- Email: [email protected]
Senescence: Is It Universal or Not?
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Opinion
Senescence: Is It Universal or Not? Sergi Munné-Bosch* Both demographic and physiological senescence have been demonstrated to occur in various organisms. However, indeterminate growers, such as some animals and most perennial plants, seem to escape the wear and tear of aging. Indeed, most angiosperms show no signs of senescence, and both negligible and negative senescence (improved physiological performance with aging) have been reported in perennial plants growing in their natural habitat. In this [5_TD$IF]opinion [6_TD$IF]article, I review recent developments in the study of senescence in perennial plants and propose that continuous growth prevents senescence. I also address the question whether senescence is a universal process. Aging Because we experience the wear and tear of aging firsthand in our own bodies and in the people closest to us, it is generally assumed that senescence is one of the most common processes in the entire spectrum of life. This is simply not true. It has recently been found that humans, at least modern ones, are outliers in age-related patterns of growth, reproduction, and mortality (pace of mortality, see Glossary) in the tree of life [1]. By comparing standardized patterns over age for 11 mammals, 12 non-mammalian vertebrates, 10 invertebrates, 12 vascular plants, and a green alga, the great variation in aging patterns between species was demonstrated. This diversity includes increasing, constant, and decreasing mortality with aging, for both long- and short-lived species. From this analysis of these diverse species, those species with indeterminate growth exhibit aging patterns that are fundamentally different from those of species with determinate growth; the 12 species of higher plants included in the study showed negligible or negative senescence [1]. By analyzing age-specific trajectories from 290 angiosperm species from the COMPADRE plant matrix database [2], including plants of various growth forms distributed globally, it was also recently found that most angiosperms (93%) show no senescence [3]. By using databases of functional traits with empirical matrix population models for 222 species, strong relationships between functional traits and plant life-histories have been observed. Species with large seeds, long-lived leaves, or dense wood have slow life-histories; compared to fast life-history species featuring small seeds, short-lived leaves, or soft wood [4]. As a result of these recent studies, renewed interest in the mechanisms underlying senescence has emerged. Currently, the universality of senescence is questioned and it is clear that we humans could benefit from studying aging in non-senescing, long-lived species, so that new approaches to extending our own lifespan can be devised. I review recent developments in the study of senescence in perennial plants, and I propose the hypothesis that continuous growth is an important mechanism that perennial plants use to prevent (or at least considerably delay) senescence. In addition, the limitations of senescence studies in perennial plants will be discussed to illustrate the complexity of studying senescence in long-lived species.
Trends Recent demographic studies show that senescence is not universal. Indeed, several species, including perennial plants, show negligible or even negative senescence, meaning improved survival and/or reproductive capacity with aging. Perennial plants are an excellent model for studying the non-universality of senescence because they pose the threat of immortality, or at least make it difficult to demonstrate any hint of senescence at the individual organism level in the wild. Recent studies using both demographic and physiological approaches, although limited in the number of species and age ranges sampled, suggest that senescence is not a major factor triggering mortality in perennial plants in the wild. Both longitudinal and cross-sectional approaches in the study of senescence have important limitations for our current knowledge in this field that could be overcome by joined efforts from ecologists and physiologists.
Perennial Plants as Indeterminate Growers
Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, 08028 Barcelona, Spain
Both demographic and physiological senescence have been demonstrated to occur in several organisms, including humans. However, indeterminate growers, including some animals and most higher plants, seem to escape the wear and tear of aging (Box 1). This is partly due to
*Correspondence: [email protected] (S. Munné-Bosch)
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http://dx.doi.org/10.1016/j.tplants.2015.07.009 © 2015 Elsevier Ltd. All rights reserved.
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Box 1. Indeterminate Growers and Senescence
Glossary
Indeterminate growers, including perennial plants, pose the threat of immortality. In the animal kingdom, indeterminate growers include basal metazoan groups such as ctenophores (comb jellies), sponges, placozoans, cnidarians (hydras, jellyfish, corals, and sea anemones), and myxozoans (Figure I). Basal metazoans typically have many pluripotent stem cells that are capable of differentiating into all types of cells in the body, providing these animals with a considerable capacity to regenerate their bodies, and in some cases potentially leading to immortality [47,48]. Perennial plants share the following physiological features with indeterminate growers in the animal kingdom:
Demographic senescence: increased mortality with aging (syn. senescence, but specific for populations). Lifespan: duration of life. Maximum potential lifespan: highest age attained by an individual (refers to species). Monocarpic: plants that reproduce only once in their life cycle (annuals or biennials). Negative senescence: mortality decreases with aging. Negligible senescence: mortality remains constant with aging. Pace of mortality: speed at which life proceeds (it can be measured by life expectancy). Physiological senescence: physiological deterioration with aging. Polycarpic: plants that reproduce at least twice in their life cycle (perennials). Reproductive senescence: reproductive capacity decreases with aging. Shape of mortality: whether mortality increases (‘senescence’), decreases (‘negative senescence’), or remains constant over age (‘negligible senescence’).
Stem cells: stem cells maintain viability during the entire lifespan of the organism. In perennial plants, part of the meristems (stem cells in plants) is not determined at reproduction, allowing continuous vegetative growth. Reiteration capacity: stem cells are capable of producing new structures at any time. Extreme examples can be observed in some trees, such as holm oaks, in which reiteration of new branches allows the survival of extremely damaged individuals. Potential immortality: the capacity to produce new organs at any time makes these individuals potentially immortal.
