Evolution of Oleosins Oil Bodies and Tapetosomes

Prokaryotes, in general, do not store TAGs as food reserves. A minor exception is Actinomyces, which produce TAGs under certain nutritional and other environmental conditions. TAGs were likely to have evolved as efficient food reserves in primitive eukaryotes by the addition of one enzyme, DAG AT, which was evolved from one of the existing acyltransferases. This enzyme diverted DAGs from the ubiquitous PL metabolic pathway to TAGs. Initially, the hydrophobic TAGs were present between the two PL layers of the ER membrane, where DAG AT was. Today, seeds of some species on occasions still have some TAGs present along the hydrophobic region of the PL bilayers in ER (Wanner et al. 1981). The presence of excess TAGs in the ER membrane would interfere with the normal functioning of ER. This problem was overcome by removal of the TAGs from ER via budding to become solitary droplets. The droplets, each containing a TAG matrix enclosed by a layer of PLs originated from ER, would be unstable. In yeasts, the droplets were made more stable through a coat of amphipathic proteins, especially the TAG synthesizing and hydrolyzing enzymes. The semistability would allow the droplets to undergo dynamic metabolic fluxes. In mammals, the droplets were modified to different forms with proteins and membranes, such that they were also semistable and amenable to metabolic fluxes. In plants, the droplets were stabilized by the evolutionary appearance of oleosins, whose long hydrophobic hairpin could stabilize the droplets so effectively that they were amenable to prolonged storage in desiccated seeds. Oleosins and their coated oil droplets have been found in diploid and triploid storage sporo-phytic cells of seeds of angiosperms and gymnosperms, haploid storage cells of female gametophytes (in seeds) in gymnosperms, haploid cells of male ga-

Fig. 3 Model for the evolution of oleosins. The 72-residue hydrophobic segment of an oleosin molecule was viewed as having evolved from the transmembrane segment of an ER protein. The shaded area and thick lines represent hydrophobic regions. These include the acyl moieties of PL (two lines joining a circle), TAGs, and the transmembrane, hydrophobic portion of an ER protein being evolved to an oleosin hairpin (enclosed column). Unshaded circles depict hydrophilic portions of PL and proteins (modified from Huang 1996)

Fig. 3 Model for the evolution of oleosins. The 72-residue hydrophobic segment of an oleosin molecule was viewed as having evolved from the transmembrane segment of an ER protein. The shaded area and thick lines represent hydrophobic regions. These include the acyl moieties of PL (two lines joining a circle), TAGs, and the transmembrane, hydrophobic portion of an ER protein being evolved to an oleosin hairpin (enclosed column). Unshaded circles depict hydrophilic portions of PL and proteins (modified from Huang 1996)

metophytes (pollen), the moss Physcomitrella (possibly in diploid sporophyte or haploid gametophytes) and the diploid sporophytic cells of floral tapetum.

The hydrophobic stretch of 72 resides in oleosins is the longest, and is actually more than twice as long as any found in any prokaryotic or eukaryotic protein. The mechanism by which it has evolved is intriguing. A hypothesis has been proposed (Fig. 3) on the basis of the following observations (Huang 1996):

1. The length of 72 residues is about four times that of a transmembrane polypeptide (~ 20 residues)

2. Several relatively hydrophilic residues are present in the middle of both antiparallel stretches

3. A certain degree of residue symmetry exists along the two antiparallel stretches

The hypothesis depicts that the long hydrophobic stretch has evolved from duplications of a transmembrane peptide of an ER protein in a primitive plant or alga. The hypothesis can be tested by comparing the amino acid sequences of the oleosin hairpins (and the corresponding nucleotide sequences) with those of transmembrane segments of proteins, especially of ER, in the most primitive organisms (currently, the moss Physcomitrella). Whereas the hairpin hydrophobic stretch is conserved, the N- and C-terminal portions have undergone extensive evolutionary changes because of limited structural and functional constraints.

Oleosin-coated oil droplets in diverse plant species can be categorized into two groups according to their structures and functions. The solitary oleosin-coated OBs in seeds and pollen store TAGs for germination and postgerminative growth in the respective organs. The tapetosomes contain clustered oleosin-coated oil droplets associated with ER-derived vesicles and store and deliver materials to the surface of maturing pollen. Whether, during evolution, solitary oleosin-coated oil droplets similar to the modern seed OBs appeared before the complex tapetosomes, or vice versa, is a matter for speculation. The most primitive plant known to contain oleosin is the moss Physcomitrella. The moss oleosin is presumably associated with storage OBs in the sporophyte or gametophytes. The moss does not have flowers or tape-tum and thus would not have analogs of tapetosomes. Brassicaceae species contain abundant tapetosomes in tapetum, whereas the maize tapetum does not have any. Thus, tapetosomes were likely to have evolved from solitary oleosin-coated TAG droplets similar to the modern OBs in seeds. Initially, these ancestral droplets, solitary or in groups, in tapetum delivered oleosins to the pollen surface. Subsequently, they became associated with vesicles that also contain materials for the pollen surface. Thus, tapetosomes are thought to have evolved to perform the overall function of packaging and storing materials for delivery to the pollen surface.

Acknowledgements The research was supported by the National Science Foundation (MCB-0131358) and the US Department of Agriculture (National Research Initiative Competitive Grant No. 2004-02429).

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