Nodulation is tightly regulated in legumes to ensure appropriate levels of nitrogen fixation without excessive depletion of carbon reserves. This balance is maintained by intimately linking nodulation and its regulation with plant hormones. It has previously been shown that ethylene and jasmonic acid (JA) are able to regulate nodulation and Nod factor signal transduction. Here, we characterize the nature of abscisic acid (ABA) regulation of nodulation. We show that application of ABA inhibits nodulation, bacterial infection, and nodulin gene expression in Medicago truncatula. ABA acts in a similar manner as JA and ethylene, regulating Nod factor signaling and affecting the nature of Nod factor-induced calcium spiking. However, this action is independent of the ethylene signal transduction pathway. We show that genetic inhibition of ABA signaling through the use of a dominant-negative allele of ABSCISIC ACID INSENSITIVE1 leads to a hypernodulation phenotype. In addition, we characterize a novel locus of M. truncatula, SENSITIVITY TO ABA, that dictates the sensitivity of the plant to ABA and, as such, impacts the regulation of nodulation. We show that ABA can suppress Nod factor signal transduction in the epidermis and can regulate cytokinin induction of the nodule primordium in the root cortex. Therefore, ABA is capable of coordinately regulating the diverse developmental pathways associated with nodule formation and can intimately dictate the nature of the plants' response to the symbiotic bacteria.
SummaryPlant hormones interact at many different levels to form a network of signaling pathways connected by antagonistic and synergistic interactions. Ethylene and jasmonic acid both act to regulate the plant's responsiveness to a common set of biotic stimuli. In addition ethylene has been shown to negatively regulate the plant's response to the rhizobial bacterial signal, Nod factor. This regulation occurs at an early step in the Nod factor signal transduction pathway, at or above Nod factor-induced calcium spiking. Here we show that jasmonic acid also inhibits the plant's responses to rhizobial bacteria, with direct effects on Nod factor-induced calcium spiking. However, unlike ethylene, jasmonic acid not only inhibits spiking but also suppresses the frequency of calcium oscillations when applied at lower concentrations. This effect of jasmonic acid is amplified in the ethylene-insensitive mutant skl, indicating an antagonistic interaction between these two hormones for regulation of Nod factor signaling. The rapidity of the effects of ethylene and jasmonic acid on Nod factor signaling suggests direct crosstalk between these three signal transduction pathways. This work provides a model by which crosstalk between signaling pathways can rapidly integrate environmental, developmental and biotic stimuli to coordinate diverse plant responses.
SUMMARYLegume root architecture involves not only elaboration of the root system by the formation of lateral roots but also the formation of symbiotic root nodules in association with nitrogen-fixing soil rhizobia. The Medicago truncatula LATD/NIP gene plays an essential role in the development of both primary and lateral roots as well as nodule development. We have cloned the LATD/NIP gene and show that it encodes a member of the NRT1(PTR) transporter family. LATD/NIP is expressed throughout the plant. pLATD/NIP-GFP promoterreporter fusions in transgenic roots establish the spatial expression of LATD/NIP in primary root, lateral root and nodule meristems and the surrounding cells. Expression of LATD/NIP is regulated by hormones, in particular by abscisic acid which has been previously shown to rescue the primary and lateral root meristem arrest of latd mutants. latd mutants respond normally to ammonium but have defects in responses of the root architecture to nitrate. Taken together, these results suggest that LATD/NIP may encode a nitrate transporter or transporter of another compound.
