Aging, stress, and senescence in plants: what can biological diversity teach us?

Abstract

Aging, stress, and senescence in plants are interconnected processes that determine longevity. We focus here on compiling and discussing our current knowledge on the mechanisms of development that long-lived perennial plants have evolved to prevent and delay senescence. Clonal and nonclonal perennial herbs of various life forms and longevities will be particularly considered to illustrate what biological diversity can teach us about aging as a universal phenomenon. Source–sink relations and redox signaling will also be discussed as examples of regulatory mechanisms of senescence at the organ level. Whether or not effective mechanisms that biological diversity has evolved to completely prevent the wear and tear of aging will be applicable to human aging in the near future ultimately depends on ethical aspects.

Aging, stress, and senescence in plants

Compared with our current understanding of senescence processes in monocarpic plants (i.e., plants that reproduce only once in their lifetime, such as annuals [e.g., maize, Zea mays L.] and biennials [e.g., radish, Raphanus sativus L.]), relatively little attention has been paid to age-related changes in perennials and what these long-lived organisms can teach us. Despite the fact that a comparison between aging in perennial plants and humans may at first glance seem naïve, studying biological diversity can serve as a sound basis for better understanding universal processes of aging among the tree of life. The more we better understand the universality of the aging process, there will probably exist more chances to apply current knowledge to prevent or delay human aging. Nevertheless, the study of aging in plants is very complex, and there is no consensus in general concepts related to this topic. With the aim of avoiding misunderstandings, we will first briefly introduce basic concepts related to aging. Before doing so, we should carefully consider the problem of scaling up, which makes us wonder whether cells, tissues/organs, or whole organisms really age. This is particularly interesting in the case of dioecious perennial herbs, plant species with males and females as separate individuals that produce new leaves every year and, as we will discuss later, live for several years and even a few centuries, despite their small size. As we will see later, it is surprising that small, nonclonal herbs such as Borderea pyrenaica can live up to 350 years, three times more than humans, or that several clonal perennial herbs (clonal plants are those that reproduce asexually so that the new individuals produced are identical to the mother plant, [1]) can be considered virtually immortal.

In aging research, the differentiation is essential between three interconnected biological processes: aging, stress, and senescence. The age of an organism is simply a measure of time; therefore, aging (i.e., increasing age) may not necessarily be seen as negative. Despite the fact that several species experience a physiological deterioration with aging (also known as senescence) and we as humans have all experienced the wear and tear of aging firsthand in our own bodies or in the people closest to us, aging is not always equivalent to senescence in all species. In a recent study, a great diversity in aging patterns was observed by comparing mammals, nonmammalian vertebrates, invertebrates, vascular plants, and a green alga, showing increasing, constant, and decreasing mortality with aging, for both long- and short-lived species. It was shown that 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 [2]. In another study analyzing age-specific trajectories from 290 angiosperm species (i.e., fruiting plants), including plants of various growth forms distributed globally, it was also found that most angiosperms (93%) show no senescence at the organism level [3], although it is generally well known that all plant species experience senescence at the organ and cellular level, this process being even beneficial for the organism in numerous instances [4]. More recently, it has been discussed how stress tolerance and resilience can increase the lifespan of long-lived perennials, so that perennial plants with extreme longevity maintain some growth capacity over millennia and can defy aging [5], although this does not mean trees aged thousands of years are immortal ([6]; see also [7]). Nonclonal perennial herbs do not show these extreme longevities (as compared with trees aged thousands of years) but can also live for centuries, which is surprising due to their small size. We will focus here on discussing the mechanisms of development in perennial herbs, with an emphasis on describing different life forms, its relationship with stress and longevity, the mechanisms that several perennial herbs have evolved to modulate senescence at the organ level, the importance of clonality in resetting the clock, and, finally, what all this knowledge teaches us about human aging.

