*Department of Biology, Portland State University, Portland, OR and Department of Integrative Biology, University of California, Berkeley, CA, respectively; contributed as Environmental Sciences and Resources Program Publication No. 290.
The dwarf mistletoes, Arceuthobium, are widely recognized as the most highly specialized of the 7 genera comprising the family Viscaceae. Within the genus, evolutionary specialization has affected the haustorial system (endophytic system) and the shoot (ectophytic system) very differently. In general, the interface of the shoot with its environment has decreased over evolutionary time while that of the endophytic system has increased.
The specialized endophytic system of Arceuthobium is illustrated in several ways. First, the endophytic system is more highly developed than in related genera, and its haustorial processes more thoroughly permeate host tissues. To paraphrase Heinricher (1924), penetration power and efficiency of the absorbing system are superior to those of other Viscaceae. Second, individual sinkers do not retain their autonomy as in related genera but rather form a complex admixture of host and parasite cells (Alosi and Calvin 1984). This highly integrated unit produces a much more intimate association between parasite and host tissues. The unique character of this unit earns it the special name "infected ray" (Srivastava and Esau 1961b). Finally, dwarf mistletoes form not only localized infections but also systemic infections (Kuijt 1960b). Other mistletoes of the Viscaceae characteristically form only localized infections that show limited spread within the host branch. Systemic infections, in contrast, spread into the host’s shoot apices and advance acropetally as host shoots elongate (Baranyay and others 1971).
Understanding the full character of the endophytic system of Arceuthobium requires basic familiarity with the infection process, bark strand and sinker morphology and anatomy, distinction of host and parasite cells, and discrete roles of host and parasite. The relationship begins when the parasite’s seed contacts the host.
A generalized life cycle for Arceuthobium is shown in figure 2.5. To begin, seed are explosively discharged into the air (fig. 2.4). Seeds that strike host leaves adhere with viscin (fig. 2.10). Moistened viscin allows seeds to slide to leaf bases where they contact host branches and germinate. When the tip of a radicle contacts a host branch, a disk-like holdfast forms (fig. 2.11). As the holdfast enlarges, it becomes closely appressed to the branch. Sometimes, hyphae-like cells at the holdfast’s margin elongate and penetrate a short distance into the host bark. These elongate cells do not reach living tissues of the host but presumably help anchor the holdfast to the branch. Beneath the holdfast, a penetration wedge develops (fig. 2.12). This wedge of parasite tissue is comprised of either just procambium (Cohen 1963) or procambium and ground meristem (Scharpf and Parmeter 1967). Primarily by mechanical force, the wedge of parasite tissue penetrates the outer, protective layers of the stem and enters the living host tissue (Scharpf and Parmeter 1967). Successfully establishing a nutritional link to the host concludes the most tenuous phase of the parasite’s life cycle. (For more complete infection details, see Cohen 1963; Kuijt 1960b; Scharpf and Parmeter 1967.)
Once infection is accomplished, the holdfast and tissues distal to it wither and disappear. A gradual swelling at the site of infection provides the only early evidence that infection has occurred. Loss of aerial portions of the mistletoe seedling means that the first shoot does not develop from the plumular pole of the embryo. Instead, all shoots develop from endophytic portions of the plant. Using terminology Groff and Kaplan (1988) proposed, Arceuthobium can be described as forming only root-borne shoots. As far as is known, it is the only genus within Viscaceae that forms exclusively root-borne shoots. Developmental events in Arceuthobium are foreshadowed during embryogeny. The shoot apex of a mature embryo is poorly developed and vacuolate; cotyledons (usually 2) are minuscule. In contrast, the root pole of the embryo is enlarged, appears meristematic, and exhibits a complex pattern of zonation (Cohen 1963).
During incubation within the host branch (table 2.1), the complex haustorial system of Arceuthobium grows and develops. Although events occurring in the early stages are not well understood, certain features are recognized.
First, a mass of tissue derived from the penetration wedge grows radially through host tissues to the vascular cambium and establishes a position within the cambial cylinder. This multicellular, radially oriented structure, which initiates a meristematic zone contiguous with that of the host cambium, is the primary haustorium (fig. 11.1A). Second, from the sides of the primary haustorium and from the initial penetration wedge, discrete strands are initiated. They grow acropetally, basipetally, and circumferentially (fig. 11.1A) within the host bark (Alosi and Calvin 1984, Sadik and others 1986a). Known as "bark strands" (also as "longitudinal strands" and "cortical strands"), they establish the basic framework for the endophytic system (Srivastava and Esau 1961b). Third, bark strands produce "sinkers" ("secondary haustoria") that grow radially to the vascular cambium (fig 11.1A). As a final stage of initial growth, the parasite differentiates into either a localized or a systemic infection type. A brief review of the salient features of localized and systemic infections will help clarify endophytic system morphology.
