An official website of the United States government
Plant 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 organism Arabidopsis 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.
more »
« less
A suberized exodermis is required for tomato drought tolerance
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.
more »
« less
- PAR ID:
- 10543506
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Publisher / Repository:
- Nature Plants
- Date Published:
- Journal Name:
- Nature Plants
- Volume:
- 10
- Issue:
- 1
- ISSN:
- 2055-0278
- Page Range / eLocation ID:
- 118 to 130
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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.more » « less
-
Dupuy, Lionel (Ed.)Root barrier cell types, such as the endodermis and exodermis, are crucial for plant acclimation to environmental stresses. Deposition of suberin, a hydrophobic polymer, in these cell layers restricts the movement of molecules and plays a vital role in stress responses. This study investigates the role of SlMYB41, SlMYB92, and SlWRKY71 transcription factors (TFs) in regulating suberin biosynthesis in the tomato (Solanum lycopersicum) root exodermis by genetic perturbation. Genetic perturbation of these TFs altered exodermal suberin deposition patterns, indicating the SlMYBs as positive regulators and SlWRKY71 as a negative regulator of suberization. RNA sequencing revealed a significant overlap between differentially expressed genes regulated by these TFs, suggesting a shared regulatory network. Gene set enrichment analyses highlighted their role in lipid and suberin biosynthesis as well as over-representation of exodermis-enriched transcripts. Furthermore, transactivation assays demonstrated that these two MYBs promote the expression of suberin-related genes, while SlWRKY71 represses them. These results indicate a complex antagonistic relationship, advancing our understanding of the regulatory mechanisms controlling exodermis suberization in tomato roots.more » « less
-
Plant cells are defined by their walls, which, in addition to providing structural support and shape, are an integral component of the nonliving extracellular space called the apoplast. Cell wall thickenings are present in many different root cell types. They come in a variety of simple and more complex structures with varying composition of lignin and suberin and can change in response to environmental stressors. The majority of these root cell wall thickenings and cell types that contain them are absent in the model plantArabidopsis thalianadespite being present in most plant species. As a result, we know very little regarding their developmental control and function. Increasing evidence suggests that these structures are critical for responding to and facilitating adaptation to a wide array of stresses that a plant root experiences. These structures function in blocking apoplastic transport, oxygen, and water loss and enhancing root penetrative strength. In this review, we describe the most common types of cell wall thickenings in the outer cell types of plant roots—the velamen, exodermal thickenings, the sclerenchyma, and phi thickenings. Their cell-type dependency, morphology, composition, environmental responsiveness, and genetic control in vascular plants are discussed, as well as their potential to generate more stress-resilient roots in the face of a changing climate.more » « less
-
Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41477-023-01567-x