Life forms, stress, and aging

Raunkiaer [8] divided plants into various groups depending on the position of perennating buds (Fig. 1). Where plants have their perennial buds—i.e., structures that contain meristematic cells—determines the species’ strategy to cope with unfavorable environmental conditions. Phanerophytes are the group on top of Raunkiaer’s classification, having their buds above 25 cm above ground—typically comprising shrubs and trees. In chamaephytes, buds are placed from the soil surface up to 25 cm above ground. In this group, we can find both perennial shrublets and herbs such as stinging nettle (Urtica dioica). Chamaephytes are believed to create a microclimate near the soil surface to avoid harsh climate [9], and they preserve their vegetative biomass throughout their life cycle. Hemicryptophytes such as ribwort plantain (Plantago lanceolata) evade extreme environmental conditions having their buds at the ground level. Finally, at the bottom of the classification, we find cryptophytes, such as B. pyrenaica, that keep their perennial buds underground (literally under rocks in this case [the so-called geophytes] or under water in other cryptophytes) and that regenerate their whole aboveground biomass every favorable season. Indeed, buds are present in very different forms depending on the plant life form [10, 11]. In the case of perennial herbs, chamaephytes conserve their aboveground biomass thanks to shoot meristems while cryptophytes resprout every season given that they “shelter” their buds, placing them on belowground organs. In this way, cryptophytes, and among them geophytes, can inhabit harsher environments, avoiding adverse environmental conditions such as freezing or scorching temperatures.

Fig. 1.

Examples of long-lived perennial herbs related to its relevance in the Raunkiaer classification. a Stinging nettle (Urtica dioica), ribwort plantain (Plantago lanceolata), and borderea (Borderea pyrenaica) as examples of a chamaephyte, a hemicryptophyte, and a cryptophyte, respectively. b Raunkiaer’s life forms of herbs. Red dots indicate the position of perennial buds

Plants display a tremendous plasticity in growth forms. Among aboveground buds (in all of them), we can find shoot apical meristems and axillary meristems which through differentiation ensure both vegetative and reproductive growth. Besides the production of reproductive structures, the activity of axillary bud meristems is particularly important for plant branching and regeneration after damage [12]. After a disturbance, for example, a very unfavorable season due to harsh environmental conditions or a fire, the shoot buds can resprout since they keep part of the buds in a dormant state. Furthermore, herbaceous plants can show a huge plasticity, even higher than that exerted by other perennials, such as shrubs and trees. Some chamaephytes can shift their life form between chamaephytes and hemicryptophytes [13]. Most of these species, such as U. dioica, have belowground buds such as rhizomes and/or stolons that enable resprouting if environmental conditions are too hard and shoot buds die. Rhizomes are underground stems that grow horizontally and produce aboveground shoots and roots, hence allowing vegetative growth of independent individuals—i.e., cloning—while stolons attain clonal growth and the formation of daughter plants through the development of procumbent stems that will develop adventitious roots [11]. On the other hand, geophytes survive unfavorable conditions thanks to the variety of belowground structures that they present, such as corms, bulbs, or tubers [11]. These structures are nonwoody swollen stems that store reserves like rhizomes and stolons, but they grow vertically instead of horizontally. There is a recent interesting approach about the evolution of belowground structures in geophytes, and it postulates that these specialized organs are rhizome-derived and that they present an advantage in more extreme landscapes [14]. This hypothesis is mainly founded in the fact that rhizomes and the other underground organs share some characteristics that ease the transition from one to the other [15]. Furthermore, clades of rhizomatous species are tightly related to clades with a high diversity of belowground structures [16]. This theory is extensively based on the phylogenetic study of Givnish et al. [15] with monocots, and even though there are some studies that might lead to the same hypothesis in dicots (e.g., [17]), further research in the latter would be of great value for understanding the evolution of belowground structures. As already mentioned, there is quite a variety of belowground structures with perennating buds, and, in fact, in some habitats, they are hugely present in several species. For instance, in a thorough study by Procheş et al. [18] on the diversity of geophytes in the Cape Region (Southern Africa), 41% of the species had corms, 32% tubers, 17% bulbs, and 10% rhizomes. Furthermore, the most represented families were from the class Monocotyledoneae (Iridaceae, Hyacinthaceae, and Orchidaceae) except for the family Oxalidaceae. Within dioecious herbs, a tuber-bearing species is B. pyrenaica, which grows every spring season in the Pyrenees from a subterranean tuber, and it is thought to confer a long lifespan to the plant as well as adaptation to their habitat [19]. An example of a dioecious species with corm-like perennating buds is Sagittaria latifolia (Alismataceae), an aquatic plant species in which both hermaphroditic and dioecious populations are commonly found and where, interestingly, bigger corms have been found for dioecious populations [20].