Localized infections, as the name implies, are contained within a limited section of host branch. The infected area usually develops a fusiform swelling (fig. 6.4) from hypertrophy and hyperplasia of host tissues and from the expanding parasite. The extent of branch swelling correlates with the extent of axial spread of the developing endophytic system (Shea 1957). In Arceuthobium campylopodum, the endophytic system was not observed in host tissue 3 cm beyond the area of swelling (Scharpf 1962). Generally, the basipetal spread of infections is about one-third greater than the acropetal spread (Hawksworth 1960b). A consistently greater basipetal spread of infections has also been observed in Phoradendron (Calvin and others 1991) and may be a general rule in localized infections. Production of shoots in localized infections is confined to swollen regions, and shoots occur in random tufts. All Arceuthobium species are capable of developing localized infections on appropriate hosts (Kuijt 1960b).
Systemic infections involve entire branches. Infections extend acropetally into regions of stem having only primary growth and even into buds (Thoday and Johnson 1930, Kuijt 1960b). The extent of basipetal spread of systemic infections remains problematic (Hawksworth 1960a,b); but it is generally considered to be somewhat less than acropetal spread (Kuijt 1960b). Typically, infected branches lack swelling and may be elongate and pendulous (fig. 6.3). Shoots in systemic infections (fig. 11.1B) generally emerge according to the age of the host stem (Kuijt 1960b). The ability to produce systemic infections is considered to be the evolutionarily advanced condition (see chapter 4) and is found consistently in only a few species of Arceuthobium. The systemic habit represents a radical departure from the growth pattern that characterizes localized infections, and it has required major changes in both ectophytic and endophytic systems.
Localized and systemic forms are stable morphological variations in Arceuthobium, but factors that determine which form develops in a particular situation are poorly understood. Important factors that have been identified include species of Arceuthobium, host, and site of the original infection (Kuijt 1960b). Some workers believe that the major factor in determining endophytic form is whether the parasite initially develops within primary or secondary tissues of the host branch (Alosi and Calvin 1984). Regardless of causes, the morphological differences between infection types are profound.
The region where bark strands grow within the host branch differ by infection type (endophytic form). In localized infections, strands grow mostly or exclusively in the outer part of the secondary phloem (Sadik and others 1986a). In systemic infections, strands initially grow in primary tissues and occur in inner cortex, phloem, and adjacent procambium (Alosi and Calvin 1984). Regardless of these early differences, strands of both infection types can initiate sinkers where they associate with secondary vascular tissue of the host. The sinkers, as indicated above, grow radially towards the host vascular cambium, displace host initials, and occupy positions within the cambial cylinder. With continued cambial activity of host and parasite, sinkers become embedded in the wood of the host (fig 11.1A). Because of sinker formation, mature regions of both infection types are similar structurally.
An endophytic network of bark strands within the host bark and radially oriented sinkers extending varying distances into host wood typifies Arceuthobium (figs. 11.1A and 11.2A); but similar systems occur in Dendrophthora (Thoday 1957), Phoradendron (Calvin 1967b), and Viscum (Sallé 1979a). Korthalsella, previously considered to be the genus most closely related to Arceuthobium, reportedly has a different endophytic plan (Thoday 1957; Fineran, personal communication). Its haustoria extend to the host wood and expand longitudinally and tangentially, thereby separating xylem from phloem. The tangentially spreading wedges may encircle the stem (Thoday 1957). Relationships between endophytic form and taxonomic affinity are uncertain. The reported endophytic differences between Arceuthobium and Korthalsella, if confirmed, would suggest that the two genera are not as closely related as once believed.
Though differences in endophytic systems generate interesting questions of evolutionary origins, generic divergence, and other issues, the task here remains to describe the character of the dwarf mistletoe. We now examine the anatomy behind the haustorial components.
