Perennials have evolved a greater resistance to exogenous H2O2 than annuals, consistent with the oxidative stress theory of aging

Zakhary, Abraam; Nagarajan, Aashika; Ngô, Charlotte; Saidajan, Marwa; Babbar, Supreet; Brown, Jason C. L.

doi:10.1007/s11756-022-01055-1

Cited by 5 publications

(6 citation statements)

References 90 publications

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“…Overall, we suggest that annuals, which are derived from perennials, both within flax specifically (Brown et al 2012) and within flowering plants generally (Zakhary et al 2022), have reduced their baseline oxidative stress tolerance to its minimal level such that no further reduction can occur, even when early flowering shortens lifespan to a greater degree, Alternatively, since the early-flowering flax populations used in this study were only established 30 years ago (Fieldes 1994), perhaps there has been an insufficient number of generations to permit these populations to physiologically adapt in response to this phenological shift. Future studies examining the relationship between flowering time and oxidative stress tolerance in annuals could be conducted using species that exhibit natural geographic variation in flowering time (e.g., Chamaecrista fasciculata; Wadgymar et al 2015).…”

Section: Early-flowering Flax Populations Were Not Less Tolerant Of O...supporting

confidence: 49%

Oxidative stress tolerance and salicylic acid levels in early-flowering populations derived from two cultivars of annual flax (Linum usitatissimum L.)

Santacroce,

Kothari,

Wang

et al. 2024

Preprint

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Based on the Oxidative Stress Theory of Aging, long-lived organisms should exhibit greater oxidative stress tolerance than short-lived organisms. For annual plants, such as flax (Linum usitatissimum L.), there is a positive correlation between flowering time and lifespan; therefore, we investigated whether early-flowering populations of two flax cultivars (Royal [R] and Stormont Cirrus [L]) exhibited lower oxidative stress tolerance than their normal-flowering controls, in the presence and absence of exogenous oxidative stress. Oxidative stress tolerance was assessed via mitochondrial uncoupling, catalase activity, and peroxide-induced cell membrane damage. We also investigated whether early-flowering flax populations exhibited different endogenous salicylic acid (SA) levels than their normal-flowering controls since SA is known to regulate both oxidative stress response and flowering time. We found no differences except that mitochondrial uncoupling was lower in early-flowering populations from the L (but not R) cultivar compared to normal-flowering controls. Perhaps L. usitatissimum has already evolved such a low oxidative stress tolerance that it cannot be further reduced in early-flowering populations. Unexpectedly, we observed that the two cultivars exhibited different responses to exogenous oxidative stress. Catalase activity was higher in response to exogenous oxidative stress in the L (but not R) cultivar, whereas peroxide-induced cell membrane damage was higher in the R (but not L) cultivar. SA may play some role in these cultivar-specific responses. As the R and L cultivars has been selected for their seed oil and fibres, respectively, the differential response of these cultivars may reflect trade-offs between oxidative stress tolerance and trait selection.

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Section: Early-flowering Flax Populations Were Not Less Tolerant Of O...supporting

confidence: 49%

Oxidative stress tolerance and salicylic acid levels in early-flowering populations derived from two cultivars of annual flax (Linum usitatissimum L.)

Santacroce,

Kothari,

Wang

et al. 2024

Preprint

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“…Alternatively, we consider that previous work in our laboratory (Zakhary et al 2022) has shown that leaves from several perennial species, including deciduous perennials, were better protected from exogenous H2O2 (at the same concentration used in the present study) in terms of membrane damage and consequent cellular electrolyte leakage. As reviewed by Pamploma et al (2006), several studies in animals have shown an inverse relationship between membrane polyunsaturated fatty acid (PUFA) content and lifespan, reflecting that PUFAs are highly susceptible to ROS attack.…”

Section: Discussionmentioning

confidence: 84%

“…While it seems plausible that H2O2 (or its free radical derivatives) can react with chlorophyll directly, thereby causing its degradation, we are unaware of any published studies that have detailed this reaction. In a previous study (Zakhary et al 2022), we exposed chlorophyll extracts directly to H2O2 and observed that it caused chlorophyll degradation, especially for chlorophyll b; therefore, a direct reaction between H2O2 and chlorophyll is a likely mechanism. Alternatively, it has been shown that light-harvesting proteins (LHPs) can be degraded by ROS (Zolla and Rinalducci 2002), and that oxidative stress can induce protein loss from chloroplasts (Kwon et al 2013), so H2O2 exposure in vivo may cause chlorophyll degradation indirectly by separating chlorophyll from the LHPs, increasing its susceptibility to intracellular degradation.…”

Section: Discussionmentioning

confidence: 93%

Degradation and repair/resynthesis rates of chlorophyll in response to oxidative stress and complete darkness differ between annual and perennial flax

