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Invited Special Paper |
2Department of Plant Biology, Cornell University, Ithaca, New York 14853 USA 3Electron Microscopy Services and Consultants, 18407 North 12th Place, Phoenix, Arizona 85022 USA 4L. H. Bailey Hortorium, Department of Plant Biology, Cornell University, Ithaca, New York 14853 USA
Received for publication December 8, 2000. Accepted for publication March 22, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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; Turgeon, 2000
). Loading is an important factor in carbon partitioning (Lucas and Wolf, 1999
; Hellmann et al., 2000
; Pego et al., 2000
); it is sensitive to abiotic stress factors such as ozone (Körner, Pelaez-Reidl, and van Bel, 1995
; Grantz and Yang, 2000
), elevated CO2 (Baxter and Farrar, 1999
; Grimmer and Komor, 1999
), sulfur dioxide (Maurousset et al., 1992
), chilling (Pawel, 1999
), mineral deficiency (Cakmak et al., 2000
), and mineral toxicity (Herren and Feller, 1997
). Loading also defines the interfaces that viruses must cross in order to enter the phloem and become systemic (Leisner and Turgeon, 1993
; Lazarowitz and Beachy, 1999
; Santa-Cruz, 1999
; Cheng et al., 2000
). Given the importance of phloem loading we should, at a minimum, be able to predict its basic properties in plants of interest. However, the distribution of loading mechanisms in various plant groups is not well understood.
There are at least two loading mechanisms. One involves passage of photoassimilate through the apoplast, followed by active uptake into the sieve elements and companion cells of the minor veins (van Bel, 1993
; Grusak, Beebe, and Turgeon, 1996
; Lalondale et al., 1999
). The second mechanism is entirely symplastic, through the plasmodesmata-connected cytoplasm, all the way from the mesophyll to the sieve elements (Turgeon, 1996, 2000
).
Since structure is often a meaningful guide to function, the comparative anatomy of minor veins should yield clues to the mechanisms of phloem loading in different plants. In this regard, plasmodesmatal frequency has been studied closely as a potential indicator of the presence, or absence, of symplastic loading. Most attention has been paid to the symplastic connections of companion cells because sieve elements typically have very few plasmodesmata joining them to any other cell but their companion cell. Much of the available information on plasmodesmatal frequency in minor vein companion cells comes from an extensive survey by Gamalei (1989, 1991)
.
Gamalei groups plants into three types, based on the relative frequency of plasmodesmata joining minor vein companion cells to surrounding cells (Gamalei, 1989
). According to this scheme, plasmodesmata are abundant (Type 1), relatively abundant (Type 1–2a), or infrequent (Type 2), varying over three orders of magnitude (Gamalei, 1991
).
Minor vein companion cells may also be grouped on the basis of morphological specialization. In some species, they are "transfer cells" with wall ingrowths (Pate and Gunning, 1969
), while in others they are "intermediary cells" with especially numerous and unevenly branched plasmodesmata linking them to the bundle sheath (Turgeon, 1996
). Companion cells without such specialized features, regardless of the number of plasmodesmata, are often called "ordinary" companion cells.
Phylogenetic analysis could help in clarifying the relationships of different phloem types, which are usually family traits (Gamalei, 1989, 1991
). Until recently this has been problematic because the evolutionary relationships of families in the angiosperms have been difficult to resolve. However, in the past few years, several phylogenetic treatments based on multiple nucleotide sequences of nuclear and plastid genes have revolutionized the interpretation of angiosperm evolution (Mathews and Donoghue, 1999
; Parkinson, Adams, and Palmer, 1999
; Qiu et al., 1999
; Soltis et al., 2000
). The conclusions reached in these analyses are in reasonable agreement.