Yellow tube sponge (Aplysina aerophoba)
Mediterranean sea-finger (Alcyonium acaule)
Holm oak (Quercus ilex)
Figure I. Examples of Indeterminate Growers. These include a sponge, a coral, and a perennial plant, with the plant showing an extraordinary reiteration capacity after the trunk was cut.
the capacity of these species to grow indefinitely. Similarly to sponges, corals, and other invertebrates, growth in perennial plants is based on a form of clonal growth. In perennial plants, the genet (the organism) is made of a colony of ramets (growth units) that are the result of the activity of meristems. This is true not only aboveground, but also belowground. Provided that the aboveground and belowground parts of a perennial plant (either a tree, a shrub, or a perennial herb) are efficiently interconnected, and each part has at least one vegetative meristem alive, the individual can continue to grow. Extremes of the great capacity of perennial plants to survive can be observed in nature. When a tree is severely damaged by cutting the trunk, for example, regrowth and sprouting are still possible owing to the ability of meristems to produce new ramets (Box 1). This is also observed in so-called moribund trees, in which accidental damage to the main trunk causes a loss of apical dominance, and new ramets are formed as a result of epicormic branch formation in the base of the trunk, as usually occurs in beech stands [5–7]. Apart from the great capacity of perennial plants for regrowth, undamaged trees, shrubs and perennial plants also have a tremendous capacity for continued growth throughout their lives. By performing a global analysis of 403 tropical and temperate tree species, it was shown that, for most species, tree carbon accumulation increases steadily with tree size [8]. Thus, large, old trees do not act simply as senescent carbon reservoirs, but actively fix large amounts of carbon comparable to those fixed by smaller trees. The apparent paradox of individual tree growth increasing with tree size, despite declining leaf-level productivity, can be explained by increases in the total leaf area of a tree that outpace the decline in productivity per unit of leaf area, among other factors [8].
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Possible confusing terms found in the literature: Chronological age/aging: measure of time (redundant). Evolution of aging: refers to ‘evolution of senescence’ (nonsense). Physiological age/aging: a measure of ‘physiological time’ (nonsense, should be replaced by ‘physiological senescence’). Programmed senescence: refers to senescence (might be redundant, for instance when referring to monocarpic senescence).
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Continuous Growth May Prevent Senescence Senescence cannot occur while growth actively continues. This holds true not only for cells, tissues, and organs, but also for entire organisms. Growth prevents senescence, as has been shown, for instance, for the well-known anti-senescence effects of the growth-promoting hormones, cytokinins in cells or leaves, and consequently in monocarpic plants. As far as meristems keep intact their capacity for growth, and their production of new ramets compensates for the loss of others, perennial plants can grow indefinitely, and senescence at the organism level cannot occur. Therefore, continuous growth at the organism level is an efficient means to prevent senescence (Figure 1). When equilibrium between the formation of new ramets and the loss of others (either by senescence or biotic/abiotic stresses) is approached, the genet as a whole reaches an equilibrium, and negligible senescence occurs at old ages. When formation of new ramets is faster than the loss of others, or plant structure is based on the production of a single aboveground structure that is renewed with more vigor every year, as happens in some perennial herbs, then negative senescence can occur. Indeed, negligible and negative senescence has been reported to occur in most perennial plants examined thus far (Table 1). Growth form, size, and environmental conditions interact with the pace and shape of aging (shape of mortality), and therefore have a tremendous effect on the control of senescence. Among perennial herbs, senescence has been shown to occur in white campion (Silene latifolia) [9] and ribwort plantain (Plantago lanceolata) [10–12], but not in the long-lived herb, borderea (Borderea
Aging
(A) Senescence
Negligible senescence
Negave senescence
Growth
Age Rejuvenaon by stem cells
(B) Mature organisms with large body size
New structures and/or repair of damaged structures
The capacity for growth is extended over me
Senescence is prevented as long as the organism can maintain homeostasis
Figure 1. Continuous Growth Prevents Senescence. (A) Senescence cannot occur during active periods of growth, therefore patterns of negligible or even negative senescence are observed. (B) Rejuvenation by stem cells (meristems) plays a key role in preventing senescence in perennial plants.