These life strategies totally contrast with that of annual plants, where all cells of the organism die within a year or less, after a first and unique reproductive period (a phenomenon also called semelparity). On the other hand, perennials do not die after the first growing season and they reproduce more than once during their life—i.e., iteroparity. Some exceptions include perennial plants that only reproduce once in their life. The period from germination to senescence and death of the whole organism in perennials—i.e., lifespan—is extremely variable depending on the life form and the species. The life form where the longest lifespans have been observed has been in phanerophytes. The oldest individual of bristlecone pine (Pinus longaeva, Pinaceae) has been reported to reach 5071 years [21] whereas King’s lomatia (Lomatia tasmanica, Proteaceae) is the most long-lived species dated with 43,600 years [22]. What is interesting about King’s lomatia is that it is a species that only reproduces clonally and only one wild-living individual is known, suggesting that species that can reproduce clonally have longer lifespans. Hence, the ability to achieve long lifespans depends on many factors but primarily on (i) clonality, which allows increasing longevity virtually to the infinite by escaping the wear and tear of aging, but then the unit of organism as an entity is lost [23], and (ii) stress tolerance, which allows attaining a greater longevity by withstanding the wear and tear of aging, although this strategy obviously has some limits, as it has been previously reviewed in long-lived trees [5]. Although perennial herbs attain smaller maximum longevities compared with trees, they also seem to have two strategies for attaining greater longevity: either the ability to maintain active buds belowground during the unfavorable season and, therefore, tolerate stress or the ability to reproduce clonally.

Source–sink relations and organ senescence in perennial herbs

The remobilization of photoassimilates and nutrients (mainly carbohydrates but also amino acids and other compounds) through the phloem from source organs to sink organs is crucial for plant performance, leaf senescence, and productivity. These source–sink transitions occur during all life stages in a plant and are regulated by complex phytohormone crosstalks [24]. The remobilization of nutrients from the seed to the developing seedling during germination has been reported to be primarily mediated by abscisic acid (ABA) and cytokinins (CKs), with ABA inhibiting and CKs promoting nutrient remobilization [25–27]. This role in germination of ABA and CKs has just been confirmed in the ornamental chamaephyte Paeonia lactiflora [28] where all the CK-related genes studied were upregulated while the synthesis of ABA was downregulated concomitantly with an upregulation of sugar metabolism. However, the role of ABA did not seem to be that arbitrary since there was a differential ABA gene expression pattern in several genes thought to have similar functions (a number related to ABA catabolism). Furthermore, in this study, gibberellins, ethylene, auxins, and brassinosteroids seemed to have a clear role in promoting germination. When reproduction starts, reserves of carbohydrates and nitrogen are transported from mature leaves to reproductive structures. This is a crucial process, where the proper progression of fruit development will determine productivity in terms of fruit and seed production (as well as seed viability). It is well known that gibberellins (GAs) promote seed germination and that they have a key role in the transition from the vegetative to reproductive state in the plant [29]. In senescent tissues, the transport of nutrients to young tissues seems to be orchestrated by several hormones related to the process of leaf senescence itself, existing a crosstalk between them [26]. While ABA, ethylene (ETH), jasmonates (JAs), and salicylic acid (SA) are known to facilitate senescence, CKs, GAs, and auxins can delay the process (see review by [30]). Nutrient remobilization usually accompanies leaf senescence, which can be prompted by environmental stresses such as drought or cold temperatures or by the developmental program of the plant. In annual species, nutrient reallocation from older tissues to new ones triggers senescence at the whole-organism level, and this massive remobilization usually occurs at the same time as reproduction [31, 32]. In dioecious perennial herbs, this remobilization might change between males and females depending on the species but will predominantly be higher in females than in males since the former generally have a greater nutrient demand during reproductive episodes. Furthermore, leaf senescence of the oldest leaves is necessary to ensure growth and survival of the organism [33].