We began this study by adding to the available data set on intermediary cells. To do this we studied the ultrastructure of the minor veins in two members of the Celastraceae, Euonymus fortunei and Celastrus orbiculatus. This family was chosen because its members have minor vein companion cells with plentiful plasmodesmata (Gamalei, 1989
) and they translocate a considerable amount of raffinose and stachyose (Zimmermann and Ziegler, 1975
), a consistent feature of species with intermediary cells (Turgeon, Beebe, and Gowan, 1993
). The presence of intermediary cells was confirmed. These species were then added to the list of plants exhibiting the intermediary cell trait, and the accumulated data on companion cell types, primarily from the papers of Gamalei (1989, 1991)
and Pate and Gunning (1969)
, were mapped to the phylogenetic tree of Soltis et al. (2000)
. The analysis indicates that intermediary cells have at least four independent points of origin. The structural evolution of minor vein phloem and the evolution of phloem loading mechanisms are discussed.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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Microscopy
Leaf tissue was fixed in 4% glutaraldehyde in 100 mmol/L sodium cacodylate buffer, pH 7.2, for 4 h at 4°C. Fixed tissue was washed in buffer and post-fixed overnight in 1% OsO4 in the same buffer at 4°C. Tissue was then dehydrated in a graded ethanol series at 4°C and embedded in either Spurr or Epon-Araldite resin (Electron Microscopy Sciences, Ft. Washington, Pennsylvania, USA). Thin sections for electron microscopy were stained with uranyl acetate and lead citrate and photographed at 60 kV with a Philips (Eindhoven, The Netherlands) EM-300 transmission electron microscope.
Carbohydrate synthesis and transport
A clear plastic bag was fitted around a mature leaf and sealed with tape. The leaf was exposed for 3 min to 14CO2 (1.0 MBq), generated in a syringe by adding an excess of 80% lactic acid to Na214CO3 (6.6 x 105 MBq/mmol). Prior to labeling, sink tissue (immature stem) was covered with aluminum foil to prevent photosynthetic uptake of inadvertently leaked gas. The labeled leaf and the sink tissue were removed following a 45-min chase in unlabeled air and quickly frozen in powdered dry ice.
Tissue was ground in liquid N2 and soluble carbohydrates were extracted in a mixture of methanol, chloroform, and water (12 : 5 : 3; v/v/v). Aqueous and nonaqueous phases were separated by addition of water, as described previously (Beebe and Turgeon, 1992
). The neutral fraction was obtained from the aqueous phases by passing it through anion and cation exchange resins (Haritatos, Ayre, and Turgeon, 2000
). The neutral fraction was taken to dryness in a heating block at 70°C under a stream of N2. Samples were rehydrated in water, spotted on silica plates, and radioactive compounds were identified by two-dimensional thin-layer chromatography as previously described (Turgeon and Gowan, 1992
). Spots were scraped from the plates and counted in Ecoscint scintillation solution (National Diagnostics, Atlanta, Georgia, USA).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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; Turgeon, Webb, and Evert, 1975
) and is now known to occur in many families. As in other species with this cell type, the intermediary cells of E. fortunei veins are located at the periphery of the vein, in contact with bundle sheath cells (Fig. 1A). They have small vacuoles and rudimentary plastids. They form the abaxial border of larger veins, and their associated, and much smaller, sieve elements are located toward the inside. There is one intermediary cell per sieve element. Phloem parenchyma cells are also present.
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Following exposure to 14CO2, radiolabeled sucrose, galactinol, raffinose, stachyose, and verbascose are synthesized in source leaf tissue (Fig. 2). Most of the label in the neutral fraction is in sucrose. In the immature stem (sink tissue), a higher percentage of the imported label is in raffinose and stachyose, the compounds predominately translocated in species with intermediary cells. This is to be expected if sucrose entering intermediary cells is used in the synthesis of raffinose and stachyose prior to export (Turgeon, 1996
). Note that galactinol is not transported, a consistent feature of translocation in species with intermediary cells (Turgeon, 1996
).
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Phylogenetic distribution and evolution of companion cell types
An evaluation of the phylogenetic distribution of companion cells is useful in many contexts, for example in comparative studies that determine the possible origins and adaptive significance of the different types. We coded the anatomical features of minor vein companion cells in a cladistic matrix, identifying the following types of companion cells as characters (see Appendix): Types 1, 1–2a, 2a, according to Gamalei's definitions; transfer cells (Gamalei's Type 2b); and intermediary cells. Because the term "intermediary cell" has been used inconsistently in the literature, we assigned this character only on the basis of published electron micrographs or drawings. Gamalei's Type 2c (kranz anatomy) was not included in the present analysis because this character, defined as it is by the association of mesophyll cells with the bundle sheath, is not directly relevant to companion cell structure or the mechanism(s) of phloem loading. In most cases the assignment to types was clear, but in others judgments were necessary when comparing results from different laboratories. Interpretation of plasmodesmatal counts is difficult (Fisher, 1990, 1991
; Botha, 1992
) and is complicated by the limited data given in some papers.
