The cytosol must flow: intercellular transport through plasmodesmata

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Highlights

  • PD are nanoscopic channels connecting plant cells across cell walls.

  • Transcription factors, RNAs, and hormones move through PD to control development.

  • Restricting PD transport is critical for cell differentiation and plant development.

  • Chloroplasts and mitochondria regulate PD transport and cell–cell signaling.

  • PD convergently evolved in plants and several algal lineages.

Plant cells are connected across cell walls by nanoscopic channels called plasmodesmata (PD), which allow plant cells to share resources and exchange signaling molecules. Several protein components of PD membranes have been identified, and recent advances in superresolution live-cell microscopy are illuminating PD ultrastructure. Restricting transport through PD is crucial for morphogenesis, since hormones and hundreds of transcription factors regularly move through PD, and this transport must stop to allow cells to begin differentiating. Chloroplasts and mitochondria regulate PD function through signal transduction networks that coordinate plant physiology and development. Recent discoveries on the relationships of land plants and their algal relatives suggest that PD have evolved independently in several lineages, emphasizing the importance of cytosolic bridges in multicellular biology.

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.

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