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Table 1. Studies of Senescence in Perennial Plants in the Past 5 Years Species
Clonal (C) vs [3_TD$IF]Non-[4_TD$IF]Clonal (NC)
Approach
Result
Relevance
Limitations
Refs
Silene latifolia
NC
Demographic/ longitudinal
Senescence
Quantitative genetic approach
Plants were stressed by resource limitation within their pots, rendering an otherwise polycarpic plant effectively monocarpic
[9]
Plantago lanceolata
NC
Demographic/ longitudinal
Senescence
Long-term study (10 years) with more than 8000 individuals sampled, including multiple cohorts; `reverse age analysis
A high proportion of individuals reproduce only once in their lifetime in their natural habitat
[10–12]
Prenanthes roanensis
C
Demographic/ cross-sectional
Negative senescence
Central and edge populations included
Size- (not age-) related changes; difficult to distinguish between ramet and genet effects
[49]
Borderea pyrenaica
NC
Demographic and physiological/ cross-sectional
Negative senescence
Longest-lived perennial herb (maximum potential lifespan of 350 years); studies include analysis of the perennial organ
Very old individuals not measured
[13–15]
NC
Physiological/ cross-sectional
Negligible senescence
Comparison of natural and garden populations; seed viability tests
Limited sampling size
[19]
Populus tremuloides
C
Physiological/ cross-sectional
Senescence
Viability analysis in pollen grains
Analysis of ramets, not genets; no information available on females of this dioecious tree
[20]
Pinus sylvestris
NC
Physiological/ cross-sectional
Negligible senescence
Specific analysis of meristem senescence by grafting procedures
Meristems of very old individuals not included
[21]
Herbs
Shrubs Cistus albidus
Trees
Database analysis including herbs, shrubs, and trees 290 species
NC
Demographic/ cross-sectional
Negligible or negative senescence in 93% of cases
Large datasets
Limited sample size for oldest individuals
[3]
36 species
NC
Demographic/ cross-sectional
Negative senescence
Large datasets
Limited sample size for oldest individuals
[50]
14 species
NC
Demographic/ cross-sectional
Negligible or negative senescence
Large datasets
Limited sample size `for oldest individuals
[1]
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pyrenaica) [13–15]. By using a quantitative genetic approach, it was found that the short-lived white campion shows an age-related decline in inflorescence production [9]. Other studies using ribwort plantain have shown that mortality risk increases with age, but only during periods of stress in natural populations [10–12,16]. In nature, this species is very short lived, and a significant proportion of individuals only reproduce once in their lifetimes [17]. The number of reproductive years per plant varies, but 1–2 years are most common (indeed, 46.7% of the population reproduced only once). The probability of flowering at least once before death was determined strongly by environmentally influenced variables, including early-life size, cohort, and block; but also varied with several interactions involving paternal lineage [16,17]. It appears therefore that both white campion and ribwort plantain show symptoms of senescence at the organism level, but it should be kept in mind that both species are very short-lived in nature and, indeed, many individuals in natural populations of these species behave as monocarpic rather than polycarpic. This is conceptually similar to what happens in other short-lived species, in which perenniality is strongly influenced not only by the environment but also by the genotype, such as those of the genus Urtica, in which some congeners are monocarpic (e.g., the annual nettle: U. urens), while others are polycarpic (e.g., the stinging nettle: U. dioica), but with monocarpic ramets [18]. At the other extreme of lifespans among herbs, borderea can live for centuries with no signs of either demographic or physiological senescence [13–15]. This is one of the very few examples in which physiological and demographic senescence have been studied in the same plant species; although demographic and physiological studies were not performed simultaneously (Box 2 summarizes the limitations of studies of senescence). In this case of extreme longevity for a perennial herb, greatly reduced growth rates and the alternative use of belowground meristems are considered to hold the secret to long life [15]. Other recent studies using woody perennials support the contention that perennial plants can escape senescence (or at least achieve long life) in the wild by growing very slowly and keeping meristems alive to old ages [19– 21].
Physiological Deterioration with Aging In humans, it is well known that parental age has a strong influence on mutations transmitted to progeny. Meiotic non-disjunction is known to increase in older mothers and base substitutions tend to increase with increasing paternal age. Hence, it is clear that germinal mutation rates are a function of both maternal and paternal age in humans [22,23]. Using a set of mutation detector lines, it has also recently been found that, in the annual, short-lived plant Arabidopsis thaliana, the reproductive age of the parents has a significant influence on the type and rate of somatic mutations in the progeny [24]. While no significant effect of parental age on base substitutions was found, frameshift mutations and transposition events increased in the progeny of older parents, an effect that was found to be stronger through the maternal line. Viability analysis of pollen grains has also shown an age-related decline in the germline in quaking aspen (Populus tremuloides) [20]. The fact that this species is clonal, however, limits the biological significance of results in terms of senescence to the organism level because ramet and genet effects can be confounded, as occurs in other studies of senescence (Table 1). Viability analysis of seeds in white-leaved rockrose (Cistus albidus) revealed symptoms of senescence in large plants grown under near-optimal conditions, but no signs of physiological deterioration with aging in small, older plants grown in their natural habitat [19]. Classic studies have shown correlative control of senescence by reproduction in monocarpic plants and in the ramets of perennial plants, the performance of a ramet being physiologically governed at the organism level [25,26]. Taken together, these studies show that monocarpic plants and the ramets of perennial plants show reproductive senescence, but that perennial plants, such as trees, can largely increase their lifespans by establishing an interconnected colony of ramets in an integrated way. Note that, for instance, the lifespans of leaves, ramets, and the entire organism can vary by many orders of magnitude in a tree.
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Box 2. Some Limitations in the Study of Senescence Approaches Used in the Study of Senescence Longitudinal Studies The researcher follows the same individuals for a given amount of time, for a minimum of 2 years. Long-term studies are very useful to follow the demography or physiology of a given population or even, in some cases, several populations from the same species, giving very robust data. Such studies are limited by the costs connected with field trips and analyses in the laboratory, especially when physiological studies are included. The main limitation is, however, that changes in climatic conditions can mask effects of aging. Cross-sectional Studies The researcher follows individuals from different ages at a given timepoint (or at multiple timepoints). Long-term studies with various timepoints during different seasons and even years, and including demographic and physiological studies, generate very useful and robust data. Such studies are limited by the possibility to (non-destructively) estimate the age of individuals as well as by costs of testing a sufficiently large number of individuals in various conditions. This approach has the advantage of measuring all individuals under the same climatic conditions but is also limited by the fact that the sampled individuals have different early-life experiences (and therefore exposure to different climatic conditions in the long term) inherent to their different age. Demographic versus Physiological Studies Demographic and physiological studies are rarely combined in studies of senescence in plants, which limits answering a key question: is demographic senescence associated with physiological senescence? Concerted efforts by ecologists and physiologists will be necessary to better characterize the universality of senescence (Figure I)
Joint efforts
Ecological approaches
Physiological approaches
More insight and beer models
Beer understanding of the universality of senescence
New approaches to prevenng senescence
Figure I. Combined Efforts by Ecologists and Physiologists Should Provide New Insights into the Universality if Senescence and Identify New Approaches for its Prevention.