Dwarf mistletoe spreads within host branches by elongation of bark strands. A strand’s growing tip is a simple, unicellular filament (Alosi and Calvin 1984, Bhandari and Nanda 1970, Kuijt 1960b). The constituent cells are 2 to 3 times longer than broad, are densely protoplasmic, and have large conspicuous nuclei (Thoday and Johnson 1930). Cells at the growing tips first elongate then divide transversely. The growing tips of Viscum are multicellular (Thoday 1951, Sallé 1979b). In Viscum, cells of the meristematic zone are elongate, are densely cytoplasmic, and have numerous dictyosomes plus a well-developed endoplasmic reticulum (Sallé 1979b). Bark strands of Viscum grow throughout the year (Sallé 1983), a feature that may also be true of Arceuthobium. Both mechanical and enzymatic action allow bark strands of Viscum to grow through host bark.
Behind the short, filamentous growing tips of Arceuthobium bark strands, cells divide longitudinally and the developing strands become multicellular. Such longitudinal divisions may take place in all subterminal cells, even the subapical cell (Kuijt 1960b). Continued enlargement of bark strands produces a core of smaller cells surrounded by larger parenchymatous cells (Bhandari and Nanda 1970). As development continues, some of the smaller diameter cells in the middle of the strand differentiate as tracheary elements and others as parenchyma (fig. 11.2A). Most, if not all, of the tracheary elements present within strands are vessel members (Kuijt 1960b). Phloem has not been observed in bark strands of the species examined to date. However, sieve elements are present in bark strands of Phoradendron (Calvin 1967b) and Viscum (Sallé 1979a).
Bark strands show a prominent tiered arrangement of cells when viewed in longitudinal section (fig. 11.2B). Even in older strands that have increased greatly in diameter, the tiered arrangement of cells may still be evident. The tiers become less distinct where sinkers merge with bark strands. Shoots, which originate on the outer side of bark strands, also alter the cell tiers (Kuijt 1960b).
Bark strands may undergo secondary growth. In localized infections of species such as Arceuthobium americanum, the amount of secondary growth may be modest (fig. 11.2C). In this species, the secondary vascular tissue laid down apparently consists only of additional tracheary elements and parenchyma. Fibers have not been observed in secondary vascular tissue of the species examined to date (Kuijt 1960b). How-ever, bark strands of large, long-lived species such as A. globosum subsp. grandicaule are expected to show extensive secondary growth. Shoots of this Mexican species may exceed 70 cm in length with a 5-cm diameter at the base. Further, the stems contain a well-developed phloem, including sieve-tube members (Calvin and others 1984). Bark strands of A. globosum should have a well-defined vascular cambium that produces abundant secondary xylem and a typical secondary phloem like that found in shoots.
The term "sinker" was first used by Solms-Laubach in 1867 (Srivastava and Esau 1961a). In common usage, the term refers to a discrete, radially oriented strand with clearly defined boundaries. These strands extend through host phloem and cambium into xylem from a ramifying system of bark strands in the cortex or phloem.
The sinker of Phoradendron shown in figure 11.2D illustrates some of these features. The sinker is clearly delimited and shows little or no intermingling of host and parasite cells. Sinkers have the same orientation in host wood as do vascular rays. Thus, their tangential, vertical, and radial extent are measures of their width, height, and length, respectively (Srivastava and Esau 1961a). The "end" of a sinker is its most deeply embedded part; but this embedded "end" is, in reality, the sinker’s initial part within the host xylem (Srivastava and Esau 1961a).
A sinker of Arceuthobium is shown in figure 11.2E. This structure differs from that of Phoradendron in significant ways. Arceuthobium sinkers lose much of their identity during development. The sinker shown is associated with host ray cells. Srivastava and Esau (1961b) proposed the name "infected ray" to describe this intergeneric, chimeral structure. Within infected rays, host cells occur in multiseriate groupings, whereas they occur as uniseriate panels in uninfected rays (fig. 11.2F). Infected rays may become large, aggregate structures through vertical and lateral fusion of individual infected rays (fig. 11.2F).
Sinkers originate as lateral emergences from bark strands and may be initiated from very young bark strands. Kuijt (1960b) illustrates a sinker arising near the tip of a bark strand by an oblique division of the single cell present at that level. Cohen (1954) asserts that sinkers arise endogenously only, but Kuijt (1960b) refutes this claim and data from Thoday and Johnson (1930) do not support it. In Viscum, sinkers arise exogenously (Sallé 1983) and grow radially in a centripetal direction.
