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The Plant Cell Sep 2023Emerging evidence indicates that in addition to its well-recognized functions in antiviral RNA silencing, dsRNA elicits pattern-triggered immunity (PTI), likely...
Emerging evidence indicates that in addition to its well-recognized functions in antiviral RNA silencing, dsRNA elicits pattern-triggered immunity (PTI), likely contributing to plant resistance against virus infections. However, compared to bacterial and fungal elicitor-mediated PTI, the mode-of-action and signaling pathway of dsRNA-induced defense remain poorly characterized. Here, using multicolor in vivo imaging, analysis of GFP mobility, callose staining, and plasmodesmal marker lines in Arabidopsis thaliana and Nicotiana benthamiana, we show that dsRNA-induced PTI restricts the progression of virus infection by triggering callose deposition at plasmodesmata, thereby likely limiting the macromolecular transport through these cell-to-cell communication channels. The plasma membrane-resident SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE 1, the BOTRYTIS INDUCED KINASE1/AVRPPHB SUSCEPTIBLE1-LIKE KINASE1 kinase module, PLASMODESMATA-LOCATED PROTEINs 1/2/3, as well as CALMODULIN-LIKE 41 and Ca2+ signals are involved in the dsRNA-induced signaling leading to callose deposition at plasmodesmata and antiviral defense. Unlike the classical bacterial elicitor flagellin, dsRNA does not trigger a detectable reactive oxygen species (ROS) burst, substantiating the idea that different microbial patterns trigger partially shared immune signaling frameworks with distinct features. Likely as a counter strategy, viral movement proteins from different viruses suppress the dsRNA-induced host response leading to callose deposition to achieve infection. Thus, our data support a model in which plant immune signaling constrains virus movement by inducing callose deposition at plasmodesmata and reveals how viruses counteract this layer of immunity.
PubMed: 37378592
DOI: 10.1093/plcell/koad176 -
Biology Open Oct 2023Cell-cell communication is a central feature of multicellular organisms, enabling division of labour and coordinated responses. Plasmodesmata are membrane-lined pores... (Review)
Review
Cell-cell communication is a central feature of multicellular organisms, enabling division of labour and coordinated responses. Plasmodesmata are membrane-lined pores that provide regulated cytoplasmic continuity between plant cells, facilitating signalling and transport across neighboring cells. Plant development and survival profoundly depend on the existence and functioning of these structures, bringing them to the spotlight for both fundamental and applied research. Despite the rich conceptual and translational rewards in sight, however, the study of plasmodesmata poses significant challenges. This Review will mostly focus on research published between May 2022 and May 2023 and intends to provide a short overview of recent discoveries, innovations, community resources and hypotheses.
Topics: Plasmodesmata; Cell Communication; Signal Transduction; Plant Development; Biology
PubMed: 37874138
DOI: 10.1242/bio.060123 -
Nature Chemical Biology Nov 2023Brassinosteroids (BRs) are steroidal phytohormones that are essential for plant growth, development and adaptation to environmental stresses. BRs act in a dose-dependent...
Brassinosteroids (BRs) are steroidal phytohormones that are essential for plant growth, development and adaptation to environmental stresses. BRs act in a dose-dependent manner and do not travel over long distances; hence, BR homeostasis maintenance is critical for their function. Biosynthesis of bioactive BRs relies on the cell-to-cell movement of hormone precursors. However, the mechanism of the short-distance BR transport is unknown, and its contribution to the control of endogenous BR levels remains unexplored. Here we demonstrate that plasmodesmata (PD) mediate the passage of BRs between neighboring cells. Intracellular BR content, in turn, is capable of modulating PD permeability to optimize its own mobility, thereby manipulating BR biosynthesis and signaling. Our work uncovers a thus far unknown mode of steroid transport in eukaryotes and exposes an additional layer of BR homeostasis regulation in plants.
Topics: Brassinosteroids; Plasmodesmata; Plant Growth Regulators; Plants; Hormones; Gene Expression Regulation, Plant; Arabidopsis Proteins
PubMed: 37365405
DOI: 10.1038/s41589-023-01346-x -
Development (Cambridge, England) Oct 2023Myosins are evolutionarily conserved motor proteins that interact with actin filaments to regulate organelle transport, cytoplasmic streaming and cell growth....