In humans, life expectancy and maximum potential lifespan have also increased greatly from hunter-gatherers to today [27]. What do long-lived trees and modern human societies have in common? A long-lived tree resembles a modern society in that both increase their maximum potential lifespan by cooperation between the sectors that integrate the whole. Very long life in some sectors in trees is attained thanks to societal organization. Sectors are formed of a colony of interconnected above and belowground ramets in a tree. It has been shown that large stature is associated with size-related hydraulic and mechanical failure, increased reproductive costs, and photosynthetic decline in large trees [28–32]. Sectoriality has been proposed as a main factor in reducing hydraulic limitations as trees age [33]; it is therefore suggested that sectoriality may play a major role in extending the lifespan of perennial plants. Global change may have an impact on patterns of mortality, and longevity may in turn play a role in forest responses to global change. By using an analysis of the evolution of the biomass dynamics of the Amazon rainforest over three decades, based on a distributed network of 321 plots, a long-term decreasing trend in carbon accumulation has recently been found [34]. Rates of net increase in aboveground biomass declined by one-third in the past decade compared to
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the 1990s. This is a consequence of growth rate increases leveling-off recently; while biomass mortality persistently increased throughout, leading to a shortening of carbon residence times. Potential drivers of the mortality increase include greater climate variability and feedback from faster growth on mortality, resulting in shortened tree longevity. Carbon dioxide fertilization effects in forests can therefore be offset by reduced tree longevity [35]. Recent increases in tree mortality rates across the western USA are correlated with global change effects, particularly increased drought [36]. Apart from extrinsic factors that might explain increased mortality over time, it has been suggested that the increased productivity may have accelerated tree [7_TD$IF]lifecycles such that trees now die younger. Faster growth exposes trees to size-related risks earlier, as evidenced by tree-ring data suggesting that faster growth shortens lifespans [37]. More detailed knowledge of the environment and physiology, and of their interaction, is therefore necessary before reasonable predictions can be made regarding widespread tree mortality triggered by global change, an aspect that should be considered in modeling [38].
Outstanding Questions Is senescence of long-lived perennials in the wild a physiological and observable phenomenon? Would senescence be observed in the wild if a sufficient number of old individuals could be sampled? Is there actually negligible or negative senescence in the wild, or is this merely a consequence of our limitations in studying senescence? How will global change affect aging patterns in the tree of life?
Concluding Remarks and Future Prospects Senescence is a very complex phenomenon that depends strongly on the species being studied and the organization scale used in the study. At the whole-plant level and among perennial plants, senescence does not appear to be a major factor with regard to triggering mortality in most perennial plants in the wild. The genotype will strongly determine the time-window during which an organism can grow, develop, and eventually senescence. Furthermore, if external conditions are too severe, we will have no chance to observe senescence in several species in the wild because external conditions will outpace any chances of senescence causing death. Finally, changes in environmental conditions, such as global change effects, could mask senescence in longitudinal studies, except that multiple cohorts are included in the analysis. Unfortunately, however, long-term variation in selective mortality and early-life environmental conditions can also mask the true aging patterns in cross-sectional studies of senescence, thus making the study of senescence in long-lived perennials extremely challenging. Because senescence increases the vulnerability of an organism, and ultimately leads to its death, it is apparently in contradiction to Darwin's theory of evolution [39]. After all, how could evolution favor a process that gradually increases mortality and decreases reproductive capacity? Weismann's initial hypothesis was that senescence evolved to the advantage of the species (e.g., by replacing worn-out individuals with younger ones), not the individual, a theory known as group selection [40]. Weismann suggested that senescence evolved because organisms that segregate germ and soma must invest additional resources to reproduce instead of maintaining the soma, and this renunciation of the soma results in senescence. Weismann's ideas later led to the disposable soma theory proposed by Williams and Kirkwood [41,42]. Medawar and Hamilton neglected the soma–germline distinction and instead identified the declining strength of selection as a sufficient explanation for senescence [43,44]. Over the past decade it has been suggested that, under natural conditions, extrinsic forces of mortality prevent senescence being observed in perennial plants [45] and that, although the weakening selective force plays a role, whether senescence evolves or not depends on the nature of the life-history constraints of the species [46]. It is suggested here that senescence does not appear to be a major factor with regard to triggering mortality in most perennial plants in the wild, at least partly because of the extraordinary capacity of perennial plants for continuous growth, which prevents senescence before this can be an observable phenomenon in the wild. It is not that senescence cannot potentially occur in perennial plants, but the possibility of accidental (exogenous) death increases so much with time that all individuals are swept away before it is an observable phenomenon. The longer the maximum lifespan for a plant species is, the more difficult is will be to demonstrate the occurrence of senescence in the wild. Some additional questions remain, however, unresolved (see Outstanding Questions).
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[1_TD$IF]Acknowledgments I am very grateful to Laura Siles and Marc Collell for providing the photographs of sponges and cnidarians in Box 1, Deborah A. Roach for critical reading of the manuscript, and Toffa Evans for English corrections. I am indebted to the Spanish Government (Project BFU2012-32057) and the Generalitat de Catalunya (ICREA Academia Prize) for supporting research in my laboratory.
