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Anatomy and Morphology |
Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, Iowa 50011-1020 USA; 3Department of Biology, University of Wisconsin, Stevens Point, Wisconsin 54481-3897 USA; and 4Department of Genetics, Development and Cell Biology, Microscopy and Nanoimaging Facility, Iowa State University, Ames, Iowa 50011-1020 USA
Received for publication March 31, 2006. Accepted for publication October 4, 2006.
ABSTRACT
Neutral (storage) oil bodies occur in leaf mesophyll cells of many angiosperms, but their literature has been largely forgotten. We review this literature and provide a survey of 302 species and hybrids from mostly north-central US species representing 113 families. Freehand cross sections of fresh leaves stained with Sudan IV verified the presence of oil. In 71 species from 24 families we observed 1–15 oil bodies per mesophyll cell. The eudicot families Asteraceae, Caprifoliaceae, Lamiaceae, and Rosaceae had the highest number of species with oil bodies, whereas few or no species in the Apiaceae, Betulaceae, Fabaceae, and Scrophulariaceae had them. Only three of 19 monocot species sampled had oil bodies. Repeat sampling of a Malus (crabapple) cultivar and a Euonymus species showed conspicuous oil bodies in mid-summer and also in mid-autumn in both attached and recently shed leaves. Oil bodies in leaf mesophyll cells are conspicuous (visible in hand cross sections using moderate magnification in unstained water mounts) in numerous species, and they occur throughout the growing season in at least some species. Neutral oil bodies in leaf mesophyll cells are not mentioned in contemporary textbooks and advanced works, but they deserve recognition as significant cellular components of many taxa, in which they may be significant sources of commercial oils.
Key Words: angiosperms • leaf anatomy • mesophyll cells • neutral oil bodies • oleosomes • spherosomes • triacylglycols • triglycerides
Two basic classes of oils occur in plants: volatile oils and neutral oils. Volatile oils are composed of low-molecular-mass terpenes that evaporate (volatilize) upon exposure to air and are aromatic. These well known and often commercially important oils accumulate in various kinds of specialized surface or internal secretory cells, glands, or cavities (Baas and Gregory, 1985
; Bakker, 1992
; Fahn, 2000
), most commonly associated with leaves. Familiar examples are the many perfume oils (e.g., jasmine, rose), and citrus, clove, Eucalptus, peppermint, and spearmint oils.
Neutral oils do not evaporate or volatilize in air, they are not aromatic, and they taste bland. Familiar examples are canola, castor, corn, linseed, and olive oils. Neutral oils are composed of triacylglycols (also called triglycerides), which are triesters of fatty acids attached to glycerol. Oils of this last class are the most common storage form of lipid in plants (Facciotti and Knauf, 1998
).
Triacylglycols can occur as independent oil bodies (sometimes called oleosomes) in the cytoplasm or as deposits within plastids. Triacylglycols from many seeds and some fruits are of economic importance; therefore they have been emphasized in the literature, so much so that it has been generally forgotten that ordinary leaf and stem cells of many, possibly even most, angiosperms also contain one or more conspicuous oil bodies as normal temporary or long-term components. In this study we retrieved leaf mesophyll oil bodies from their present obscurity with an overview of relevant but neglected literature, followed by the results of a survey of fresh leaves of 302 selected species and hybrids to determine the presence or absence of oil bodies, and discuss the use of the term oleosome. It is important to reestablish basic, descriptive knowledge of foliar oil bodies and to determine their distribution among angiosperms because such information is the basis for studies of their physiological role as well as their possible commercial utilization.
To provide proper perspective on how oil bodies in leaves have been considered and identified, we conducted an extensive, although not exhaustive, literature search that included introductory and specialized textbooks as well as primary sources dealing specifically with leaf mesophyll oil bodies. The results of this perusal of the literature indicate that various terms have been assigned to oil-containing cell inclusions. The following four sections provide a coherent introductory overview that bears on the results and discussion presented in this study.
These sections mostly follow a historical time line, so it will be helpful first to present the current understanding of what oil bodies are and where they are said to occur. Authors of three recent studies (Hsieh and Huang, 2004
; Jolivet et al., 2004
; Siloto et al., 2006
) agree that an oil body is a sphere of triacylglycerol bounded by a phospholipids monolayer embedded with, and covered by, unique proteins called oleosins. Oil bodies are said to occur in seeds, fruits, embryos, endosperm, pollen grains, and anther tapetum. Leaves are not mentioned. Similar, if not identical, oil bodies called lipid droplets occur in many animal cells (Martin and Parton, 2006
).
Textbook descriptions
Most recent introductory botany textbooks (we sampled a dozen) state that oils accumulate in leucoplasts, which are described as colorless plastids capable of becoming chloroplasts, amyloplasts, or elaioplasts (oil-storing plastids) depending on local conditions. Elaioplasts are said to occur most commonly in seeds (e.g., Muller, 1979
; Berg, 1997
; Mauseth, 1998
; Stern, 2000
, Uno et al., 2001
; and six other textbooks). Raven et al. (1986)
also mentioned leucoplasts, but this was the only text that described independent lipid droplets, which the authors said were formerly called spherosomes. They lack a bounding membrane but were said to be possibly coated with protein. None of the general botany textbooks we examined mentioned leaf mesophyll cells as a location for any oil bodies.
