The organs of multicellular species consist of cell types that must function together to perform specific tasks. One critical organ function is responding to internal or external change. Some cellspecific responses to changes in environmental conditions are known, but the scale of cell-specific responses within an entire organ as it perceives an environmental flux has not been well characterized in plants or any other multicellular organism. Here, we use cellular profiling of five Arabidopsis root cell types in response to an influx of a critical resource, nitrogen, to uncover a vast and predominantly cell-specific response. We show that cellspecific profiling increases sensitivity several-fold, revealing highly localized regulation of transcripts that were largely hidden from previous global analyses. The cell-specific data revealed responses that suggested a coordinated developmental response in distinct cell types or tissues. One example is the cell-specific regulation of a transcriptional circuit that we showed mediates lateral root outgrowth in response to nitrogen via microRNA167, linking small RNAs to nitrogen responses. Together, these results reveal a previously cryptic component of cell-specific responses to nitrogen. Thus, the results make an important advance in our understanding of how multicellular organisms cope with environmental change at the cell level.cell sorting ͉ microRNA ͉ lateral roots ͉ auxin response ͉ transcriptional analysis
Biological nitrogen fixation in legumes occurs in nodules that are initiated in the root cortex following Nod factor recognition at the root surface, and this requires coordination of diverse developmental programs in these different tissues. We show that while early Nod factor signaling associated with calcium oscillations is limited to the root surface, the resultant activation of Nodule Inception (NIN) in the root epidermis is sufficient to promote cytokinin signaling and nodule organogenesis in the inner root cortex. NIN or a product of its action must be associated with the transmission of a signal between the root surface and the cortical cells where nodule organogenesis is initiated. NIN appears to have distinct functions in the root epidermis and the root cortex. In the epidermis, NIN restricts the extent of Early Nodulin 11 (ENOD11) expression and does so through competitive inhibition of ERF Required for Nodulation (ERN1). In contrast, NIN is sufficient to promote the expression of the cytokinin receptor Cytokinin Response 1 (CRE1), which is restricted to the root cortex. Our work in Medicago truncatula highlights the complexity of NIN action and places NIN as a central player in the coordination of the symbiotic developmental programs occurring in differing tissues of the root that combined are necessary for a nitrogen-fixing symbiosis.
The mechanisms regulating cell layer organisation in developing plant organs are fundamental to plant growth, but remain largely uninvestigated. We have studied the receptor kinase-encoding ARABIDOPSIS CRINKLY4 gene and shown that its expression is restricted to the L1 cell layer of most meristems and organ primordia, including those of the ovule integuments. Insertion mutations show that ARABIDOPSIS CRINKLY4 is required for regulation of cellular organisation during the development of sepal margins and ovule integument outgrowth. We show that ARABIDOPSIS CRINKLY4 encodes a functional kinase that, in ovules and possibly other tissues, is abundant in anticlinal and the inner periclinal plasma membrane of 'outside' cells. We propose that ARABIDOPSIS CRINKLY4 may be involved in maintaining L1 cell layer integrity by receiving and transmitting signals from neighbouring L1 cells and/or from underlying cell layers.
The study of the regulation and cellular dynamics of receptor kinase signaling in plants is a rapidly evolving field that promises to give enormous insights into the molecular control of signal perception. In this study, we have analyzed the behavior of the L1-specific receptor kinase ARABIDOPSIS CRINKLY4 (ACR4) from Arabidopsis thaliana in planta and have shown it to be present in two distinct compartments within cells. These represent protein export bodies and a population of internalized vesicles. In parallel, deletion analysis has shown that a predicted b-propeller-forming extracellular domain is necessary for ACR4 function. Nonfunctional ACR4 variants with deletions or point mutations in this domain behave differently to wild-type fusion protein in that they are not internalized to the same extent. In addition, in contrast with functional ACR4, which appears to be rapidly turned over, they are stabilized. Thus, for ACR4, internalization and turnover are linked and depend on functionality, suggesting that ACR4 signaling may be subject to damping down via internalization and degradation. The observed rapid turnover of ACR4 sets it apart from other recently studied plant receptor kinases. Finally, ACR4 kinase activity is not required for protein function, leading us to propose, by analogy to animal systems, that ACR4 may hetero-oligomerize with a kinase-active partner during signaling. Plant and animal receptor kinases have distinct evolutionary origins. However, with other recent work, our study suggests that there has been considerable convergent evolution between mechanisms used to regulate their activity.
We face major agricultural challenges that remain a threat for global food security. Soil microbes harbor enormous potentials to provide sustainable and economically favorable solutions that could introduce novel approaches to improve agricultural practices and, hence, crop productivity. In this review we give an overview regarding the current state-of-the-art of microbiome research by discussing new technologies and approaches. We also provide insights into fundamental microbiome research that aim to provide a deeper understanding of the dynamics within microbial communities, as well as their interactions with different plant hosts and the environment. We aim to connect all these approaches with potential applications and reflect how we can use microbial communities in modern agricultural systems to realize a more customized and sustainable use of valuable resources (e.g., soil).
Significance Species display a range of plastic phenotypes that presumably have evolved as a result of adaptation to heterogeneous environments. We asked whether the genetic mechanisms that underlie adaptation across populations also determine the response of an individual plant to environmental cues in Arabidopsis . Using an integrative root phenotyping approach, genes that underlie natural variation in root architecture across populations were shown to control plasticity responses within an individual. Together, our results uncover a genetic mechanism underlying the phenotypic plasticity of an individual and phenotypic diversity across natural variants.
Nitrate is both a nutrient and a potent signal that stimulates plant growth. Initial experiments in the late 1950s showing that nitrate enhances nitrate reductase (NR) activity after several hours of treatment have now progressed to transcriptome studies identifying over 1000 genes that respond to muM levels of nitrate within minutes. The use of an Arabidopsis NR-null mutant allowed the identification of genes that respond to nitrate when the production of downstream metabolites of nitrate is blocked. Further dissection of the nitrate response is now possible using new bioinformatic tools such as Sungear to perform comparative studies of multiple transcriptome responses across different laboratories and environmental conditions. These analyses have identified genes and pathways (e.g. nitrate assimilation, pentose phosphate pathway, and glycolysis) that respond to nitrate under a variety of conditions (context-independent). Most of these genes and pathways are ones that were identified using the NR-null mutant as responding directly to nitrate. By contrast, other processes such as protein synthesis respond only under a subset of conditions (context-dependent). Data from the NR-null mutant suggest these latter processes may be regulated by downstream nitrogen metabolites.
Leguminous plants possess the almost unique ability to enter symbiosis with soil-resident, nitrogen fixing bacteria called rhizobia. During this symbiosis, the bacteria physically colonize specialized organs on the roots of the host plant called nodules, where they reduce atmospheric nitrogen into forms that can be assimilated by the host plant and receive photosynthates in return. In order for nodule development to occur, there is extensive chemical cross-talk between both parties during the formative stages of the symbiosis. The vast majority of the legume family are capable of forming root nodules and typically rhizobia are only able to fix nitrogen within the context of this symbiotic association. However, many legume species only enter productive symbiosis with a few, or even single rhizobial species or strains, and vice-versa. Permitting symbiosis with only rhizobial strains that will be able to fix nitrogen with high efficiency is a crucial strategy for the host plant to prevent cheating by rhizobia. This selectivity is enforced at all stages of the symbiosis, with partner choice beginning during the initial communication between the plant and rhizobia. However, it can also be influenced even once nitrogen-fixing nodules have developed on the root. This review sets out current knowledge about the molecular mechanisms employed by both parties to influence host range during legume-rhizobia symbiosis.
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