How do perennial plants avoid senescence?

If you know, please tell me! The following is part of a pre-proposal that Brigitte and I are submitting to NSF. This is our justification for continuing to spend a week each summer counting fruits on a small shrubby, not particularly attractive plant. I mean, other than the fantastic hiking and fishing in the area.
Senescence is a widely observed phenomenon describing the decrease in survival and fertility rates with advancing age. There are three traditional explanations for the evolution of senescence (Salguero-Gomez et al 2013): mutation accumulation where negative mutations affecting organisms late in life persist at higher rates, antagonistic pleiotropy where genes that produce positive traits early also produce negative effects later in life, and disposable soma where physiological deterioration occurs because of unavoidable tradeoffs between survival and reproduction. However Mittleldorf and Martins (2014) rejected all three of these in favor of programmed life span where individual death leads to lineage level benefits due to population turnover or increased evolvability. None of these explanations of the evolution of senescence address why stress can extend life expectancy (reviewed in Ristow and Schmeisser 2011).

In contrast to animals most flowering plants show no senescence (Baudisch et al. 2013). This is thought to stem from the plastic growth, complex life history, and modular morphology of plants. Hence, plant demographers typically focus on the effect of plant stage (plant size or developmental stage like seeds, vegetative plants, flowering plant) on population dynamics rather than age (e.g., Tenhumberg et al. 2009, Eckberg et al. 2012). Recently the role of whole-plant senescence for plant demography and evolution has attracted renewed attention (e.g., Caswell and Salguero‐Gómez 2013, Salguero‐Gómez et al. 2013). While most research on understanding whole-plant senescence has focused on organisms with clonal or asexual reproduction we have a surprisingly poor understanding of senescence or the lack thereof in plants reproducing exclusively via seeds. In this proposal we explore the effect of abiotic and biotic stressors on possible senescence avoidance mechanisms in the obligate sexually reproducing, herbaceous plant Astragalus scaphoides.

The escape of senescence by asexually producing plants is believed to be due to clonal reproduction producing rejuvenated offspring (e.g., Harper 1977). There are several mechanisms by which non-clonal plants could avoid senescence. Plants can be rejuvenated artificially by trimming or grafting (references in Wyka 1999, Caswell and Salguero‐Gómez 2013). In the field plants may reset the aging clock by remaining underground for one or more growing seasons (prolonged dormancy, Tuomi et al. 2013) or shrinking under adverse environmental conditions (Salguero‐Gómez and Casper 2010). Theoretically, plasticity in growth rates can produce negative senescence (higher fecundity and survival in older individuals, Vaupel et al. 2004). The possibility of negative senescence has also been predicted using selection gradients to quantify selection intensity or selection pressure (contra-senescent selection gradients, Caswell and Salguero‐Gómez 2013). That study predicted that age specific selection gradients can differ for large and small plants. However, when the model was applied to 36 plant species ranging from mosses to trees the authors found most plants die before reaching a size that is large enough for contra-senescent selection to take place. Environmental conditions that extend life expectancy could reveal contra-senescence.

Both shrinking and prolonged dormancy carry opportunity costs of lost photosynthesis or reduced future reproduction. If the magnitude of these opportunity costs is influenced by growing conditions (e.g. reduced photosynthesis or reproduction in drought years) we would expect the propensity of engaging in rejuvenating mechanisms to increase during periods of stress. Consistent with this hypothesis the probability of entering prolonged dormancy is influenced by environmental stress such as defoliation (e.g., Ehrlén 2003) and drought (e.g., Lesica and Steele 1994, Vaughton and Ramsey 2001). Opportunity costs will also depend on the duration of stress. For instance, the benefit of staying underground is diminished if poor growing conditions continue for several years, which should select for plasticity in plant response to stress. Hence, we expect the propensity to shrink or enter/remain in prolonged dormancy to decrease with increasing duration of stress.

Figure 1 Annual temperature and precipitation anomalies at the study sites using the PRISM data (http://www.prism.oregonstate.edu/) (1986-2013)

Our 10 year vision for this project is that we will explore how abiotic and biotic stressors interact with Senescence Avoidance Mechanisms (SAMs) in the long-lived, iteroparous plant A. scaphoides by analyzing a potentially 38 year duration demographic data set. An analysis of a subset of this data set concluded that prolonged dormancy leads to rejuvenation in A. scaphoides (Tuomi et al 2013). Prolonged dormancy is a common phenomenon among plants (Shefferson 2009), but has not previously been associated with avoiding senescence. It is quite possible that prolonged dormancy sets the aging clock back in other species as well. Using the full data set and the freely available climate data from the PRISM Climate Group (Fig. 1) we will assess the effect of past extreme weather events (precipitation and/or temperature) on the proposed SAM. Adding an additional 10 years to the current 28 years of data will increase the number of extreme weather events present in the database, leading to improved power to detect non-linear effects of weather on senescence. Further we will evaluate the effect of chronic stress on senescence by reducing nutrient limitation and herbivore pressure for the next 10 years on a subset of the monitored plants. Short term experiments will not provide sufficient temporal replication to evaluate interactions with weather and other stressors. The effect of releasing cumulative stress may also not appear until the treatments have been maintained for a substantial proportion of the species expected lifespan. We evaluate the following three hypotheses:

H1: SAMs increase lifetime fitness by allowing individual plants to escape senescence.

H2: Short term stresses caused by temperature and precipitation anomalies interact with SAMs to increase lifetime fitness at low frequencies but decrease lifetime fitness at high frequencies.

H3: Reducing chronic stressors by annually adding nitrogen and excluding herbivores will (a) decrease the frequency of SAMs; and (b) allow the oldest plants to demonstrate contra-senescence (survival and fecundity increasing with age) because life expectancy increases.

A. scaphoides is the ideal study system for addressing these research questions. First, we have access to a long-term demographic data set of four populations covering nearly 40 years by the end of the proposed study. Elizabeth Crone (Tufts University) has collected demographic data on A. scaphoides 1999-2014. In 2013 the PIs Tyre and Tenhumberg joined the project and will have sole responsibility for it from 2015 onwards. Demographic studies recording plant age directly are rare, and, hence, most conclusions about the effect of age on plants are based on size to age conversion algorithms (age x stage-dependent models are constructed from single stage-specific projection matrices, e.g. Baudisch et al. 2013, Caswell and Salguero‐Gómez 2013). This conversion relies on the notion that individuals grow older, but their vital rates are affected only by their size. In this study we do not rely on size to age conversion algorithms because our data set tracks individuals of known age. Second, A. scaphoides plants are long lived (longevity is approximately 21 years, Ehrlèn and Lehtilä 2002) allowing the analysis of sequential rejuvenating events as well as the effect of accumulation of stress over several years. Third, A. scaphoides’ life history is shaped by its low resource environment, and responds quickly to environmental stress. For instance, a single season of drought or defoliation reduced flowering and survival probability, and increased dormancy rates (Gremer and Sala 2013). Previous studies in this system focused on the effects of weather on flowering, or the effect of a single perturbation on all vital rates. What remains to be done is a synthetic analysis that simultaneously evaluates the effect of weather, herbivory and nutrient availability on age dependent plant vital rates.

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