Plant anatomy texts might be expected to say more about oil bodies, which are anatomical features of cells. Haberlandt's 1914
classic work is closest to the older literature that will be described later, but he did not cite any of it, simply mentioning briefly that minute glyceride droplets or vesicles occur suspended in storage cells. He did not mention their occurrence in leaf cells. Eames and MacDaniels (1947) and Dickison (2000) only reiterated the leucoplast story as in general botany texts, but Cutter (1978)
distinguished between leucoplasts with oil (elaioplasts) and spherosomes (oil bodies) that lack a boundary membrane. She said that elaioplasts are mostly in monocotyledons and that both elaioplasts and spherosomes occur mostly dispersed in the cytoplasm of cells in seeds. Fahn (1990)
also mentioned spherosomes but did not specify any cells where they occur. Esau (1975)
said that elaioplasts are common in liverworts and monocotyledons and that spherosomes are highly mobile cytoplasmic granules of 0.25–1.00 µm in diameter that contain lipids and proteins. She did not mention, however, any cell type in which they occur. Esau (1977)
, in a section on lipid globules (p. 35), mentioned that spherosomes have a unit membrane but that other lipid droplets lack a membrane. No cell types were specified for the occurrence of the membraneless globules or droplets. Plant physiology texts in recent years have provided details of oil body structure and described their developmental origin from endoplasmic reticulum (ER), but like other textbooks they mention only that oil bodies occur in seeds (e.g., Hopkins, 1995
; Taiz and Zeiger, 2002
). It is evident from these examples that textbook descriptions for oil bodies/oil droplets/elaioplasts/oleosomes/spherosomes are varied and that leaf mesophyll cells have not been mentioned as locations.
Research studies
There are numerous volumes on lipids in plants, far too many to cite, and the same can be said for books on plant cell ultrastructure. From the latter, however, the succinct description of spherosomes by Gunning and Steer (1975)
is worth quoting: "Spherosomes are a heterogeneous collection of objects that float around in the cell, usually with a spherical shape that arises by minimization of their surface area by forces of surface tension." The major category of spherosome they mentioned was the lipid droplet, which lacks a membrane but is bounded instead by an outer layer of oriented lipid molecules. They glossed over the distribution of these bodies, merely stating that lipid droplets are "... abundant in some cells and sparse or absent in others."
Yatsu et al. (1971)
determined from microscopic and biochemical analyses that oil droplets and spherosomes, which had long been maintained as two different entities, are really identical. They suggested that the term "oleosome," which had been used decades earlier for such bodies, now be used for all oil droplets lacking a unit membrane boundary.
An oleosome is therefore currently defined as a spherical triacylglycol droplet with a half-unit boundary membrane consisting of a single phospholipid and protein layer (Facciotti and Knauf, 1998
). Napier et al. (2001)
identified this protein as an oleosin and said that oleosomes in seeds are mostly 0.6–2.0 µm in diameter, a size range that they speculated allows for efficient packaging and mobilization during germination. They regarded the oleosome as a product of the endoplasmic reticulum (ER). Oleosins are inserted into the ER endomembrane system, and from this origin they extend as the boundary layer around each oleosome as it is budded off.
Facciotti and Knauf (1998)
stated that oleosomes "... are almost exclusively accumulated in the cotyledons and/or the endosperm of developing embryos. Besides seeds, the mesocarp tissues of oil-palm and avocado fruit are the only known tissues capable of storing significant amounts of triglycerides." Huang (1992)
stated that triacylglycerols are the storage form of lipids throughout the plant kingdom, and in angiosperms they are restricted mostly to seeds and some fruits, but pollen is also a storage site.
These specialized reviews and books are the main sources that the more general textbooks rely on for information about topics such as this. One can therefore appreciate that statements such as those just quoted have been a significant influence in dropping oleosomes in leaf mesophyll cells from the contemporary body of knowledge.
Oil body occurrence in leaf cells
Why have oil bodies in leaf mesophyll cells been neglected? Part of the answer certainly involves a shift in late 19th and early 20th centuries from observing freehand sections of living leaves to the almost exclusive study of microtomed sections of leaf samples killed and preserved in aqueous or alcoholic fixatives followed by a typical ethanol dehydration, which dissolves lipids. Repeated explicit or at least implied statements in introductory and advanced texts and specialized reviews that oleosomes occur only in seeds and some fruits are another factor. But the literature, especially of the 19th and early 20th century, includes several reports and surveys of oil bodies in leaf cells.
A useful review of published oil body and elaioplast studies from 1835 to the 1930s, including what are now called oleosomes, is included in Faull (1935)
. The key study she cited for oleosomes in leaf cells was the Ph.D. dissertation of Lidforss (1893)
.
