Focus on the Role of the Abiotic Environment on Interactions Between Plants and Microbes.

Interactions between plants and microbes are shaped by the physical world that surrounds them. In nature, the abiotic environment is complex, and factors such as nutrient and water availability, humidity, wind, carbon dioxide levels, salt, pollutants, and temperature all affect the growth and physiology of plants and microbes as well as their interactions. Much of our mechanistic understanding of plant-microbe interactions comes from experiments done in carefully controlled conditions. This Focus Issue looks at how aspects of the abiotic environment affect these plant-microbe interactions, and, conversely, how plant-microbe interactions affect host response to abiotic stress.[Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2022.Additional content is available on the Focus on the Role of the Abiotic Environment on Interactions Between Plants and Microbes.Complete Genome Sequence of Curtobacterium sp. C1, a Beneficial Endophyte with the Potential for In-Plant Salinity Stress AlleviationProteasomal Degradation of JAZ9 by Salt- and Drought-Induced Ring Finger 1 During Pathogen Infection.

At the Crossroads of Salinity and Rhizobium-Legume Symbiosis.

Legume roots interact with soil bacteria rhizobia to develop nodules, de novo symbiotic root organs that host these rhizobia and are mini factories of atmospheric nitrogen fixation. Nodulation is a sophisticated developmental process and is sensitive to several abiotic factors, salinity being one of them. While salinity influences both the free-living partners, symbiosis is more vulnerable than other aspects of plant and microbe physiology, and the symbiotic interaction is strongly impaired even under moderate salinity. In this review, we tease apart the various known components of rhizobium-legume symbiosis and how they interact with salt stress. We focus primarily on the initial stages of symbiosis since we have a greater mechanistic understanding of the interaction at these stages.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Focus on How Plants Engage With Beneficial Microorganisms While at the Same Time Restricting Pathogens.

Plants live in a world filled with microbes, and spend their lives engaged in the delicate dance of nurturing beneficial interactions while simultaneously reducing disease-causing interactions. How do plants engage with beneficial microorganisms while at the same time restricting pathogens? was recently selected in a crowd-sourced effort as the top, unanswered question in the field of molecular plant-microbe interactions. Elaborating on this question and setting the stage for this focus issue, the Top10 review by Thoms, Liang and Haney examines the way multiple inputs are integrated to initiate programs of immunity or mutualistic symbiosis, and how this shapes the microbiome. This comprehensive review describes the current landscape of the field, focusing on the plant-microbe-soil continuum, but providing ideas for extending these concepts to leaves, where much of the research on immunity has centered. Other papers in this issue examine the simultaneous interaction of plants with beneficial and pathogenic microorganisms, as well as many diverse relationships with beneficial microbes that can improve plant health by increasing access to nutrients or by decreasing disease.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Salt Stress Enhances Early Symbiotic Gene Expression in Medicago truncatula and Induces a Stress-Specific Set of Rhizobium-Responsive Genes.

Salt stress is a major agricultural concern inhibiting not only plant growth but also the symbiotic association between legume roots and the soil bacteria rhizobia. This symbiotic association is initiated by a molecular dialogue between the two partners, leading to the activation of a signaling cascade in the legume host and, ultimately, the formation of nitrogen-fixing root nodules. Here, we show that a moderate salt stress increases the responsiveness of early symbiotic genes in Medicago truncatula to its symbiotic partner, Sinorhizobium meliloti while, conversely, inoculation with S. meliloti counteracts salt-regulated gene expression, restoring one-third to control levels. Our analysis of early nodulin 11 (ENOD11) shows that salt-induced expression is dynamic, Nod-factor dependent, and requires the ionic but not the osmotic component of salt. We demonstrate that salt stimulation of rhizobium-induced gene expression requires NSP2, which functions as a node to integrate the abiotic and biotic signals. In addition, our work reveals that inoculation with S. meliloti succinoglycan mutants also hyperinduces ENOD11 expression in the presence or absence of salt, suggesting a possible link between rhizobial exopolysaccharide and the plant response to salt stress. Finally, we identify an accessory set of genes that are induced by rhizobium only under conditions of salt stress and have not been previously identified as being nodulation-related genes. Our data suggest that interplay of core nodulation genes with different accessory sets, specific for different abiotic conditions, functions to establish the symbiosis. Together, our findings reveal a complex and dynamic interaction between plant, microbe, and environment.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

What are the Top 10 Unanswered Questions in Molecular Plant-Microbe Interactions?

