Loss of Vegetative Regenerative Capacity

Often, monocarpic plants cease their vegetative growth fairly abruptly early in their reproductive phase (Nooden, 1980; Kelly and Davies, 1988; Reekie, 1999). Conversely, the perennial polycarpic pattern requires continued vegetative growth (Thomas et al, 2000). This prominent shift (diversion) in growth-related allocation of resources in monocarpy seems to be part of a reproductive strategy that optimizes reproductive output for these plants (Section V below). Not only does this shift (divert) the allocation of assimilates from the vegetative parts to the reproductive structures, but there is often redistribution (withdrawal) of nutrients already invested in the vegetative parts. This diversion/withdrawal is often quite prominent, and it has given rise to the nutrient exhaustion explanation for the cause of monocarpic senescence which will be discussed below.

Cessation of growth may be caused by a simple arrest of the apex growth or by senescence and death of the shoot apex (Nooden, 1980). Pea is a prime example of apex senescence (Lockhart and Gottschall, 1961; Kelly and Davies, 1988).

On the surface, it seems that nutrient diversion or withdrawal might cause or contribute directly to the cessation of growth in the reproductive phase of monocarpic plants, but numerous inconsistencies exist (Nooden, 1980). For example, parthenocarpic cucumber fruits do not cause growth cessation as seed-bearing fruits do even though they seem to represent about the same amount of diversion/withdrawal as seed-bearing fruits (McCollum, 1934). Furthermore, fruit removal does not reinstate shoot growth in many species, e.g., soybean (Nooden, 1980). Thus, the shutdown of vegetative growth seems to be under a more direct control, separate from nutrient diversion.

Implicit in the review by Kelly and Davies (1988) is the idea that monocarpic plants, particularly peas, die because the shoot apex dies. The evidence against this idea is discussed in greater detail elsewhere (Nooden, 1980), but even in peas, the locus Veg causes death of the apex without inducing the corresponding monocarpic senescence (Reid and Murfet, 1984). Moreover, decapitation does not induce senescence in plants; in fact, it usually inhibits senescence of the lower leaves (Nooden, 1980). So, what is the role of apex death in monocarpic senescence? These look like separate processes, and careful distinction between them will prevent controversy.

Nonetheless, cessation of apex growth and of continued growth or regeneration of the plant, e.g., leaf production, may be necessary for monocarpic senescence; that is the plant will not die if it keeps growing and producing new vegetative structures. For example, in Arabidopsis, continued regeneration of photosynthetic parts extends the life of the plant (Nooden and Penny, 2001).

B. Nutrient (and Hormone) Deficiencies

Variations of the deficiency (exhaustion death) idea have been the dominant explanations for causality in monocarpic senescence. Because nutrients were observed to accumulate in the seeds at the same time that the vegetative parts, particularly the leaves, were losing nutrients and dying, it was believed that the developing fruits caused a nutrient deficiency in the vegetative parts (Molisch, 1938). The nutrient deficiency ideas in turn fall into two subgroups: (1) withdrawal and (2) diversion. These are not entirely different, and they may work together; however, it seems simpler to discuss them separately.

1. Nutrient withdrawal (redistribution)

The basic idea here is that the developing fruits withdraw minerals and/or carbohydrates from the vegetative parts thereby killing them. This is the original form of the exhaustion death hypothesis (Hildebrand, 1882; Molisch, 1938), and it has emphasized N and P, which are often limiting from the plant's environment and are quite mobile within the plant. There certainly is an enormous old literature showing correlations to support this idea in many monocarpic plants. As the fruits develop, carbohydrates, N, P, and other mobile minerals exit from the vegetative parts, particularly the leaves, and reciprocally accumulate in the fruits, particularly the seeds (Molisch, 1938; Nooden, 1980; Marschner, 1995). However, this interplay between source (e.g., leaves) and sink (e.g., seeds) is more complex than a simple withdrawal (Nooden, 1988). For example, leaves may continue to move nutrients toward their base after detachment, which physically disconnects them from the sinks.