Abstract. The polymeric immunoglobulin receptor (pig-R) is responsible for the receptor-mediated transcytosis of polymeric immunoglobulins (IgA and IgM) across various epithelia. We have expressed the cDNA for the plg-R in Madin-Darby canine kidney (MDCK) cells and found that this system mimics that found in vivo (Mostov, K. E., and D. L. Deitcher. 1986. Cell. 46:613-621). We have now investigated the postendocytotic pathway of the ligand for the plg-R. After a 5-min internalization at the basolateral surface, ,'~45 % of internalized ligand recycles to the basolateral medium and 30% is transcytosed to the apical medium.We have also examined why transcytosis of ligand is unidirectional, going only from basolateral to apical, but not from apical to basolateral. Several factors could explain this, such as proteolytic cleavage of the plg-R at the apical surface, decreased apical endocytosis of ligand, or an intracellular sorting event. In this report, we show that the protease inhibitor, leupeptin, inhibits the cleavage of the plg-R but does not alter the unidirectionality of transcytosis. In addition, we demonstrate that there is a significant amount of apical endocytosis of ligand (70% of that observed basolaterally).Finally, we demonstrate that apically endocytosed ligand can return only to the apical surface. Thus, once ligand reaches the apical surface, it is 'trapped" and cannot return to the basolateral surface. We propose that the unidirectionality of transcytosis is the resuit of intracellular sorting, and that this results from a signal(s) present on the plg-R. p OLYMERIC immunoglobulins (IgA and IgM) are transported across a variety of epithelia into external secretions. This process of transcytosis is mediated by a receptor that is synthesized and expressed at the cell surface of these transporting epithelia (Mostov and Simister, 1985). This polymeric immunoglobulin receptor (pig-R) ~ is targeted to the basolateral surface of epithelial cells after synthesis in the rough endoplasmic reticulum and processing in the Golgi stacks. At the basolateral surface, polymeric immunoglobulins bind to the pIg-R and are internalized via receptor-mediated endocytosis. Receptor and ligand are then transported to the apical surface where the extracellular portion of the receptor is cleaved and released along with its ligand (Brandtzaeg, 1974; Mostov and Blobel, 1982;Solari and Kraehenbuhl, 1984). The extracellular portion of the receptor thus formed is termed secretory component (SC).The biosynthesis and subsequent receptor-mediated transcytosis of plgR serves as an excellent model system for the study of protein traffic in polarized epithelial cells. We have Dr. Mostov's present address is the Department of Anatomy, University of California, San Francisco, California 94143.1. Abbreviations used in this paper: pig-R, polymeric immunoglobulin receptor; SC, secretory component. characterized the plg-R in a cell culture system by using a retroviral expre~i,~n vector to express the plg-R cDNA in Madin-Darby canine kidney (M...
The LATD gene of the model legume, Medicago truncatula, is required for the normal function of three meristems, i.e. the primary root, lateral roots and nitrogen-fixing nodules. In latd mutants, primary root growth eventually arrests, resulting in a disorganized root tip lacking a presumptive meristem and root cap columella cells. Lateral root organs are more severely affected; latd lateral roots and nodules arrest immediately after emerging from the primary root, and reveal a lack of organization. Here we show that the plant hormone, abscisic acid (ABA), can rescue the latd root, but not nodule, meristem defects. Growth on ABA is sufficient to restore formation of small, cytoplasm-rich cells in the presumptive meristem region, rescue meristem organization and root growth and formation of root cap columella cells. In contrast, inhibition of ethylene synthesis or signaling fails to restore latd primary root growth. We find that latd mutants have normal levels of ABA, but exhibit reduced sensitivity to the hormone in two other ABA-dependent processes: seed germination and stomatal closure. Together, these observations demonstrate that the latd mutant is defective in the ABA response and indicate a role for LATD-dependent ABA signaling in M. truncatula root meristem function.
Plants modulate root growth in response to changes in the local environment, guided by intrinsic developmental genetic programs. The hormone Abscisic Acid (ABA) mediates responses to different environmental factors, such as the presence of nitrate in the soil, water stress and salt, shaping the structure of the root system by regulating the production of lateral roots as well as controlling root elongation by modulating cell division and elongation. Curiously, ABA controls different aspects of root architecture in different plant species, perhaps providing some insight into the great diversity of root architecture in different plants, both from different taxa and from different environments. ABA is an ancient signaling pathway, acquired well before the diversification of land plants. Nonetheless, how this ancient signaling module is implemented or interacts within a larger signaling network appears to vary in different species. This review will examine the role of ABA in the control of root architecture, focusing on the regulation of lateral root formation in three plant species, Arabidopsis thaliana, Medicago truncatula and Oryza sativa. We will consider how the implementation of the ABA signaling module might be a target of natural selection, to help contribute to the diversity of root architecture in nature.
Abscisic acid (ABA) signaling plays a major role in root system development, regulating growth and root architecture. However, the precise localization of ABA remains undetermined. Here, we present a mechanism in which nitrate signaling stimulates the release of bioactive ABA from the inactive storage form, ABA-glucose ester (ABA-GE). We found that ABA accumulated in the endodermis and quiescent center of Arabidopsis thaliana root tips, mimicking the pattern of SCARECROW expression, and (to lower levels) in the vascular cylinder. Nitrate treatment increased ABA levels in root tips; this stimulation requires the activity of the endoplasmic reticulum-localized, ABA-GE-deconjugating enzyme b-GLUCOSIDASE1, but not de novo ABA biosynthesis. Immunogold labeling demonstrated that ABA is associated with cytoplasmic structures near, but not within, the endoplasmic reticulum. These findings demonstrate a mechanism for nitrate-regulated root growth via regulation of ABA accumulation in the root tip, providing insight into the environmental regulation of root growth.
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