Lidforss (1893)
more than a century ago began his introduction with this statement: "It has long been known that oil is an important seed reserve, but very little attention has been paid to oil deposits in the mesophyll of leaves, with the exception of the oil drops known to occur in chloroplasts" (p. 1, our translation). Remarkably, this statement is also true today. His literature review mentioned nine earlier papers, dating from 1863 to 1891, which included reports of what would now be called oil bodies in leaf mesophyll cells. Lidforss surveyed fresh leaves of Swedish field- and greenhouse-grown plants from 191 species of 140 genera from 37 families of dicots and a small sample of monocots (seven species from six genera of only two families—Orchidaceae and Cyperaceae). In summary, the great majority of species he surveyed had either a single conspicuous oil body per mesophyll cell or a cluster of smaller oil bodies per cell. Such inclusions were almost always visible under the microscope without any special treatment (i.e., freehand sections mounted in water), although he did mention using various chemicals to identify them as oils. His major finding was that oil bodies are usually a normal anatomical component of leaf mesophyll cells. As was common in that era, however, Lidforss included no illustrations.
Lidforss reported that oil bodies ranged from 1 µm to a remarkable 18 µm in diameter, and examples of 10 µm and larger were common. Sambucus nigra had the largest examples, but these occurred only in leaves on vigorous branches; shade leaves had much smaller ones. The few monocots that he examined had rather inconspicuous oil bodies, or none. His information on Gramineae came entirely from Monteverde (1890)
, who had reported oil bodies in assimilating cells of numerous species (not enumerated in the summary translation from his original Russian dissertation of 81 pages).
Petit (1901
, 1902
) published a two-part, nonillustrated survey of 250 species of angiosperms examined by procedures similar to those of Lidforss (1893)
. Petit seems to have observed oil bodies in fewer species than did Lidforss; although Petit's numbers were not specified very clearly, one can roughly envision that he observed oil bodies in 60–70% of species from 29 dicot families. In the Apetalae and among 18 families of monocots, however, they were uncommon.
Price (1912)
described a single spherical oil drop, each larger than a chloroplast, per palisade cell of cherry laurel (Prunus laurocerasus) leaves. These conspicuous inclusions, as seen in freehand leaf cross sections, dissolved in alcohol, indicating lipids. Addoms and Mounce (1932)
reported that cranberry leaves had little starch but stored food mostly in the form of oil, which implies the presence of oil bodies.
Perner's 1958
review of spherosomes (his term also included oleosomes) did not mention them in leaf mesophyll cells, and Sorokin (1955, p. 229) at about the same time stated "The whole science of plant enzymology disregards the existence of visible spherosomes or other lipid globules in plant cells ..." Her statement summarizes the general amnesia about oil bodies except for those in seeds and fruits.
In the mint family (Lamiaceae), Lersten and Curtis (1998)
found a single oil body 5–6 µm in diameter in each mesophyll cell of Physostegia virginiana. They uncovered a previous report by Mullan (1933)
, as well as a mention by Lidforss' (1893) of 17 mint species from 14 genera with oil bodies. Peracino et al. (1990–1991
) showed multiple lipid bodies in mesophyll cells of Mentha spicata, which they reported to be each larger than a chloroplast.
Because grasses are of great economic importance, there have been a few studies of their leaf mesophyll oil bodies, beginning with the earliest observations (despite his misleading dissertation title) from several species by Monteverde (1890)
. Petit (1902)
, however, found oil bodies to be scarce among the few grass species he examined. Chonan et al. (1981)
reported clusters of lipid bodies, which sometimes seemed to merge into one, as well as large, single lipid bodies in rice leaf mesophyll cells. These same workers (Chonan et al., 1984
) later surveyed 40 Kranz and non-Kranz grass species from five subfamilies and 10 tribes. Lipid bodies 3–6 µm in diameter occurred almost exclusively in the non-Kranz grasses surveyed, with the exception of Eragrostis curvula.
Oleosomes in mesophyll cells of the flag leaf of wheat were reported to range up to 14 µm in diameter and to persist through leaf maturity and senescence (Parker and Murphy, 1981
). Their analysis (Murphy and Parker, 1984
) showed the composition of these oleosomes to be 50–60% triglycerides and 15–40% esters of wax, by mass.
A somewhat different phenomenon occurs among at least some of the 16 species of the neotropical grass genus Lasiacis.Davidse and Morton (1973)
illustrated abundant oil bodies in the inner epidermal cells of the soft, leaflike glumes and sterile lemma of the spikelets. Oil bodies did not appear until the grain was almost mature, but none formed if pollination or fertilization did not occur.
Finally, the two major literature compendia of dicot systematic plant anatomy should be mentioned. They provide information on oil bodies, but it is not easily retrievable. The two volumes of Solereder (1908)
, which summarized 19th century work, merely devoted part of one paragraph to "fat bodies." Solereder (p. 1109) stated that they "... are found in the assimilatory tissue (especially the palisade-tissue) ... of species belonging to numerous Orders, and are occasionally doubly refractive." A later two-volume work on dicotyledon vegetative anatomy (Metcalfe and Chalk, 1950
) has variously worded brief comments, unfortunately without citations, about fat and oil deposits in leaves from 21 families. Some of these comments are undoubtedly based on references cited earlier in our overview, but other references were probably sources as well.
