Telomerase, telomeric DNA and associated proteins together represent a complex, finely tuned and functionally conserved mechanism that ensures genome integrity by protecting and maintaining chromosome ends. Changes in its components can threaten an organism's viability. Nevertheless, molecular innovation in telomere maintenance has occurred multiple times during eukaryote evolution, giving rise to species/taxa with unusual telomeric DNA sequences, telomerase components or telomerase-independent telomere maintenance. The central component of telomere maintenance machinery is telomerase RNA (TR) as it templates telomere DNA synthesis, its mutation can change telomere DNA and disrupt its recognition by telomere proteins, thereby leading to collapse of their end-protective and telomerase recruitment functions. Using a combination of bioinformatic and experimental approaches, we examine a plausible scenario of evolutionary changes in TR underlying telomere transitions. We identified plants harbouring multiple TR paralogs whose template regions could support the synthesis of diverse telomeres. In our hypothesis, formation of unusual telomeres is associated with the occurrence of TR paralogs that can accumulate mutations, and through their functional redundancy, allow for the adaptive evolution of the other telomere components. Experimental analyses of telomeres in the examined plants demonstrate evolutionary telomere transitions corresponding to TR paralogs with diverse template regions.

Centre of Plant Structural and Functional Genomics Institute of Experimental Botany of the Czech Academy of Sciences Olomouc CZ 779 00 Czech Republic

Department of Cell Biology and Radiobiology Institute of Biophysics of the Czech Academy of Sciences Brno CZ 61265 Czech Republic

Grupo de Investigación en Recursos Naturales Amazónicos GRAM Facultad de Ingenierías y Ciencias Básicas and Herbario Etnobotánico del Piedemonte Andino Amazónico Instituto Tecnológico del Putumayo ITP Mocoa Putumayo Colombia

Institut Botànic de Barcelona Passeig del Migdia S N Barcelona 08038 Catalonia Spain

Laboratory of Functional Genomics and Proteomics NCBR Faculty of Science Masaryk University Brno CZ 61137 Czech Republic

Mendel Centre for Plant Genomics and Proteomics CEITEC Masaryk University Brno CZ 62500 Czech Republic

Potato Research Institute Havlíčkův Brod Ltd Havlíčkův Brod CZ 58001 Czech Republic

School of Biological Sciences University of Portsmouth King Henry Building King Henry 1 St Portsmouth PO1 2DY UK

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Telomeres and telomerase: active but complex players in life-history decisions

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