Relatively few aspects of the relationship between the physiology of dwarf mistletoes and that of their hosts have been studied (Gill and Hawksworth 1961, Hawksworth 1958). The general physiology of mistletoes has been reviewed by Knutson (1979, 1983) and that of parasitic higher plants by Atsatt (1983). Although there are more than 200 publications on various aspects of dwarf mistletoe physiology, there have been no previous attempts to synthesize this scattered literature. Most studies of dwarf mistletoe physiology have dealt with water relations, photosynthesis, and carbon transport from host to parasite. A few attempts have been made to culture these parasites in vitro, and some recent research has focused on the role of growth regulators in the hostparasite interaction.
All mistletoes must move water and nutrients from the host to the parasite. The osmotic concentration of the parasite’s cell sap must therefore be higher than that of the host (Fisher 1983, Hartel 1937). Some early physiological studies of the dwarf mistletoes compared osmotic concentrations of parasite and host: Arceuthobium douglasii on Pseudotsuga menziesii in Utah (Harris 1934, Korstian 1924a); A. americanum on Pinus contorta in Utah (Korstian 1924a); A. cyanocarpum on P. flexilis in Colorado (Harris 1934); and A. vaginatum subsp. cryptopodum on P. ponderosa in Arizona (Korstian 1924a) and Utah (Harris 1934). Average osmotic concentration of the mistletoes was19.5 bars compared to17.5 for the hosts. Even though differences between host and parasite are relatively small, osmotic concentration may limit the distribution of dwarf mistletoes in some parts of their hosts’ range. For example, A. vaginatum subsp. cryptopodum is absent on P. ponderosa near its lower elevational limits in Colorado and the Southwest, where osmotic concentration differences are the least (Hawksworth 1959b). Mark and Reid (1971) reported that water potential gradients enabled A. americanum to obtain water from Pinus contorta in Colorado, even when the host was under considerable water stress. The average water potential of the parasite was21.3 bars compared to14.7 bars for the host.
The most intensive studies of water relations in dwarf mistletoes were by Fisher (1975, 1983) and Fisher and Reid (1976) for Arceuthobium americanum on Pinus contorta and A. vaginatum subsp. cryptopodum on P. ponderosa in Colorado. They used thermocouple psychrometers to monitor the airstream before and after it passed through cuvettes enclosing transpiring tissues. On a surface area basis, transpiration rates of the dwarf mistletoe were as much as 4 times the transpiration rates for the host. In other tests, infected pine seedlings were grown in cultures with solutions containing various concentrations of polyethylene glycol to obtain osmotic potentials from 0 to15 bars. The dwarf mistletoes generally showed a lower water potential than the host, varying from3 bars among well-watered hosts to6 bars for hosts under the severest water stress.
Tocher and others (1984) studied the water relations of several dwarf mistletoe-infected seedlings: Pinus contorta / Arceuthobium americanum, P. ponderosa / A. campylopodum, and Tsuga heterophylla / A. tsugense. Transpiration rates for the mistletoes on pine were at least 8 times greater than that of their hosts under all conditions of moisture stress and darkness. The differences were greatest (up to 60 times), however, when the host was under the greatest water stress. Transpiration rates of host and parasite were comparable only for T. heterophylla growing under well-watered conditions. Quraishi and others (1977) observed that transpiration rates of A. oxycedri in Pakistan were about 4 times that of its host, Juniperus excelsa.
Kirkpatrick (1989) studied water relations of Pinus contorta infected by Arceuthobium americanum in central Oregon. Null-balance porometry was used to measure water vapor conductance of infected trees in vivo. Under optimal moisture conditions (May and June), conductance in the dwarf mistletoe was usually less than that in the host. Under summer drought conditions (August and September), however, conductance in the parasite was typically from 2 to 5 times that of the host.
Dwarf mistletoes, therefore, typically exhibit higher levels of transpiration than their hosts. If abundant moisture is available, then these differences are not great; but when the host is under moisture stress, the dwarf mistletoes maintained their high transpiration rates, thus greatly magnifying the differences. We suggest that the high transpiration rates observed in all mistletoes, in contrast to their hosts, increases mineral acquisition by mistletoes, which generally are considered to be nutrient sinks (Lamont 1983b).
One of the earliest studies to determine the direction of nutrient flow between host and parasite was by Weir (1916b). He removed all needles from small trees of Pinus contorta infected by Arceuthobium americanum and from comparable uninfected trees. After 2 years, uninfected trees were dead, but infected trees were still alive; these results perhaps suggest that there had been some translocation of nutrients from parasite to host.