Among the key players of source–sink communication, CKs regulate the transport of assimilates to sink tissues [34–36] and not only of carbon assimilates but also of nitrogen [37, 38]. A revealing finding by Beck and Wagner [39] further confirmed the crucial function of CKs in nutrient transport and in sink strength: by CK application in U. dioica, they found that the transport of assimilates could totally be reverted in favor of the shoots, evidencing CKs’ role in biomass distribution. Later, it was also proven that this signaling of CKs occurs not only in leaves but also in reserve organs such as tubers of the perennial Nicotiana tabacum [40]. The signaling pathway by which CKs can modulate sugar metabolism lies in its ability to activate cell wall invertases which, in turn, change the sucrose to hexose ratio ([41]; Fig. 2a). Higher concentrations of glucose inhibit a key protein kinase for sugar metabolism, senescence, and many other plant processes, the sucrose nonfermenting-related kinase 1 (SnRK1), which is activated especially under nonfavorable conditions [42, 43]. Hence, given that SnRK1 is a promoter of senescence, lower intracellular levels of CKs in source tissues would lead to senescence. However, the role of SnRK1 in source–sink communication is not that simple, and it can have quite different roles depending on the environmental conditions, the organ, and the phase of the life cycle of the plant (Fig. 2). For instance, the overexpression of SnRK1 in Arabidopsis leaves led to reduced starch accumulation in seedlings [44] whereas the overexpression in Solanum tuberosum resulted in a higher accumulation of carbohydrates in tubers [45]. This role of nutrient remobilization of CKs also seems to exist in dioecious perennial herbs: Oñate et al. [19] found higher contents of CKs, particularly those of the bioactive cytokinin trans-zeatin, in younger tissues of the long-lived B. pyrenaica compared with senescing ones.

Fig. 2.

Source–sink relations between mature and new tissues in perennial herbs and the role of hormones. a A proposed model of the hormonal and sugar source–sink communication between old and new tissues under optimal conditions. In source leaves, GAs stimulate the synthesis of sucrose and promote the translocation of nutrients to the phloem. Auxin creates a gradient with sink tissues to enable the transport of photoassimilates. The translocation of sugars to the phloem decreases the contents of sucrose in source tissues which decreases, in turn, the proportion of hexoses and activates SnRK1. SnRK1 is an inhibitor of the transcription factor EIN3 and, hence, of ETH signaling. This results in resource remobilization with a progressive senescence of source leaves. In sink tissues, the contents of sucrose increase due to the translocation from source tissues. The increased levels of sucrose promote the synthesis of auxin via PIFs, and auxin, in turn, stimulates the synthesis of sucrose, creating a positive feedback. CKs, with the help of auxin, activate CW Inv, thus contributing to sucrose unloading from the phloem. The action of CW Inv increases the ratio of hexoses which inhibit SnRK1 and therefore senescence. b A proposed model of the hormonal and sugar source–sink communication between old tissues and new tissues under stress conditions. Under an environmental stress, ABA, JA, and SA contents increase in mature tissues. ABA promotes the remobilization of sugars promoting the activity of β-amylase, which converts starch into sucrose. At the same time, it inhibits SKINs, leading to the inactivation of SnRK1 and to ETH synthesis. JA and SA have antagonistic effects: JA inhibits the production of sugars through the inhibition of RuBisCo while SA promotes the synthesis of sugars. The induction of ETH signaling promotes a rapid senescence of source tissues. In sink tissues, there is a reduced growth due to the lower levels of sucrose translocated from source tissues, but senescence still does not occur. If the stress is sustained and harsh, there will not be translocation of sucrose at all; hexoses will no longer inhibit SnRK1, and this will lead to massive senescence. ABA abscisic acid, AUX auxin, CKs cytokinins, CW Inv cell wall invertases, EIN3 ETHYLENE INSENSITIVE3, ETH ethylene, GAs gibberellins, JA jasmonic acid, PIFs phytochrome-interacting factors, SA salicylic acid, SnRK1 sucrose nonfermenting-related kinase 1