Controversy persists as to the exact manner in which sinkers are initiated. Some workers claim that initiation occurs only when a bark strand contacts host vascular cambium. The initiation of at least some sinkers in Phoradendron does occur in this manner (Calvin 1967b). Others claim that sinkers originate from bark strands located in host phloem and grow centripetally towards the vascular cambium, possibly following the course of vascular rays. Kuijt (1960b) produced a convincing illustration of a sinker being initiated by a bark strand situated at the outer periphery of the secondary phloem. Whether one or both forms of sinker initiation occur in Arceuthobium remains problematic.
Regardless of how a sinker gets started, once it arrives at the vascular cambium it establishes a position within the cambial cylinder. The manner of the sinker’s subsequent growth is also controversial. Some authors believe that an intercalary meristem forms in continuity with the host cambium and that with coordinated cambial activity the sinker becomes embedded in host wood (Thoday and Johnson 1930; Srivastava and Esau 1961a). Others have suggested that the intercalary meristem occurs at the "neck" of the sinker where the sinker joins with the bark strand (Cohen 1954, Kuijt 1960b). Parke (1951) suggested that two meristems occur: one at the juncture of bark strand and sinker and another contiguous with the host cambium. Alosi and Calvin (1984) observed a distinct intercalary meristem juxtaposed to the host cambium, but they also observed cell arrangements that suggested more diffuse meristematic activity at the juncture with bark strands. A sinker cambial zone contiguous with the host cambium has been shown convincingly for Phoradendron (Calvin 1967b) and Viscum (Sallé 1979a). Sallé has further shown that meristematic activity in sinkers of Viscum, in contrast to that of bark strands, does not occur in winter. The meristematic cells do not synthesize nuclear DNA nor do they divide. Instead, their activity coincides with that of the host vascular cambium.
The shape of individual sinkers varies with age and between genera. Arceuthobium, sinker ends may be only one cell wide, but many sinkers become wider with age (fig. 11.3A). Further, wide sinkers may be more or less dilated at the boundaries of xylem increments. Height of sinkers also may increase with age. The end of a sinker may be one or only a few cells high (Srivastava and Esau 1961a). Thus, sinkers increase in width and height with age and eventually appear wedge-shaped when viewed in both cross and radial sections of host branches. Phoradendron sinker ends are high, sometimes exceeding 1 cm (Calvin 1967b), but they actually may decrease in height over time. Also, some Phoradendron sinkers are displaced from the vascular cambium (Calvin 1967b). When this occurs, the sinker portion embedded in the xylem becomes isolated from the main body of the endophytic system. Loss of sinkers from the cambial zone possibly occurs in Arceuthobium too, but because most sinkers are intimately associated with host rays, the situation is more complex.
Distinguishing host from parasite tissues can be difficult, but several workers offer criteria for the task (Alosi and Calvin 1984, Srivastava and Esau 1961a). Several different cell types are found within infected rays. Alosi and Calvin (1984) identified 5 different kinds within infected rays of host phloem (fig. 11.3B-C):
Within host xylem, infected rays may contain 4 kinds of cells (fig. 11.3A):
Not all cell types identified above are necessarily present in a given infected ray. Some examples will illustrate this point. Srivastava and Esau (1961a) showed that sinkers may be initiated independently of host rays and may continue through an entire growth increment before they become associated with ray cells. Association with ray cells occurs through conversion of fusiform initials to ray initials adjacent to a parasite sinker (Alosi and Calvin 1984). Further, normally only a moderate percentage of infected rays contain parasite tracheary elements (see below). Finally, not all conifers have ray tracheids. Such cells occur only sporadically in Abies (Core and others 1979). Thus, infected rays within host xylem would be expected to lack ray tracheids.
A major focus of research on parasitic plants concerns the nature of vascular connections established between host and parasite (Sallé 1983). Because sieve elements are lacking in sinkers of Arceuthobium and because phloem tissue is difficult to study, many workers have focused on the question of xylem-to-xylem continuity between host and parasite. Direct xylem continuity (fig. 11.3A) has been shown to occur in many mistletoes (Kuijt 1977), including Arceuthobium (Kuijt 1960b, Srivastava and Esau 1961a, Thoday and Johnson 1930). Recently, however, several workers (Lamont 1983b, Pate and others 1990, Kuijt 1991) have questioned the importance of such connections in mistletoes and other parasitic plants. Thus, investigations of the nature and extent of xylem-to-xylem connections in Arceuthobium assume new importance.