This article is part of the Top 10 Unanswered Questions in MPMI invited review series.The past few decades have seen major discoveries in the field of molecular plant-microbe interactions. As the result of technological and intellectual advances, we are now able to answer questions at a level of mechanistic detail that we could not have imagined possible 20 years ago. The MPMI Editorial Board felt it was time to take stock and reassess. What big questions remain unanswered? We knew that to identify the fundamental, overarching questions that drive our research, we needed to do this as a community. To reach a diverse audience of people with different backgrounds and perspectives, working in different areas of plant-microbe interactions, we queried the more than 1,400 participants at the 2019 International Congress on Molecular Plant-Microbe Interactions meeting in Glasgow. This group effort resulted in a list of ten, broad-reaching, fundamental questions that influence and inform our research. Here, we introduce these Top 10 unanswered questions, giving context and a brief description of the issues. Each of these questions will be the subject of a detailed review in the coming months. We hope that this process of reflecting on what is known and unknown and identifying the themes that underlie our research will provide a framework to use going forward, giving newcomers a sense of the mystery of the big questions and inspiring new avenues and novel insights.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Genotype-specific effects of ericoid mycorrhizae on floral traits and reproduction in Vaccinium corymbosum.

PREMISE: Most plants interact with mycorrhizal fungi and animal pollinators simultaneously. Yet, whether mycorrhizae affect traits important to pollination remains poorly understood and may depend on the match between host and fungal genotypes. Here, we examined how ericoid mycorrhizal fungi affected flowering phenology, floral traits, and reproductive success, among eight genotypes of highbush blueberry, Vaccinium corymbosum (Ericaceae). We asked three overarching questions: (1) Do genotypes differ in response to inoculation? (2) How does inoculation affect floral and flowering traits? (3) Are inoculated plants more attractive to pollinators and less pollen limited than non-inoculated plants of the same genotype? METHODS: To examine these questions, we experimentally inoculated plants with ericoid mycorrhizal fungi, grew the plants in the field, and measured flowering and floral traits over 2 years. In year 2, we conducted a hand-pollination experiment to test whether plants differed in pollen limitation. RESULTS: Inoculated plants had significantly higher levels of colonization for some genotypes, and there were significant floral trait changes in inoculated plants for some genotypes as well. On average, inoculated plants produced significantly larger floral displays, more fruits per inflorescence, and heavier fruits with lower sugar content, than non-inoculated, control plants. Hand pollination enhanced the production of fruits, and fruit mass, for non-inoculated plants but not for those that were inoculated. CONCLUSIONS: Our results demonstrate that inoculation with ericoid mycorrhizal fungi enhanced flowering and altered investment in reproduction in genotype-specific ways. These findings underscore the importance of examining belowground symbionts and genotype-specific responses in their hosts to fully understand the drivers of aboveground interactions.

Comparison of Vacuum MALDI and AP-MALDI Platforms for the Mass Spectrometry Imaging of Metabolites Involved in Salt Stress in Medicago truncatula.

Matrix-assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) is routinely used to determine the spatial distributions of various biomolecules in tissues. Recently, there has been an increased interest in creating higher resolution images using sources with more focused beams. One such source, an atmospheric pressure (AP) MALDI source from MassTech, has a laser capable of reaching spatial resolutions of 10 µm. Here, the AP-MALDI source coupled with a Q Exactive HF Orbitrap platform is compared to the commercial MALDI LTQ Orbitrap XL system using Medicago truncatula root nodules. AP-MALDI parameters, such as the S-lens value, capillary temperature, and spray voltage, were optimized on the Q Exactive-HF platform for optimal detection of plant metabolites. The performance of the two systems was evaluated for sensitivity, spatial resolution, and overall ability to detect plant metabolites. The commercial MALDI LTQ Orbitrap XL was superior regarding the number of compounds detected, as at least two times more m/z were detected compared to the AP-MALDI system. However, although the AP-MALDI source requires a spatial resolution higher than 10 µm to get the best signal, the spatial resolution at 30 µm is still superior compared to the 75 µm spatial resolution achieved on the MALDI platform. The AP-MALDI system was also used to investigate the metabolites present in M. truncatula roots and root nodules under high salt and low salt conditions. A discriminative analysis with SCiLS software revealed m/z ions specific to the control and salt conditions. This analysis revealed 44 m/z ions present at relatively higher abundances in the control samples, and 77 m/z enriched in the salt samples. Liquid chromatography-tandem MS was performed to determine the putative molecular identities of some of the mass ions enriched in each sample, including, asparagine, adenosine, and nicotianamine in the control samples, and arginine and soyasaponin I in the salt treated samples.

Differences in Selected HIV Care Continuum Outcomes Among People Residing in Rural, Urban, and Metropolitan Areas-28 US Jurisdictions.

