Photo-oxidative stress markers reveal absence of physiological deterioration with ageing in Borderea pyrenaica, an extraordinarily long-lived herb

Abstract

In animals, age-associated disorders are believed to be connected to shifts in the antioxidant/pro-oxidant balance in favour of oxidative stress. However, the contribution of oxidative stress to ageing in long-lived perennials has not been explored to date. Here, we tested age- and sex-related changes in several photo-oxidative stress markers in Borderea pyrenaica, a small dioecious geophyte relict of the Tertiary with one of the longest life spans ever recorded for a non-clonal herb (more than 300 years). Given that survival increases with age in B. pyrenaica, we hypothesized that oxidative stress does not increase with ageing because the species develops improved anti-oxidant defence. In three field samplings performed during 2008, 2010 and 2011 in the Central Pyrenees (NE Spain), we examined the effects of ageing and sex on photosynthetic pigment levels, PSII integrity (Fv /Fm ratio), lipid peroxidation, and the extent of photo and anti-oxidant protection in chloroplasts. Furthermore, we explored whether age and sex affect plant response to severe natural desiccation. Both male and female plants maintained chlorophyll levels intact, as well as the Fv/Fm ratio and the levels of lipid peroxidation, irrespective of age. This finding suggests the absence of age-associated oxidative stress at the organismal level. Furthermore, photoprotection mechanisms were found to be similarly efficient in the oldest individuals as in juvenile plants, in terms of xanthophyll cycle de-epoxidation and accumulation of low-molecular-weight antioxidants (carotenoids and tocopherols). Indeed, females over 100 years of age were the most resistant to severe desiccation, maintaining higher leaf hydration levels, less chlorophyll degradation and better PSII integrity under stress than females below 100 years, males below or above 100 years, and juveniles. Synthesis. Neither males nor females of the extraordinarily long-lived B. pyrenaica show age-dependent signs of oxidative stress. This observation suggests that age-induced oxidative stress is not a universal feature of ageing in perennial plants. Indeed, females older than 100 years showed signs of negative senescence, in that they registered improved physiological performance with increasing age. Neither males nor females of the extraordinarily long-lived Borderea pyrenaica show age-dependent signs of oxidative stress. This observation suggests that age-induced oxidative stress is not a universal feature of ageing in perennial plants. Indeed, females older than 100 years showed signs of negative senescence, in that they registered improved physiological performance with increasing age. © 2013 The Authors. Journal of Ecology © 2013 British Ecological Society. [The definitive version is available at www3.interscience.wiley.com] ; We are very grateful to Toffa Evans for English corrections and Miquel Salicrú for his help in statistical analyses. The research conducted by S.M.-B's laboratory was supported through grants BFU2012-32057, BFU2009-07294 and BFU2009-06045, awarded by the Spanish Government, and an ICREA Academia award, funded by the Generalitat de Catalunya. M.B.G. was also supported by the Spanish National project CGL2010-21642 and the National Parks Project 430/211. The Regional Government of Aragón allowed this study and granted the required permissions. We thank Miguel A. Saz for supplying the climatic data recorded at the closest meteorological station to the plant population in the Ordesa and Monte Perdido National Park. We are indebted to Laia Arrom and Jana Cela for their invaluable help during sampling. ; Peer Reviewed