The most detailed study of xylem-to-xylem contacts in Arceuthobium is that of Srivastava and Esau (1961b) for several species of Arceuthobium occurring on seven different coniferous hosts. Their study focused entirely on relationships of sinkers to host xylem and they reported the following salient findings:
The above observations suggest that dimorphism of sinkers may occur in Arceuthobium. Only about 15% of sinkers contain xylem, and of these slightly less than 50% have direct connections with host xylem. Thus, a large number of sinkers carry out their function without direct xylem connections, and even more do so with no tracheary elements at all. Finding that sinkers in Arceuthobium have different physiological roles would not be surprising. Schmid and Lindeman (1979) reported that Phoradendron californicum has dimorphic sinkers, of which uniseriate sinkers contain only parenchyma and multiseriate sinkers contain both tracheary elements and parenchyma. In their study, only about 2.5% of sinkers were multiseriate. Although the percentage of sinkers with xylem was lower in Phoradendron than in Arceuthobium, observations indicate that only a small percentage of vascularized sinkers is adequate to serve the needs of a parasite. Another suggestion that comes from these studies is that xylem-to-xylem connections are important. Srivastava and Esau (1961b) indicated that such connections between host and parasite were a consistent feature of all host–parasite combinations studied.
In sinkers with tracheary elements, parasite xylem is normally continuous from the wood across the cambium (fig. 11.3D) and secondary phloem to the bark strands (fig. 11.3E). This is true in Arceuthobium (Srivastava and Esau 1961a), as well as in other Viscaceae (Calvin 1967b, Sallé 1979a). It is therefore unusual that such xylem continuity did not occur in A. campylopodum growing on Pinus sabiniana (Srivastava and Esau 1961a). In this species, xylem was abundant in bark strands and in the sinker portion embedded in host wood but absent in sinker parts embedded in host cambium and phloem. A similar lack of continuity was noted by Parke (1951) for infections of A. douglasii on Pseudotsuga menziesii. Further studies are needed to determine if these absences in xylem continuity were related to sinker development or whether they characterize "mature" sinkers.
A major problem for investigations of host–parasite tissue relationships has been the ability to reliably discriminate between host and parasite cells. With light microscopy, cell determinations are difficult. At the ultrastructural level, however, distinctions between host and parasite can be made more easily (Alosi and Calvin 1985). Parenchyma cells of the parasite can be identified by an abundance of electron-dense lipid bodies, characteristic plastids and mitochondria, chromocentric nuclei, and distinctive cell wall features. For the ultrastructural details of the Arceuthobium endophytic system, see Alosi and Calvin (1985); Sadik and others (1986b); Tainter (1971); and Weber and Nietfeld (1984). Other Viscaceae investigated include Korthalsella (Fineran 1987; Coetzee and Fineran 1987, 1989) and Viscum (Sallé 1979b, 1983). Ultrastructural studies dealing with other parasitic angiosperms are numerous but not included here.
Most ultrastructural studies have focused on the interface between Arceuthobium and host tissues, particularly in the xylary portion of sinkers. A few observations, however, pertain to interface features in the region of the phloem. In A. oxycedri, a zone of crushed cells often occurs around large bark strands and around that part of the primary haustorium embedded in host phloem (Sadik and others 1986b). This layer of crushed cells is thought to be a barrier to transfer of materials between host and parasite. Where sinkers are embedded in host phloem, Alosi and Calvin (1985) observed one-sided, imperforate sieve areas of host sieve cells joining very thin-walled, pitted regions of parasite cells. In older sinkers, the portion embedded in host phloem may be enclosed in a layer of highly vacuolated sheath cells (fig. 11.3C) similar to that of bark strands (Srivastava and Esau 1961b). Where this occurs, the centrally located vascular tissue connecting the xylary portion of sinkers to bark strands is further separated from the conducting elements in host phloem. Older sinkers within host phloem (fig. 11.3F) may also show a tiered arrangement of cells much like that seen in bark strands.
