Patterns

In terms of longevity, plants fall mostly into three categories: annual, biennial, and perennial. When considering whole plant senescence, however, it seems better to classify them as monocarpic (semelparous) or polycarpic (iteroparous) which emphasizes their senescence pattern and its relationship to reproduction. Monocarpy(ic) refers to a life cycle with one reproductive episode followed by death, and polycarpy(ic) to more than one reproductive episode (Hildebrand, 1882; Molisch, 1938). The terms monocarpy and polycarpy predate semelpary and iteropary by about a century and would normally take precedence (Nooden, 1980). Generally, monocarpic plants show a rapid, distinctive degeneration (monocarpic senescence) toward the end of their reproductive phase, while polycarpic plants undergo a more gradual decline. Usually, monocarpic plants are annual or biennial; however, a few are monocarpic perennials, and there are some variable (facultative) types (Nooden, 1988). Far more is known about monocarpic senescence than about the decline of polycarpic plants (Nooden, 1988), yet even this is quite incomplete. This summary will deal primarily with monocarpic senescence which is senescence in the physiologists' sense (Chapters 1 and 23). Senescence of polycarpic plants is less clear and also less tractable to physiological analysis; this is discussed below in Section IV.

C. What is Whole Plant Senescence?

The scope of whole plant senescence needs to be considered. For example, is it a cellular phenomenon or a system phenomenon? Considerable evidence indicates that most individual cells or even most parts such as shoot cuttings can continue to live long beyond the source plant (system) if they are excised and cultured under favorable conditions (Nooden, 1980, 1988). Therefore, whole plant senescence is primarily a system phenomenon.

It is not known whether monocarpic plants die as a result of organ failure or global failure, but one could argue that leaf senescence, and therefore organ failure, is particularly important (Nooden, 1988). Nonetheless, the different organs influence each other and are therefore tied together in the whole organism. Thus, it is not entirely clear which organ should be measured, but given the importance of the leaves, it is reasonable to continue using them and photosynthesis-related parameters as measures of senescence, at least until better criteria are established.

D. Senescence Parameters

Traditionally, whole plant senescence has been viewed primarily in terms of leaf senescence and that is measured mainly through chloroplastic parameters, e.g., chlorophyll loss, decreased photosynthesis, total leaf protein (mostly in the chloroplast protein) or nitrogen (Chapter 1). This emphasis on chloroplastic parameters at the whole plant level is understandable, because (a) these changes are the most conspicuous manifestations of the senescence syndrome and (b) many of the whole plant studies have been directed at developmental changes of these parameters. While chloroplast degeneration is certainly a prominent feature of the broad senescence syndrome, it may not be part of the primary (causal) senescence pathway, i.e., leaves do not die just because their chloroplasts have degenerated (Chapter 1). If we knew precisely the primary steps of the senescence process, these steps would be good measures of senescence, but that will have to wait (Chapter 1).

Since death is the end result of senescence, that could serve as a measure. However, so far, little effort has gone into defining criteria for organism death, and that may be due to the difficulty of defining the end point (Nooden and Penney, 2001). Ideally, that end point would be the death of the last living cell, but this seems impossible to measure. Often, however, the dying organs, e.g., leaves, collapse quickly, so their death can be measured easily.

E. Importance of Chronological Age

The issue of the extent to which monocarpic senescence is linked to age has already been discussed in Chapter 1; however, it has special implications in whole plant senescence. While it is true that monocarpic senescence progresses with age, it has been known for a long time that senescence is not simply a result of growing older (Leopold, 1961; Nooden and Leopold, 1978). Perhaps, the simplest demonstration of this is the prolongation of the life of leaves that have been excised and rooted (Molisch, 1938). Also, individual leaves on a plant may senesce in an order different ("nonsequential") from their chronological age (Resende, 1964; Pate etal., 1983; Mondal and Choudhuri, 1984). In addition, the correlative controls are able to override age and accelerate or retard senescence of the whole plant or its parts. For example, using soybean explants (a leaf with one or more pods and a subtending stem segment), it can be shown that monocarpic senescence is related to the developmental stage of the pod, not the age of the leaf (Nooden, 1985). In other words, leaf senescence is a product of internal controls, not simply passive aging. These degenerative changes should not be called aging (Chapter 1; Nooden and Leopold, 1978).

Evidence indicates that some important processes including regenerative ability (Nooden, 1980; Grbic and Bleecker, 1995; Weaver et al., 1998) do diminish with age. Furthermore, Arabidopsis leaves, and presumably other short-lived plants, seem to be built to last only a limited time (Bleecker and Patterson, 1997; Nooden and Penney, 2001), and therefore, age may be an important factor in their decline. Nonetheless, senescing Arabidopsis leaves do show changes in gene expression characteristic of leaf senescence (Quirino et al., 1999), so a typical senescence program appears to be taking place anyhow.

F. Correlative Controls

Anyone who has watched plants develop over their life cycle will readily accept that there must be a lot of internal coordination, i.e., many correlative controls (the influence of one part of an organism on another). Often, hormones mediate these controls (Leopold and Nooden, 1984). The reproductive and senescence phases of monocarpic plants are also subject to a network of correlative controls, and an effort to summarize what is known about these controls has been made for soybean (Nooden, 1984).

In monocarpic plants where senescence and death closely follow reproductive development, it should not be surprising that this senescence (monocarpic senescence) is often controlled by the developing reproductive structures (see Molisch, 1938; Sax, 1962; Nooden, 1980). In these cases, removal of the reproductive structures or prevention of their development (e.g., sterility mutations) usually prolongs the life of the plant. Soybean, cucumber and mignonette are prime examples. On the other hand, there are some prominent exceptions (Nooden, 1988). For example, grain head removal may not always delay senescence in some of the grasses such as corn and wheat; indeed, this may actually accelerate senescence. In Arabidopsis, the longevity of the rosette leaves is not controlled by the reproductive structures even though plant longevity is (Hensel et al., 1993; Nooden and Penney, 2001). While control by the reproductive structures will be emphasized here, it is important to note that other patterns may exist in particular species, particularly in the grass family. In addition, it follows that treatments altering reproductive development, particularly fruit development, likewise affect monocarpic senescence. Failure to recognize this important correlative control can lead to unnecessary controversy.