While all genera were classified here as belonging to a single type, there are many examples of multiple-companion cell types within the minor veins of a single species. In many plants with intermediary cells, such as Euonymus fortunei (Fig. 1A) and Coleus blumei (Fisher, 1986
), the minor veins also have an "ordinary" companion cell that corresponds to Type 2a. Intermediary cells are found with transfer cells in single veins of Acanthus mollis (van Bel et al., 1992
). These combinations of cell types are also present in members of the Scrophulariaceae; Asarina scandens even has modified intermediary cells with transfer-cell-wall ingrowths and reduced plasmodesmatal numbers (Turgeon, Beebe, and Gowan, 1993
). Such variety in companion cell types has fueled reasonable speculation that more than one mechanism of phloem loading can operate within a given species, either simultaneously or at different times. In the present study, intermediary-cell or transfer-cell characteristics were given precedence and coded if these cells were present with other cell types.
The cladistic matrix was mapped onto a well-supported phylogenetic tree. The recent three-gene analysis of angiosperm taxa (Soltis et al., 2000)
including 567 selected angiosperm species was used for this purpose. Shortest trees for the matrix were found using the parsimony ratchet (Nixon, 1999
) in <36 h as implemented in Winclada (Nixon, 2000
) using Nona (Goloboff, 1999) as the tree search engine. Efforts with PAUP failed to discover shortest trees after months of analysis (Soltis et al., 2000
). A large set of shortest trees generated by ratchet analyses was used to generate a strict consensus tree with Winclada. The companion cell character was added to the 3-gene 567-taxon matrix, and taxa for which data were not available or uncertain were scored as missing. Wherever possible, genera for which phloem anatomy is known were coded directly in the matrix, but for some representatives there was no equivalent genus in the molecular matrix. In some of these cases, as discussed below, a closely related confamilial genus was coded for the phloem character (Appendix). While subject to revision as more phloem data are added, this is a conservative approach because it can only overestimate the number of origins of the types, not underestimate them. All taxa scored as missing for the phloem loading character were then automatically pruned from the consensus tree within Winclada, producing a tree topology for 135 taxa that is a fully congruent subset of the topology with all taxa. The phloem character was then mapped onto selected trees using unambiguous optimization (all possible states assigned to each node, so that only character changes that occur under all possible optimizations are shown), and each state character state assignment mapped as a different color (Fig. 3). Alternative optimizations ("fast" = ACCTRAN and "slow" = DELTRAN) were also evaluated and compared, but due to space limitations are not presented here.
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Type 1
Abundant plasmodesmata in minor vein companion cells (Type 1) is parsimoniously interpreted as the ancestral condition in conifers and angiosperms. Although there is ambiguity in the magnoliid clade when we analyze the molecular matrix under conservative optimization (Fig. 3), this is not the case with "slow" (DELTRAN) optimization (not shown). Therefore, we defer to Gamalei's conclusion, based on analysis of the Takhtajan system (Gamalei, 1989, 1991
), that Type 1 is ancestral, because his data set includes many genera not represented in the present analysis.
It should be noted that, from a typological perspective, comparisons of plasmodesmatal frequencies in the phloem of angiosperms and conifers is problematic: in the conifers, parenchymatous elements associated with sieve elements are Strasburger (albuminous) cells, not true companion cells. Strasburger cells are unlike true companion cells of angiosperms in that they are rarely derived from a common mother cell with the sieve element (Schulz, 1990).
Although Type 1 is distributed broadly throughout the angiosperms, most occurrences can be explained as retentions from the base of the angiosperm clade. However, there are at least two independent origins in the Salicaceae and the "Fagales" clade (in the broad sense, including Betulaceae, Juglandaceae, etc.; previously often called the "Higher Hamamelididae" [see Nixon, 1989
]).
