Plant plasmodesmata bridges form through ER-dependent incomplete cytokinesis

Abstract

Diverging from conventional cell division models, plant cells undergo incomplete division to generate plasmodesmata communication bridges between daughter cells. While fundamental for plant multicellularity, the mechanisms governing bridge stabilization, as opposed to severing, remain unknown. We found that the endoplasmic reticulum (ER) is decisive in promoting incomplete cytokinesis by inhibiting local abscission events. ER tubes within contracting cell plate fenestrae create energy barriers preventing full closure. Contraction ceases upon encountering a metastable ER-plasma membrane tubular structure, leading to plasmodesmata formation. This process relies on the ER-tethers multiple C2 domains and transmembrane domain proteins 3, 4, and 6, which act as ER stabilizers, preserving ER position and integrity in nascent bridges. Our findings unveil the mechanisms through which plants undergo incomplete division to promote intercellular communication.One-Sentence SummaryUninterrupted ER connections obstruct abscission, causing incomplete cytokinesis and plasmodesmata formation in plants.

Distributing Plant Developmental Regulatory Proteins via Plasmodesmata

“…While the ER may have a general role in fostering cell plate synthesis [ 24 ], the ER strands that traverse the cell plate are critical to the establishment of primary plasmodesmata [ 22 ] ( Figure 1 A). Such bridging strands of ER between the two daughter cells appear to resist the cell plate remodeling processes that close and smoothen the cell plate membrane compartment [ 24 , 25 , 26 ]. The strand of ER persists throughout cell plate maturation and becomes tightly appressed, ultimately forming the desmotubule proper [ 18 , 22 ] ( Figure 1 A).…”

“…Their N-terminal C2-domains can interact with the inner leaflet of the plasma membrane, while the C-terminus traverses the ER membrane [ 35 , 36 ]. Recently, MCTPs were shown to accumulate and oligomerize early during plasmodesmal biogenesis, and in their absence, densities of primary plasmodesmata markedly dropped [ 26 ]. Additionally, the MCTP C-terminal domain inserted in the ER membrane was found to have ER-tubulizing properties, akin to reticulons [ 26 ].…”

“…Recently, MCTPs were shown to accumulate and oligomerize early during plasmodesmal biogenesis, and in their absence, densities of primary plasmodesmata markedly dropped [ 26 ]. Additionally, the MCTP C-terminal domain inserted in the ER membrane was found to have ER-tubulizing properties, akin to reticulons [ 26 ]. Thus, MCTPs are tethering proteins with an aptitude to stabilize and constrict ER strands traversing the cell plate, thereby contributing to successful plasmodesma formation ( Figure 1 A).…”

“…For the spoke-like elements to act as springs that ‘memorize’ a basic position for the desmotubule as assumed in the model, they would need to have a very rigid interaction with the plasmodesmal membrane systems and a very low rate of turnover (at least compared with the timescale that the pressure difference would occur over). Key molecular candidates for constituting spokes-like elements with such properties are the earlier-discussed MCTP-type ER-to-plasma membrane tethering proteins, as they form immobile, high-molecular-weight complexes [ 26 ]. Although the biological relevance of the pressure differential-induced closure of plasmodesmata remains to be studied, a possible biological role could be that such a mechanism acts as a biomechanical safety valve; closing plasmodesmata upon rapid differences in turgor pressure, arising, for instance, from cell wall or membrane damage in one cell, would protect neighboring cells from sudden shifts in their cytosolic contents.…”

“…Plants 2024, 13, 684 3 of 23 strands of ER between the two daughter cells appear to resist the cell plate remodeling processes that close and smoothen the cell plate membrane compartment [24][25][26]. The strand of ER persists throughout cell plate maturation and becomes tightly appressed, ultimately forming the desmotubule proper [18,22] (Figure 1A).…”