The exhaustion death idea and this mainly correlational evidence were questioned long ago (Mothes and Engelbrecht, 1952; Leopold etal.,1959), mainly because male plants show the same monocarpic senescence as female plants in some species such as hemp and spinach even though their reproductive sinks are quite small. Although foliar applications of mineral nutrients sometimes does delay monocarpic senescence, numerous non-correlations such as the failure of foliar fertilizing to prevent monocarpic death have usually been ignored (Nooden, 1980,1988). Nonetheless, the nutrient exhaustion hypothesis is widely accepted.

Rather little direct testing of the nutrient withdrawal ideas has been carried out as contrasted to simple gathering of correlational data and that testing is mostly with soybean. Soybean seems to be the classic example of massive nutrient redistribution causing death during monocarpic senescence, yet it offers some of the clearest evidence against the nutrient deficiency ideas. Some of these experiments are more complex and are discussed elsewhere (Nooden, 1988), but three simple tests with clear results are from:

a. Soybean explants. When these cuttings, which include a leaf, one or more pods and a subtending stem (a nutritional unit), are fed a solution of minerals resembling xylem sap through the transpiration stream, the minerals have only a slight delaying effect, not prevention, of leaf senescence (Nooden, 1988; Mauk et al., 1990). This is not what the nutrient withdrawal hypothesis would predict.

b. Steam-girdling (phloem destruction) the leaf petiole in pod-bearing soybeans does not block pod induction of leaf senescence even though it blocks nutrient withdrawal (Fig. 15-1; Wood et al., 1986). Indeed, the blocked leaves build up high concentrations of starch (Fig. 15-2). Again, these data seem contradictory to the nutrient withdrawal idea. The control, a steam-girdled leaf on a depodded plant, also accumulates starch but does not turn yellow, so the phloem blockage does not cause accumulation of toxins.

c. Depodding (or removal of the seeds) after all or most of the nutrient withdrawal has occurred still prevents leaf senescence and plant death in soybean (Nooden, 1980,1988). The lethal effect of the seeds occurs very late, when the seeds are yellowing. Similar observations have been reported for cucumber and bean (Leopold et al., 1959).

Interestingly, even in soybean where the filling pods seem to place a particularly heavy demand on the parent plant, the growing seeds can be supplied from current assimilation rather than redistribution if senescence is prevented (Nooden et al., 1979; Nooden, 1985, 1988). Some interesting observations made on wheat warrant mention here. Steam-girdling or severing the connection between the sink (filling grains) and the source (flag leaves) causes carbohydrate accumulation in the leaves and promotes senescence (Lazan et al., 1983; Frölich and Feller, 1991). The sugar-deficiency idea is generally entertained as a facet of nutrient diversion, so it will be discussed below in that context.

2. Nutrient (and hormone) diversion

There are many variations of this idea, but in general, the developing fruits (or other large sinks) are believed to divert the supply of essential nutrients (or hormones) creating a deficiency(ies) which ultimately proves lethal to the vegetative parts.

Figure 15-1. Steam-girdling in the petiole of a pod-bearing soybean plant (Nooden and Murray, 1982). This treatment blocks nutrient withdrawal from the leaf but not the induction of leaf senescence (yellowing) by the pods.

Among the hormones that could be involved here, the best candidate is cytokinin which plays a well-established antisenescence role (Van Staden et al, 1988), but there is direct evidence against this kind of diversion of cytokinins in soybean (Nooden and Letham, 1993).

One avenue for diversion is the transpiration stream, but the transpiration rate of the fruits is small relative to the leaves (Nooden, 1988). In addition, defruiting causes the stomata in the leaves to close and thereby diminishes their transpiration. Therefore, the fruits do not compete with the leaves for hormones and nutrients coming up from the roots by diverting the transpiration stream.

