Figure - available from: Nature Plants
This content is subject to copyright. Terms and conditions apply.
The nkcbp mutant shows defects of symbiosome development and bacteroid differentiation a–f, Ultrastructures of nodules in the nitrogen-fixing zone of WT (a, c and e) and nkcbp mutants (b, d and f) at 14 dpi. ITs harbour the colonized rhizobia (a and b) in infected cells. In WT symbiotic cells, the central vacuole contains numerous defective rhizobia or undifferentiated bacteroids upon degradation (c), and well-developed symbiosomes are radially distributed around the central vacuole (e), while in nkcbp, small vacuoles are in symbiotic cells (d), which contain a large portion of incompletely differentiated symbiosomes, exhibiting dysplastic morphology, an enlarged peribacteroid space and disorganized symbiosome membrane (f). V, central vacuoles; FV, fragmented vacuole in infected nkcbp cells; red circles indicate abnormal differentiated bacteroids; red arrows mark the bacteria inside the infected threads; red asterisks indicate the bacteroids with dysplastic morphology; red arrowheads indicate abnormal symbiosome membrane. Nodules of SEM were randomly selected from 36 plants with at least three biological replicates. Scale bars, 2 μm (a–f). g, DNA content of DAPI-stained bacteroids from WT and nkcbp mutants measured by flow cytometry. The nodules used for flow cytometry were from at least 21 plants with three biological replicates. P1 represents the total signal counts excluding the cell debris. P2 represents the signal counts including just single bacteroid signals. P3 represents the bacteriod counts of the same area of WT and nkcbp mutants at lower fluorescence level. P4 represents the bacteriod counts of the same area of WT and nkcbp mutants at higher fluorescence level. WT: P1 = 25,487; P2 = 24,170; P3 = 2,458, P4 = 6,507; nkcbp mutant: P1 = 24,896; P2 = 24,591; P3 = 2,339, P4 = 5,281.
Source publication
Symbioses between legumes and rhizobia require establishment of the plant-derived symbiosome membrane, which surrounds the rhizobia and accommodates the symbionts by providing an interface for nutrient and signal exchange. The host cytoskeleton and endomembrane trafficking systems play central roles in the formation of a functional symbiotic interf...
Citations
... The nodulation-specific kinesin-like calmodulin-binding protein (nKCBP), a plant-specific microtubulebased kinesin motor, evolves exclusively through gene duplication in legumes. Interestingly, despite nKCBP sharing conserved biochemical functions with its homologs, it demonstrates a nodule-rich expression pattern and is hijacked by rhizobia to control central vacuole formation and rhizobia endosymbiosis in Medicago symbiotic cells by modulating vacuolar vesicle fusion and crosslinking microtubules with actin (Zhang et al., 2022). ...
The legume–rhizobium symbiosis represents the most important system for terrestrial biological nitrogen fixation on land. Efficient nitrogen fixation during this symbiosis depends on successful rhizobial infection and complete endosymbiosis, which are achieved by complex cellular events including cell-wall remodeling, cytoskeletal reorganizations, and extensive membrane expansion and trafficking. In this review, we explore the dynamic remodeling of the plant-specific cell wall-membrane system-cytoskeleton (WMC) continuum during symbiotic nitrogen fixation. We focus on key processes linked to efficient nitrogen fixation, including rhizobial uptake, infection thread formation and elongation, rhizobial droplet release, cytoplasmic bridge formation, and rhizobial endosymbiosis. Additionally, we discuss the advanced techniques for investigating the cellular basis of root-nodule symbiosis and provide insights into the unsolved mysteries of robust symbiotic nitrogen fixation.
... Compared with the control, the symbiosis membrane was thinner in the infiltrated cells of the MoS 2 NPs treatment group, which facilitated the BNF capacity (Figure 5c). 40 On the other hand, the nodules treated with MoS 2 NS and Na 2 MoO 4 showed less rhizobial infestation and symbiont formation as demonstrated by the smaller and diffuse toluidine blue staining, indicating that BNF was significantly inhibited (Figure 5c). Nitrogenases are very sensitive to ROS, and reducing ROS in nodules is beneficial to BNF capacity. ...
