Is Petal Senescence Due to Sugar Starvation?

Senescence occurs at every stage of plant development. Shriveling of the cotyledons in young plants and the seasonal recurrence of leaf yellowing are obvious examples. Similarly, after pollination, petals have fulfilled their biological role and become senescent. Despite this ubiquity, however, the molecular events that initiate senescence have thus far remained a mystery. Thimann et al. (1977) hypothesized that sugar starvation is the direct cause of leaf senescence. Later work with Arabidopsis plants, grown in the light, showed that leaves exhibit reduced expression of photosynthetic genes, after a fixed time span. The decrease in photosynthesis was followed by expression of senescence-associated genes, apparently induced by sugar starvation. If Arabidopsis leaves were held in darkness, the ensuing low carbohydrate levels also induced expression of senescenceassociated genes (Hensel et al., 1993; Quirino et al., 2000; Lam et al., 2001). However, other arguments may favor the opposite hypothesis: An increase rather than a decrease in sugar levels induces leaf senescence. Arabidopsis and tomato (Lycopersicon esculentum) plants in which hexokinase (which acts as a sugar sensor) was overexpressed, exhibited accelerated leaf senescence, and transgenic Arabidopsis plants expressing antisense hexokinase showed delayed senescence. Additionally, sugar levels were highest in tobacco (Nicotiana tabacum) leaves that were about to senesce, compared with younger and older leaves on the same plant, and sugar treatment hastened senescence of tobacco leaf discs (Masclaux et al., 2000; Yoshida, 2003). Petal senescence may also be due to sugar starvation or sugar accumulation. Sugar starvation may be involved because application of sugars to cut flowers generally delays visible senescence. A role for sugar starvation is also suggested by the similarities between starvation-induced changes in cell physiology and those observed before cell death during senescence. However, sugar concentrations are still high when petals show the first visible senescence symptoms. What then is the role of sugars, if any, in petal senescence? Three alternative models about the cause of petal senescence are shown in Figure 1. Degradation of polysaccharides, proteins, lipids, and nucleic acids results in mobilization of sugars and nitrogenous compounds, before visible senescence. These mobile molecules are transported, through the phloem, to other plant parts. Mobilization is common to all three models. There are at least three conceivable signals for mobilization: maturation, starvation, and sugar accumulation. According to the standard model (Fig. 1A), the maturation and starvation signals act independently. According to Thimann’s model (Fig. 1B), the maturation signal results in starvation, and starvation causes expression of genes involved in mobilization. Finally, if sugar accumulation were a signal for senescence (Fig. 1C), it may also act on genes that induce mobilization. A maturation signal may precede sugar accumulation. Advanced senescence symptoms are accompanied by cell death. At least two types of cell death are described in plants. The first, of which the hypersensitive response to invading micro-organisms is an example, is limited to a relatively low number of cells and exhibits a short time between external stimulus and death. In the hypersensitive response, rapid cell death is required as the dead cells pose a barrier to the intruding organism. The second type, of which leaf and petal senescence are examples, is characterized by export of valuable materials and takes considerably more time. This Update article discusses how mobilization and cell death are related and examines the possible role of sugars as a signal for petal cell death. It will emphasize the close similarities between starvationinduced changes in cell physiology and those observed upon senescence. It will nonetheless be concluded that there is, at present, no good reason to accept the hypothesis for either sugar starvation or sugar accumulation as a general signal for petal cell death, in flowers of intact plants. The discussion is mostly relevant to petal senescence but also draws some parallels with leaf senescence and may have a bearing to senescence-related cell death in general.