Pausing of Golgi Bodies on Microtubules Regulates Secretion of Cellulose Synthase Complexes in Arabidopsis  

Abstract

Plant growth and organ formation depend on the oriented deposition of load-bearing cellulose microfibrils in the cell wall. Cellulose is synthesized by plasma membrane-bound complexes containing cellulose synthase proteins (CESAs). Here, we establish a role for the cytoskeleton in intracellular trafficking of cellulose synthase complexes (CSCs) through the in vivo study of the green fluorescent protein (GFP)-CESA3 fusion protein in Arabidopsis thaliana hypocotyls. GFP-CESA3 localizes to the plasma membrane, Golgi apparatus, a compartment identified by the VHA-a1 marker, and, surprisingly, a novel microtubule-associated cellulose synthase compartment (MASC) whose formation and movement depend on the dynamic cortical microtubule array. Osmotic stress or treatment with the cellulose synthesis inhibitor CGA 325'615 induces internalization of CSCs in MASCs, mimicking the intracellular distribution of CSCs in nongrowing cells. Our results indicate that cellulose synthesis is coordinated with growth status and regulated in part through CSC internalization. We find that CSC insertion in the plasma membrane is regulated by pauses of the Golgi apparatus along cortical microtubules. Our data support a model in which cortical microtubules not only guide the trajectories of CSCs in the plasma membrane, but also regulate the insertion and internalization of CSCs, thus allowing dynamic remodeling of CSC secretion during cell expansion and differentiation.

Identification and Dynamics of Arabidopsis Adaptor Protein-2 Complex and Its Involvement in Floral Organ Development

“…Cell wall biogenesis is likely to require endocytosis because a null mutation of the dynamin-related protein DRP1A reduces cellulose synthesis, leading to impaired cell expansion in various tissues (Collings et al, 2008). A potential target of endocytosis involved in cell wall biogenesis is the cellulose synthase complex, of which internalization under stress conditions has been observed (Crowell et al, 2009). Another reason may be related to phytohormones.…”

Patterning of plant cell wall deposition by cortical microtubules

“…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 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 .…”

“…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.…”

“…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 .…”