The adaptation of plant growth to terrestrial habitats is tightly linked with the continuous evolution of the carbohydrate-rich matrix that surrounds all plant cells like a wall. The cell walls provide structure for upright growth and defense against pathogens, but they also facilitate the growth and morphogenesis of each cell. The main scaffold and load-bearing component of the walls is cellulose, which is a fibrillary sugar polymer made up by multiple, laterally aggregating 1,4 β-glucan chains. Large cellulose synthase (CESA) complexes (CSC) synthesize cellulose at the plant cell plasma membrane, where it is integrated into the cell walls in a highly regulated manner. The significance of cellulose as the Earth’s most abundantly occurring biopolymer and as a main constraint for plant growth, underpins the importance of studying cellulose synthesis. However, how the CSCs assemble and synthesize cellulose and how these mechanims evolved are hardly known. In this study, we challenged the plasticity of CESA activity, by generating thirty-two chimeric proteins, using two evolutionary distant CESAs (Arabidopsis thaliana, AtCESA6 and Marchantia polymorpha, MpCESA1) and by the attempt to adopt CSLF6-like catalytic activity, synthesizing 1,3;1,4 mixed-linkage β-glucan. By fluorescently labeling the chimeras and transiently expressing these in N. benthamiana leaves, we show that AtCESA6 tolerates bigger mutational alterations than MpCESA1 before their respective wild type behaviors are impaired. However, none of the CESAs produced altered polysaccharides. Interestingly, MpCESA1 appeared compatible with the endogenous Tobacco CSC dynamics. In this liverwort species, only two CESA paralogs are harbored in the assembled genome. Here, preliminary investigations of the Marchantia CESAs revealed that these are differentially expressed and that MpCESA1 knockdown resulted in dwarfism and developmental defects. Ubiquitously expressed fluorescence-labeled MpCESA1 in gemma tissue exhibited distinct behavior in comparison to its dynamics in N. benthamiana cells, whereas MpCESA1 activity in the rhizoids suggested a conserved mechanism across the plant kongdom for tip-growing cells. Using freeze-fracture transmission electron microscopy we could clearly discern rosette-type complexes in the rhizoid plasma membranes. We find M. polymorpha to be an excellent model system to study the synthesis mechanism and dynamics of CSCs. CESA catalytic specificity is very robust and, in this aspect, Marchantia polymorpha contitutes a promising platform for studying its evolution and flexibility.