Oleosome function in leaf mesophyll cells
It can be reasonably speculated that oil bodies of mesophyll cells in most species probably act as intermediate storage products of photosynthesis, although their absence from Kranz-type grasses (Chonan et al., 1984
) and their persistence in the wheat flag leaf (Murphy and Parker, 1984
) suggest other possibilities for some plants.
Another possible function for oil bodies is adaptation to cold temperatures. Pihakaski et al. (1987)
reviewed some of the literature about this and showed that a sclerophyllous, evergreen cushion plant of arctic and subarctic regions, Diapensia lapponica (Diapensiaceae), has a single large lipid body in each mesophyll cell during warmer months, but many smaller lipid bodies per mesophyll cell during cold months. They speculated that this change helps to lower the freezing point of cells.
MATERIALS AND METHODS
During summer, plants or plant parts of 302 species and hybrids representing 113 angiosperm families were collected at various times of day, mostly from localities in and around the University of Wisconsin, Stevens Point, including some growing in the university greenhouses. Examples of a few species were collected and examined in Ames, Iowa. Species were identified by Dr. Robert Freckmann, curator of the herbarium at the University of Wisconsin, Stevens Point. Voucher specimens for plants collected in the Stevens Point area were deposited in the university herbarium.
Each leaf was sectioned freehand with an ethanol-cleaned razor blade, and a few sections were mounted immediately in a drop of water on a standard microscope slide. Sudan IV dye (Biological Stain Commission Certification #AcZ-2) dissolved in 95% ethanol (Jensen, 1962
) was added to test for oil. This reagent turns oil drops bright orange just before they gradually dissolve in the ethanol. The presence or absence of oil bodies in intact cells was observed with bright-field optics (see end of Results section), and selected photomicrographs were taken to show the range of variation among the 113 families (Figs. 1–8). The film negative from each selected taxon was digitized using a PowerLook (http://www.umax.com) 3000 scanner, processed in Adobe (http://www.adobe.com) PhotoShop 7.0, and made into a plate using Adobe Illustrator 10.0. Figure 9 was downloaded from the Angiosperm Phylogeny Group (APG, 2003) website and modified in PhotoShop and Illustrator.
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Yatsu et al. (1971)
, Facciotti and Kanauf (1998), and Napier et al. (2001)
have collectively provided ultrastructural and biochemical criteria for the oleosome. Their implied, if not explicitly stated, conclusion is that all triglyceride oil bodies should be called oleosomes. We do not use the term oleosome here, however, because we did not use biochemical or ultrastructural procedures and because we looked at leaves, not seeds. Therefore, we use instead the general term "oil body" throughout the remainder of this study when dealing with our results.
The survey included herbs, shrubs, and trees. Of the 302 species surveyed among 113 families of magnoliids, eudicots, and monocots, 71 (23%) contained oil bodies, and these species were from 26 (23%) of the 113 families (see end of Results section and Fig. 9). Only leaves of these taxa were observed; no other organs were tested for the presence of oil bodies.
Figures 1–8 illustrate selected examples of different sizes and numbers of oil bodies per cell from the species in this survey. Oil bodies were observed mostly in leaf palisade cells and in some spongy parenchyma cells, never in epidermal cells or cells making up the vascular bundles. A single oil body per cell was seen frequently. Figure 1 shows several isolated, intact palisade cells of Ambrosia psilostachya (Asteraceae), each with a single oil body 3–4 µm in diameter per cell. Somewhat larger single oil bodies occur in Erigeron annuus (Asteraceae), as seen in an unstained preparation (Fig. 2). Figure 3 illustrates the dark color imparted by Sudan IV. A crabapple (Malus hybrid Snowdrift) leaf contains a large single oil body and one or two smaller ones per palisade cell (Fig. 4).
Multiple oil bodies per cell were less common, but striking in appearance when encountered. Figure 5 shows palisade cells of bull thistle (Cirsium vulgare; Asteraceae), each of which contains several, and Fig. 6 is of one cell with at least 10 clustered oil bodies.
Two species sampled in summer were reexamined in mid-autumn. Malus hybrid Snowdrift in Fig. 4 from mid-June was seen to have similar, perhaps even more conspicuous, oil bodies in late October. A representative mesophyll cell from an autumn leaf still on the plant has about four large oil bodies that occupy a considerable portion of the cell volume (Fig. 7). Leaves collected shortly after they dropped from the plant had similar oil bodies even though the cells otherwise had degenerate chloroplasts. The same was true for Euonymus alata (Celastraceae), which had numerous oil bodies in each greatly elongated palisade cell in midsummer. Leaflets sampled in early autumn (Fig. 8) and even in late October in both the attached and newly shed state were similar (not shown).
We did not observe oil bodies in leaf epidermal cells of any of the species in this survey. There was no mention of epidermal oil deposits in the references of the literature overview, except those noted in onion leaves by Sorokin (1955)
, who called them spherosomes.