G. The Causes of Whole Plant Senescence

In monocarpic senescence, a central question is how do the developing reproductive structures cause the death of the plant. While the reproductive structures may be the most important correlative controllers in monocarpic senescence, other parts also participate. For example, the roots play an important role in maintaining leaves, apparently mainly through their production of cytokinins (Molisch, 1938; Van Staden et al., 1988). The flux of cytokinins from the roots to the leaves has been shown to decrease during monocarpic senescence in a variety of plants ranging from rice to beans (Van Staden et al., 1988). In soybean, it can be shown that the decrease in cytokinin production by the roots is necessary, but not itself sufficient, for monocarpic senescence, and the developing pods induce the decline in cytokinin production (Nooden and Letham, 1993). The ways by which the developing fruit can induce monocarpic senescence will be discussed further below in Section III.

H. Evolution and Differences among Monocarpic Species

Another special issue surrounding whole plant senescence has to do with differences among species. Clearly, monocarpy has evolved independently several times from polycarpy, and there are some significant differences, particularly in the correlative and hormonal controls (Stebbins, 1974; Nooden, 1980; Young and Augspurger, 1991). These differences pose a dilemma with regard to making generalizations about monocarpic senescence in different species. It seems best to try to formulate a general picture covering monocarpic senescence in all species, but to recognize that differences may exist.

II. Complexity and the Rules of Evidence

Of all the fields that we are acquainted with, this one has suffered most from unnecessary controversy. No doubt, this is due to the complexity of whole plant senescence, and it seems necessary to discuss some of these cases in very specific terms in order to clarify the issues looming in this field and to prevent reoccurrence. Three specific cases will be described and the evidence will be laid out; the reader can judge for himself/herself. Without a doubt, the most significant problems surround the mechanism or cause of monocarpic senescence.

First, some rules of evidence for causality. In 1876, Koch laid an important foundation for these rules that have become known as Koch's postulates (see e.g., Thimann, 1955) which grew out of his studies on the causes of disease. Just the correlation of the presence or absence of a bacterium with the occurrence/absence of a disease is not sufficient to establish that the bacterium is the cause of the disease. It must also be shown that introducing the bacterium into a healthy organism produces the disease. A similar set of problems exist in establishing which hormones control particular plant processes. Even if the application of a hormone causes an effect, this does not prove that the hormone normally regulates that process. Jacobs (1979) has developed an extension of Koch's postulates for analyzing hormonal controls, and this requires additional manipulations to establish a causal connection between a hormone and a putative effect in a whole plant. For example, the putative source of the hormone should be removed to block the effect on the target and then exogenous hormone is added back in place of the hormone source to reinstate the effect on the target. Some analogous manipulations have been used in studying causality in monocarpic senescence, but the advent of molecular biology and better genetic tools will offer additional criteria.

Monocarpic senescence has been viewed as exhaustion death or nutrient deficiency death based on observations that nutrients were redistributed from the leaves to the developing fruits in monocarpic plants (Hildebrand, 1882; Molisch, 1938). In many monocarpic plants, there is a good correlation between nutrient accumulation in the fruits and whole plant senescence. Thus, the exhaustion death idea does have some intuitive appeal. Some are thoroughly convinced by simple correlation evidence; others are not (Nooden, 1988; Grabau, 1995). Significantly, this correlation does not hold for many situations (Nooden, 1980, 1988). As in the cases cited above, more than simple correlation is required to establish a causal connection.

Second, probably as a result of complexity, one may encounter conflicting data within the same paper. For example, in one of the most widely cited papers on whole plant senescence, depodding of soybean plants appeared to decrease photosynthesis, yet did not decrease overall dry weight accumulation (Wittenbach, 1983). Since the decrease in photosynthesis in depodded plants has been interpreted to show that monocarpic senescence (if measured simply by photosynthetic rate) is not controlled by the reproductive structures, it seems important to resolve a contradiction like this (Nooden and Guiamet, 1989).

Third, non-use of available data—the literature in this field is widely scattered, and often highly relevant data are buried within papers not focused on senescence. While these factors add to the challenges posed by complexity, this is the kind of drawing together that reviewers are supposed to do (or at least try). One prominent case of particular importance here is the proposal that the developing fruits create a deficiency in carbohydrates, i.e., sugars, that leads to the death of monocarpic plants at the end of the reproductive phase (Kelly and Davies, 1988; Sklensky and Davies, 1993). Much of this discussion focuses on the garden pea with emphasis on senescence of the shoot apex as the cause of the death of the plant. This hypothesis is, like most of the earlier nutrient withdrawal and diversion hypotheses, based primarily on a correlation between the distribution/redistribution of dry matter and photosynthate. The following lines of contrary evidence, mostly in the mainstream senescence literature, are not reconciled with this hypothesis: (1) Application of sucrose to the pea shoot apex does not prevent its death (Lockhart and Gottschall, 1961). (2) Sucrose applications may actually promote senescence rather than retard it (see Section IIIB below). (3) Carbohydrate levels often increase rather than decrease during senescence (see Section IIIB below). These observations seem incompatible with the carbohydrate deficiency mechanism proposed.

The problems outlined here reflect the status of the field of whole plant senescence and to some extent its past culture, and it seems necessary to consider them in order to move forward.

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