An official website of the United States government
Abstract Plant viruses rely on intercellular trafficking via plasmodesmata (PD) to move between cells in their hosts. This ability is conferred by virus encoded movement proteins (MPs), which can increase plasmodesmal permeability and intercellular trafficking independent of other viral proteins. Callose dynamics in the cell walls surrounding PD have a critical role in determining plasmodesmal flux, with decreased callose levels correlates with increased trafficking. Notably, PD callose levels are both increased and decreased during virus infection, suggesting that there are regulatory responses to the virus. Here, we found that auxin and brassinosteroid (BR) exert opposing effects on PD connectivity. While auxin enhances intercellular trafficking primarily by promoting PD density, BR restricts connectivity by reducing reduced PD biogenesis and increasing callose accumulation. We identified genes involved in auxin and BR signaling as Most of those genes encode membrane-associated proteins. We identified the receptor-like protein RLP15 as a critical upstream regulator of intracellular auxin homeostasis through stabilization of the ER-localized auxin transporter PILS5. In parallel, negative regulators of PD permeability including ERECTA, PPI, CER3, and DEAL2 define a host connectivity restraint network. These findings point to an auxin-BR module as a nexus for determining the degree of changes in plasmodesmal permeability that is elicited by the viral MP. Together with changes in callose dynamics at PD, this regulatory node allows plants to maintain homeostasis of intercellular trafficking, possibly contributing to maintenance of cell and tissue integrity during infection. Significance StatementPlant viruses encode movement proteins (MP) which increase plasmodesmal permeability to allow the local cell-to-cell trafficking of viral entities. This study identifies a non-canonical auxin-BR antagonistic module that regulates plasmodesmal connectivity in response to the changes triggered by viral movement protein early in the infection cycle. We demonstrate that MP30, encoded by the tobacco mosaic virus, rewires BR’s and auxin’s roles in controlling intercellular communication by interfering with membrane proteins associated with these hormonal pathways. By defining this hormonal nexus, our findings reveal a sophisticated host-pathogen interface where plants attempt to maintain intercellular homeostasis during the onset of viral pathogenesis.
more »
« less
This content will become publicly available on January 13, 2027
Plasmodesmal regulation: context matters
Abstract The essence of multicellular life lies in the dynamic tension between unity and autonomy of individual cells achieved through diverse molecular and structural mechanisms. Plants have evolved plasmodesmata as an elegant solution to this fundamental challenge, creating cytoplasmic bridges that enable both local and systemic communication despite constraints imposed by their rigid cell walls. An emerging paradigm reveals that the core molecular machinery brings about context-dependent, multi-faceted regulation of plasmodesmal permeability through integration with various cellular signaling pathways. In this context, regulation through callose accumulation and degradation has been established as the primary mechanism controlling plasmodesmal permeability. Recent studies now reveal that this regulation is signal-specific and mechanistically diverse, giving rise to the same apparent endpoint of closure with different biological outcomes depending on the signaling context. This creates biological specificity through convergence on shared callose-regulating mechanisms. Understanding how regulatory complexes assemble, achieve signal specificity, and integrate diverse cellular inputs represents a critical frontier in plant biology. In this review, we discuss the molecular players, regulatory mechanisms, and integrative signaling networks that support this paradigm.