The following information identifies the 302 species from 113 families from angiosperm (Angiospermae, Anthophyta, Magnoliophyta, etc.) taxa surveyed in this study for the presence of oil bodies in leaf mesophyll cells. Nomenclature follows Griffiths (1994)
for cultivated plants and Kartesz (1994)
for noncultivated plants. The taxa are divided into families, genera, and species and are organized (from top to bottom) as shown in Fig. 9, which is a modification of fig. 1 in APG (2003). Our modified phylogenetic tree in Fig. 9 shows orders/families not observed (no indicator), orders/families observed with (dots), or without oil bodies (circles) present. The numbers in parentheses indicate the number of families observed.
Our survey recognized nine families that the APG (2003) angiosperm classification regards as merged with other families. We have retained these families because they are mostly familiar and of long standing. They are listed, however, as part of their respective orders as recognized by APG. These families and their current APG families: Asclepiadaceae (=Apocynaceae), Chenopodiaceae (=Amaranthaceae), Empetraceae (=Ericaceae), Hippocastanaceae (=Celastraceae), Hydrophyllaceae (=Boraginaceae), Monotropaceae (=Ericaceae), Pyrolaceae (=Ericaceae), Tiliaceae (=Malvaceae), and Lemnaceae (=Araceae).
Figure 9 includes all the orders and families with species that were tested in this study, with the exception of the Boraginaceae (in which APG includes the Hydrophyllaceae). In Fig. 9 we show that APG (2003) placed the Boraginaceae in the Eusterids I category (APG, 2003; p. 420), but it is not assigned to any order.
In the following inclusive paragraph, all of the taxa observed are listed in the descending order they are presented in Fig. 9, beginning with Nymphaeaceae. The families, genera, and species that tested positive for oil bodies are boldfaced. Species without asterisks were sampled only in Wisconsin. A single asterisk (*) indicates a species sampled only from Ames, Iowa. Two asterisks (**) indicate a species sampled from both Ames and Stevens Point. In the latter case, the results were the same for both locations.
Nymphaeaceae: Nymphaea odorata Ait.; PIPERALES: Aristolochiaceae: Aristolochia macrophylla Lam., Asarum canadense L.; Saururaceae: Saururus cernuus L.; LAURALES: Calycanthaceae: Calycanthus floridus L.; MAGNOLIALES: Magnoliaceae: Magnolia stellata (Sieb. & Zucc.) Maxim.; ACORALES: Acoraceae: Acorus americanus (Raf.) Raf.; ALISMATALES: Alismataceae: Alisma triviale Pursh, Sagittaria latifolia Willd.; Araceae: Arisaema triphyllum (L.) Schott, Calla palustris L., Symplocarpus foetidus (L.) Salisb. ex Nutt.; Hydrocharitaceae: Elodea nuttallii (Planch.) St. John; Lemnaceae: Lemna minor L.; ASPARAGALES: Alliaceae: Allium fistulosum L.; Iridaceae: Gladiolus L., Iris germanica L., I. versicolor L.; Orchidaceae: Cypripedium reginae Walt.; DIOSCOREALES: Dioscoreaceae: Dioscorea villosa L.; LILIALES: Liliaceae: Aletris farinosa L., Convallaria majalis L., Maianthemum canadense Desf., Narcissus pseudonarcissus L., Uvularia sessilifolia L., Yucca filamentosa L.; Smilacaceae: Smilax lasioneura Hook.; POALES: Cyperaceae: Carex intumescens Rudge, C. lacustris Willd., Cyperus esculentus L., Eleocharis ovata (Roth) Roemer & J.A. Schultes; Juncaceae: Luzula acuminata Raf., L. multiflora (Ehrh.) Lej.; Poaceae: Glyceria canadensis (Michx.) Trin., Leersia oryzoides (L.) Sw., Miscanthus sacchariflorus (Maxim.) Franch., Panicum miliaceum L., Phalaris arundinacea L., Spartina pectinata Link, Zizania aquatica L.; Sparganiaceae: Sparganium eurycarpum Engelm. ex Gray; Typhaceae: Typha latifolia L.; COMMELINALES: Commelinaceae: Commelina communis L., Tradescantia bracteata Small ex Britt., Scirpus acutus Muhl. ex Bigelow, S. atrocinctus Fern.; Pontederiaceae: Pontederia cordata L.; ZINGIBERALES: Cannaceae: Canna generalis L.H. Bailey; CERATOPHYLLALES: Ceratophyllaceae: Ceratophyllum demersum L.; RANUNCULALES: Berberidaceae: Berberis thunbergii