Understandably, the major candidate for nutrient diversion is photosynthate, specifically sucrose, and that is the major theme of the reviews by Kelly and Davies (1988) and Sklensky and Davies (1993). Likewise, in soybean, it has been concluded that the "high rate of photosynthate utilization by developing fruits decreases the photosynthate available for leaf maintenance processes" (Egli and Crafts-Brandner, 1996). If sucrose deprivation caused monocarpic senescence, then exogenous applications of sugar should be effective in preventing leaf senescence, but sugar applications actually promote senescence in a variety of tissues (Table 15-1) except for some leaves placed in darkness (Goldthwaite and Laetsch, 1967; Thimann, Tetley and Krivak, 1977). Similarly, sucrose applications do not prevent pea apex senescence (Lockhart and Gottschall, 1961), which is central to the mechanism of monocarpic senescence envisioned by Davies etal. (Kelly and Davies, 1988;

Figure 15-2. Effects of phloem destruction (steam-girdling) treatments on senescence (chlorophyll loss) and starch accumulation in the leaves of pod-bearing soybean plants (Wood et al., 1986). A and C are fresh leaves taken from control plants at late podfill (A) or from plants treated as shown in Fig. 15-1 (C). B and D are the same leaves (A and C respectively) after clearing and staining with I2 for starch. These figures show that steam-girdling the petiole blocks the withdrawal of starch from that leaf but does not block the yellowing (chlorophyll loss) induced by the pods.

Figure 15-2. Effects of phloem destruction (steam-girdling) treatments on senescence (chlorophyll loss) and starch accumulation in the leaves of pod-bearing soybean plants (Wood et al., 1986). A and C are fresh leaves taken from control plants at late podfill (A) or from plants treated as shown in Fig. 15-1 (C). B and D are the same leaves (A and C respectively) after clearing and staining with I2 for starch. These figures show that steam-girdling the petiole blocks the withdrawal of starch from that leaf but does not block the yellowing (chlorophyll loss) induced by the pods.

Sklensky and Davies, 1993). Furthermore, numerous studies on a wide range of species including soybean (Egli et al., 1980) show that the sugar concentrations in the leaves of plants undergoing monocarpic senescence may actually increase rather than decrease as required for the sugar deficiency mechanism [see Nooden et al. (1997) for some of these references]. Indeed, several reports attribute leaf senescence in a wide range of species to elevated carbohydrate levels (Allison and Weinmann, 1970; Mandahar and Garg, 1975; Hall and Milthorpe, 1977; Lazan et al, 1983; Araus and Tapia, 1987; Ceppi et al., 1987; Schaffer et al, 1991; Prioul and Schwebel-Dugue, 1992; Fischer et al., 1998). Some of these reports involve experimental manipulation of senescence, so they go beyond simply correlating with the normal progression of senescence. For some time, carbohydrate accumulation has been believed to exert a feed-back influence on photosynthetic capacity, and this can now be attributed to repression of photosynthesis-related genes (Azcon-Bieto, 1986; Sheen, 1994; Koch, 1996; Paul and Foyer, 2001). Proceeding a step further, Wood et al. (1986) found that steam-girdling a petiole in a pod-bearing soybean plant does not block the pod-induced senescence of that leaf (Fig. 15-1, discussed above) even as it blocks nutrient flux out of the leaf and causes a massive accumulation of starch (Fig. 15-2). This array of data seems incompatible with the sugar deficiency mechanism proposed by Davies et al. Further discussion of the pros and cons of the nutrient deficiency ideas can be found elsewhere (Nooden, 1980, 1988; Grabau, 1995).

Table 15-1. Senescence-promoting Effects of Sugars

Species

Part used

(common name)

Light conditions

Observations

References

Leaf disks

Phaseolus vulgaris (common bean)

Darkness

0.01-0.1 M sucrose, glucose or fructose accelerates chlorophyll but apparently not protein loss

Goldthwaite and Laetsch, 1967

Leaf disks

Xanthium pennsylvanicum (cocklebur)

3000 lux continuous

0.01 M sucrose or glucose promotes chlorophyll loss, but NaCl does not

Khudairi, 1970

Detached leaves

Spinacia oleracea

9 h per day, 16 ^m

0.05 M glucose feed through the transpiration

Krapp etal., 1991

(spinach)

light m-1 s-2

stream promotes loss of chlorophyll, protein, Rubisco and several Calvin cycle enzymes

Leaf disks from young

Nicotinia tobacum

16 h per day, 20 ^m

50 mM glucose causes decreases in chloro-

Wingler et al., 1998

and mature leaves

(tobacco)

light m-1 s-2

phyll and hydroxypyruvate reductase; an osmotic agent (sorbitol) does not

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