Distributing Plant Developmental Regulatory Proteins via Plasmodesmata

Abstract

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.

Keywords: KNOTTED1; SHORTROOT; intercellular communication; non-cell-autonomous transcription factors; plant meristem; plasmodesmata.

Figure 1

Schematic depiction of biogenesis of plasmodesmata and plasmodesmata morphotypes. (A) Primary plasmodesmata are synthesized during cytokinesis. A portion of the newly forming cell wall segment termed the cell plate in a dividing cell (left) is shown enlarged on the right. Here, strands of ER traverse the expanding cell plate to ultimately mature into plasmodesmata. In this process, ER strands bridging the expanding cell plate are stabilized by MCTP tethering factors and potentially synaptotagmins (SYTs). ER strands are shaped into the desmotubule, likely by membrane constriction via MCTP and reticulon (RTN)-type proteins. (B) Two means of secondary plasmodesmal biogenesis can be distinguished: a new plasmodesmal channel can be inserted in close proximity to an already existing plasmodesma through a process called ‘twinning’ (left). Furthermore, de novo biogenesis creates plasmodesmata via membrane penetration into an often thinned cell wall segment independent from an existing plasmodesma (right). (C) Different plasmodesma morphotypes and their possible transitions. Simple plasmodesmata can originate from either primary or de novo biogenesis. Simple plasmodesmata can become twinned plasmodesmata via twinning (see (B)). On highly specialized intercellular interfaces, simple plasmodesmata can attain specialized morphologies, such as a funnel-shaped morphology. Complex plasmodesmata are characterized by a central cavity and a branched desmotubule and can arise through the modification of simple or twinned plasmodesmata, but they can also arise during de novo secondary biogenesis. X- or Y-shaped plasmodesmata have an unresolved relationship with the various transitions (being intermediaries during twinning or transformation toward a complex morphotype; dashed arrows). Yellow arrows among (A–C) point to the plasmodesmal morphologies that the biogenic processes can give rise to.

Figure 2

Modulation of plasmodesmata conductivity by local cell wall modification and a proposed mechanism for pressure-induced plasmodesmata conductivity regulation. (A) When callose (indicated in blue) levels in the cell wall at plasmodesmata are low, the neck region of the symplastic tunnel is open, resulting in a relatively high SEL. (B) When callose levels at plasmodesmata are high, especially at the plasmodesmal entrance, the neck region is constricted resulting in a smaller SEL and less conductivity. (C) Schematic representing plasmodesmata between two cells with a low difference in pressure. Spokes-like elements (possibly formed by tethering proteins) keep the desmotubule in place. (D) When pressures between two cells differ strongly, the ER at the plasmodesma on the side of the cell with the higher pressure is pressed against the plasma membrane, causing the entrance of the cytoplasmic sleeve to close.

Figure 3

Examples of cargo-dependent regulatory mechanisms that control intercellular transport capacity of proteins carrying developmental instructions. (A) Non-targeted proteins (depicted by blue rectangles) like LFY travel from cell to cell via diffusion (and possibly advection). The rate of intercellular movement of these proteins is dependent on the dimensions of the cytosolic sleeve, the diffusive properties of the protein, and its concentration gradient across a cellular interface, but it does not involve active modification of either the cargo or plasmodesmal apparatus (processes described in (B–E)). Note that the translocation steps depicted in (B–E) may still be diffusion-driven. (B) The transcription factors TMO7 and SHR require a transient nuclear localization to become mobile from cell to cell. The processes occurring in the nucleus that enable the mobility of these proteins are unknown. SHR is retained in the nucleus of the neighboring cell by interaction with SCR, preventing SHR from moving to other cells. (C) Involvement of endosomes and the cytoskeleton in enabling intercellular protein movement. SHR localizes to endosomes via interaction with SIEL, enabling intercellular movement of SHR. The SIEL and SHR association is understood to be functionally relevant at endosomes, but it could possibly already happen in the nucleus (depicted in (B)) or the cytosol. SHR-associated endosomes (brown) are paused from moving by the microtubule cytoskeleton-associated KinG, during which an unknown mechanism promotes the intercellular movement capacity of SHR. Additionally, another cytoskeleton-based activity is involved in regulating KN1 protein transportability. The microtubule-associated MPB2C binds misfolded KN1 proteins, possibly preventing these proteins from moving to neighboring cells. (D) Chaperonins act in a receiving cell to refold proteins that traverse plasmodesmata in an unfolded state, such as KN1. (E) Members of the MCTP family tether the ER and plasma membrane at plasmodesmata. FT is a transcriptional regulator that physically interacts with FTIP1 (MCTP1), and this interaction fosters FT intercellular mobility via an unknown molecular mechanism.