While Type 1 companion cells are apparently ancestral in the angiosperms, this does not necessarily mean that symplastic phloem loading is also ancestral. There is no compelling reason to believe that the phloem loading mechanism is predicted solely by plasmodesmatal frequency. Most of the physiological evidence for symplastic phloem loading has been derived from plants with intermediary cells (Turgeon, 1996
). Loading in Aucuba (Type 1) is insensitive to the sucrose transport inhibitor p-chloromercuribenzenesulfonic acid, indicating a symplastic pathway (Hoffmann-Thoma, van Bel, and Ehlers, 2001
), but Liriodendron tulipifera, also a Type 1 plant, loads from the apoplast (Goggin, Medville, and Turgeon, 2001
). Clearly, more work is required to determine the nature of phloem loading in ancestral angiosperms.
Intermediary cells
Intermediary cells have at least four independent points of origin (Olea/Verbascum clade, cucurbits, Hydrangea clade, and Euonymus [this paper]). The precursor of intermediary cells in the Hydrangea clade is Type 1. The precursor in the Olea/Verbascum clade is ambiguous, based on current data, but it could be from Type 1. In contrast, the other two known groups with intermediary cells are derived on the molecular tree from Type 1–2a, which have substantially fewer plasmodesmata than either Type 1 companion cells or intermediary cells. Minimally, intermediary cells are not a specialized form of Type 1 in all cases, even though both have abundant plasmodesmata. In an evolutionary context, intermediary cells should not be considered a subtype of Type 1.
Because all species known to translocate large amounts of raffinose and stachyose have intermediary cells, it is a reasonable assumption that the presence of this cell type will be confirmed in other families by examining Type 1 plants that translocate these sugars in quantity (Zimmermann and Ziegler, 1975
). Such families include the Bignoniaceae, Buddleiaceae, Clethraceae, and Juglandaceae.
Confirmation that members of the Bignoniaceae and Buddleiaceae have this character would unify almost the entire Olea/Verbascum clade. Confirmation that members of the Juglandaceae and Clethraceae have intermediary cells would indicate at least two more points of origin.
Type 1–2a
With some exceptions, there is a general tendency throughout the angiosperms for reduction in plasmodesmatal numbers, rather than a gain. For example, Type 1–2a (moderate numbers of plasmodesmata) is derived in all major clades. In almost all cases the precursor state is ambiguous but the derivation is generally from Type 1 with "slow" optimization (not shown). The tree provides an indication of which taxa need to be sampled in order to determine whether there is a pattern in the origins of this type.
Type 2a
"Ordinary" companion cells originate from many sources: Type 1 (Nelumbo, Exacum), 1–2a (Ailanthus, Cneorum), transfer cells (Digitalis), and intermediary cells (Pinquilla). Although this almost always involves loss of plasmodesmata numbers, derivation from transfer cells, which typically have fewer plasmodesmata than "ordinary" companion cells, indicates that plasmodesmata frequency can also increase.
Not all genera with Type 2a companion cells are shown as such in the present analysis. As discussed above, Type 2a companion cells are commonly found in the same veins with intermediary cells. In addition, some genera (e.g., Plantago; Gamalei, 1989
) have species with either transfer cells or Type 2a cells; they are listed here as having the former.
Type 2a is generally thought to be common in crop plants and for that reason considerable effort has been devoted to studying the physiology and molecular biology of apoplastic loading. However, because there are many independent points of origin of Type 2a companion cells, caution should be exercised in extrapolating conclusions derived from any one model species (e.g., Nicotiana tabacum) to other Type 2a plants.
Few of the monocot species in the phylogenetic analysis of Soltis et al. (2000)
have been studied by phloem anatomists. Nevertheless, some tentative conclusions are possible. The sieve element-companion cell complexes of Zea (Evert, Eschrich, and Heyser, 1978
) and Oryza (Chonan, Kawahara, and Matsuda, 1985
) have few plasmodesmatal connections to surrounding cells and can thus be classified as Type 2a. Other monocot species have been examined, especially grasses, and all are similar in the relative symplastic isolation of the conducting cells in minor vein phloem (both thick- and thin-walled sieve tubes: Kuo, O'Brien, and Canny, 1974
; Robinson-Beers and Evert, 1991
; Botha and van Bel, 1992
; Botha and Cross, 1997
). Exceptions to this rule are Commelina (van Bel, van Kesteren, and Papenhuijzen, 1988
) and members of the Arecaceae (Gamalei, 1989
), which are Type 1–2a. (Tradescantia is substituted in our analysis for Commelina.)