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49. Aikens, M.L. and Roach, B.A. (2014) Population dynamics in central and edge populations of a narrowly endemic plant. Ecology 95, 1850–1860 50. Caswell, H. and Salguero-Gómez, R. (2013) Age, stage and senescence in plants. J. Ecol. 101, 585–595
Opinion
Senescence: Is It Universal or Not? Sergi Munné-Bosch* Both demographic and physiological senescence have been demonstrated to occur in various organisms. However, indeterminate growers, such as some animals and most perennial plants, seem to escape the wear and tear of aging. Indeed, most angiosperms show no signs of senescence, and both negligible and negative senescence (improved physiological performance with aging) have been reported in perennial plants growing in their natural habitat. In this [5_TD$IF]opinion [6_TD$IF]article, I review recent developments in the study of senescence in perennial plants and propose that continuous growth prevents senescence. I also address the question whether senescence is a universal process. Aging Because we experience the wear and tear of aging firsthand in our own bodies and in the people closest to us, it is generally assumed that senescence is one of the most common processes in the entire spectrum of life. This is simply not true. It has recently been found that humans, at least modern ones, are outliers in age-related patterns of growth, reproduction, and mortality (pace of mortality, see Glossary) in the tree of life [1]. By comparing standardized patterns over age for 11 mammals, 12 non-mammalian vertebrates, 10 invertebrates, 12 vascular plants, and a green alga, the great variation in aging patterns between species was demonstrated. This diversity includes increasing, constant, and decreasing mortality with aging, for both long- and short-lived species. From this analysis of these diverse species, those species with indeterminate growth exhibit aging patterns that are fundamentally different from those of species with determinate growth; the 12 species of higher plants included in the study showed negligible or negative senescence [1]. By analyzing age-specific trajectories from 290 angiosperm species from the COMPADRE plant matrix database [2], including plants of various growth forms distributed globally, it was also recently found that most angiosperms (93%) show no senescence [3]. By using databases of functional traits with empirical matrix population models for 222 species, strong relationships between functional traits and plant life-histories have been observed. Species with large seeds, long-lived leaves, or dense wood have slow life-histories; compared to fast life-history species featuring small seeds, short-lived leaves, or soft wood [4]. As a result of these recent studies, renewed interest in the mechanisms underlying senescence has emerged. Currently, the universality of senescence is questioned and it is clear that we humans could benefit from studying aging in non-senescing, long-lived species, so that new approaches to extending our own lifespan can be devised. I review recent developments in the study of senescence in perennial plants, and I propose the hypothesis that continuous growth is an important mechanism that perennial plants use to prevent (or at least considerably delay) senescence. In addition, the limitations of senescence studies in perennial plants will be discussed to illustrate the complexity of studying senescence in long-lived species.
Trends Recent demographic studies show that senescence is not universal. Indeed, several species, including perennial plants, show negligible or even negative senescence, meaning improved survival and/or reproductive capacity with aging. Perennial plants are an excellent model for studying the non-universality of senescence because they pose the threat of immortality, or at least make it difficult to demonstrate any hint of senescence at the individual organism level in the wild. Recent studies using both demographic and physiological approaches, although limited in the number of species and age ranges sampled, suggest that senescence is not a major factor triggering mortality in perennial plants in the wild. Both longitudinal and cross-sectional approaches in the study of senescence have important limitations for our current knowledge in this field that could be overcome by joined efforts from ecologists and physiologists.
Perennial Plants as Indeterminate Growers
Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, 08028 Barcelona, Spain
Both demographic and physiological senescence have been demonstrated to occur in several organisms, including humans. However, indeterminate growers, including some animals and most higher plants, seem to escape the wear and tear of aging (Box 1). This is partly due to
*Correspondence: [email protected] (S. Munné-Bosch)
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http://dx.doi.org/10.1016/j.tplants.2015.07.009 © 2015 Elsevier Ltd. All rights reserved.
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Box 1. Indeterminate Growers and Senescence
Glossary
Indeterminate growers, including perennial plants, pose the threat of immortality. In the animal kingdom, indeterminate growers include basal metazoan groups such as ctenophores (comb jellies), sponges, placozoans, cnidarians (hydras, jellyfish, corals, and sea anemones), and myxozoans (Figure I). Basal metazoans typically have many pluripotent stem cells that are capable of differentiating into all types of cells in the body, providing these animals with a considerable capacity to regenerate their bodies, and in some cases potentially leading to immortality [47,48]. Perennial plants share the following physiological features with indeterminate growers in the animal kingdom:
Demographic senescence: increased mortality with aging (syn. senescence, but specific for populations). Lifespan: duration of life. Maximum potential lifespan: highest age attained by an individual (refers to species). Monocarpic: plants that reproduce only once in their life cycle (annuals or biennials). Negative senescence: mortality decreases with aging. Negligible senescence: mortality remains constant with aging. Pace of mortality: speed at which life proceeds (it can be measured by life expectancy). Physiological senescence: physiological deterioration with aging. Polycarpic: plants that reproduce at least twice in their life cycle (perennials). Reproductive senescence: reproductive capacity decreases with aging. Shape of mortality: whether mortality increases (‘senescence’), decreases (‘negative senescence’), or remains constant over age (‘negligible senescence’).
Stem cells: stem cells maintain viability during the entire lifespan of the organism. In perennial plants, part of the meristems (stem cells in plants) is not determined at reproduction, allowing continuous vegetative growth. Reiteration capacity: stem cells are capable of producing new structures at any time. Extreme examples can be observed in some trees, such as holm oaks, in which reiteration of new branches allows the survival of extremely damaged individuals. Potential immortality: the capacity to produce new organs at any time makes these individuals potentially immortal.