Myosins are evolutionarily conserved motor proteins that interact with actin filaments to regulate organelle transport, cytoplasmic streaming and cell growth. Plant-specific class XI myosin proteins direct cell division and root organogenesis. However, the roles of plant-specific class VIII myosin proteins in plant growth and development are less understood. Here, we investigated the function of an auxin-regulated class VIII myosin, Arabidopsis thaliana MYOSIN 1 (ATM1), using genetics, transcriptomics and live cell microscopy. ATM1 is associated with the plasma membrane and plasmodesmata within the root apical meristem (RAM). Loss of ATM1 function results in decreased RAM size and reduced cell proliferation in a sugar-dependent manner. Auxin signaling and transcriptional responses were dampened in atm1-1 roots. Complementation of atm1-1 with a tagged ATM1 driven under the native ATM1 promoter restored root growth and cell cycle progression. Genetic analyses of atm1-1 seedlings with HEXOKINASE 1 (HXK1) and TARGET OF RAPAMYCIN COMPLEX 1 (TORC1) overexpression lines indicate that ATM1 is downstream of TOR. Collectively, these results provide previously unreported evidence that ATM1 functions to influence cell proliferation in primary roots in response to auxin and sugar cues.
Topics: Arabidopsis; Arabidopsis Proteins; Gene Expression Regulation, Plant; Indoleacetic Acids; Meristem; Myosins; Plant Roots; Sugars
PubMed: 37306290
DOI: 10.1242/dev.201762 -
Molecular Plant Pathology Dec 2023The genus Potyvirus is considered as the largest among plant single-stranded (positive-sense) RNA viruses, causing considerable economic damage to vegetable and fruit... (Review)
Review
The genus Potyvirus is considered as the largest among plant single-stranded (positive-sense) RNA viruses, causing considerable economic damage to vegetable and fruit crops worldwide. Through the coordinated action of four viral proteins and a few identified host factors, potyviruses exploit the endomembrane system of infected cells for their replication and for their intra- and intercellular movement to and through plasmodesmata (PDs). Although a significant amount of data concerning potyvirus movement has been published, no synthetic review compiling and integrating all information relevant to our current understanding of potyvirus transport is available. In this review, we highlight the complexity of potyvirus movement pathways and present three potential nonexclusive mechanisms based on (1) the use of the host endomembrane system to produce membranous replication vesicles that are targeted to PDs and move from cell to cell, (2) the movement of extracellular viral vesicles in the apoplasm, and (3) the transport of virion particles or ribonucleoprotein complexes through PDs. We also present and discuss experimental data supporting these different models as well as the aspects that still remain mostly speculative.
Topics: Potyvirus; Viral Proteins; Plant Diseases; Nicotiana
PubMed: 37571979
DOI: 10.1111/mpp.13383 -
The Plant Genome Dec 2023As conserved regulatory agents, noncoding RNAs (ncRNAs) have an important impact on many aspects of plant life, including growth, development, and environmental... (Review)
Review
As conserved regulatory agents, noncoding RNAs (ncRNAs) have an important impact on many aspects of plant life, including growth, development, and environmental response. Noncoding RNAs can travel through not only plasmodesma and phloem but also intercellular barriers to regulate distinct processes. Increasing evidence shows that the intercellular trans-kingdom transmission of ncRNAs is able to modulate many important interactions between plants and other organisms, such as plant response to pathogen attack, the symbiosis between legume plants and rhizobia and the interactions with parasitic plants. In these interactions, plant ncRNAs are believed to be sorted into extracellular vesicles (EVs) or other nonvesicular vehicles to pass through cell barriers and trigger trans-kingdom RNA interference (RNAi) in recipient cells from different species. There is evidence that the features of extracellular RNAs and associated RNA-binding proteins (RBPs) play a role in defining the RNAs to retain in cell or secrete outside cells. Despite the few reports about RNA secretion pathway in plants, the export of extracellular ncRNAs is orchestrated by a series of pathways in plants. The identification and functional analysis of mobile small RNAs (sRNAs) are attracting increasing attention in recent years. In this review, we discuss recent advances in our understanding of the function, sorting, transport, and regulation of plant extracellular ncRNAs.
Topics: Gene-Environment Interaction; RNA Interference; RNA, Untranslated; RNA, Plant; Plants
PubMed: 36444889
DOI: 10.1002/tpg2.20289 -
Journal of Plant Physiology Apr 2024Root growth and development need proper carbon partitioning between sources and sinks. Photosynthesis products are unloaded from the phloem and enter the root meristem... (Review)
Review
Root growth and development need proper carbon partitioning between sources and sinks. Photosynthesis products are unloaded from the phloem and enter the root meristem cell by cell. While sugar transporters play a major role in phloem loading, phloem unloading occurs via the plasmodesmata in growing root tips. The aperture and permeability of plasmodesmata strongly influence symplastic unloading. Recent research has dissected the symplastic path for phloem unloading and identified several genes that regulate phloem unloading in the root. Callose turnover and membrane lipid composition alter the shape of plasmodesmata, allowing fine-tuning to adapt phloem unloading to the environmental and developmental conditions. Unloaded sugars act both as an energy supply and as signals to coordinate root growth and development. Increased knowledge of how phloem unloading is regulated enhances our understanding of carbon allocation in plants. In the future, it may be possible to modulate carbon allocation between sources and sinks in a manner that would contribute to increased plant biomass and carbon fixation.
