Widespread horizontal gene transfer between plants and bacteria.

Plants host a large array of commensal bacteria that interact with the host. The growth of both bacteria and plants is often dependent on nutrients derived from the cognate partners, and the bacteria fine-tune host immunity against pathogens. This ancient interaction is common in all studied land plants and is critical for proper plant health and development. We hypothesized that the spatial vicinity and the long-term relationships between plants and their microbiota may promote cross-kingdom horizontal gene transfer (HGT), a phenomenon that is relatively rare in nature. To test this hypothesis, we analyzed the Arabidopsis thaliana genome and its extensively sequenced microbiome to detect events of horizontal transfer of full-length genes that transferred between plants and bacteria. Interestingly, we detected 75 unique genes that were horizontally transferred between plants and bacteria. Plants and bacteria exchange in both directions genes that are enriched in carbohydrate metabolism functions, and bacteria transferred to plants genes that are enriched in auxin biosynthesis genes. Next, we provided a proof of concept for the functional similarity between a horizontally transferred bacterial gene and its Arabidopsis homologue in planta. The Arabidopsis DET2 gene is essential for biosynthesis of the brassinosteroid phytohormones, and loss of function of the gene leads to dwarfism. We found that expression of the DET2 homologue from Leifsonia bacteria of the Actinobacteria phylum in the Arabidopsis det2 background complements the mutant and leads to normal plant growth. Together, these data suggest that cross-kingdom HGT events shape the metabolic capabilities and interactions between plants and bacteria.

Fine-scale diversity of microbial communities due to satellite niches in boom and bust environments.

Recent observations have revealed that closely related strains of the same microbial species can stably coexist in natural and laboratory settings subject to boom and bust dynamics and serial dilutions, respectively. However, the possible mechanisms enabling the coexistence of only a handful of strains, but not more, have thus far remained unknown. Here, using a consumer-resource model of microbial ecosystems, we propose that by differentiating along Monod parameters characterizing microbial growth rates in high and low nutrient conditions, strains can coexist in patterns similar to those observed. In our model, boom and bust environments create satellite niches due to resource concentrations varying in time. These satellite niches can be occupied by closely related strains, thereby enabling their coexistence. We demonstrate that this result is valid even in complex environments consisting of multiple resources and species. In these complex communities, each species partitions resources differently and creates separate sets of satellite niches for their own strains. While there is no theoretical limit to the number of coexisting strains, in our simulations, we always find between 1 and 3 strains coexisting, consistent with known experiments and observations.

Complementary resource preferences spontaneously emerge in diauxic microbial communities.

Many microbes grow diauxically, utilizing the available resources one at a time rather than simultaneously. The properties of communities of microbes growing diauxically remain poorly understood, largely due to a lack of theory and models of such communities. Here, we develop and study a minimal model of diauxic microbial communities assembling in a serially diluted culture. We find that unlike co-utilizing communities, diauxic community assembly repeatably and spontaneously leads to communities with complementary resource preferences, namely communities where species prefer different resources as their top choice. Simulations and theory explain that the emergence of complementarity is driven by the disproportionate contribution of the top choice resource to the growth of a diauxic species. Additionally, we develop a geometric approach for analyzing serially diluted communities, with or without diauxie, which intuitively explains several additional emergent community properties, such as the apparent lack of species which grow fastest on a resource other than their most preferred resource. Overall, our work provides testable predictions for the assembly of natural as well as synthetic communities of diauxically shifting microbes.

Optimal BR signalling is required for adequate cell wall orientation in the Arabidopsis root meristem.

Plant brassinosteroid hormones (BRs) regulate growth in part through altering the properties of the cell wall, the extracellular matrix of plant cells. Conversely, feedback signalling from the wall connects the state of cell wall homeostasis to the BR receptor complex and modulates BR activity. Here, we report that both pectin-triggered cell wall signalling and impaired BR signalling result in altered cell wall orientation in the Arabidopsis root meristem. Furthermore, both depletion of endogenous BRs and exogenous supply of BRs triggered these defects. Cell wall signalling-induced alterations in the orientation of newly placed walls appear to occur late during cytokinesis, after initial positioning of the cortical division zone. Tissue-specific perturbations of BR signalling revealed that the cellular malfunction is unrelated to previously described whole organ growth defects. Thus, tissue type separates the pleiotropic effects of cell wall/BR signals and highlights their importance during cell wall placement.