Nisbett,

Alokozai,

et al. 2023

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Among plants, there is considerable variation in maximum lifespan, with annuals living less than one year and perennials living up to 43 600 years. This lifespan variation may reflect differential investment of limited energy resources, with perennials investing more energy into biomolecular damage prevention and/or repair than annuals in order to ensure their persistence over multiple seasons. The present study evaluated this prediction using chlorophyll from annual and perennial flax (Linum L.). We investigated the degradation and repair/resynthesis rates of chlorophyll in response to two different stressors: oxidative stress and complete darkness. Chlorophyll levels were measured using two different techniques: image colour analysis and spectrophotometry. While chlorophyll degradation rates in response to oxidative stress did not differ between annuals and perennials, chlorophyll repair rates following such exposure were significantly higher in perennials, for both chlorophyll a and b, consistent with our predictions. When plants were subjected to complete darkness, chlorophyll degradation rates were significantly lower in perennials than annuals, as predicted; however, when plants were subsequently reintroduced to natural photoperiod, chlorophyll resynthesis rates did not consistently differ between annuals and perennials, though they tended to be higher in the latter, as expected. Overall, our study illuminates that evolutionary transitions between life history strategies in plants have been accompanied by some physiological modifications to chlorophyll dynamics that permit perennial species to better maintain chlorophyll levels in the face of exogenous stressors, which may contribute to their increased longevity.

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“…On this basis, it is possible that the high concentration of exogenous H2O2 used in this study overwhelmed the antioxidant defences of the plants-even the bolstered antioxidant defences of perennials-leading to widespread damage in both annuals and perennials. Indeed, previous work in our laboratory (Zakhary et al 2022) has shown that leaves from several perennial species, including deciduous perennials, were better protected from exogenous H2O2 in terms of cell death, so the fact that they were not better protected from H2O2 in terms of chlorophyll degradation is intriguing. Perhaps the greater resistance to cell death observed in H2O2-treated leaves in our previous study, where the same H2O2 concentration was used (30mM), was due to enhanced resistance to oxidative stress by cell membranes, which would preserve membrane integrity, the loss of which is a hallmark characteristic of necrotic cell death (van Doorn et al 2011), rather than increased antioxidant levels.…”

Section: Discussionmentioning

confidence: 95%

“…It is also noteworthy that chlorophyll b exhibited a significantly higher repair rate than chlorophyll a, especially in perennials. Our previous work (Zakhary et al 2022) has shown that chlorophyll b is more susceptible to H2O2-induced damage, so it makes sense that the capacity to resynthesize this version of chlorophyll should be prioritized. It is known that chlorophyll b is synthesized from the oxidation of a methyl group within chlorophyll a, a process which involves the enzyme chlorophyll a oxygenase (Tanaka et al 1998), so differences in the activity and/or expression of this enzyme may be a key factor that distinguishes annuals from perennials in terms of their lifespan.…”

Section: Discussionmentioning

confidence: 99%

Antioxidant and chlorophyll dynamics differ between perennial flax (Linum perenne and Linum lewisii) and annual flax (Linum usitatissimum and Linum grandiflorum).

Nisbett

Alokozai

Elias

et al. 2022

Preprint

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Among plants, there is considerable variation in maximum lifespan, with annual species living less than one year and perennial species living as long as 43 600 years. According to the Oxidative Stress Theory of Aging, the maximum lifespan of an organism is partly determined by the rate at which it accumulates oxidative damage to its biomolecules. Consequently, perennial species have likely evolved mechanisms to slow down the accumulation of biomolecular oxidative damage relative to annual species. The present study aimed to evaluate this prediction using annual and perennial flax ( Linum ). While there are several mechanisms by which the accumulation of oxidative damage to biomolecules can be reduced, we focused on the role of antioxidants and biomolecular damage repair. Epicotyl growth and leaf production of annual—but not perennial—species were significantly affected by supplementation with exogenous ascorbic acid or glutathione, suggesting that annuals may have lower levels of endogenous antioxidants than perennials. Furthermore, while rates of chlorophyll degradation in response to exogenous H 2 O 2 did not differ between annual and perennial species, rates of chlorophyll resynthesis following such exposure were 2-fold faster in perennial species, whether assessed via image colour or spectrophotometric analysis, reflecting their greater capacity to repair oxidative damage to chlorophyll compared to annuals. Similarly, when plants were exposed to complete darkness for several days, chlorophyll degradation rates were significantly lower in perennials than annuals, perhaps because annuals quickly redistributed resources from leaves to flowers. When subsequently reintroduced to natural light cycles, chlorophyll resynthesis occurred 2-fold more quickly in perennials than annuals. Overall, our study illuminates that the evolutionary transitions between life history strategies in plants have been accompanied by physiological modifications to antioxidant and chlorophyll dynamics that reflect the need for perennial species to delay the aging process in order to survive for multiple growing seasons.

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Perennials have evolved a greater resistance to exogenous H2O2 than annuals, consistent with the oxidative stress theory of aging

Cited by 5 publications

References 90 publications

Oxidative stress tolerance and salicylic acid levels in early-flowering populations derived from two cultivars of annual flax (Linum usitatissimum L.)

Oxidative stress tolerance and salicylic acid levels in early-flowering populations derived from two cultivars of annual flax (Linum usitatissimum L.)

Degradation and repair/resynthesis rates of chlorophyll in response to oxidative stress and complete darkness differ between annual and perennial flax

Antioxidant and chlorophyll dynamics differ between perennial flax (Linum perenne and Linum lewisii) and annual flax (Linum usitatissimum and Linum grandiflorum).

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