Transfer cells
The defining characteristic of transfer cells is the presence of wall ingrowths (Pate and Gunning, 1969
). They typically have few plasmodesmatal connections to surrounding cells. Transfer cells correspond to Gamalei's Type 2b (Gamalei, 1989
).
Two types of transfer cells, A-Type and B-Type, have been identified in the phloem of minor veins (Pate and Gunning, 1969
). A-type are companion cells; wall ingrowths in these cells enhance phloem loading by increasing the capacity for uptake of photoassimilate from the apoplast (Wimmers and Turgeon, 1991
).
The role of B-type transfer cells has not been firmly established. We noted in a study of Arabidopsis (Haritatos, Medville, and Turgeon, 2000
) that B-type transfer cells are phloem parenchyma cells and speculated that the most likely role for the ingrowths is to enhance photoassimilate secretion—not uptake—into the apoplast in the vicinity of the sieve elements and companion cells. Therefore it seems prudent to make a distinction between the two transfer cell types, excluding B-type in the present analysis, which focuses on companion cells and phloem loading (uptake) mechanisms. The only plants from the Gamalei data set that are included in this phylogenetic analysis are A-type (as confirmed by B. E. S. Gunning, Australian National University, Canberra, Australia). None of the four monocot genera listed as having transfer cells by Gamalei (1989)
are included. This seems especially judicious given that one of them (Zostera) has B-Type, but not A-type transfer cells (Barnabus, Butler, and Steinke, 1986
).
Since A-type transfer cells and Type 2a companion cells generally have few plasmodesmata joining them to surrounding cells, it might be reasonable to deduce, on typological grounds, that the former derived from the latter by evolving wall ingrowths that make loading from the apoplast more efficient (Gamalei, 1989
). However, in the phylogenetic analysis the transfer-cell character derives rarely, if ever, from Type 2a. There are many independent points of origin of transfer cells. In several cases the derivation is ambiguous, but it may have occurred from Type 1 (Impatiens) and has more obviously occurred from Type 1–2a (Helianthemum, Linum). Furthermore, minor vein companion cells of Tamarix have transfer-cell-wall ingrowths (B. E. S. Gunning, Australian National University, Canberra, Australia, personal communication) and also have relatively abundant plasmodesmata (Type 1–2a; Gamalei, 1989
). The same combination of characters is found in Sonchus (Fisher, 1991
). Just as intermediary cells should not be considered a subtype of Type 1, transfer cells should not necessarily be considered a subtype of Type 2a in the evolutionary sense.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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Phylogenetic analysis also provides clues to the adaptive significance of specific traits. For example, transfer cells have many independent points of origin in derived groups, signifying that they have evolved, or have been lost, relatively quickly in response to environmental conditions or changes in growth habit. On the other hand, Type-1 companion cells are ancestral and found widely in entire lineages, indicating that the trait more often reflects shared evolutionary history than it does recent adaptation.
In this regard it is worth noting the unusual finding that Salix babylonica, a Type-1 species (Gamalei, 1989
), exhibits none of the typical characteristics of phloem loading (Turgeon and Medville, 1998
). This is the only plant in which the absence of phloem loading has been documented. Since Type 1 is basal in the angiosperms, it could be concluded that the absence of phloem loading is also ancestral (Turgeon and Medville, 1998
). However, our analysis indicates that Type 1 in Salix is a derived condition. Therefore, there is no a priori reason to believe that the absence of phloem loading is widespread.
As these examples indicate, framing ecophysiological questions in an evolutionary context provides a rational basis for the study of phloem structure and phloem loading.
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FOOTNOTES |
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5 Author for correspondence (ert2{at}cornell.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSLITERATURE CITED |
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