Plants have two ways of giving directions to cell wall builders

Cellulose is the most abundant biopolymer on the planet and intimately touches all of our lives – the clothes we wear, the food we eat, the buildings we live in. It’s not just a useful thing for us though. Plant cells use specific arrangements of cellulose microfibrils (essentially tiny cables of cellulose) to keep their cells intact as they grow and to produce the wide-variety of cell shapes that build plants. Getting the arrangement of cellulose microfibrils right is therefore rather important. Plant cells have long been thought to arrange cellulose microfibrils in their cell walls through directional guidance of cellulose synthase complexes (protein complexes that make cellulose microfibrils) along microtubules close to the cell surface. It turns out however that this is not the whole story. A substantial proportion of cellulose synthase complexes move across the cell surface well away from any nearby microtubules. In their recent paper in Current Biology, Norwich-based Jordi Chan & Enrico Coen, working in Arabidopsis, build on this to propose a second mechanism for how plants control orientation of their cellulose microfibrils.

Chan & Cohen observe that about half of cellulose synthase complexes moving in microtubule-devoid areas of the cell surface (termed autonomous complexes) initially moved in a straight line but then suddenly changed direction. In about 35% of these cases, the autonomous complex turned to follow the direction of another autonomous complex that had recently passed. This indicates that autonomous complexes moving separately from microtubules can be re-orientated by the ‘trail’ left by another autonomous complex. Whatever aspect of this ‘trail’ was capable of re-orientating other autonomous complexes was clearly stable, as it could re-orient other autonomous complexes for up to 19 minutes after passing by (a long time in the scale of subcellular movements). Chan & Cohen propose that it is the cellulose microfibril recently laid by an autonomous complex that is capable of re-orientating other passing autonomous complexes. Consistent with this, treatment with a drug known to randomise cell wall architecture also increased the randomness of autonomous complex trajectories.

Plants may have two methods for organising the orientation of cellulose microfibrils in their cell wall, one using microtubules at the cell surface as a guiding mechanism and another using recently deposited cellulose microfibrils in the cell wall as a guiding mechanism. To investigate how these two mechanisms may overlap, Chan & Coen monitored what happened when autonomous complex trajectories encountered a microtubule. Interestingly, half of the autonomous complex trajectories changed direction upon encountering a microtubule and subsequently followed the direction of the microtubule. By contrast, microtubule-directed complexes were never seen to re-orientate when encountering an autonomous complex trail. Moreover, the overall alignment of newly-emerged autonomous complex trajectories was found to follow the overall direction of microtubules. Microtubule-guidance therefore seems to when guidance mechanisms collide and to control broad orientation of cellulose microfibrils.

The big question that arises from this is why do plants need two mechanisms to control their cellulose orientation, particularly if one seems to inform the other?  Well, as Chan & Cohen point out, other organisms may also have such a dual system for organising their cell walls. This has been proposed for some bacteria. If dual systems do indeed exist for organising cell wall fibre deposition in various kingdoms, then this would seem a pretty good system to rely on. Chan & Cohen speculate that ‘Having dual guidance may therefore provide a general mechanism to ensure both strong coherence and flexibility of response, allowing effective regulation of the growth and strength of cell walls’. It may be that the autonomous guidance mechanism allows for rapid amplification of changes in cellulose microfibril arrangement set out by a microtubule-guided dominant orientating mechanism. This could be particularly useful for allowing rapid responses to a need to change cell wall arrangement if microtubule transport, or changes in microtubule organisation, turn out to be rate-limiting. Given that a substantial proportion of cellulose synthase complexes have been observed in Arabidopsis well away from microtubules, this newly-described mechanism may prove to be a major contributor to supporting plant growth.