IN THIS ISSUE

Sucrose Synthase and the Fruit of Its Labor

Evolutionary selective pressures have clearly induced animals and plants alike to place a premium on liberal locomotive abilities. Because the root systems of plants define a sedentary existence, however, angiosperms in particular invest significant energies in exploiting the mobility of animals. Such exploitation, in fact, is one of the most fascinating evolutionary trends to have marked the biology of angiosperm reproduction. The enormous expenditure of genetic resources for the elaboration of distinctive floral chromophores that appeal to insects, or of scents that can attract the blindest of bats, is waged solely to recruit pollen-dispersing vectors.

Seed dispersal is a second aspect of plant reproduction that is often facilitated by animal motility. Organs such as burrs—which, botanically speaking, are seed-bearing fruits—are shed so as to adhere to the fur, feathers, and skin of mobile animals. Similarly, the deployment of carbohydrate into edible fruits, thereby endowing them with their characteristic sweet and sour tastes, can function to entice foraging animals, often with the result that ingested seeds are distributed quite considerable distances. The fact that the average American consumes between 250 and 300 pounds of fruit annually bespeaks the success of angiosperms, albeit with the occasional intervention of horticulturists, in appealing to the human palate.

The contingencies that lead to savory fruits, of course, are not only of agronomic and gastronomic interest. Indeed, fruit development and growth encompass a variety of questions that are basic to plant biology, many of which are only now beginning to be addressed at the molecular level. The investment of plant resources into fruit production makes evolutionary reproductive sense, but what are the mechanisms that cue floral organs for de-velopment into fruit? How does the plant negotiate the distribution of its assimilated carbon to the developing fruit so as to determine the balance between productive and aborted fruit set?

Whereas the hormonal, genetic, and enzymatic bases of fruit ripening have been elaborated in some detail, relatively little is known about the molecular events of early fruit development. Nevertheless, the early development of tomato fruit, which may be taken as a model system, can be divided into two phases (Gillaspy et al. 1993 ). The first of these is characterized by rapid cell division, and is followed by a period of cell expansion and limited division that allows for fruit enlargement. Only recently have molecular data been collected that corroborate the recognition of these two early phases. Specifically, heightened cyclin-dependent kinase activity is detectable through the first phase, whereas endoreduplication tends to characterize the expanding cells of the second (Joubes et al. 1999 ). The genetic programs that account for early fruit development have yet to be elaborated, although at least one homeotic gene involved in development of the Arabidopsis silique has been identified (Gu et al. 1998 ).

To the extent that fruits are typical sink organs that grow as a function of the photosynthetic assimilate that they receive, at least some of the molecular players that participate in fruit growth can be inferred. The activities and regulation of those enzymes and transporters that provide the fruit sink with sugars would seem to warrant particular investigation. Indeed, sugars that travel from source leaves (principally in the form of sucrose) to the fruit via the phloem serve not only as the carbon material for the construction of developing fruit tissues, but also act to regulate a variety of plant genes that may be more intimately involved in development per se (Koch 1996 ).

In this issue of THE PLANT CELL, on pages 2407–2418, D'Aoust et al. explore the dependency of tomato fruit production on sucrose synthase, an enzyme that is central to the metabolic interplay of sucrose, hexoses, and starch synthesis. The enzyme, catalyzing the reversible conversion of sucrose into fructose and UDP–glucose, has been studied in several plant species and is generally regarded to represent the dominant cytosolic activity that cleaves the glycosidic bond of sucrose. In potato plants, sucrose synthase has been regarded as the first catalyst on the metabolic pathway from sucrose to starch as well as a determinant of sink strength in tubers (see Zrenner et al. 1995 ). In the case of Lycopersicon esculentum, the enzyme has similarly been implicated in regulating the import of sucrose into the fruit (Wang et al. 1993 ). To investigate this possibility more fully, D'Aoust et al. explore the effects of antisense inhibition of the fruit-specific sucrose synthase in tomato.

The authors have generated a number of lines containing an antisense sucrose synthase transgene that leads to significantly reduced fruit sucrose synthase activities. The most obvious result of the antisense strategy is the significant diminution in the number of fruits produced per plant. The reduction in fruit yield is not due to a reduced rate of flowering, but rather arises from a greater tendency of the plants to abort fruit sets. But the more telling story of sucrose synthase and fruit production comes from following the development of the transgenic fruit over time and, further, by correlating the levels of reduced sucrose synthase activity among the lines with differences in fruit characteristics.