Multistability and regime shifts in microbial communities explained by competition for essential nutrients.

Microbial communities routinely have several possible species compositions or community states observed for the same environmental parameters. Changes in these parameters can trigger abrupt and persistent transitions (regime shifts) between such community states. Yet little is known about the main determinants and mechanisms of multistability in microbial communities. Here, we introduce and study a consumer-resource model in which microbes compete for two types of essential nutrients each represented by multiple different metabolites. We adapt game-theoretical methods of the stable matching problem to identify all possible species compositions of such microbial communities. We then classify them by their resilience against three types of perturbations: fluctuations in nutrient supply, invasions by new species, and small changes of abundances of existing ones. We observe multistability and explore an intricate network of regime shifts between stable states in our model. Our results suggest that multistability requires microbial species to have different stoichiometries of essential nutrients. We also find that a balanced nutrient supply promotes multistability and species diversity, yet make individual community states less stable.

Interdependent Nutrient Availability and Steroid Hormone Signals Facilitate Root Growth Plasticity.

Plants acquire essential elements from inherently heterogeneous soils, in which phosphate and iron availabilities vary. Consequently, plants have developed adaptive strategies to cope with low iron or phosphate levels, including alternation between root growth enhancement and attenuation. How this adaptive response is achieved remains unclear. Here, we found that low iron accelerates root growth in Arabidopsis thaliana by activating brassinosteroid signaling, whereas low-phosphate-induced high iron accumulation inhibits it. Altered hormone signaling intensity also modulated iron accumulation in the root elongation and differentiation zones, constituting a feedback response between brassinosteroid and iron. Surprisingly, the early effect of low iron levels on root growth depended on the brassinosteroid receptor but was apparently hormone ligand-independent. The brassinosteroid receptor inhibitor BKI1, the transcription factors BES1/BZR1, and the ferroxidase LPR1 operate at the base of this feedback loop. Hence, shared brassinosteroid and iron regulatory components link nutrient status to root morphology, thereby driving the adaptive response.

High Resolution Quantification of Crystalline Cellulose Accumulation in Arabidopsis Roots to Monitor Tissue-specific Cell Wall Modifications.

Plant cells are surrounded by a cell wall, the composition of which determines their final size and shape. The cell wall is composed of a complex matrix containing polysaccharides that include cellulose microfibrils that form both crystalline structures and cellulose chains of amorphous organization. The orientation of the cellulose fibers and their concentrations dictate the mechanical properties of the cell. Several methods are used to determine the levels of crystalline cellulose, each bringing both advantages and limitations. Some can distinguish the proportion of crystalline regions within the total cellulose. However, they are limited to whole-organ analyses that are deficient in spatiotemporal information. Others relying on live imaging, are limited by the use of imprecise dyes. Here, we report a sensitive polarized light-based system for specific quantification of relative light retardance, representing crystalline cellulose accumulation in cross sections of Arabidopsis thaliana roots. In this method, the cellular resolution and anatomical data are maintained, enabling direct comparisons between the different tissues composing the growing root. This approach opens a new analytical dimension, shedding light on the link between cell wall composition, cellular behavior and whole-organ growth.

Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation.