Soybean (Glycine max) is a crop of global significance and has low reliance on N fertilizers due to its biological nitrogen fixation (BNF) capacity, which harvests ambient N2 as a critical ecosystem service. BNF can be severely compromised by abiotic stresses. Enhancing BNF is increasingly important not only to alleviate global food insecurity but also to reduce the environmental impact of agriculture by decreasing chemical fertilizer inputs. However, this has proven challenging using current genetic modification or bacterial nodulation methods. Here, we demonstrate that a single application of a low dose (10 mg/kg) of molybdenum disulfide nanoparticles (MoS2 NPs) can enhance soybean BNF and grain yield by 30%, compared with conventional molybdate fertilizer. Unlike molybdate, MoS2 NPs can more sustainably release Mo, which then is effectively incorporated as a cofactor for the synthesis of nitrogenase and molybdenum-based enzymes that subsequently enhance BNF. Sulfur is also released sustainably and incorporated into biomolecule synthesis, particularly in thiol-containing antioxidants. The superior antioxidant enzyme activity of MoS2 NPs, together with the thiol compounds, protect the nodules from reactive oxygen species (ROS) damage, delay nodule aging, and maintain the BNF function for a longer term. The multifunctional nature of MoS2 NPs makes them a highly effective strategy to enhance plant tolerance to abiotic stresses. Given that the physicochemical properties of nanomaterials can be readily modulated, material performance (e.g., ROS capturing capacity) can be further enhanced by several synthesis strategies. This study thus demonstrates that nanotechnology can be an efficient and sustainable approach to enhancing BNF and crop yield under abiotic stress and combating global food insecurity.
... TPXL and MAP65, together with AURORA 1, form a mitotic module to regulate MT functions for supporting the infection-thread formation of rhizobia during legume endosymbiosis [211]. Rhizobia hijack a plant-specific kinesin motor to crosslink MTs with actin filaments for controlling central vacuole formation to achieve symbiosome development and nitrogen fixation [212]. Substantial MT remodeling has been observed in arbuscule-containing cells [213,214]. ...
Microtubules (MTs) are essential elements of the eukaryotic cytoskeleton and are critical for various cell functions. During cell division, plant MTs form highly ordered structures, and cortical MTs guide the cell wall cellulose patterns and thus control cell size and shape. Both are important for morphological development and for adjusting plant growth and plasticity under environmental challenges for stress adaptation. Various MT regulators control the dynamics and organization of MTs in diverse cellular processes and response to developmental and environmental cues. This article summarizes the recent progress in plant MT studies from morphological development to stress responses, discusses the latest techniques applied, and encourages more research into plant MT regulation.
... In nodule cells, bacteroid positioning correlates with characteristic microtubule rearrangements [75], wherein the pattern in root nodules was found to be host-plant specific [75]. The nodulation-specific kinesin-like calmodulin-binding protein (nKCBP), which crosslinks microtubules with the actin cytoskeleton, controls central vacuole morphogenesis in symbiotic cells in M. truncatula [76]. ...
Symbiosis between leguminous plants and soil bacteria rhizobia is a refined type of plant–microbial interaction that has a great importance to the global balance of nitrogen. The reduction of atmospheric nitrogen takes place in infected cells of a root nodule that serves as a temporary shelter for thousands of living bacteria, which, per se, is an unusual state of a eukaryotic cell. One of the most striking features of an infected cell is the drastic changes in the endomembrane system that occur after the entrance of bacteria to the host cell symplast. Mechanisms for maintaining intracellular bacterial colony represent an important part of symbiosis that have still not been sufficiently clarified. This review focuses on the changes that occur in an endomembrane system of infected cells and on the putative mechanisms of infected cell adaptation to its unusual lifestyle.
Legumes establish symbiosis with rhizobia by forming a symbiotic interface that enables cross‐kingdom exchanges of signaling molecules and nutrients. However, how host organelles interact with symbiosomes at the symbiotic interface remains elusive during rhizobia endosymbiosis. Here, symbiotic cells are reconstructed using 3D scanning electron microscopy (SEM) and uncover that the host endoplasmic reticulum (ER) undergoes dynamic expansion to gradually enwrap symbiosomes, facilitating their compartmentalization and endosymbiosis. Consistently, altering ER lamellar expansion by overexpressing MtRTNLBs, the reticulons responsible for ER tubulation, impairs rhizobia accommodation and symbiosome development. Intriguingly, unfolded protein response (UPR)‐marker genes, bZIP60 and IRE1A/B, show continuously activated expression during nodule development, and the two UPR‐deficient mutants, ire1b, and bzip60, exhibit compromised ER biogenesis and defective symbiosome development. Collectively, the findings underpin ER expansion and UPR activation as two key events in rhizobia accommodation and reveal an intrinsic coupling of ER morphology with proper UPR during root nodule symbiosis.
