A suberized exodermis is required for tomato drought tolerance

Abstract

SUMMARYPlant roots integrate environmental signals and developmental programs using exquisite spatiotemporal control. This is apparent in the deposition of suberin, an apoplastic diffusion barrier, which regulates the entry and exit of water, solutes and gases, and is environmentally plastic. Suberin is considered a hallmark of endodermal differentiation, but we find that it is absent in the tomato endodermis during normal development. Instead, suberin is present in the exodermis, a cell type that is absent in the model organismArabidopsis thaliana. Here, we uncover genes driving exodermal suberization and describe its effects on drought responses in tomato, unravelling the similarities and differences with the paradigmatic Arabidopsis endodermis. Cellular resolution imaging, gene expression, and mutant analyses reveal loss of this program from the endodermis, and its co-option in the exodermis. Functional genetic analyses of the tomato MYB92 transcription factor and ASFT enzyme demonstrate the importance of exodermal suberin for a plant water-deficit response. Controlling the degree of exodermal suberization could be a new strategy for breeding climate-resilient plants.

A Functional Exodermal Suberin is Key for Plant Nutrition and Growth in Potato

“…This early ability of exodermis to fully suberize the complete cylinder is a common feature in potato adventitious roots as seen in different commercial varieties as well as a wild relative, regarding hydroponics or soil culture ( Figure 1B , Figure 1C ) (Łotocka et al, 2016). The early suberization of exodermis is also common for tomato or pepper (Cantó-Pastor et al, 2022), and this differs from other crop plants, suggesting a common pattern within Solanaceae family. In comparison, endodermal cell remains for longer (or even permanently) in the state I of differentiation and, in regions where exodermis suberization is fully completed, some endodermal cells, specifically those localized in the phloem pole, progress to state II of suberization ( Figure 1C, 1D, Figure 2 ).…”

Regulation and Function of a Polarly Localized Lignin Barrier in the Exodermis

“…The endodermis and exodermis have been compared in composition and apoplastic barrier function in tomato (Kajala et al 2021; Cantó-Pastor et al 2022). Two hypotheses can be formulated as to the mechanisms that give rise to the similarities in this first stage of exodermal and endodermal differentiation - that they are governed by similar developmental factors or that they are determined by distinct regulatory mechanisms.…”

Cross-species single-cell annotation with orthologous marker gene groups

“…Tomato root is an ideal system because single-cell clusters were assigned based on comparison with bulk cell type-speci c expression analysis with promoter-GFP marker lines and cell sorting. The cell type assignment in tomato provides a higher con dence in the celltype identities 4,14 (Supplementary Fig. 5) as compared to species without such data.…”

“…Single-cell RNA sequencing (scRNA-seq) technology has been widely used in identifying and characterizing various cell types in numerous tissues from different plant species [1][2][3][4][5][6] . Efforts to apply this technology in the model plant Arabidopsis have bene ted from the extensive knowledge of cell-type identity markers 7,8 .…”