Alex Cantó-Pastor

The increasing frequency and severity of droughts pose a major threat to agriculture, food security and ecosystems. Plants respond to water deficit by adjusting growth and metabolism to enhance survival; these adjustments impact the soil microorganisms interacting with plant roots. Plants establish symbiotic relationships with arbuscular mycorrhizal fungi which supply soil nutrients in exchange for carbon metabolites via an intricate dual-species interface within roots. These fungi are dependent upon host-derived photosynthates and are thus potentially vulnerable to plant perturbations during drought. Here, we demonstrate that the plant-mycorrhizal relationship is dynamic when water becomes limiting. During water deficit, rice de-prioritizes nutrient acquisition gene regulatory networks, including its AM symbiotic program, in a strategy conserved with tomato. The fungal symbiont correspondingly represses its growth, undergoing metabolic quiescence, coupled with decommissioning of hyphae within the host’s root. Following re-watering, the host re-engages with its partner fungus, re-invigorating fungal growth and arbuscule establishment. This coordinate, reversible and enduring inter-organismal association may aid host survival under transient stress, but suggests that mutualisms in native and crop plants are potentially fragile in increasingly erratic climates.

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.

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 from Arabidopsis 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 the SlSCZ and SlEXO1 transcription factors, and these two factors genetically interact to control its polar deposition. Several target genes that act downstream of SlSCZ and SlEXO1 in 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.

Root barrier cell types, like 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 and SlWRKY71 negative regulators 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 overrepresentation 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. Highlight: MYB and WRKY transcription factors collaboratively regulate suberin biosynthesis in the tomato root exodermis. Antagonistic interactions may fine-tune suberization or act as a break to stop overaccumulation.

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 organism Arabidopsis thaliana. Here we demonstrate that the suberin regulatory network has the same parts driving suberin production in the tomato exodermis and the Arabidopsis endodermis. 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.

Summary: Inorganic phosphate (Pi) is a necessary macronutrient for basic biological processes. Plants modulate their root system architecture (RSA) and cellular processes to adapt to Pi deprivation albeit with a growth penalty. Excess application of Pi fertilizer, on the contrary, leads to eutrophication and has a negative environmental impact. We compared RSA, root hair elongation, acid phosphatase activity, metal ion accumulation, and brassinosteroid hormone levels of Solanum lycopersicum (tomato) and Solanum pennellii, which is a wild relative of tomato, under Pi sufficiency and deficiency conditions to understand the molecular mechanism of Pi deprivation response in tomato. We showed that S. pennellii is partially insensitive to phosphate deprivation. Furthermore, it mounts a constitutive response under phosphate sufficiency. We demonstrate that activated brassinosteroid signaling through a tomato BZR1 ortholog gives rise to the same constitutive phosphate deficiency response, which is dependent on zinc overaccumulation. Collectively, these results reveal an additional strategy by which plants can adapt to phosphate starvation.

Multicellular organisms control interactions with their environment through the development of specialized barriers in specific cell types. A conserved barrier in plant roots is the endodermal Casparian strip (CS). The CS is made of polymerized lignin and forms a ring-like structure that seals the apoplastic space between the endodermal cells. Most angiosperms also have another root cell type, the exodermis, that is reported to form a barrier. Our understanding of exodermal developmental and molecular regulation, as well as function, is limited as this cell type is absent from the model species Arabidopsis thaliana . Using tomato ( Solanum lycopersicum ) as a model system we demonstrate that in this species, the exodermis does not form a CS. Instead, it forms a polar lignin cap with an equivalent barrier function to the endodermal CS. We demonstrate that although endodermal regulators are conserved between Arabidopsis and tomato, exodermal differentiation occurs by a distinct regulatory pathway involving the SlSCZ and SlEXO1 transcription factors. Although the exodermis and endodermis both produce barriers that restrict mineral ion uptake, they have unique and overlapping roles in their selectivity. Whether conservation and similarities between the endodermis and exodermis exist in other species remains to be determined. Nonetheless, in tomato, these distinct lignin structures have a convergent function with different genetic regulations.

SUMMARY: 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.

Plant species have evolved myriads of solutions to adapt to dynamic environments, including complex cell type development and regulation. To understand this diversity, we profiled tomato root cell type translatomes and chromatin accessibility. Using xylem differentiation in tomato, relative to Arabidopsis, examples of functional innovation, repurposing and conservation of transcription factors are described. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Translatome analyses of rice, tomato and Arabidopsis tissues suggest that root meristems are more conserved, and that 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 conserved between plants and animals. One Sentence Summary: Pan-species cell type translatome and chromatin accessibility data reveal novelty, conservation and repurposing of gene function.