The phenomenon of plant root tips sensing moisture gradient in soil and growing towards higher water potential is designated as root hydrotropism, which is critical for plants to survive when water is a limited factor. Molecular mechanisms regulating such a fundamental process, however, are largely unknown. Here we report our identification that cytokinins are key signaling molecules directing root growth orientation in a hydrostimulation (moisture gradient) condition. Lower water potential side of the root tip shows more cytokinin response relative to the higher water potential side. Consequently, two cytokinin downstream type-A response regulators, ARR16 and ARR17, were found to be up-regulated at the lower water potential side, causing increased cell division in the meristem zone, which allows the root to bend towards higher water potential side. Genetic analyses indicated that various cytokinin biosynthesis and signaling mutants, including the arr16 arr17 double mutant, are significantly less responsive to hydrostimulation. Consistently, treatments with chemical inhibitors interfering with either cytokinin biosynthesis or cell division completely abolished root hydrotropic response. Asymmetrically induced expression of ARR16 or ARR17 effectively led to root bending in both wild-type and miz1, a previously known hydrotropism-defective mutant. These data demonstrate that asymmetric cytokinin distribution is a primary determinant governing root hydrotropism.Cell Research (2019) 29:984-993; https://doi.
Root growth is maintained by the continuous division of cells in the apical meristem. ROOT MERISTEM GROWTH FACTOR 1 (RGF1) is a critical peptide hormone regulating root stem cell niche maintenance. Previous studies discovered that five closely related leucine-rich repeat receptor-like protein kinases (LRR-RLKs), named RGF1 INSENSITIVES (RGIs) or RGF1 RECEPTORS (RGFRs), are able to perceive the RGF1 signal and redundantly control root stem cell niche maintenance. RGF1 regulates root meristem activity mainly via two downstream transcription factors, PLETHORA 1 (PLT1) and PLT2. Regulatory proteins connecting cell surface RGF1-RGI1 and nuclear PLTs, however, were not identified. Here, we report that the mitogen-activated protein (MAP) kinase kinase 4 (MKK4) and MAP kinase 3 (MPK3) were coimmunoprecipitated with RGI1-FLAG after Arabidopsis seedlings were treated with RGF1. Genetic and biochemical assays confirmed that MKK4 and MKK5, and their downstream targets MPK3 and MPK6, are essential RGI-dependent regulators of root meristem development. In addition, we found that the MKK4/MKK5-MPK3/MPK6 module functions downstream of YDA, a MAPKKK. Our results demonstrate that RGF1-RGI1 regulate the expression of PLT1/PLT2 via a YDA-MKK4/MKK5-MPK3/MPK6 signaling cascade.
Receptor-like protein kinases (RLKs) play key roles in regulating plant growth, development and stress adaptations. There are at least 610 RLKs (including receptor-like cytoplasmic kinases) in Arabidopsis. The functions of the majority of RLKs have not yet been determined. We previously generated promoter::GUS transgenic plants for all leucine-rich repeat (LRR)-RLKs in Arabidopsis and analyzed their expression patterns during various developmental stages. We found the expression of two LRR-RLKs, MUSTACHES (MUS) and MUSTACHES-LIKE (MUL), are overlapped in lateral root primordia. Independent mutants, mus-3 mul-1 and mus-4 mul-2, show a significantly decreased emerged lateral root phenotype. Our analyses indicate that the defects of the double mutant occur mainly at stage I of lateral root development. Exogenous application of auxin can dramatically enhance the transcription of MUS, which is largely dependent on AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19. MUS and MUL are inactive kinases in vitro but are phosphorylated in planta, possibly by an unknown kinase. The kinase activity of MUS is dispensable for its function in lateral root development. Many cell wall related genes are down regulated in mus-3 mul-1. In conclusion, we identified MUS and MUL, two kinase-inactive RLKs, in controlling the early development of lateral root primordia likely via regulating cell wall synthesis and remodeling.
Rooting is a key innovation during plant terrestrialization. RGFs/GLVs/CLELs are a family of secreted peptides, playing key roles in root stem cell niche maintenance and pattern formation. The origin of this peptide family is not well characterized. RGFs and their receptor genes, RGIs, were investigated comprehensively using phylogenetic and genetic analyses. We identified 203 RGF genes from 24 plant species, representing a variety of land plant lineages. We found that the RGF genes originate from land plants and expand via multiple duplication events. The lineage-specific RGF duplicates are retained due to their regulatory divergence, while a majority of RGFs experienced strong purifying selection in most land plants. Functional analysis indicated that RGFs and their receptor genes, RGIs, isolated from liverwort, tomato, and maize possess similar biological functions with their counterparts from Arabidopsis in root development. RGFs and RGIs are likely coevolved in land plants. Our studies shed light on the origin and functional conservation of this important peptide family in plant root development.
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