PURPOSE: The HIV care continuum is used to monitor success in HIV diagnosis and treatment among persons living with HIV in the United States. Significant differences exist along the HIV care continuum between subpopulations of people living with HIV; however, differences that may exist between residents of rural and nonrural areas have not been reported. METHODS: We analyzed the Centers for Disease Control and Prevention's National HIV Surveillance System data on adults and adolescents (≥13 years) with HIV diagnosed in 28 jurisdictions with complete reporting of HIV-related lab results. Lab data were used to assess linkage to care (≥1 CD4 or viral load test ≤3 months of diagnosis), retention in care (≥2 CD4 and/or viral load tests ≥3 months apart), and viral suppression (viral load <200 copies/mL) among persons living with HIV. Residence at diagnosis was grouped into rural (<50,000 population), urban (50,000-499,999 population), and metropolitan (≥500,000 population) categories for statistical comparison. Prevalence ratios and 95% CI were calculated to assess significant differences in linkage, retention, and viral suppression. FINDINGS: Although greater linkage to care was found for rural residents (84.3%) compared to urban residents (83.3%) and metropolitan residents (81.9%), significantly lower levels of retention in care and viral suppression were found for residents of rural (46.2% and 50.0%, respectively) and urban (50.2% and 47.2%) areas compared to residents of metropolitan areas (54.5% and 50.8%). CONCLUSIONS: Interventions are needed to increase retention in care and viral suppression among people with HIV in nonmetropolitan areas of the United States.

Environmental nitrate signals through abscisic acid in the root tip.

Roots respond to changes in environmental nitrate with a localized stimulation of ABA levels in the root tip. This rise in ABA levels is due to the action of ER-localized ß-GLUCOSIDASE 1, which releases bioactive ABA from the inactive ABA-glucose ester. The slow rise in root tip ABA levels stimulates expression of nitrate metabolic enzymes and simultaneously activates a negative feedback loop involving the protein phosphatase, ABI2, which reduces nitrate influx via the AtNPF6.3 transceptor. The rise in root-tip localized ABA also negatively regulates expression of the SCARECROW transcription factor, thus providing a sensitive mechanism for modulating root growth in response to environmental changes.

Environmental Nitrate Stimulates Abscisic Acid Accumulation in Arabidopsis Root Tips by Releasing It from Inactive Stores.

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.

Abscisic Acid: Hidden Architect of Root System Structure.

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 and lateral root organ defective/NUMEROUS INFECTIONS AND POLYPHENOLICS modulate root elongation via reactive oxygen species in Medicago truncatula.

Abscisic acid (ABA) modulates root growth in plants grown under normal and stress conditions and can rescue the root growth defects of the Medicago truncatula lateral root-organ defective (latd) mutant. Here, we demonstrate that reactive oxygen species (ROS) function downstream of ABA in the regulation of root growth by controlling cell elongation. We also show that the MtLATD/NUMEROUS INFECTIONS AND POLYPHENOLICS (NIP) nitrate transporter is required for ROS homeostasis and cell elongation in roots and that this balance is perturbed in latd mutants, leading to an excess of superoxide and hydrogen peroxide and a corresponding decrease in cell elongation. We found that expression of the superoxide-generating NADPH oxidase genes, MtRbohA and MtRbohC (for respiratory burst oxidase homologs), is increased in latd roots and that inhibition of NADPH oxidase activity pharmacologically can both reduce latd root ROS levels and increase cell length, implicating NADPH oxidase function in latd root growth defects. Finally, we demonstrate that ABA treatment alleviates ectopic ROS accumulation in latd roots, restores MtRbohC expression to wild-type levels, and promotes an increase in cell length. Reducing the expression of MtRbohC using RNA interference leads to increased root elongation in both wild-type and latd roots. These results reveal a mechanism by which the MtLATD/NIP nitrate transporter and ABA modulate root elongation via superoxide generation by the MtRbohC NADPH oxidase.

A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants.

Members of the plant NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER (NRT1/PTR) family display protein sequence homology with the SLC15/PepT/PTR/POT family of peptide transporters in animals. In comparison to their animal and bacterial counterparts, these plant proteins transport a wide variety of substrates: nitrate, peptides, amino acids, dicarboxylates, glucosinolates, IAA, and ABA. The phylogenetic relationship of the members of the NRT1/PTR family in 31 fully sequenced plant genomes allowed the identification of unambiguous clades, defining eight subfamilies. The phylogenetic tree was used to determine a unified nomenclature of this family named NPF, for NRT1/PTR FAMILY. We propose that the members should be named accordingly: NPFX.Y, where X denotes the subfamily and Y the individual member within the species.

Control of root architecture and nodulation by the LATD/NIP transporter.

The Medicago truncatula LATD/NIP gene is essential for the development of lateral and primary root and nitrogen-fixing nodule meristems as well as for rhizobial invasion of nodules. LATD/NIP encodes a member of the NRT1(PTR1) nitrate and di-and tri-peptide transporter family, suggesting that its function is to transport one of these or another compound(s). Because latd/nip mutants can have their lateral and primary root defects rescued by ABA, ABA is a potential substrate for transport. LATD/NIP expression in the root meristem was demonstrated to be regulated by auxin, cytokinin and abscisic acid, but not by nitrate. LATD/NIP's potential function and its role in coordinating root architecture and nodule formation are discussed.

Competing on talent analytics.

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A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula.

Legume 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 promoter-reporter 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.

Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula.

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.

Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant.

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.

Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation.

Plant 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.