Yellow tube sponge (Aplysina aerophoba)
Mediterranean sea-finger (Alcyonium acaule)
Holm oak (Quercus ilex)
Figure I. Examples of Indeterminate Growers. These include a sponge, a coral, and a perennial plant, with the plant showing an extraordinary reiteration capacity after the trunk was cut.
the capacity of these species to grow indefinitely. Similarly to sponges, corals, and other invertebrates, growth in perennial plants is based on a form of clonal growth. In perennial plants, the genet (the organism) is made of a colony of ramets (growth units) that are the result of the activity of meristems. This is true not only aboveground, but also belowground. Provided that the aboveground and belowground parts of a perennial plant (either a tree, a shrub, or a perennial herb) are efficiently interconnected, and each part has at least one vegetative meristem alive, the individual can continue to grow. Extremes of the great capacity of perennial plants to survive can be observed in nature. When a tree is severely damaged by cutting the trunk, for example, regrowth and sprouting are still possible owing to the ability of meristems to produce new ramets (Box 1). This is also observed in so-called moribund trees, in which accidental damage to the main trunk causes a loss of apical dominance, and new ramets are formed as a result of epicormic branch formation in the base of the trunk, as usually occurs in beech stands [5–7]. Apart from the great capacity of perennial plants for regrowth, undamaged trees, shrubs and perennial plants also have a tremendous capacity for continued growth throughout their lives. By performing a global analysis of 403 tropical and temperate tree species, it was shown that, for most species, tree carbon accumulation increases steadily with tree size [8]. Thus, large, old trees do not act simply as senescent carbon reservoirs, but actively fix large amounts of carbon comparable to those fixed by smaller trees. The apparent paradox of individual tree growth increasing with tree size, despite declining leaf-level productivity, can be explained by increases in the total leaf area of a tree that outpace the decline in productivity per unit of leaf area, among other factors [8].
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Possible confusing terms found in the literature: Chronological age/aging: measure of time (redundant). Evolution of aging: refers to ‘evolution of senescence’ (nonsense). Physiological age/aging: a measure of ‘physiological time’ (nonsense, should be replaced by ‘physiological senescence’). Programmed senescence: refers to senescence (might be redundant, for instance when referring to monocarpic senescence).
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Continuous Growth May Prevent Senescence Senescence cannot occur while growth actively continues. This holds true not only for cells, tissues, and organs, but also for entire organisms. Growth prevents senescence, as has been shown, for instance, for the well-known anti-senescence effects of the growth-promoting hormones, cytokinins in cells or leaves, and consequently in monocarpic plants. As far as meristems keep intact their capacity for growth, and their production of new ramets compensates for the loss of others, perennial plants can grow indefinitely, and senescence at the organism level cannot occur. Therefore, continuous growth at the organism level is an efficient means to prevent senescence (Figure 1). When equilibrium between the formation of new ramets and the loss of others (either by senescence or biotic/abiotic stresses) is approached, the genet as a whole reaches an equilibrium, and negligible senescence occurs at old ages. When formation of new ramets is faster than the loss of others, or plant structure is based on the production of a single aboveground structure that is renewed with more vigor every year, as happens in some perennial herbs, then negative senescence can occur. Indeed, negligible and negative senescence has been reported to occur in most perennial plants examined thus far (Table 1). Growth form, size, and environmental conditions interact with the pace and shape of aging (shape of mortality), and therefore have a tremendous effect on the control of senescence. Among perennial herbs, senescence has been shown to occur in white campion (Silene latifolia) [9] and ribwort plantain (Plantago lanceolata) [10–12], but not in the long-lived herb, borderea (Borderea
Aging
(A) Senescence
Negligible senescence
Negave senescence
Growth
Age Rejuvenaon by stem cells
(B) Mature organisms with large body size
New structures and/or repair of damaged structures
The capacity for growth is extended over me
Senescence is prevented as long as the organism can maintain homeostasis
Figure 1. Continuous Growth Prevents Senescence. (A) Senescence cannot occur during active periods of growth, therefore patterns of negligible or even negative senescence are observed. (B) Rejuvenation by stem cells (meristems) plays a key role in preventing senescence in perennial plants.