DC., Caulophyllum thalictroides (L.) Michx., Podophyllum peltatum L.; Menispermaceae: Menispermum canadense L.; Fumariaceae: Dicentra spectabilis (L.) Lem.; Ranunculaceae: Cimicifuga racemosa (L.) Nutt., Clematis virginiana L., Ranunculus abortivus L., R. acris L., Thalictrum dasycarpum Fisch. & Ave-Lall.; Buxaceae: Buxus microphylla Sieb. & Zucc., Pachysandra terminalis Sieb. & Zucc.; CARYOPHYLLALES: Amaranthaceae: Amaranthus retroflexus L.; Caryophyllaceae: Cerastium nutans Raf., Gypsophila paniculata L., Moehringia lateriflora (L.) Fenzl, Myosoton aquaticum (L.) Moench, Saponaria officinalis L., Silene latifolia Poir.; Chenopodiaceae: Beta vulgaris L., Chenopodium album L.; Droseraceae: Drosera rotundifolia L.; Molluginaceae: Mollugo verticillata L.; Nyctaginaceae: Mirabilis nyctaginea (Michx.) MacM.; Polygonaceae: Polygonum pensylvanicum L.*, P. virginianum L., Rumex acetosella L., R. crispus L.; Portulacaceae: Portulaca oleracea L.; SANTALALES: Santalaceae: Comandra umbellata (L.) Nutt.; SAXIFRAGALES: Cercidophyllaceae: Cercidophyllum japonicum Sieb. & Zucc.; Crassulaceae: Sedum aizoon L.; Grossulariaceae: Ribes alpinum L.; Haloragaceae: Myriophyllum spicatum L.; Hamamelidaceae: Hamamelis virginiana L.; Saxifragaceae: Chrysosplenium americanum Schwein. ex Hook., Saxifraga pensylvanica L.; Vitaceae: Parthenocissus quinquefolia (L.) Planch., Vitis labrusca L.; CROSSOSOMATALES: Staphyleaceae: Staphylea trifolia L.; GERANIALES: Geraniaceae: Geranium maculatum L.; MYRTALES: Lythraceae: Decodon verticillata (L.) Ell., Lythrum salicaria L.; Onagraceae: Circaea lutetiana L., Epilobium angustifolium L., Oenothera fruticosa L.; CELASTRALES: Celastraceae: Celastrus orbiculatus Thunb., Euonymus atropurpurea Jacq.; MALPIGHIALES: Clusiaceae: Hypericum kalmianum L., H. perforatum L.; Euphorbiaceae: Acalypha virginica L., Euphorbia corollata L., E. polychroma Kerner, Ricinus communis L.; Linaceae: Linum usitatissimum L.; Salicaceae: Populus deltoides Bartr. ex Marsh.*, P. xcanadensis Moench, P. tremuloides Michx., Salix babylonica L., S. petiolaris Sm.; Violaceae: Viola sororia Willd., V. tricolor L.; OXALIDALES: Oxalidaceae: Oxalis stricta L.; FABALES: Fabaceae: Amphicarpaea bracteata (L.) Fern., Baptisia alba (L.) Vent.*, B. tinctoria (L.) R.Br. ex Ait.f., Desmodium glutinosum (Muhl. ex Willd.) Wood, Gleditsia triacanthos L., Gymnocladus dioicus (L.) K. Koch, Lathyrus venosus Muhl. ex Willd., Lotus corniculatus L., Lupinus perennis L., Maackia amurensis Rupr. & Maxim., Robinia pseudoacacia L., Trifolium arvense L., T. campestre Schreb., Vicia americana Muhl. ex Willd., V. villosa Roth; Polygalaceae: Polygala paucifolia Willd.; ROSALES: Cannabaceae: Humulus lupulus L.; Elaeagnaceae: Elaeagnus commutata Bernh. ex Rydb.; Moraceae: Morus alba L.; Rhamnaceae: Rhamnus cathartica L.; Rosaceae:Amelanchier arborea (Michx.f.) Fern., Filipendula rubra (Hill) B.L. Robins., Fragaria virginiana Duchesne, Geum canadense Jacq., Malus pumila P. Mill.**, Neviusia alabamensis Gray, Potentilla arguta Pursh, P. recta L., Prunus tomentosa Thunb., Rhodotypus scandens (Thunb.) Makino, Rosa glauca Pourr., R. rugosa Thunb., Rubus allegheniensis Porter, R. hispidus L., R. idaeus L., Sorbaria sorbifolia (L.) A. Braun, Spiraea japonica L.f., S. tomentosa L., S. xvanhouttei (Briot) Zab.; Ulmaceae: Ulmus americana L.; Urticaceae: Boehmeria cylindrica (L.) Sw., Urtica dioica L.; CUCURBITALES: Cucurbitaceae: Cucurbita pepo L., Echinocystis lobata (Michx.) Torr. & Gray; FAGALES: Betulaceae: Alnus glutinosa (L.) Gaertn., A. incana (L.) Moench, Betula papyrifera Marsh., B. utilis D. Don, Carpinus caroliniana Walt.; Fagaceae: Castanea dentata (Marsh.) Borkh.,Quercus alba L., Q. imbricaria Michx., Q. rubra L.; Juglandaceae: Carya cordiformis (Wangenh.) K. Koch, Juglans cinerea L.; Myricaceae: Comptonia peregrina (L.) Coult.; BRASSICALES: Brassicaceae: Arabis lyrata L., Armoracia rusticana P.G. Gaertn., B. Mey. & Scherb., Barbarea vulgaris Ait. f., Berteroa incana (L.) DC., Capsella