Besides CKs, ABA also has an important role in source–sink communications, particularly under environmental stress and tightly interconnected with SnRK1 ([46]; Fig. 2b). ABA accumulates in tissues under abiotic stress, and it is considered a stress hormone that stops growth and triggers the synthesis of several senescence-related genes [47]. For instance, it has been shown to interact with SnRK1 under stress, inhibiting its activity through the SnRK1-interacting negative regulators (SKINs), preventing nutrient remobilization to growing seedlings and, hence, growth [48], which could eventually provoke tissue death if the stress is sustained. It is interesting to highlight the differential accumulation of SKINs depending on the tissue—being present in the nucleus and in the cytoplasm—which could explain the different roles of SnRK1 in sugar metabolism [49], and, hence, in nutrient remobilization. Contrastingly, ABA has just been recently shown to act as a promoter of nutrient remobilization by upregulating the expression of genes related to α-amylase activity in rice both under nonstressful conditions [50] and under mild water stress [51]. Furthermore, Lee et al. [52] have recently reported that ABA positively correlated with sucrose levels in the phloem in Brassica napus at the time of bolting. In the dimorphic species U. dioica, higher contents of ABA were found in nonreproductive shoots compared with reproductive shoots [53]. Additionally, in B. pyrenaica, ABA contents were also higher in senescent tissues [19], suggesting that in dioecious plants, ABA besides acting as a stress signal could also have this same role of nutrient remobilization. ETH also has a close relationship with SnRK1. Recently, the α-subunit AKIN10 conforming to SnRK1 has been proven to inhibit the transcription factor ETHYLENE INSENSITIVE3 (EIN3) in A. thaliana [54]. In this manner, SnRK1 would be regulating the rapid progression of senescence promoted by ETH, thus preventing a sudden death of plant cells within the organ (Fig. 2a). However, under stress, this signaling might change. Bauerfeind et al. [55] found in the perennial ornamental Petunia hybrida an upregulation of ETH-related genes of metabolism and perception under chilling stress in source leaves. Furthermore, in the perennial Jatropha curcas, genes related to the synthesis of ethylene were upregulated after seven days of drought, which coincided with an upregulation of both chlorophyll degradation genes and ABA signaling genes [56], evidencing the universal crosstalk between ETH and ABA in senescence.

Other phytohormones that have an essential role in plant stress responses and senescence and, hence, in nutrient remobilization are JA and SA. They are generally considered to promote senescence and to act as signals under stress, both abiotic (see review by [57] for JA; and [58] for SA) and biotic (see review by [59] for JA; and [60] for SA). JA has been reported to inhibit allocation of resources to reproduction under stress [61, 62, 63]. Even though this could seem like a direct regulating effect of JA, it is more plausible that it is the consequence of a higher resource allocation to defense [64, 65]. In fact, JAs are long known to inhibit the activity of the enzyme RuBisCo [66], and, therefore, photosynthesis under stress and the accumulation of photosynthates (Fig. 2b). JAs were also described to promote tuber formation in Solanum tuberosum [67], but it was later confirmed that it was more of an indirect effect than a direct relationship between JAs and sugar transport [68]. A possible mechanism for this indirect relationship could be the crosstalk between JAs and ABA [69, 70]. JAs have been reported to act antagonistically to SA (e.g., [71–73]). SA has been classically attributed to stress responses, but some studies have shown its possible role as a promoter of nutrient remobilization (Fig. 2b). For instance, Agtuca et al. [74] reported, using the radioisotope ¹¹CO₂, that root SA application increased root biomass and carbon fixation in leaves as well as photosynthate transport in roots and sugar contents in leaves under nonstressful conditions. Furthermore, accumulation of sugars in source tissues in SWEET sugar transporter mutants led to an enhanced response of the SA-mediated defense both under no-stress conditions and under a biotic stressor [75]. Like JAs’ role in nutrient remobilization, SA response also appears to be a result of an accumulation of assimilates that would enable a higher resource allocation to defense, which, in turn, in the case of dioecious plants, could result in dissimilar resource allocation in males and females.

