Chromoplasts of Tomato Fruits. I. Ultrastructure of Low‐pigment and High‐beta Mutants. Carotene Analyses

Abstract

Three pigment lines of the tomato cultivar ‘Pearson’ with isogenic backgrounds were studied to determine the relationship between certain carotenoids and the development of chromoplasts during fruit ripening. The lines were normal red (r+/r+), in which about 90% of the carotenoids in the ripe fruit is lycopene; high‐beta (B/B) mutant, in which beta‐carotene is the major pigment and the mature fruit color is deep orange ; and low‐pigment (r/r) mutant, in which carotenoids are drastically reduced and the mature fruit is pale yellow‐orange. This paper reports pigment analyses for the three lines and the ultrastructural changes in plastids of the two mutant lines. Very young, pale green fruits contain proplastids with limited lamellar structure. As the fruits reach the mature green stage, the plastids in all three lines develop into typical chloroplasts. Differences in pigment content and in ultrastructure among the lines are not apparent until ripening commences. In the low‐pigment mutant carotenoids are reduced as ripening progresses and no carotenoid crystalloids are formed. As chlorophyll decreases the fruits become pale yellow. The grana become disorganized and the thylakoids appear to separate at the partitions and tend to be arrayed in lines, some still with their ends overlapping. Globules increase slightly in number. In the high‐beta mutant the grana break down during ripening and globules increase greatly in size and number. Beta‐carotene, presumed to be largely in the globules, crystallizes into elongated or druse type forms which may distort the globules. The crystals may affect the shape of the chromoplasts; long crystals may extend the length of the plastid to over 15 μ. Thylakoid plexes with a regular lattice structure sometimes occur in the chromoplasts of the high‐beta mutant. Granules resembling aggregations of phytoferritin particles occur in the chromoplasts of both of these mutants.

Plastid gene expression during fruit ripening in tomato

“…Ultrastructural and physiological alterations, the drastic degradation of thylakoid membranes, and the decrease of the chlorophyll content occur during chloroplast/chromoplast differentiation in tomato (21,22,28,33,39). These events are consistent with the molecular data presented here.…”

“…This chloroplast/chromoplast transition is one example of tissue-specific differentiation of plastids found throughout plant development (56). The ultrastructural changes observed during chloroplast/chromoplast conversion in tomato fruit include the disappearance of the thylakoid membrane system and the degradation of chlorophyll (21,22,39,51). Since the lightharvesting chlorophyll a/b binding proteins are unstable without chlorophyll, it is assumed that the photosynthetic apparatus breaks down during conversion (2,3,20).…”

Expression of nuclear and plastid genes for photosynthesis-specific proteins during tomato fruit development and ripening

“…Although the physiology of tomato fruit development and ripening has been well characterized, it is unknown if the plastid number per cell changes during cell growth and expansion. However, earlier electron microscopic observations (17,18,37) indicate that the existing cellular chloroplast population differentiates into chromoplasts during fruit ripening. In addition we find that the plastid/nuclear DNA ratio is constant 373 throughout the fruit development and ripening process (data not shown).…”

“…During fruit formation, development and function of chloroplasts in pericarp tissue is similar to that of chloroplasts in leaf tissue. At the onset of fruit ripening, the photosynthetically active pericarp chloroplasts differentiate into carotenoid-producing chromoplasts (3,17,18,37). We are interested to understand the interaction of nuclear and plastid genomes during the development and differentiation process, as well as the coordination of gene expression in the two compartments.…”

“…Based on measurements of photosynthetic activity in mature green fruit (34) it is most likely that during fruit development chloroplasts in the pericarp tissue are photosynthetically active. At the onset of fruit ripening chlorophyll and the thylakoid membrane system disappear rapidly and lycopene starts to accumulate as a major carotenoid in the differentiating chloroplast (3,17,18,37). This is accompanied by a decrease in the level of mRNA for several chloroplast-encoded, photosynthesis-specific poly-*To whom offprint requests should be addressed.…”