In the xylary part of sinkers, various kinds of cell contacts occur. Host tracheids may abut sinker parenchyma (fig. 11.3A). Where this occurs, half-bordered pits of the host cell occur opposite portions of the parasite wall with very irregular surface features; as a consequence, the plasmalemma has a highly convoluted profile (Alosi and Calvin 1985). In adjacent cytoplasm, parallel arrays of endoplasmic reticulum are common. Viewed at high magnification, the irregular ingrowths of cell wall resemble the plasmatubule-like structures illustrated by Fineran (1987) for Euphrasia (Scrophulariaceae). Because living host and parasite cells are commonly contiguous (fig. 11.2E), some investigators question whether or not symplastic union occurs between host and parasite. Although Tainter (1971) reported the presence of plasmodesmata between cells of Arceuthobium pusillum and host needle trace phloem parenchyma, other observers (Alosi and Calvin 1985, Coetzee and Fineran 1987, Sallé 1979b) doubt the union of host and parasite cells is symplastic. The cell wall interface of host and parasite is fused and contains pits, but symplastic connections between parasite and host are now thought not to occur. However, workers occasionally see half-plasmodesmata at the host–parasite interface that appear to be aligned (Alosi and Calvin 1985). Parasite parenchyma cells typically have a smaller tangential diameter than host cells, prominently thickened, nonlignified walls, and abundant plasmodesmatal connections, indicating a high level of symplastic continuity.
Anatomical studies have shown that symplastic union does not occur between Arceuthobium and its coniferous hosts (Alosi and Calvin 1985; Sadik and others 1986b). Thus, the transfer of materials between host and parasite must occur via an apoplastic route (Alosi 1979). Direct tracheary element connections could facilitate transfer of materials between host and parasite. The presence of such connections in all Arceuthobium species studied by Srivastava and Esau (1986a), as well as in other Viscaceae (Calvin 1967b, Sallé 1979a), suggests they are an important part of the overall strategy of water and nutrient uptake. On the other hand, only a small percentage of sinkers appear to have direct xylary connections, and some of these sinkers lack xylem continuity across the vascular cambium and phloem to the vascular tissue of bark strands.
Another possible route for water and nutrient uptake is the apoplastic continuum provided by walls of adjacent host and parasite parenchyma cells. In an eloquent set of experiments, Coetzee and Fineran (1987, 1989) showed that in Korthalsella water and nutrients (including the amino acid, lysine) can be transferred from host to parasite parenchyma via this extensive pathway of adjoining parenchyma cell walls. Because so many Arceuthobium sinkers lack tracheary elements, the continuum demonstrated by Coetzee and Fineran is probably an important route for transfer of water and nutrients. The possession of plasmatubule-like ingrowths by interface parenchyma cells of both Arceuthobium (Alosi and Calvin 1985) and Korthalsella (Fineran 1987, Coetzee and Fineran 1987) lends further support to this view. Support for movement via the apoplastic continuum also comes from the work of Sadik and others (1986b). These workers have shown high levels of acid phosphatase and ATPase activity at the level of plasmalemma, plasmodesmata, and some small endocytotic and exocytotic vesicles in sinkers. They interpret such activity as a sign of intense, active transfer processes in the xylary part of sinkers. Although the relative importance of alternative pathways (symplastic and apoplastic) is problematic, evidence suggests that both pathways are involved in water and nutrient uptake. The latter pathway, the apoplastic continuum provided by walls of adjacent host and parasite parenchyma, should allow for selectivity in nutrient uptake. Finally, it also seems likely that dwarf mistletoe sinkers are dimorphic and thus differ not only in structure but also in function.
Graniferous tracheary elements have been found in the endophytic system of Arceuthobium (Fineran 1985, Weber and Nietfeld 1984), as well as in their stems, leaves, and fruits (chapter 10). After the bases of shoots are killed by steam, host-fixed carbon compounds are no longer transported into shoots even though transpiration continues (Hull and Leonard 1964b). Observations such as these must be considered in any hypotheses concerning water economy and nutrient transfer in Arceuthobium.
Srivastava and Esau (1961b) state, "the most pronounced abnormalities in the xylem anatomy of an infected host occur in the rays." These abnormalities are especially evident in Arceuthobium because sinkers of dwarf mistletoes form almost exclusively within host rays. The significance of these highly complex, intergeneric structures (infected rays) as an evolutionary innovation becomes clear if one considers certain anatomical and physiological features of both host and parasite. Relevant features in Pinus (Zimmermann 1983) include
Important features of Arceuthobium (Srivastava and Esau 1961b) include both the reported ability to stimulate the production of additional host cells within infected rays and the ability to stimulate formation of new host rays. When these individual features are considered together, it becomes clear that infected rays provide the "ultimate" apoplastic continuum. This system is more extensive and dynamic in Arceuthobium than observed in other genera of Viscaceae. An appreciation of these features of infected rays gives new meaning to Heinricher’s (1924) view that the penetration power and the efficiency of the absorbing system of Arceuthobium are superior to those of other Viscaceae.