Topics: Phloem; Plants; Biological Transport; Meristem; Carbon
PubMed: 38428153
DOI: 10.1016/j.jplph.2024.154203 -
Plants (Basel, Switzerland) Aug 2023In order to adapt to sessile life and terrestrial environments, vascular plants have developed highly sophisticated cells to transport photosynthetic products and... (Review)
Review
In order to adapt to sessile life and terrestrial environments, vascular plants have developed highly sophisticated cells to transport photosynthetic products and developmental signals. Of these, two distinct cell types (i.e., the sieve element (SE) and companion cell) are arranged in precise positions, thus ensuring effective transport. During SE differentiation, most of the cellular components are heavily modified or even eliminated. This peculiar differentiation implies the selective disintegration of the nucleus (i.e., enucleation) and the loss of cellular translational capacity. However, some cellular components necessary for transport (e.g., plasmalemma) are retained and specific phloem proteins (P-proteins) appear. Likewise, MYB (i.e., ) and NAC (i.e., and ) transcription factors (TFs) and OCTOPUS proteins play a notable role in SE differentiation. The maturing SEs become heavily dependent on neighboring non-conducting companion cells, to which they are connected by plasmodesmata through which only 20-70 kDa compounds seem to be able to pass. The study of sieve tube proteins still has many gaps. However, the development of a protocol to isolate proteins that are free from any contaminating proteins has constituted an important advance. This review considers the very detailed current state of knowledge of both bound and soluble sap proteins, as well as the role played by the companion cells in their presence. Phloem proteins travel long distances by combining two modes: non-selective transport via bulk flow and selective regulated movement. One of the goals of this study is to discover how the protein content of the sieve tube is controlled. The majority of questions and approaches about the heterogeneity of phloem sap will be clarified once the morphology and physiology of the plasmodesmata have been investigated in depth. Finally, the retention of specific proteins inside an SE is an aspect that should not be forgotten.
PubMed: 37687278
DOI: 10.3390/plants12173033 -
The Plant Cell Aug 2023Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as...
Effective cellular signaling relies on precise spatial localization and dynamic interactions among proteins in specific subcellular compartments or niches, such as cell-to-cell contact sites and junctions. In plants, endogenous and pathogenic proteins gained the ability to target plasmodesmata, membrane-lined cytoplasmic connections, through evolution to regulate or exploit cellular signaling across cell wall boundaries. For example, the receptor-like membrane protein PLASMODESMATA-LOCATED PROTEIN 5 (PDLP5), a potent regulator of plasmodesmal permeability, generates feed-forward or feed-back signals important for plant immunity and root development. However, the molecular features that determine the plasmodesmal association of PDLP5 or other proteins remain largely unknown, and no protein motifs have been identified as plasmodesmal targeting signals. Here, we developed an approach combining custom-built machine-learning algorithms and targeted mutagenesis to examine PDLP5 in Arabidopsis thaliana and Nicotiana benthamiana. We report that PDLP5 and its closely related proteins carry unconventional targeting signals consisting of short stretches of amino acids. PDLP5 contains 2 divergent, tandemly arranged signals, either of which is sufficient for localization and biological function in regulating viral movement through plasmodesmata. Notably, plasmodesmal targeting signals exhibit little sequence conservation but are located similarly proximal to the membrane. These features appear to be a common theme in plasmodesmal targeting.
Topics: Arabidopsis Proteins; Plasmodesmata; Arabidopsis; Membrane Proteins; Carrier Proteins
PubMed: 37225403
DOI: 10.1093/plcell/koad152 -
Plants (Basel, Switzerland) Feb 2024During plant development, mobile proteins, including transcription factors, abundantly serve as messengers between cells to activate transcriptional signaling cascades... (Review)
Review
During plant development, mobile proteins, including transcription factors, abundantly serve as messengers between cells to activate transcriptional signaling cascades in distal tissues. These proteins travel from cell to cell via nanoscopic tunnels in the cell wall known as plasmodesmata. Cellular control over this intercellular movement can occur at two likely interdependent levels. It involves regulation at the level of plasmodesmata density and structure as well as at the level of the cargo proteins that traverse these tunnels. In this review, we cover the dynamics of plasmodesmata formation and structure in a developmental context together with recent insights into the mechanisms that may control these aspects. Furthermore, we explore the processes involved in cargo-specific mechanisms that control the transport of proteins via plasmodesmata. Instead of a one-fits-all mechanism, a pluriform repertoire of mechanisms is encountered that controls the intercellular transport of proteins via plasmodesmata to control plant development.
PubMed: 38475529
DOI: 10.3390/plants13050684