ROS, redox signaling, and oxidative damage in long-lived perennial herbs

Reactive oxygen species (ROS) have an essential role in all aerobic organisms as signaling molecules if accumulated transiently and in small quantities [76–78], in a phenomenon known as redox signaling. In plants, ROS take part in a myriad of processes related to plant development, including leaf senescence and stress tolerance [79–82]. ROS homeostasis, if imbalanced with an excessive accumulation of ROS and/or a depletion of antioxidant defenses, can lead to cellular damage in membranes—i.e., oxidative stress—and, if sustained, can ultimately lead to irreversible oxidative damage and cell death. Furthermore, the accumulation of ROS is tightly linked to aging—i.e., the free radical theory of aging [83], a theory that has also been investigated in perennial herbs [84]. Even though ROS are produced in all living organisms, the production in chloroplasts is particularly prominent due to photosynthesis. Tocochromanols are amphipathic molecules found in biological membranes of a huge diversity of organisms, from cyanobacteria to angiosperms and humans, and include tocopherols, tocotrienols, and plastochromanol-8, among other compounds [85]. The capacity to synthesize tocopherols seems, however, to be restricted to cyanobacteria and all organisms pertaining to the plant kingdom, where tocopherols occur universally, with some exceptions, including organisms containing apicoplasts or residual plastids as a holdover from its algal past, including the malaria parasite (Plasmodium falciparum, [86, 87]) or Euglena longa, a close nonphotosynthetic relative of Euglena gracilis harboring a plastid organelle of enigmatic function [88]. Tocochromanols are lipophilic antioxidants that, together with ascorbate glutathione and enzymatic antioxidants (e.g., ascorbate peroxidases and glutathione reductase), scavenge ROS, counteracting their detrimental effects. Most particularly, α-tocopherol or vitamin E—the most biologically active form [89]—scavenges the singlet oxygen (¹O₂) produced from the excitation of chlorophylls in the reaction centers of photosystem II (Fig. 3, [90]). Furthermore, α-tocopherol acts synergistically with another lipophilic antioxidant, β-carotene, to prevent the peroxidation by ¹O₂ [91, 92]. In fact, singlet oxygen can be highly toxic due to its high reactivity [93]. Less reactive ROS other than ¹O₂ formed in the chloroplast membrane are the superoxide anion (O₂^•−) and hydrogen peroxide (H₂O₂), which is formed by the dismutation of superoxide anion by superoxide dismutase (SOD) in photosystem I when there is an overreduction of electron transport components (Fig. 3). Fe-dependent SOD scavenges O₂^•− converting it into H₂O₂ and avoiding the formation of the super reactive hydroxyl radical (OH^•). Conversely, since it can travel through different cell compartments, H₂O₂ is scavenged by several antioxidants such as the ascorbate–glutathione cycle or catalase. Indeed, superoxide and hydrogen peroxide are moderately reactive, but they can form by the Fenton reaction of the hydroxyl radical (OH^•), the most reactive of the ROS [94], which can also be scavenged by tocopherols (Fig. 3).

Fig. 3.

Formation of reactive oxygen species in chloroplasts. When triple-state chlorophyll forms (³P680) in the reaction centers of PSII, singlet oxygen, ¹O₂, is produced, which can be effectively scavenged by α-tocopherol and β-carotene. The superoxide anion, O₂^•−, is produced in PSI by a reduction of O₂ in the absence of acceptors like ferredoxin (Fd) or NADP⁺. Superoxide anion is usually further converted into hydrogen peroxide, H₂O₂, by SOD in the Haber-Weiss reaction. If hydrogen peroxide is not effectively scavenged, it will accumulate and become the most reactive of the ROS: the hydroxyl radical, OH^•, will be produced by the Fenton reaction. Cyt b6f cytochrome b6f complex, PC plastocyanin, PQ pool plastoquinone pool, PSI photosystem I, PSII photosystem II, SOD superoxide dismutase

Perennial plants must be constantly adapting to changing environmental conditions, and these may imply several environmental stresses that, in turn, can provoke oxidative stress. Therefore, they need potent antioxidant mechanisms to maintain ROS homeostasis. For instance, in a long-lived herb relict to high altitudes in the Iberian Peninsula and northern Africa, Saxifraga longifolia, lipid peroxidation decreased with high altitude, coinciding with an increase in the contents of α-tocopherol, which evidences that vitamin E is a crucial mechanism of adaptation to high altitude in this plant [95]. In U. dioica, a long-lived herb, the populations of which can persist for decades due to their vegetative growth by rhizomes [96], and juvenile plants (ca. 4 months old) presented higher amounts of β-carotene compared with older plants (ca. 1 year old) which correlated with lower amounts of α-tocopherol [53]. In older plants, however, this relationship was just the contrary, concomitant with a slight physiological decrease (i.e., lower chlorophyll contents), suggesting an antagonistic age-dependent relationship between these two antioxidants in this dioecious perennial herb. This physiological decrease with maturity in U. dioica was further confirmed in a study with mature plants having a higher lipid peroxidation [97]. Furthermore, flowering plants were more sensitive to a nutrient and water deficit, also showing a higher lipid peroxidation. These findings suggest that U. dioica plants do suffer physiological deterioration with age, supporting the free radical theory of aging in plants, at least comparing juvenile and mature plants. In a study testing for a connection between oxidative stress and age in the long-lived dioecious herb B. pyrenaica [84], it was found that oxidative stress markers such as α-tocopherol levels and the extent of lipid peroxidation did not vary within age groups under both optimal and water stress conditions, thus suggesting that the free radical theory cannot be applied in this long-lived dioecious perennial herb, which indeed has been considered a case of negligible senescence (wherein overall performance of the individual does not decrease with age). It appears therefore from these studies that dioecious perennial herbs can withstand the wear and tear of aging, but that maturity intrinsically leads to higher oxidative stress, at least in some species, a stress that is efficiently managed by changes in the endogenous antioxidant system.

