CHLOROPLAST SPECIALIZATION IN DICOTYLEDONS POSSESSING THE C 4 ‐DICARBOXYLIC ACID PATHWAY OF PHOTOSYNTHETIC CO 2 FIXATION

The C4-dicarboxylic-acid pathway of photosynthetic CO2 fixation found in tropical grasses has recently been demonstrated in members of the Amaranthaceae and Chenopodiaceae. In the tropical grasses this C02-fixation pathway is correlated with specialized leaf anatomy and chloroplast structure. This investigation was undertaken to determine if leaf cells of some representatives of these other families had structural features similar to those of tropical grasses. The leaf anatomy of Amaranthus edulis and a variety of Atriplex species is very similar and it resembles that of grasses such as sugar cane. Prominent bundle sheaths are surrounded by a layer of palisade cells. Bundle-sheath cells of Am. edulis have large chloroplasts containing much starch, but the chloroplasts have grana. The palisade cells have much smaller chloroplasts containing very little starch. The bundle-sheath cell chloroplasts of At. lentiformis have grana, their profiles tend to be ovoid, and they contain abundant starch grains. The palisade cell chloroplasts contain little starch and their profiles are discoid. The bundle-sheath cells of both species contain mitochondria which are much larger than those in the palisade cells. The chloroplasts in both types of cells in both species have a highly developed peripheral reticulum. This reticulum is composed of anastomosing tubules which are contiguous with the inner plastid membrane. The leaf anatomy and cell ultrastructure of these dicots are similar to those of the tropical grasses possessing this new photosynthetic carbon-fixation pathway. These morphological features are interpreted as adaptations for the rapid transport of precursors and end products of photosynthesis. A hypothesis is presented stating that the uniquie morphological and biochemical characters of these plants represent adaptations for efficient and rapid carbon fixation in environments where water stress frequiently limits photosynthesis. HATCH and Slack (1966) demonstrated that the photosynthetic carbon fixation pathway in sugar cane differs from the conventional Calvin cycle. After 1 sec in C'402, 93 % of the fixed radioactivity was found in oxaloacetate, malate, and aspartate. They have investigated carbon fixation pathways in a variety of monocotyledon and dicotyledon species, and the "cane-type" or C4-dicarboxylic acid pathway of photosynthetic carbon fixation has been found in species of the following genera of grasses: Zea, Sorghum, Paspalum, Axonopus, Digitaria, Chloris, Eragrostis (Hatch, Slack, and Johnson, 1967). A species of Cyperus also possessed this pathway. Phosphopyruvate carboxylase is considered to be the major photosynthetic C02-fixing enzyme in these taxa (Slack and Hatch, 1967). These grasses possess other features in common. They are characterized by their high rates of photosynthesis at high light IReceived 24 October 1967. This work was supported by a grant from Tate and Lyle, Ltd., and by NSF Grant GB-6066. The technical assistance of Janet Burr and Ian Price is gratefully acknowledged. intensities (Burr et al., 1957; Hesketh and Moss, 1963; El-Sharkawy and Hesketh, 1965), by their failure to "leak" respiratory CO2 during the light period (El-Sharkawy, Loomis, and Williams, 1967), and by low CO2 compensation values (Moss, 1962). In addition, Dr. Bruce Smith (Division of Geology, California Institute of Technology) has recently shown that these tropical grasses have much higher '3C/12C ratios than temperate grasses (personal communication). It has also been known for many years that the chloroplasts in the bundle-sheath cells of tropical grasses differed from the chloroplasts in the surrounding mesophyll cells. Rhoades and Carvalho (1944) demonstrated this in maize and sorghum on the basis of light microscopy, but the details of these dimorphic chloroplasts were only revealed by studies with the electron microscope. These were made on maize by Hodge, McLean, and Mercer (1955), on a variety of tropical grasses by Johnson (1964), and on sugar cane by Laetsch, Stetler, and Vlitos (1965). In these plants the mature chloroplasts in the promi[The JOURNAL for August (55: 745-874) was issued 1 August 1968] AMERICAN JOURNAL OF BOTANY, AVol. 55: No. 8, 1968