Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments

Abstract

Plant cell morphogenesis relies on the organization and function of two polymer arrays separated by the plasma membrane: the cortical microtubule cytoskeleton and cellulose microfibrils in the cell wall. Studies using in vivo markers confirmed that one function of the cortical microtubule array is to drive organization of cellulose microfibrils by guiding the trajectories of active cellulose synthase (CESA) complexes in the plasma membrane, thus orienting nascent microfibrils. Here we provide evidence that cortical microtubules also position the delivery of CESA complexes to the plasma membrane and interact with small CESA-containing compartments by a mechanism that permits motility driven by microtubule depolymerization. The association of CESA compartments with cortical microtubules was greatly enhanced during osmotic stress and other treatments that limit cellulose synthesis. On recovery from osmotic stress, delivery of CESA complexes to the plasma membrane was observed in association with microtubule-tethered compartments. These results reveal multiple functions for the microtubule cortical array in organizing CESA in the cell cortex.

Patterning of plant cell wall deposition by cortical microtubules

“…This concept is supported by the strong link between microtubules and cellulose synthesis [38][39][40] , and the observation that the cell wall is remodelled in altered gravity conditions 89,99,100 . One could therefore hypothesize that cell wall remodelling in plants in altered gravity conditions is mediated by an altered microtubule array organization.…”

“…The movement of CesA complexes through the plasma membrane is thought to be driven by the force that is generated by the addition of UDP-glucose molecules to cellulose microfibrils 43 . Although cortical microtubules do not provide the force for CesA complex motility per se, CesA complexes are preferentially inserted into the plasma membrane at locations where cortical microtubules reside and since cortical microtubules are attached to the plasma membrane, they template the motility direction of CesA complexes and thus of cellulose microfibril deposition [38][39][40] . Cells are able to control the orientation in which cellulose is deposited 38 , but are also able to modify the orientation of 1 the cortical microtubules, and thus of cellulose deposition and cell growth, in response to environmental cues, such as light 44 .…”

“…The patterning of cortical microtubules is important, since the cortical microtubules control the direction of cellulose microfibril deposition [38][39][40][41] . During cell wall deposition cellulose synthase (CesA) complexes move through the plasma membrane depositing cellulose microfibrils 42 .…”

“…The plant cell wall consists of a matrix of polysaccharides, with crystalline cellulose microfibrils as the load-bearing component 2 . Like in primary (expanding) cell walls, cortical microtubules recruit cellulose synthase complexes to the plasma membrane 39,40,52 that synthesize the cellulose microfibrils which are incorporated in the existing cell wall matrix 42 . Cortical microtubule arrays in developing xylem cells resemble the secondary cell wall patterns 52,78 .…”

“…During growth, the microtubule array is dictating the deposition of the primary cell walls, in particular of the biopolymer cellulose, into evenly dispersed layers. Cellulose is synthesised by large membrane-spanning cellulose synthase (CesA) complexes 42 , which are inserted in close proximity to, and move along cortical microtubules [38][39][40]52 . The cortical microtubule array thus provides a local bias for where cellulose deposition is required.…”