Evolutionary acquisition of a primitive light-dependent nuclear relocation in Marchantia polymorpha

Arabidopsis thaliana is known to position nuclei on the bottom wall of leaf cells, distancing genetic material from external stresses, and, in response to intense blue light, it relocates them to the side walls to escape UV-induced DNA damage. However, how this protective system evolved in land plants remains unclear. Here, we show that Chara corallina, the charophyte alga, has no light-dependent nuclear relocation and that Marchantia polymorpha, a modern relative of the earliest land plants, has a nuclear positioning system distinct from that of Arabidopsis: it positions nuclei on the upper walls of the epidermal cells of the young thalli in the dark and even in prolonged intense light. We also show that, in response to intense blue light, M. polymorpha has the ability to immediately move nuclei from the upper to the side walls in an actin filament-dependent manner similarly to Arabidopsis. However, the relocation is transient and the nuclei return to the upper walls depending on two cytoskeletal components (actin filaments and microtubules). Together, these findings suggest that light-dependent nuclear relocation was initially established in bryophytes and then diverged as land plants evolved.