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Table 1. Studies of Senescence in Perennial Plants in the Past 5 Years Species
Clonal (C) vs [3_TD$IF]Non-[4_TD$IF]Clonal (NC)
Approach
Result
Relevance
Limitations
Refs
Silene latifolia
NC
Demographic/ longitudinal
Senescence
Quantitative genetic approach
Plants were stressed by resource limitation within their pots, rendering an otherwise polycarpic plant effectively monocarpic
[9]
Plantago lanceolata
NC
Demographic/ longitudinal
Senescence
Long-term study (10 years) with more than 8000 individuals sampled, including multiple cohorts; `reverse age analysis
A high proportion of individuals reproduce only once in their lifetime in their natural habitat
[10–12]
Prenanthes roanensis
C
Demographic/ cross-sectional
Negative senescence
Central and edge populations included
Size- (not age-) related changes; difficult to distinguish between ramet and genet effects
[49]
Borderea pyrenaica
NC
Demographic and physiological/ cross-sectional
Negative senescence
Longest-lived perennial herb (maximum potential lifespan of 350 years); studies include analysis of the perennial organ
Very old individuals not measured
[13–15]
NC
Physiological/ cross-sectional
Negligible senescence
Comparison of natural and garden populations; seed viability tests
Limited sampling size
[19]
Populus tremuloides
C
Physiological/ cross-sectional
Senescence
Viability analysis in pollen grains
Analysis of ramets, not genets; no information available on females of this dioecious tree
[20]
Pinus sylvestris
NC
Physiological/ cross-sectional
Negligible senescence
Specific analysis of meristem senescence by grafting procedures
Meristems of very old individuals not included
[21]
Herbs
Shrubs Cistus albidus
Trees
Database analysis including herbs, shrubs, and trees 290 species
NC
Demographic/ cross-sectional
Negligible or negative senescence in 93% of cases
Large datasets
Limited sample size for oldest individuals
[3]
36 species
NC
Demographic/ cross-sectional
Negative senescence
Large datasets
Limited sample size for oldest individuals
[50]
14 species
NC
Demographic/ cross-sectional
Negligible or negative senescence
Large datasets
Limited sample size `for oldest individuals
[1]
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pyrenaica) [13–15]. By using a quantitative genetic approach, it was found that the short-lived white campion shows an age-related decline in inflorescence production [9]. Other studies using ribwort plantain have shown that mortality risk increases with age, but only during periods of stress in natural populations [10–12,16]. In nature, this species is very short lived, and a significant proportion of individuals only reproduce once in their lifetimes [17]. The number of reproductive years per plant varies, but 1–2 years are most common (indeed, 46.7% of the population reproduced only once). The probability of flowering at least once before death was determined strongly by environmentally influenced variables, including early-life size, cohort, and block; but also varied with several interactions involving paternal lineage [16,17]. It appears therefore that both white campion and ribwort plantain show symptoms of senescence at the organism level, but it should be kept in mind that both species are very short-lived in nature and, indeed, many individuals in natural populations of these species behave as monocarpic rather than polycarpic. This is conceptually similar to what happens in other short-lived species, in which perenniality is strongly influenced not only by the environment but also by the genotype, such as those of the genus Urtica, in which some congeners are monocarpic (e.g., the annual nettle: U. urens), while others are polycarpic (e.g., the stinging nettle: U. dioica), but with monocarpic ramets [18]. At the other extreme of lifespans among herbs, borderea can live for centuries with no signs of either demographic or physiological senescence [13–15]. This is one of the very few examples in which physiological and demographic senescence have been studied in the same plant species; although demographic and physiological studies were not performed simultaneously (Box 2 summarizes the limitations of studies of senescence). In this case of extreme longevity for a perennial herb, greatly reduced growth rates and the alternative use of belowground meristems are considered to hold the secret to long life [15]. Other recent studies using woody perennials support the contention that perennial plants can escape senescence (or at least achieve long life) in the wild by growing very slowly and keeping meristems alive to old ages [19– 21].
Physiological Deterioration with Aging In humans, it is well known that parental age has a strong influence on mutations transmitted to progeny. Meiotic non-disjunction is known to increase in older mothers and base substitutions tend to increase with increasing paternal age. Hence, it is clear that germinal mutation rates are a function of both maternal and paternal age in humans [22,23]. Using a set of mutation detector lines, it has also recently been found that, in the annual, short-lived plant Arabidopsis thaliana, the reproductive age of the parents has a significant influence on the type and rate of somatic mutations in the progeny [24]. While no significant effect of parental age on base substitutions was found, frameshift mutations and transposition events increased in the progeny of older parents, an effect that was found to be stronger through the maternal line. Viability analysis of pollen grains has also shown an age-related decline in the germline in quaking aspen (Populus tremuloides) [20]. The fact that this species is clonal, however, limits the biological significance of results in terms of senescence to the organism level because ramet and genet effects can be confounded, as occurs in other studies of senescence (Table 1). Viability analysis of seeds in white-leaved rockrose (Cistus albidus) revealed symptoms of senescence in large plants grown under near-optimal conditions, but no signs of physiological deterioration with aging in small, older plants grown in their natural habitat [19]. Classic studies have shown correlative control of senescence by reproduction in monocarpic plants and in the ramets of perennial plants, the performance of a ramet being physiologically governed at the organism level [25,26]. Taken together, these studies show that monocarpic plants and the ramets of perennial plants show reproductive senescence, but that perennial plants, such as trees, can largely increase their lifespans by establishing an interconnected colony of ramets in an integrated way. Note that, for instance, the lifespans of leaves, ramets, and the entire organism can vary by many orders of magnitude in a tree.
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Box 2. Some Limitations in the Study of Senescence Approaches Used in the Study of Senescence Longitudinal Studies The researcher follows the same individuals for a given amount of time, for a minimum of 2 years. Long-term studies are very useful to follow the demography or physiology of a given population or even, in some cases, several populations from the same species, giving very robust data. Such studies are limited by the costs connected with field trips and analyses in the laboratory, especially when physiological studies are included. The main limitation is, however, that changes in climatic conditions can mask effects of aging. Cross-sectional Studies The researcher follows individuals from different ages at a given timepoint (or at multiple timepoints). Long-term studies with various timepoints during different seasons and even years, and including demographic and physiological studies, generate very useful and robust data. Such studies are limited by the possibility to (non-destructively) estimate the age of individuals as well as by costs of testing a sufficiently large number of individuals in various conditions. This approach has the advantage of measuring all individuals under the same climatic conditions but is also limited by the fact that the sampled individuals have different early-life experiences (and therefore exposure to different climatic conditions in the long term) inherent to their different age. Demographic versus Physiological Studies Demographic and physiological studies are rarely combined in studies of senescence in plants, which limits answering a key question: is demographic senescence associated with physiological senescence? Concerted efforts by ecologists and physiologists will be necessary to better characterize the universality of senescence (Figure I)
Joint efforts
Ecological approaches
Physiological approaches
More insight and beer models
Beer understanding of the universality of senescence
New approaches to prevenng senescence
Figure I. Combined Efforts by Ecologists and Physiologists Should Provide New Insights into the Universality if Senescence and Identify New Approaches for its Prevention.
