Development specifies, diversifies and empowers root immunity

Abstract

Roots are a highly organised plant tissue consisting of different cell types with distinct developmental functions defined by cell identity networks. Roots are the target of some of the most devastating diseases and possess a highly effective immune system. The recognition of microbe- or plant-derived molecules released in response to microbial attack is highly important in the activation of complex immunity gene networks. Development and immunity are intertwined, and immunity activation can result in growth inhibition. In turn, by connecting immunity and cell identity regulators, cell types are able to launch a cell type-specific immunity based on the developmental function of each cell type. By this strategy, fundamental developmental processes of each cell type contribute their most basic functions to drive cost-effective but highly diverse and, thus, efficient immune responses. This review highlights the interdependence of root development and immunity and how the developmental age of root cells contributes to positive and negative outcomes of development-immunity cross-talk.

Keywords: cell identity; pattern-triggered immunity; plant growth; root body plan; root development.

Figure 1. Functions of specific root cell types in plant development and immune responses to (pathogenic) microbes

The plant root body plan follows a strict cell type‐based organisation that determines the root's structure and equips it with functional plasticity to respond to changing environments. Consequently, each cell type fulfils specific tasks during plant development and in interaction with beneficial or pathogenic microbes. The outermost cell types, i.e. epidermis and root cap, promote nutrient availability and uptake in and from the soil. All cell types participate in the transport of water and/or nutrients towards the vasculature. Some root cell types have additional specific functions, e.g. in sensing physical stimuli during growth (root cap cells), lateral root formation (pericycle) or shootward transport of signalling molecules (phloem). Cell types such as the root cap, epidermis, cortex, endodermis and xylem produce various defence‐related substances or establish physical barriers to fend off or prevent the spread of potentially harmful microbial intruders. Besides this, root cap, epidermis and endodermis can affect the assembly of the root microbiome, e.g. by altering the nutrient composition in the rhizosphere. In addition, root hair and cortex cells can accommodate beneficial rhizobia, endophytes or mycorrhizal fungi, respectively. See text for references.

Figure 2. Development‐ and immunity‐related signalling processes are interconnected

(A) In mature cells in the differentiation zone (DZ), cell identity TFs (in orange) regulate gene networks that determine cell type‐specific functions in root development and immune responses to (pathogenic) microbes. This cell type‐specific interconnection of development with immune responses results in a highly versatile, and thus robust, overall root immunity. (B) Immunity interferes with developmental signalling and inhibits growth in younger, mitotically active cells of the root apical meristem (RAM) and elongation zone (EZ), e.g. via negatively regulating the activity of the cell cycle.

Figure 3. TFs connect cell identity and immunity gene networks to confer robust, cell type‐specific immunity

In the epidermis and other cell types, respective cell identity TFs pair up with immunity‐associated TFs to regulate cell type‐specific expression of immunity genes by binding to their promoters. This strategy allows the launch of cell type‐specific immune responses according to the specific developmental functions of each cell type. The interconnection of development/cell identity with cell type‐specific immunity gene networks diversifies the overall root immunity and may add to the robustness and adaptive plasticity of root responses to microbes under varying environments (compare Rich‐Griffin et al, 2020).