The cytosol must flow: intercellular transport through plasmodesmata
Graphical abstract
Section snippets
PD: a primer
Cell–cell signaling and transport in plants is facilitated by nanoscopic channels called PD, often as small as 30 nm in diameter and 100 nm in length, that cross the cell wall and connect neighboring cells [4, 5, 6, 7] (Figure 1). PD have three distinct structural components: a central strand of tightly compressed endoplasmic reticulum (ER), called the ‘desmotubule’; a surrounding membrane that is continuous with the plasma membrane of the cells it connects; and in between these membranes, a
The structure of PD
For decades, most of our knowledge of PD relied on ultrastructural studies using transmission electron microscopy (TEM). These studies revealed that PD form either during cell division (primary PD) when strands of ER are trapped as the cell plate forms, or after cell division (secondary PD) through unknown mechanisms that rely on localized modification of the cell wall [22]. Many PD are straight channels, but some are branched and complex, especially in the nonvascular tissue of older leaves,
Transport through PD
Molecules move rapidly through the cytoplast, mostly through convection generated by cytoplasmic streaming (with diffusion contributing to a lesser extent), where they will eventually encounter PD [41]. Since nearly all plant cells are connected by PD, this means that most molecules — including proteins — have ample opportunity to move from one cell to another. This is confirmed by the simple observations that heterologous fluorescent proteins, such as GFP, and large fluorescent dyes, such as
PD control differentiation and development
Since plant cells are in constant communication via PD, cells often need to isolate themselves by reducing PD transport to differentiate and acquire a new genetic program. Indeed, PD transport is often drastically restricted around regions of cells during morphogenesis, including during embryogenesis, inflorescence development, and lateral root formation [6, 46, 47, 48, 60, 61, 62, 63••, 64] (Figure 3). Exploring the lateral root example, Benitez-Alfonso et al. showed that PD transport around
Intracellular regulators of intercellular transport: organelle-nucleus-PD signaling
Genetic screens revealed that chloroplasts and mitochondria are critical regulators of PD function and formation, leading to exciting discoveries about the complex signaling networks underlying intercellular transport and communication in plants (described in depth elsewhere [4, 5, 67, 68]). Disruptions in chloroplast or mitochondrial genome expression trigger signal transduction pathways that affect nuclear gene expression, which in turn cause increased PD transport and the formation of more
The convergent evolution of PD
PD-like structures have evolved independently in multiple lineages of brown and green algae [71] (Figure 4), leading to the prevailing hypothesis that PD support the evolution of complex, parenchymatous multicellular forms [1] in organisms whose cells are surrounded by cellulosic cell walls. PD form in all land plants (embryophytes) studied to date, including liverworts, mosses, hornworts, and polysporangiophytes (‘vascular’ plants). Our understanding of embryophyte PD evolution needs revision
Conclusion
Since the divergence of animals, plants, fungi, and algae from a single-celled eukaryote over 1.5 billion years ago, each of these lineages independently evolved multicellularity. Cell–cell signaling in complex multicellular organisms requires extensive adaptations, including some convergent adaptations (e.g., remarkably similar PD in brown algae, various green algae, and plants) and many divergent adaptations (gap junctions, for example, have very little similarity to PD). Unlike animal cells,
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
This work was supported by NSF pre-doctoral fellowships to JOB and AMR (DGE 1106400) and gift funds to PCZ.
References (72)
- et al.
Plasmodesmata dynamics are coordinated by intracellular signaling pathways
Curr Opin Plant Biol
(2013) - et al.
The role of mobile small RNA species during root growth and development
Curr Opin Cell Biol
(2012) - et al.
Developmental patterning by gradients of mobile small RNAs
Curr Opin Genet Dev
(2014) - et al.
Callose biosynthesis regulates symplastic trafficking during root development
Dev Cell
(2011) - et al.
A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins
PLoS Path
(2010) - et al.
Parallels between nuclear-pore and plasmodesmal trafficking of information molecules
Planta
(2000) - et al.
A developmental framework for complex plasmodesmata formation revealed by large-scale imaging of the Arabidopsis leaf epidermis
Plant Cell
(2013) - et al.
Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states
Plant Physiol
(2001) - et al.
Investigating plasmodesmata genetics with virus-induced gene silencing and an Agrobacterium-mediated GFP movement assay
- et al.
Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots
Proc Natl Acad Sci U S A
(2006)
An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants
Science
Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling
Dev Cell
Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata
Proc Natl Acad Sci U S A
The origins of multicellular organisms
Evol Dev
The evolutionary-developmental origins of multicellularity
Am J Bot
Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein
Science
Plasmodesmata paradigm shift: regulation from without versus within
Annu Rev Plant Biol
Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses
J Exp Bot
Developmental control of plasmodesmata frequency, structure, and function
Cellular pathways for viral transport through plasmodesmata
Protoplasma
Intercellular protein movement: deciphering the language of development
Annu Rev Cell Dev Biol
Stomata and plasmodesmata
Protoplasma
Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer yellow
Planta
Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants
Annu Rev Cell Dev Biol
Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana
Development
Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport
Proc Natl Acad Sci U S A
Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function
Science
Plasmodesmata formation and cell-to-cell transport function are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis
Proc Natl Acad Sci U S A
A comparison of two methods of microinjection for assessing altered plasmodesmal gating in tissues expressing viral movement proteins
Plant J
Plasmodesmata: channels for intercellular signaling during plant growth and development
Plasmodesmata: channels for viruses on the move
Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function
Protoplasma
The cytoskeleton in plasmodesmata: a role in intercellular transport?
J Exp Bot
Plasmodesmata viewed as specialised membrane adhesion sites
Protoplasma
Biology of callose (β-1,3-glucan) turnover at plasmodesmata
Protoplasma
A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis
Plant Cell
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