more »
« less
- Award ID(s):
- 2054685
- PAR ID:
- 10695634
- Editor(s):
- Liesche, Johannes
- Publisher / Repository:
- Journal of Experimental Botany
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 77
- Issue:
- 8
- ISSN:
- 0022-0957
- Page Range / eLocation ID:
- 2177 to 2196
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Soil salinization is a growing global threat that limits crop productivity. To cope with sodium (Na⁺) stress, plants have evolved tolerance mechanisms, including excluding Na⁺ from shoot tissues and tolerating elevated Na⁺ within shoots through tissue- and cellular-level mechanisms. Most current knowledge of Na⁺ accumulation comes from organ- or whole-plant measurements that lack the spatial resolution needed to resolve cellular tolerance mechanisms. Here, we used histological approaches to map leaf Na⁺ distribution in tomato (Solanum) species with contrasting salt-tolerance strategies. In the Na⁺-excluding domesticated tomato (cv. M82), Na⁺ was largely confined to the bundle sheath, whereas Na⁺-including wild relatives accumulated Na⁺ throughout the blade mesophyll. Consistent with these cell population-specific Na⁺ patterns, M82, but notS. pennellii, exhibited reduced symplastic transport and plasmodesmal permeability under salt stress. A genetic screen combined with transcriptome profiling implicatedPlasmodesmata-Located Protein 1(PDLP1), a regulator of callose-mediated plasmodesmal closure, in establishing symplastic domains in M82 that restrict Na⁺ movement into the mesophyll. Moreover,PDLP1expression negatively correlated with mesophyll Na+levels across wild and domesticated tomatoes. Collectively, these results link cellular Na⁺ enrichment patterns to symplastic connectivity and suggest thatPDLP1-mediated regulation of plasmodesmata contributes to leaf-level salt-tolerance strategies. HighlightsCell type-specific Na⁺ accumulation differs between domesticated tomato (Solanum lycopersicumcv. M82) and its wild relativeS. pennellii.Additional salt-tolerant wild tomato relatives exhibit leaf Na⁺ enrichment patterns similar toS. pennellii.Salt stress reduces symplastic transport and plasmodesmal permeability in M82 leaves but not inS. pennellii.An introgression line (IL6-4) between the two tomato species, which carriesS. pennellii Plasmodesmata-Located Protein 1(SpPDLP1), showsS. pennellii-like Na⁺ enrichment patterns.PDLP1expression shows a negative correlation with mesophyll Na+levels across tomato species.more » « less
-
Abstract 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.more » « less
-
McSteen, Paula (Ed.)Abstract RAF-like kinases, members of the mitogen-activated protein kinase kinase kinase (MAPKKK) family, are central integrators of external and internal signals in plant stress responses and growth regulation. These kinases mediate signaling through multiple hormone pathways, including abscisic acid-dependent and -independent pathways, ethylene signaling, and rapid auxin responses. Unlike typical MAPKKKs that function through kinase cascades, RAF-like kinases primarily employ direct phosphorylation of downstream targets and dynamic subcellular localization to mediate specific physiological responses. Here, we review the emerging roles of RAF-like kinases in Arabidopsis thaliana, highlighting their integrative functions in hormone signaling, stress responses, and growth control. The complex interplay between different RAF-like kinase subgroups and their diverse cellular targets underscores the intricate regulatory mechanisms plants have evolved to coordinate environmental responses with development.more » « less
-
Abstract The bone-morphogenetic protein (BMP)-SMAD signal transduction pathway regulates fundamental cellular processes such as fate specification, tissue patterning, and stem cell homeostasis across metazoans and has a conserved signaling architecture. However, the quantitative dynamics of SMAD signaling and regulatory strategies governing pathway activity show a wide range of variation across developmental and stem-cell systems. In the present review, we summarize insights from six major biological contexts—Drosophila embryo, germline stem cells, and the larval and pupal wing discs; the Danio rerio (zebrafish) embryo; and human pluripotent stem cells—to compare how BMP signals are measured, manipulated, modeled, and integrated. We begin by outlining the canonical BMP signaling pathway and the mechanisms of BMP gradient formation across developmental systems, highlighting how conserved pathway components contribute to the formation of system-specific spatial profiles. We then summarize intracellular Smad dynamics and how endogenous pathway dynamics are measured through quantitative imaging of the phosphorylated Smad. Next, we examine how BMP signaling is interpreted through tiered transcriptional responses of downstream target genes. Next, we summarize the mechanistic and computational models of integrated gradient formation, signal transduction, and gene regulation across the presented systems. These insights reveal unifying design principles and performance objectives that govern BMP-SMAD signaling across species and cell types and frame open questions for future cross-species and translational studies.more » « less