Root nodule symbiosis within nitrogen-fixing clade (NFC) plants is thought to have arisen from a single gain followed by massive losses in the genomes of ancestral non-nodulating plants. However, molecular evidence supporting this model is limited. Here, we confirm through bioinformatic analysis that NODULES WITH ACTIVATED DEFENSE1 (NAD1) is present only in NFC plants and is thus an NFC-specific gene. Moreover, NAD1 was specifically expressed in nodules. We identified three conserved nodulation-associated cis-regulatory elements (NACE1–3) in the promoter of LjNAD1 from Lotus japonicus that are required for its nodule specific expression. A survey of NFC plants revealed that NACE1 and NACE2 are specific to the Fabales and Papilionoideae, respectively, while NACE3 is present in all NFC plants. Moreover, we found that Nodule inception (NIN) directly binds to all three NACEs to activate NAD1 expression. Mutation of L. japonicus LjNAD1 resulted in the formation of abnormal symbiosomes with enlarged symbiosome space and frequent breakdown of bacteroids in nodules, resembling phenotypes reported for Medicago truncatula Mtnad1 and Mtnin mutants. These data point to NIN–NAD1 as an important module regulating rhizobial accommodation in nodules. The regulation of NAD1 by NIN in the NFC ancestor represent an important evolutionary adaptation for nodulation.
Revealing the mechanisms underlying soil microbial community assembly is a fundamental objective in molecular ecology. However, despite increasing body of research on overall microbial community assembly mechanisms, our understanding of subcommunity assembly mechanisms for different prokaryotic and fungal taxa remains limited. Here, soils were collected from more than 100 sites across southwestern China. Based on amplicon high-throughput sequencing and iCAMP analysis, we determined the subcommunity assembly mechanisms for various microbial taxa. The results showed that dispersal limitation and homogenous selection were the primary drivers of soil microbial community assembly in this region. However, the subcommunity assembly mechanisms of different soil microbial taxa were highly variable. For instance, the contribution of homogenous selection to Crenarchaeota subcommunity assembly was 70%, but it was only around 10% for the subcommunity assembly of Actinomycetes, Gemmatimonadetes and Planctomycetes. The assembly of subcommunities including microbial taxa with higher occurrence frequencies, average relative abundance and network degrees, as well as wider niches tended to be more influenced by homogenizing dispersal and drift, but less affected by heterogeneous selection and dispersal limitation. The subcommunity assembly mechanisms also varied substantially among different functional guilds. Notably, the subcommunity assembly of diazotrophs, nitrifiers, saprotrophs and some pathogens were predominantly controlled by homogenous selection, while that of denitrifiers and fungal pathogens were mainly affected by stochastic processes such as drift. These findings provide novel insights into understanding soil microbial diversity maintenance mechanisms, and the analysis pipeline holds significant value for future research.
Arabidopsis thaliana is currently the most-studied plant species on earth, with an unprecedented number of genetic, genomic, and molecular resources having been generated in this plant model. In the era of translating foundational discoveries to crops and beyond, we aimed to highlight the utility and challenges of using Arabidopsis as a reference for applied plant biology research, agricultural innovation, biotechnology, and medicine. We hope that this review will inspire the next generation of plant biologists to continue leveraging Arabidopsis as a robust and convenient experimental system to address fundamental and applied questions in biology. We aim to encourage lab and field scientists alike to take advantage of the vast Arabidopsis datasets, annotations, germplasm, constructs, methods, molecular and computational tools in our pursuit to advance understanding of plant biology and help feed the world’s growing population. We envision that the power of Arabidopsis-inspired biotechnologies and foundational discoveries will continue to fuel the development of resilient, high-yielding, nutritious plants for the betterment of plant and animal health and greater environmental sustainability.