The mechanisms ensuring balanced growth remain a critical question in developmental biology. In plants, this balance relies on spatiotemporal integration of hormonal signaling pathways, but the understanding of the precise contribution of each hormone is just beginning to take form. Brassinosteroid (BR) hormone is shown here to have opposing effects on root meristem size, depending on its site of action. BR is demonstrated to both delay and promote onset of stem cell daughter differentiation, when acting in the outer tissue of the root meristem, the epidermis, and the innermost tissue, the stele, respectively. To understand the molecular basis of this phenomenon, a comprehensive spatiotemporal translatome mapping of Arabidopsis roots was performed. Analyses of wild type and mutants featuring different distributions of BR revealed autonomous, tissue-specific gene responses to BR, implying its contrasting tissue-dependent impact on growth. BR-induced genes were primarily detected in epidermal cells of the basal meristem zone and were enriched by auxin-related genes. In contrast, repressed BR genes prevailed in the stele of the apical meristem zone. Furthermore, auxin was found to mediate the growth-promoting impact of BR signaling originating in the epidermis, whereas BR signaling in the stele buffered this effect. We propose that context-specific BR activity and responses are oppositely interpreted at the organ level, ensuring coherent growth.

Activity of the brassinosteroid transcription factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 blocks developmental reprogramming in response to low phosphate availability.

Plants feature remarkable developmental plasticity, enabling them to respond to and cope with environmental cues, such as limited availability of phosphate, an essential macronutrient for all organisms. Under this condition, Arabidopsis (Arabidopsis thaliana) roots undergo striking morphological changes, including exhaustion of the primary meristem, impaired unidirectional cell expansion, and elevated density of lateral roots, resulting in shallow root architecture. Here, we show that the activity of two homologous brassinosteroid (BR) transcriptional effectors, BRASSINAZOLE RESISTANT1 (BZR1) and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 (BES1)/BZR2, blocks these responses, consequently maintaining normal root development under low phosphate conditions without impacting phosphate homeostasis. We show that phosphate deprivation shifts the intracellular localization of BES1/BZR2 to yield a lower nucleus-to-cytoplasm ratio, whereas replenishing the phosphate supply reverses this ratio within hours. Phosphate deprivation reduces the expression levels of BR biosynthesis genes and the accumulation of the bioactive BR 28-norcastasterone. In agreement, low and high BR levels sensitize and desensitize root response to this adverse condition, respectively. Hence, we propose that the environmentally controlled developmental switch from deep to shallow root architecture involves reductions in BZR1 and BES1/BZR2 levels in the nucleus, which likely play key roles in plant adaptation to phosphate-deficient environments.

Root growth is modulated by differential hormonal sensitivity in neighboring cells.

Coherent plant growth requires spatial integration of hormonal pathways and cell wall remodeling activities. However, the mechanisms governing sensitivity to hormones and how cell wall structure integrates with hormonal effects are poorly understood. We found that coordination between two types of epidermal root cells, hair and nonhair cells, establishes root sensitivity to the plant hormones brassinosteroids (BRs). While expression of the BR receptor BRASSINOSTEROID-INSENSITIVE1 (BRI1) in hair cells promotes cell elongation in all tissues, its high relative expression in nonhair cells is inhibitory. Elevated ethylene and deposition of crystalline cellulose underlie the inhibitory effect of BRI1. We propose that the relative spatial distribution of BRI1, and not its absolute level, fine-tunes growth.

Brassinosteroids in growth control: how, when and where.

The steroid hormones brassinosteroids take on critical roles during various plant growth processes, including control of cell proliferation and cell elongation. In this review, we discuss different strategies that have advanced our understanding of brassinosteroid function. Approaches observing whole-plant responses uncovered regulatory brassinosteroids-dependent modules controlling cell elongation. In these regulatory modules, downstream components of the brassinosteroid signaling pathway directly interact with other hormonal and environmental pathways. In alternative approaches, brassinosteroid activity has been dissected at the tissue and cellular level of above- and below-ground organs. These studies have determined the importance of brassinosteroids in cell cycle progression and in timing of cell differentiation. In addition, they have demonstrated that local reduction of the hormone sets organ boundaries. Finally, these studies uncovered the capacity of the epidermal-derived brassinosteroid signaling to control organ growth. Thus, inter-cellular communication is intimately involved in brassinosteroid-mediated growth control. The current challenge is therefore to decipher the spatiotemporal distribution of brassinosteroid activity and its impact on coherent growth and development.