Anaphase-staged chromosomes from the ninth generation of telomerase-deficient Arabidopsis. Two anaphase bridges are shown here. Credit: Photo courtesy of Karel Riha, Texas A&M University, USA.

Plant genomes betray a past characterized by vast chromosomal rearrangements and changes in ploidy, often caused by the union of genomes of different plant varieties. In their recent report, Riha and colleagues uncover further evidence of the plasticity and resilience of plants towards genomic changes by showing that Arabidopsis can better withstand the erosion of telomeres — the chromosome ends — than animals can.

Chromosomes need to protect themselves from the wear and tear that results from the inefficient replication of their ends. As a protective measure, both ends of eukaryotic chromosomes are capped by a nucleoprotein complex — the telomere. These ends are replicated by a reverse transcription mechanism catalysed by the enzyme telomerase. Without telomerase, telomeres gradually shorten until cells, sensing an emergency, activate DNA checkpoints that lead to cell-cycle arrest, senescence and apoptosis.

In this study, the fate of four lines of telomerase-deficient Arabidopsis plants was examined over ten generations. Physiologically, the mutant plants appeared normal until generation 5 (G5), after which their condition gradually worsened. The first defects were seen in vegetative structures such as leaves, whereas later-generation phenotypes affected the reproductive organs. Unexpectedly, although these plants are sterile, their vegetative shoot meristems (from which gametes derive) expand into an amorphous mass of dedifferentiated cells. This growth is unusual for a phenotype that is normally characterized by cell-cycle arrest and death, but is consistent with the increased tumour incidence seen in telomerase-deficient mice.

At the molecular level, genomes are destabilized by the absence of telomerase — a phenomenon that can be gauged in plants by the number of end-to-end fusions that occur between the shortened chromosomes, and from the chromosome bridges that form during anaphase. These bridges were apparent in plants from G5 onwards, although anaphase was not delayed as a result. Chromosome ends were clearly beginning to erode in early-generation plants, but surprisingly, some telomeres became longer from one generation to the next. This indicates that the plants might be able to engage telomerase-independent mechanisms for lengthening the telomeres. The fate of telomerase-deficient mice is very different: their fertility and development decline over several generations until the mice become sterile by the sixth generation. At this stage, cells have ceased cycling in the face of total genomic catastrophe.

Although metazoans wouldn't swap their dynamic lives for one rooted in the ground, the genome organization of plants and their response to genomic stresses might teach us a thing or two about telomeres and genome stability.