces asymmetric expression of its target gene LBD16 in lateral root founder cells. This differential expression pattern is regulated by posttranslational modification of ARF7 with the small ubiquitin-like modifier (SUMO) protein. SUMOylation negatively regulates ARF7 DNA binding activity. ARF7 SUMOylation is required to recruit the Aux/IAA (indole-3-acetic acid) repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that SUMO-dependent regulation of auxin response controls root branching pattern in response to water availability.

Lateral roots are crucial for increasing surface area of root systems to explore heterogeneous soil environments. Major advances have recently been made in the model plant Arabidopsis thaliana to elucidate the cellular basis of lateral root development and the underlying gene regulatory networks that control morphogenesis of the new root organ. This has provided the foundation on which to understand the sophisticated adaptive mechanisms that regulate how plants pattern their root branching to match the spatial availability of resources like water and nutrients in their external environment. We review new insights into the molecular, cellular and environmental regulation of LR development in Arabidopsis.

Plant roots exhibit plasticity in their branching patterns to forage efficiently for heterogeneously distributed resources, such as soil water. The xerobranching response represses lateral root formation when roots lose contact with water. Here, we show that xerobranching is regulated by radial movement of the phloem-derived hormone abscisic acid, which disrupts intercellular communication between inner and outer cell layers through plasmodesmata. Closure of these intercellular pores disrupts the inward movement of the hormone signal auxin, blocking lateral root branching. Once root tips regain contact with moisture, the abscisic acid response rapidly attenuates. Our study reveals how roots adapt their branching pattern to heterogeneous soil water conditions by linking changes in hydraulic flux with dynamic hormone redistribution.

Root branching is influenced by the soil environment and exhibits a high level of plasticity. We report that the radial positioning of emerging lateral roots is influenced by their hydrological environment during early developmental stages. New lateral root primordia have both a high degree of flexibility in terms of initiation and development angle towards the available water. Our observations reveal how the external hydrological environment regulates lateral root morphogenesis. Main textThe soil environment contains a variety of niches for a growing root to explore. This complex environment consists of nutrient rich areas, air pockets, stones etc. and strongly varies in its moisture distribution, to which we refer as the hydrological landscape. The ability of a root system to absorb water and nutrients efficiently from a heterogeneous medium depends on its architecture and its ability to adapt to the available potential resources 1 . For example, plants generate lateral roots in nutrient rich patches and reduce branching in dry areas 2,3 . Similarly, roots emerge on that side of the primary root, which is in contact with moisture, a mechanism called hydropatterning 4,5 . Here we show that lateral root morphogenesis is steered by the available moisture during lateral root primordia initiation, while outgrowth stages and plasticity in organogenesis are likely directed by lateral root flanking cells.

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