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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 -
The New Phytologist Apr 2024
Topics: Cell Communication; Plant Proteins; Plasmodesmata
PubMed: 38363008
DOI: 10.1111/nph.19610 -
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 -
Annual Review of Plant Biology Feb 2024Multicellularity has emerged multiple times in evolution, enabling groups of cells to share a living space and reducing the burden of solitary tasks. While unicellular... (Review)
Review
Multicellularity has emerged multiple times in evolution, enabling groups of cells to share a living space and reducing the burden of solitary tasks. While unicellular organisms exhibit individuality and independence, cooperation among cells in multicellular organisms brings specialization and flexibility. However, multicellularity also necessitates intercellular dependence and relies on intercellular communication. In plants, this communication is facilitated by plasmodesmata: intercellular bridges that allow the direct (cytoplasm-to-cytoplasm) transfer of information between cells. Plasmodesmata transport essential molecules that regulate plant growth, development, and stress responses. They are embedded in the extracellular matrix but exhibit flexibility, adapting intercellular flux to meet the plant's needs. In this review, we delve into the formation and functionality of plasmodesmata and examine the capacity of the plant communication network to respond to developmental and environmental cues. We illustrate how environmental pressure shapes cellular interactions and aids the plant in adapting its growth. Expected final online publication date for the , Volume 75 is May 2024. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
PubMed: 38424063
DOI: 10.1146/annurev-arplant-070623-093110 -
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 -
Annual Review of Plant Biology Feb 2024Leaves form veins whose patterns vary from a single vein running the length of the leaf to networks of staggering complexity where huge numbers of veins connect to other... (Review)
Review
Leaves form veins whose patterns vary from a single vein running the length of the leaf to networks of staggering complexity where huge numbers of veins connect to other veins at both ends. For the longest time, vein formation was thought to be controlled only by the polar, cell-to-cell transport of the plant hormone auxin; recent evidence suggests that is not so. Instead, it turns out that vein patterning features are best accounted for by a combination of polar auxin transport, facilitated auxin diffusion through plasmodesmata intercellular channels, and auxin signal transduction-though the latter's precise contribution remains unclear. Equally unclear remain the sites of auxin production during leaf development, on which that vein patterning mechanism ought to depend. Finally, whether that vein patterning mechanism can account for the variety of vein arrangements found in nature remains unknown. Addressing those questions will be the exciting challenge of future research. Expected final online publication date for the , Volume 75 is May 2024. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
PubMed: 38382907
DOI: 10.1146/annurev-arplant-062923-030348 -
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 -
The New Phytologist Jul 2024Plasmodesmata are plasma membrane-lined connections that join plant cells to their neighbours, establishing an intercellular cytoplasmic continuum through which... (Review)
Review
Plasmodesmata are plasma membrane-lined connections that join plant cells to their neighbours, establishing an intercellular cytoplasmic continuum through which molecules can travel between cells, tissues, and organs. As plasmodesmata connect almost all cells in plants, their molecular traffic carries information and resources across a range of scales, but dynamic control of plasmodesmal aperture can change the possible domains of molecular exchange under different conditions. Plasmodesmal aperture is controlled by specialised signalling cascades accommodated in spatially discrete membrane and cell wall domains. Thus, the composition of plasmodesmata defines their capacity for molecular trafficking. Further, their shape and density can likewise define trafficking capacity, with the cell walls between different cell types hosting different numbers and forms of plasmodesmata to drive molecular flux in physiologically important directions. The molecular traffic that travels through plasmodesmata ranges from small metabolites through to proteins, and possibly even larger mRNAs. Smaller molecules are transmitted between cells via passive mechanisms but how larger molecules are efficiently trafficked through plasmodesmata remains a key question in plasmodesmal biology. How plasmodesmata are formed, the shape they take, what they are made of, and what passes through them regulate molecular traffic through plants, underpinning a wide range of plant physiology.
Topics: Plasmodesmata; Biological Transport; Plants; Plant Cells
PubMed: 38494438
DOI: 10.1111/nph.19666 -
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