Therefore, having a fine-tuned network signaling upon stress, involving hormones and antioxidants together with ROS, is crucial to acclimate and/or adapt to the environment. ROS have also been reported to play an important role in bud dormancy, and this is particularly important for crop deciduous trees that undergo a dormancy winter period. In perennial plants, the ability to maintain perennating buds for the next growing season is the key for resilience and stability of populations [98, 99]. For instance, many shrubs and trees from temperate climatic regions avoid adverse seasons by losing all, or partially, their photosynthetic aboveground biomass—i.e., deciduous or semideciduous plants. They renew their entire canopy every good season thanks to the fact that they maintain their shoot meristems in a dormant state. These dormant buds are protected by some structural tissues such as cataphylls—i.e., small reduced scale-like leaves produced at the beginning of shoot growth—or hypsophylls—i.e., small reduced bracteole-like leaves produced at the termination of shoot growth [100–102]. And indeed, ROS are believed to break dormancy in deciduous trees (see [103]). Within geophytes, this dormancy is slightly different; instead of having perennial shoot buds, they have belowground perennial buds. For instance, in B. pyrenaica, which is a tropical species relict from the Tertiary [104], the secret of its survival during different changes in climate is thought to lie underground [97, 105]. Having persistent buds underground in the form of tubers allows the plant to renew its aboveground biomass every year, avoiding the harsher conditions of the unfavorable season. No differences in physiological stress indicators nor in phytohormones were found within different ages (<50 years, 50–100 years, and >100 years) in B. pyrenaica [97], except for decreased levels of trans-zeatin in the most mature females, but this was related to a higher reproductive effort. The authors did find clear phytohormone signals of physiological decay related to senescence such as high ABA or low IAA contents in leaves of the individuals after reproduction, which is associated with the renewal of the shoot every season. Oñate et al. [97] conclude in their study that having the tubers of B. pyrenaica five meristems strongly reduces the likelihood of suffering from the wear and tear of aging due to organ regeneration every year and the low accumulation of mutations at the meristem level, thus allowing the plant to be a centenarian. But what occurs inside the tubers? Do they avoid senescence like shoots? Morales and Munné-Bosch [105] found lower amounts of lipid peroxidation in tubers, concomitant with improved hydration and increased α-tocopherol contents with increasing age, thus suggesting negligible senescence at the organism level in plants growing in their natural habitat, despite the fact that every year all aboveground tissues experience senescence at the organ level.

Resetting the clock: clonality in perennial plants

Clonal plants inhabit a wide range of habitats due to their ability to adapt to heterogenous environments [106, 107], and because of this ability, they are very good competitors for resources, with invasive species being numerous [108]. For instance, it was estimated that 70% of species were clonal in temperate floras [108] and more recently 52.7% of Central Europe’s flora [109]. These numbers lead to believe that clonals may have an advantage over nonclonals in colonizing habitats.

Clonal plants propagate through clonal growth organs such as stolons, rhizomes, and roots, and having one or another type of propagation implies different ecological strategies [110]. For instance, in a very thorough study of the evolution of clonal growth organs, Herben and Klimešová [111] found that stolons have a high spreading distance and produce larger numbers of offspring together with hypogeo-rhizomes compared with other types of clonal structures. On the other hand, stolons are the less persistent while rhizomes are the ones that contribute more to bud bank size. These belowground organs are not exclusive for clonal plants, and they can be found in nonclonals too. In fact, there are many species that can shift from clonal to reproductive propagation such as U. dioica or P. lanceolata (Fig. 1), and as we will discuss later, this is probably one of the keys to perennial herbs’ success. In some exceptional cases, there are clonal populations that strictly reproduce asexually. This has a great effect on the genetic structure of populations: the genetic variation within populations will tend to increase whereas among populations, the genotypic diversity will tend to decrease [112, 113]. Nevertheless, there are few instances where this can be beneficial for some species. For instance, Meloni et al. [114] found that strict clonality was beneficial for the endangered insular endemic Ruta microcarpa. Furthermore, in another phylogenetically informed analysis, it has been observed that clonal growth seems to be present when the environment is more constant and disturbances are low, enabling plants’ expansion [115]. These findings lead to believe that the ability to shift between clonal and reproductive growth—i.e., plasticity—could be the key for perennial herbs’ success.