bursa-pastoris (L.) Medik., Sisymbrium altissimum L.; MALVALES: Cistaceae: Helianthemum canadense (L.) Michx.; Thymelaeaceae: Dirca palustris L.; Tiliaceae: Tilia americana L.; SAPINDALES: Aceraceae:Acer cissifolium (Sieb. & Zucc.) K. Koch, A. platanoides L., A. rubrum L.; Anacardiaceae: Rhus aromatica Ait., R. hirta L.; Hippocastanaceae: Aesculus glabra Willd.; Rutaceae: Phellodendron amurense Rupr., Zanthoxylum americanum P. Mill.; EUASTERIDS I: Boraginaceae: Lithospermum canescens (Michx.) Lehm, Myosotis laxa Lehm., Pulmonaria officinalis L.; Hydrophyllaceae: Hydrophyllum virginianum L.; CORNALES: Cornaceae: Cornus canadensis L.; Hydrangeaceae:Hydrangea arborescens L.; ERICALES: Balsaminaceae: Impatiens capensis Meerb.; Empetraceae: Empetrum nigrum L.; Ericaceae: Oxydendrum arboreum (L.) DC.,Vaccinium angustifolium Ait.; Monotropaceae: Monotropa uniflora L.; Polemoniaceae: Phlox paniculata L.; Primulaceae: Lysimachia quadrifolia L., Trientalis borealis Raf.; Pyrolaceae: Pyrola elliptica Nutt.; Sarraceniaceae: Sarracenia purpurea L.; Styracaeae: Halesia carolina L.; GENTIANALES: Apocynaceae: Apocynum androsaemifolium L.; Asclepiadaceae: Asclepias incarnata L., A. syriaca L.*, A. tuberosa L.;: Gentianaceae: Gentiana andrewsii Griseb.; Rubiaceae: Cephalanthus occidentalis L., Galium triflorum Michx., Houstonia longifolia Gaertn., Mitchella repens L.; LAMIALES: Acanthaceae: Ruellia humilis Nutt.; Bignoniaceae: Catalpa speciosa (Warder) Warder ex Engelm.; Lamiaceae: Glechoma hederacea L., Lamium maculatum L., Leonurus cardiaca L., Lycopus americanus Muhl. ex W. Bart., Nepeta cataria L., Prunella vulgaris L., Stachys tenuifolia Willd., Teucrium canadense L.; Lentibulariaceae: Utricularia vulgaris L.; Oleaceae: Chionanthus virginicus L.; Plantaginaceae: Plantago rugelii Decne.; Scrophulariaceae: Digitalis grandiflora P. Mill., Linaria vulgaris P. Mill., Nuttalanthus canadensis (L.) D.A. Sutton, Pedicularis canadensis L., P. lanceolata Michx., Scrophularia lanceolata Pursh, Verbascum blattaria L., V. thapsus L., Veronica scutellata L., Veronicastrum virginicum (L.) Farw.; Verbenaceae:Phryma leptostachya L., Verbena hastata L.; SOLANALES: Convolvulaceae: Calystegia sepium (L.) R. Br.; Solanaceae: Lycopersicon esculentum Mill., Solanum dulcamara L., S. nigrum L.; AQUIFOLIALES: Aquifoliaceae: Ilex verticillata (L.) Gray; APIALES: Apiaceae: Aegopodium podagraria L., Cicuta maculata L., Heracleum maximum Bartr., Levisticum officinale W.D.J. Koch, Sanicula marilandica L., Sium suave Walt., Zizia aurea (L.) W.D.J. Koch; Araliaceae: Aralia elata (Miq.) Seem., A. nudicaulis L.; ASTERALES: Asteraceae: Achillea millefolium L., Ambrosia psilostachya DC., A. trifida L.*, Arctium minus Bernh.*, Artemisia campestris L., A. ludoviciana Nutt.**, Aster umbellatus P. Mill., Cirsium arvense (L.) Scop., C. muticum Michx., C. vulgare (Savi) Ten., Conyza canadensis (L.) Cronq.**, Coreopsis lanceolata L., Crepis tectorum L., Dahlia coccinea Cav., Erigeron annuus (L.) Pers.*, E. strigosus Muhl. ex Willd., Eupatorium perfoliatum L., Euthamia graminifolia (L.) Nutt., Gnaphalium obtusifolium L., Helianthus annuus L.**, H. giganteus L., H. tuberosus L., Heliopsis helianthoides (L.) Sweet, Hieracium piloselloides Vill., Krigia biflora (Walt.) Blake, Lactuca biennis (Moench) Fern., L. floridana (L.) Gaertn.*, L. serriola L.*, Leucanthemum vulgare Lam., Liatris ligulistylis (A. Nels.) K. Schum.*, Matricaria discoidea DC., Prenanthes alba L.**, Rudbeckia laciniata L.*, R. triloba L., Silphium perfoliatum L.*, Solidago canadensis L.*,S. gigantea Ait., S. juncea Ait., S. rugosa P.Mill., Tanacetum balsamita L., T. vulgare L., Tragopogon dubius Scop., Zinnia elegans Jacq.; Campanulaceae: Campanula glomerata L., Platycodon grandiflorum (Jacq.) A. DC.; DIPSACALES: Caprifoliaceae: Lonicera sempervirens L., L.xbella Zabel, Sambucus canadensis L., S. racemosa L., Symphoriocarpus albus (L.) Blake, Viburnum lentago L.; Valerianaceae: Valeriana officinalis L.; Weigela florida (Bunge) A. DC.