The macroscopic consequences of inhibiting the enzyme in vivo are not particularly striking upon observation of fruit at a few weeks after anthesis: The sucrose (and glucose) content is equivalent in transgenic and wild-type fruit. Rates of transgenic fruit growth are not markedly different from those of control fruit, moreover, and measurements of sucrose import into fruits and its conversion to starch also fail to differentiate between antisense-inhibited and control plants. As the authors point out, the steadfastness of starch synthesis, which is in contrast to the findings from the antisense-inhibited potato system, is in part due to a tomato fruit invertase activity that, at mid to late stages of development, is no less than three orders of magnitude greater than that of potato tubers.

But the invertase content of the tomato can clearly not compensate for all of the metabolic consequences of reduced sucrose synthase activity. Indeed, in the early stages of fruit development (~7 days after anthesis), the loss of sucrose synthase activity in the transgenic L. esculentum plants is evident in multiple ways. For example, fruits that are set during the first week of transgenic plant flowering grow more slowly than do those of control plants. Correspondingly, and in contrast to the observations made at a few weeks after anthesis, rates of sucrose unloading into young fruit are greatly retarded in plants with low levels of sucrose synthase. To account for the difference between the normal rate of sucrose import in older and the retarded rate in younger transgenic fruit, the authors refer to the established difference in fruit development at one as opposed to multiple weeks post anthesis. Specifically, the younger fruit, characterized by smaller cells undergoing rapid division, is viewed as containing less vacuolar space to accommodate invertase, whereas the older fruit, as already noted, is rich in invertase by virtue of larger cell, and thus vacuolar, volumes. In this way, the greater levels of sucrose-metabolizing activity provided by invertase would be envisaged, in more mature fruit, to compensate for reductions of sucrose synthase.

Whatever compensatory enzymatic mechanisms may be at play in the cells of the authors' transgenic fruit, the role established for sucrose synthase in controlling sucrose import, at early stages of development at least, is an intriguing finding that should not be taken for granted. As pointed out in a recent review, the partitioning of photoassimilate in plants is not merely a function of the metabolic activities of source and sink tissues (Lalonde et al. 1999 ). Rather, specific mechanisms of sugar sensing are basic to plant development, whereby both intra- and intercellular concentrations of carbohydrates are monitored so as to regulate processes of sugar transport. There is good evidence, for example, that the catalytic turnover of glucose by hexokinase is essential to sugar sensing in plants, just as it is in yeast (see Smeekens and Rook 1997 ). Furthermore, the involvement of sucrose synthase, along with other enzymes of sugar metabolism, has been reported recently in the monitoring plant carbon flux (Zeng et al. 1999 ). Thus, D'Aoust et al. appear to touch on an emerging theme in plant biology—the contribution of sugar-metabolizing enzymes such as sucrose synthase to sugar sensing, assimilate import to sink tissues, and specific developmental programs.

REFERENCES

D'Aoust, M.-A., Yelle, S., and Nguyen-Quoc, B. (1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and sucrose unloading capacity of young fruit. Plant Cell 11:2407-2418[Abstract/Free Full Text].

Gillaspy, G., Ben-David, H., and Gruissem, W. (1993) Fruits: A developmental perspective. Plant Cell 5:1439-1451[Free Full Text].

Gu, Q., Ferrandiz, C., Yanofsky, M.D., and Martienssen, R. (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509-1517[Abstract].

Joubès, J., Phan, T.-H., Just, D., Rothan, C., Bergounioux, C., Raymond, P., and Chevalier, C. (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol. 121:857-869[Abstract/Free Full Text].

Koch, K.E. (1996) Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Mol. Biol. 47:509-540[CrossRef][Web of Science].

Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J.W., Frommer, W.B., and Ward, J.M. (1999) The dual function of sugar carriers: Transport and sugar sensing. Plant Cell 11:707-726[Free Full Text].

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Wang, F., Sanz, A., Brenner, M.L., and Smith, A. (1993) Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiol. 101:321-327[Abstract].

Zeng, Y., Wu, Y., Avigne, W.T., and Koch, K.E. (1999) Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol. 121:599-608[Abstract/Free Full Text].

Zrenner, R., Salanoubat, M., Willmitzer, L., and Sonnewald, U. (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7:97-107[CrossRef][Web of Science][Medline].

Related articles in Plant Cell:

Antisense Inhibition of Tomato Fruit Sucrose Synthase Decreases Fruit Setting and the Sucrose Unloading Capacity of Young Fruit

Marc-André D'Aoust, Serge Yelle, and Binh Nguyen-Quoc
Plant Cell 1999 11: 2407-2418. [Abstract] [Full Text]  

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