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

Abstract

Summary 1.In animals, age-associated disorders are believed to be connected to shifts in the antioxidant/prooxidant balance in favour of oxidative stress. However, the contribution of oxidative stress to ageing in long-lived perennials has not been explored to date.2. 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. 3. 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 (F v /F m 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. 4. Both male and female plants maintained chlorophyll levels intact, as well as the F v /F m ratio and the levels of lipid peroxidation, irrespective of age. This finding suggests the absence of ageassociated 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. 5. Synthesis. Neither males nor females of the extraordinarily long-lived B. pyrenaica show agedependent 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.

Adaptation of the Long-Lived Monocarpic Perennial, Saxifraga longifolia to High Altitude

“…This was not observed here in either studied population. Small sizes throughout their lifespan, as it happens in perennial herbs (García et al, 2011;Morales et al, 2013;, may protect S. longifolia plants from the potential negative effects of aging. It appears, therefore, that whole-plant senescence in this species may be attributed to reproduction and extrinsic factors, such as drought stress, but not to ageing, as only very small individuals (, 30 mm diameter) die more frequently in the two lowest populations.…”

Perennial Roots to Immortality ,

“…1). Interestingly, fecundity of this species increases with aging, representing a case of negative senescence (Garcia et al, 2011;Morales et al, 2013). If mortality falls as size increases and if size increases with age, then mortality will fall with age, and negative senescence occurs (Vaupel et al, 2004).…”

Implications of clonality for ageing research

“…The plant literature is indeed not exception to ecological examples of how propagation and modular partitioning may slow down or even reset the biological watch. The herbaceous perennial plant Borderea pyrenaica does not show any signs of physiological (Morales et al 2013) or demographic (García et al 2011) deterioration with age; in this case, the species is known to have a highly modular design in its shoot apical meristem arrangement (García et al 2011). Similarly, recently, Mencuccini et al (2013) have shown a lack of physiological decline in Scots pine (Pinus sylvestris) module performance grafted onto older genets.…”