In humans, life expectancy and maximum potential lifespan have also increased greatly from hunter-gatherers to today [27]. What do long-lived trees and modern human societies have in common? A long-lived tree resembles a modern society in that both increase their maximum potential lifespan by cooperation between the sectors that integrate the whole. Very long life in some sectors in trees is attained thanks to societal organization. Sectors are formed of a colony of interconnected above and belowground ramets in a tree. It has been shown that large stature is associated with size-related hydraulic and mechanical failure, increased reproductive costs, and photosynthetic decline in large trees [28–32]. Sectoriality has been proposed as a main factor in reducing hydraulic limitations as trees age [33]; it is therefore suggested that sectoriality may play a major role in extending the lifespan of perennial plants. Global change may have an impact on patterns of mortality, and longevity may in turn play a role in forest responses to global change. By using an analysis of the evolution of the biomass dynamics of the Amazon rainforest over three decades, based on a distributed network of 321 plots, a long-term decreasing trend in carbon accumulation has recently been found [34]. Rates of net increase in aboveground biomass declined by one-third in the past decade compared to
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the 1990s. This is a consequence of growth rate increases leveling-off recently; while biomass mortality persistently increased throughout, leading to a shortening of carbon residence times. Potential drivers of the mortality increase include greater climate variability and feedback from faster growth on mortality, resulting in shortened tree longevity. Carbon dioxide fertilization effects in forests can therefore be offset by reduced tree longevity [35]. Recent increases in tree mortality rates across the western USA are correlated with global change effects, particularly increased drought [36]. Apart from extrinsic factors that might explain increased mortality over time, it has been suggested that the increased productivity may have accelerated tree [7_TD$IF]lifecycles such that trees now die younger. Faster growth exposes trees to size-related risks earlier, as evidenced by tree-ring data suggesting that faster growth shortens lifespans [37]. More detailed knowledge of the environment and physiology, and of their interaction, is therefore necessary before reasonable predictions can be made regarding widespread tree mortality triggered by global change, an aspect that should be considered in modeling [38].
Outstanding Questions Is senescence of long-lived perennials in the wild a physiological and observable phenomenon? Would senescence be observed in the wild if a sufficient number of old individuals could be sampled? Is there actually negligible or negative senescence in the wild, or is this merely a consequence of our limitations in studying senescence? How will global change affect aging patterns in the tree of life?
Concluding Remarks and Future Prospects Senescence is a very complex phenomenon that depends strongly on the species being studied and the organization scale used in the study. At the whole-plant level and among perennial plants, senescence does not appear to be a major factor with regard to triggering mortality in most perennial plants in the wild. The genotype will strongly determine the time-window during which an organism can grow, develop, and eventually senescence. Furthermore, if external conditions are too severe, we will have no chance to observe senescence in several species in the wild because external conditions will outpace any chances of senescence causing death. Finally, changes in environmental conditions, such as global change effects, could mask senescence in longitudinal studies, except that multiple cohorts are included in the analysis. Unfortunately, however, long-term variation in selective mortality and early-life environmental conditions can also mask the true aging patterns in cross-sectional studies of senescence, thus making the study of senescence in long-lived perennials extremely challenging. Because senescence increases the vulnerability of an organism, and ultimately leads to its death, it is apparently in contradiction to Darwin's theory of evolution [39]. After all, how could evolution favor a process that gradually increases mortality and decreases reproductive capacity? Weismann's initial hypothesis was that senescence evolved to the advantage of the species (e.g., by replacing worn-out individuals with younger ones), not the individual, a theory known as group selection [40]. Weismann suggested that senescence evolved because organisms that segregate germ and soma must invest additional resources to reproduce instead of maintaining the soma, and this renunciation of the soma results in senescence. Weismann's ideas later led to the disposable soma theory proposed by Williams and Kirkwood [41,42]. Medawar and Hamilton neglected the soma–germline distinction and instead identified the declining strength of selection as a sufficient explanation for senescence [43,44]. Over the past decade it has been suggested that, under natural conditions, extrinsic forces of mortality prevent senescence being observed in perennial plants [45] and that, although the weakening selective force plays a role, whether senescence evolves or not depends on the nature of the life-history constraints of the species [46]. It is suggested here that senescence does not appear to be a major factor with regard to triggering mortality in most perennial plants in the wild, at least partly because of the extraordinary capacity of perennial plants for continuous growth, which prevents senescence before this can be an observable phenomenon in the wild. It is not that senescence cannot potentially occur in perennial plants, but the possibility of accidental (exogenous) death increases so much with time that all individuals are swept away before it is an observable phenomenon. The longer the maximum lifespan for a plant species is, the more difficult is will be to demonstrate the occurrence of senescence in the wild. Some additional questions remain, however, unresolved (see Outstanding Questions).
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[1_TD$IF]Acknowledgments I am very grateful to Laura Siles and Marc Collell for providing the photographs of sponges and cnidarians in Box 1, Deborah A. Roach for critical reading of the manuscript, and Toffa Evans for English corrections. I am indebted to the Spanish Government (Project BFU2012-32057) and the Generalitat de Catalunya (ICREA Academia Prize) for supporting research in my laboratory.
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49. Aikens, M.L. and Roach, B.A. (2014) Population dynamics in central and edge populations of a narrowly endemic plant. Ecology 95, 1850–1860 50. Caswell, H. and Salguero-Gómez, R. (2013) Age, stage and senescence in plants. J. Ecol. 101, 585–595