This survey, to determine the presence of oil bodies in the mesophyll of leaves of 113 angiosperm families, represented by 302 species, was conducted in two locations (Wisconsin and Iowa) and used species that were available. Therefore, the results obtained were not intended to be a systematic collection of species with the aim of uncovering any phylogenetic relationships, even though the species collected and analyzed were from a relatively large number of families. With this caveat, no statistical analyses can be conducted nor is it appropriate to draw systematic conclusions using a cladogram (Fig. 9) of these families and genera. Figure 9, however, provides a distribution of taxa containing oil bodies using the presently accepted APG cladogram (APG, 2003
). The following percentages provide a general impression of the presence of oil bodies observed in the mesophyll of leaves of the species studied: 22.3% of the 113 families had one or more species with oil bodies; and of the 302 species in these families, 23.7% had oil bodies. Of the magnoliid and eudicot families, 22.2% had oil bodies, whereas only 15.8% of the monocot families had them. Of the 213 magnoliid and eudicot species, 24.5% had oil bodies, whereas only 7.3% of the 41 monocot species had them.
Five eudicot families (with 3–44 species each) displayed relatively high percentages of oil bodies: Asclepiadaceae (3 spp.) = 100%; Asteraceae (44 spp.) = 63.6%; Fagaceae (4 spp.) = 100%; Lamiaceae (8 spp.) = 87.5%; and Rosaceae (19 spp.) = 42.1%. Only one monocot family showed a high percentage of oil bodies, the Iridaceae (3 spp.) = 66.7%.
DISCUSSION
The significance of this study is that our literature overview and original, live species survey have revived knowledge of a largely forgotten feature of angiosperm anatomy, that oil bodies are a characteristic feature of leaf mesophyll cells (palisade and spongy parenchyma) in many angiosperms. The surveys by Lidforss (1893)
and Petit (1901, 1902), as well as our present one on 113 families and 302 species of angiosperms, also support a hypothesis that oil bodies are more common in magnoliids and eudicots (24.5%) than in monocots (7.3%) surveyed. We emphasize, however, that virtually all observations so far have been on temperate-zone species. If the far more numerous subtropical and tropical angiosperms were surveyed, different results might emerge in terms of the numbers, sizes, and relative abundance of oil bodies observed in mesophyll cells.
Our survey, along with those mentioned previously, provides an outline of the distribution of oil bodies among angiosperm leaves. However, more frequent and detailed observations over various times of day, months of the growing season, and different weather, geographical, and environmental conditions are needed to determine the constancy of oil bodies in a given species reported to have them. In addition, observations are needed as to whether oil bodies ever occur in species reported to lack them, under variations of the conditions just mentioned.
Our observations of the retention of oil bodies in leaves of two angiosperm species up to the end of the growing season, and even after leaves were shed, appear to be the first reports of such a phenomenon in eudicots. Parker and Murphy (1981)
reported oil body retention in the flag leaf of wheat into senescence. What this means in terms of the possible functional role(s) of oil bodies in the life of a plant organ cannot be speculated on at this time without further observations and experimentation.
Oil bodies in mesophyll cells can occupy as much as an estimated 15% of cell volume, depending on the species. It is possible that the mesophyll oil bodies of species now grown for their seed oils are identical to the seed oil bodies (oleosomes), and therefore leaves of these species could be processed to add to the overall yield of the plant. Some species with only leaf mesophyll (vs. seed) oil bodies might provide enough oil to make them commercially useful, depending on the chemical composition of the oil and the ease of extraction. These possibilities are worth pursuing given the importance of seed oils.
Finally, the issue of the use of the term oleosome vs. oil body still requires further histochemical, biochemical, and ultrastructural study with regard to identifying the presence or absence of a boundary around them composed of a unit membrane or other partial lipid–protein interfaces. Also, the size range and origin(s) of these foliar oil bodies is/are still speculative as is the nature of their chemical composition. This study and the previous reports we have cited, however, provide a better understanding of the variety of taxa in which these oil bodies (or oleosomes) are either present or absent and the possibility that some may become sources for potential commercial use and further study.
FOOTNOTES
1 The authors thank S. Szczytko, University of Wisconsin-Stevens Point (UWSP), for technical assistance and advice. The authors especially thank Ms. Anna Gardner (in memoriam) for modifying the APG phylogenetic tree (Fig. 9). Specimen preparations and oil body analyses were done at UWSP, and light microscopy was done at UWSP and the Bessey Microscopy Facility, Iowa State University (ISU). The study was funded in part by a UWSP Personal Development Committee grant to J.D.C. and R.F. Partial support was also provided by the Dept. of Ecology, Evolution and Organismal Biology and Genetics and Dept. of Development and Cell Biology at ISU. 
2 Author for correspondence (e-mail: hth{at}iastate.edu
)
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