Clonality has been tightly linked with long lifespans of plant species. It is generally hypothesized that the fact that clonal plants normally reproduce without sexual recombination may pose an advantage in longevity over nonclonal plants because they do not accumulate as many mutations in their shoot meristematic tissues and gametes—one of the main causes of potential senescence and, eventually, lower fitness [116]. This occurs, besides an absence of sexual reproduction, because clonal plants replace their aboveground biomass frequently; hence, even though some oxidative stress-related mutations might appear in their shoot meristems, these will be replaced in a short time. This could represent a resetting of the aging clock. Indeed, clonality is tightly related to long lifespans and is thought to be the only way to virtual immortality at the organism level in plants [5, 117].

What can biological diversity teach us?

Perennial bud banks are decisive for the thriving of perennial herbs and for their capacity to “reset the clock,” avoiding the excessive accumulation of somatic mutations and resulting in longer lifespans. The ability to reset the clock in perennial herbs is determined by the great diversity of perennial buds they present which is related to the different mechanisms they possess to face the wear and tear of aging—i.e., a fine-tuned signaling network for stress tolerance, clonality, modularity, and dormancy (Fig. 4). Sexually dimorph perennial herbs are good models to elucidate and understand the mechanisms of aging and development in the tree of life. It is interesting to note the fact that the most long-lived perennial herb known, B. pyrenaica, is the slowest growing perennial herb described thus far, a dioecious herb with a singular bud bank and a tuber with five meristems that intercalate their activation to resprout throughout the years, therefore maintaining their totipotent tissues in a dormant state for years and accumulating less somatic mutations than a meristem that would resprout every year. Another determinant factor of negligible senescence in dioecious perennial plants in nature is their capacity to withstand environmental stress, and plants like B. pyrenaica are very efficient in doing so by resprouting every spring and then senescing quickly at the organ level after storing photoassimilates in the tuber to avoid the harsher conditions that winter poses aboveground. Thanks to these and other mechanisms, these plants can avoid physiological deterioration and withstand the wear and tear of aging. But are these mechanisms comparable to humans’ development and aging? Humans present male and female individuals, just like dioecious perennial herbs. We also must maintain a redox homeostasis to avoid the peroxidation of our membranes, and we, in fact, can take antioxidant supplements to effectively prevent some age-related diseases. We also avoid harsher environmental conditions such as extreme temperatures by moving to another place. Therefore, from a very general point of view, we do not use completely different mechanisms compared with most long-lived dioecious perennial herbs. Although the molecular mechanisms underlying age-related oxidative stress may strongly differ between dioecious herbaceous perennials and humans, all organisms may effectively manage ROS under stress, and the major difference relies on the absence of capacity of humans to fully regenerate all their tissues, although several organs have the intrinsic ability to regenerate and significant progress thanks to biomedicine has recently been made in this respect [118, 119]. Dioecious perennial plants illustrate that (i) reducing stress is an effective means to increase lifespan and (ii) the only way to escape aging is through sexual reproduction or clonality and neither cannot be achieved without a loss of the individuality. A compartmentation of damage (given by modularity) together with organ regeneration, as perennial herbs do, is indeed essential to achieve greater longevities in humans. This will come no doubt with further technological advances but at the end will have important ethical limitations: will we replace our brains for new ones but empty of information with the sole aim of surviving as individuals? What will be the associated biological, ethical, and societal costs?

Fig. 4.

Lessons from long-lived perennials. a Growth, reproduction, and senescence define aging in humans. b Mechanisms to attain greater longevity in dioecious perennial herbs, which show negligible senescence in their natural habitat (see text for details).

Author contributions

SMB conceived and designed the review. MPL and SMB wrote the manuscript and prepared the figures.

Declarations

Competing interests

The authors declare they have no competing interests.