Ageing in plants

Abstract

Ageing in green plants differs in some fundamental ways from the process in animals. The seasonal cycle and persistence of a plant is governed by a combination of the determinate or indeterminate status of meristems (growth centres) and the cell death and disposal strategies employed by plants to generate well-adapted anatomies and morphologies. The degree of perenniality depends on the balance between exploratory growth and the wave of tissue death that succeeds it, and extremes of longevity can arise by relatively minor changes in the quantitative relationship between growth and death. The senescence and elimination of organs and tissues are related to the internal reallocation of resources but are programmed phases in the integrated development of the whole plant and do not represent a kind of ageing by stress or starvation. Meristems of long-lived plants accumulate genetic damage but selection mechanisms exist within the organism to control genetic load, and even to exploit somatic mutations that confer adaptive benefits. It is concluded that most plants do not age in the strict gerontological sense and that extremely long-lived forms like trees and clonal creeping perennials are sustained by selection and correction at the level of semi-autonomous cell lineages.

Introduction

Plants present challenges to general theories of biological ageing. The subject of ageing seen from the viewpoint of a plant scientist raises a series of questions, some of which may not feature prominently amongst the concerns that preoccupy gerontologists. For example, there is the issue of definitions. An organism gets from a state of viability to death by any of a number of routes, many of which either do not involve ageing at all, or in which ageing is a secondary or peripheral influence. By what criteria do we know that something is or is not (a) alive; (b) aged? Do we have definitions that allow us to say that an organism is really dead and not in diapause or some such suspended state? For instance, the only way to tell if a mature desiccated seed is still viable is to germinate it. The comparative biology of ageing reveals a whole range of lifestyles. There are individuals such as lobsters that appear not to age at all, organisms that certainly do age but usually die by accident (for example wild mice, which are almost invariably lost to predation or disease before they have a chance to grow old), species such as humans that age and in which death is frequently a consequence of ageing, and organisms that can be rejuvenated (some invertebrates, for example).

There are special difficulties in trying to translate ageing behaviour from one level of biological organisation to another. What do we mean by an individual? Is a tree, or a coral, or a sponge, or a slime-mould a single organism or a population? There is a ‘scaling down’ problem—what is the relationship (if any) between actuarial or demographic definitions of ageing and the behaviour of the individuals in the population? For example, life tables say that women in developed countries live on average 3 years longer than men do. Does this mean that women begin to age 3 years later, or at a slower rate than men, or what?

Turning to the nature of ageing itself, we see that all sorts of biological processes fail or decline with age, but which are symptoms and which causes, dictating the progress and nature of ageing? There is a problem of ‘scaling up’—is there or is there not a relationship between ageing of component parts or systems, on the one hand, and of the whole organism on the other? What is the relationship between cell/tissue/organ death and survival of the whole plant? We know that eyesight, blood pressure, joints, mental processes all degenerate with age in humans, but what has this to do with dying? Is it meaningful to think in terms of a ‘master’ reaction, a specific component that deteriorates with age and passes one or more critical threshold leading directly to whole-organism decline?

Of particular significance for plants is the question of resource capture and allocation in relation to ageing. Is ageing a kind of starvation or neglect process, and what meaning does this have for autotrophic organisms, in which raw materials and energy are generally not limiting? What is the contribution of non-optimal (stressful) environments to ageing (is ageing the same thing as being weatherbeaten)? And how is the integration of an ageing period into the full lifecycle related to organism lifespan? Finally there are questions about the mechanisms of ageing. Is ageing a failure of processes that normally defend against it? What are the cost-benefit trade-offs of repair, maintenance and durable construction? How is this related to the distinction between germline and soma, and what does this mean for plants in which there is no such distinction? What about ageing avoidance, and is ageing a failure to escape from influences that invoke the ageing response? Have organisms been able to channel the inevitability of ageing into processes that benefit their ecological and evolutionary fitness and what influence has this had on the programmes for cell death and senescence? How can natural selection act to evolve genes with specific functions in ageing? What are ‘ageing genes’ like and can they be mutated, mapped and isolated? What are their environmental sensitivities? And can we do anything about ageing by tinkering with these genes?

Here I select some aspects of plant ageing that address questions posed above. One concerns the relationship between longevity of the whole organism and that of its parts. Then the significance of resource capture for senescence is considered. The discussion ends with some comments from the botanical perspective on the significance of accumulated mutations in the ageing of long-lived plant species.