Rediske and Shea (1961) noted that a significant proportion of radioactive photosynthate (mostly sucrose) produced by Arceuthobium americanum was translocated into its Pinus contorta host. These results, however, have not been confirmed by subsequent workers, and the present consensus is that there is little, if any, translocation of parasite-derived photosynthates from dwarf mistletoes to their host plants.
The most comprehensive studies of photosynthesis and carbon transport in Arceuthobium were by Hull and Leonard (1964a, 1964b) and Leonard and Hull (1965). They examined 8 species of dwarf mistletoes in California and concluded that mistletoes derived organic nutrition primarily from their hosts. The endophytic system and shoots accumulated labeled assimilates from their hosts at all seasons of the year. The dwarf mistletoes carried on limited photosynthesis, but no labeled carbon assimilates migrated through the endophytic system into the host. There was, however, limited translocation of labeled phosphorus from parasite to host, apparently through the apoplast.
Chlorophyll content of dwarf mistletoe seeds and shoots is on the order of 0.24 to 0.48 mg/g (Hull and Leonard 1964b, Tocher and others 1984), which is about 10 to 25% of the chlorophyll level of their hosts’ foliage. The chlorophyll a/b ratio in Arceuthobium ranges from 1.3 to 2.8.
The growing hypocotyl of Arceuthobium is chlorophyllous, but the importance of photosynthesis in its establishment and early growth has been debated (Cohen 1963, Scharpf 1970). Muir (1975) reported that seeds of A. occidentale were photosynthetically able to fix small amounts of carbon dioxide, comparable to that of shoots (Hull and Leonard 1964b). Muir (1975) suggested that this source could provide significant levels of energy and carbohydrates during germination. Tocher and others (1984) and Gustafson and Tocher (1980) also concluded that Arceuthobium seeds fixed carbon dioxide.
How much of the photosynthate used by dwarf mistletoes is produced by the parasite and how much is derived from the host has been the subject of a few studies. You (1985) suggests that most of the photosynthates used by Arceuthobium chinense growing on Keteleeria in China are derived from the host. Hull and Leonard (1964b) reported that dwarf mistletoes produce about 30% of their needed photosynthates. Rey and others (1991) suggested that A. oxycedri parasitizing juniper in France produces about 50% of its needed photosynthate. However, this species has a deeper green color than any other (see fig. 16.126) and may, therefore, have a higher chlorophyll content and greater photosynthetic activity than other dwarf mistletoes. It appears unlikely that such exceedingly reduced species as A. minutissimum (see fig. 16.123, 16.124) or A. pusillum (see fig. 16.86) can contribute significant photosynthate to their extensive endophytic systems. These species are characterized by large, systemic infections and are exceedingly damaging to their hosts.
Rates of dark respiration for Pinus contorta shoots infected by Arceuthobium americanum were significantly lower than for comparable uninfected shoots (Wanner and Tinnin 1986), but dwarf mistletoe shoots exhibited higher respiration rates than host foliage.
Lamont (1983b) presented an excellent review of mineral nutrition in both mistletoe families. The dwarf mistletoes, as do mistletoes generally, selectively absorb minerals from their hosts and act as nutrient sinks. McDowell (1964) reported that concentrations of nitrogen, phosphorus, potassium, and magnesium were higher in Arceuthobium campylopodum than in its host, Pinus ponderosa. In contrast, calcium levels were lower in the mistletoe than in the host, which is consistent with parasitic phanerogams generally (Lamont 1983b).
Singh and Carew (1989) analyzed concentrations of a number of elements (N, P, K, Mg, Na, Ca, Fe, Zn, Mn, Cu, Al, and Ni) in the foliage, bark, and wood of uninfected Picea mariana trees as well as trees infected by Arceuthobium pusillum. They did not, however, detect meaningful differences in macronutrient or micronutrient concentrations for any of the plant parts analyzed.
The dwarf mistletoes do not produce all the assimilates they need and thus must appropriate most of them from their hosts. This accumulation of assimilates, or "nutrient sink," is likely the result of changes in the host induced by growth substances, particularly cytokinins (Knutson 1979, Livingston and others 1984). Paquet (1979) studied the relative concentrations of cytokinins in Arceuthobium douglasii and its host, Pseudotsuga menziesii and in A. tsugense on Tsuga heterophylla. In general, concentrations of cytokinins were from 2 to 10 times higher in mistletoes than in their hosts. Zeatin riboside was the most common cytokinin, but zeatin and N6-adenosine were also present in smaller amounts.
Schaffer and others (1983) examined cytokinins in a dwarf mistletoe that induces witches’ brooms, Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa, and in one that does not, A. occidentale on P. sabiniana. Cytokinins were less concentrated in the species that does not induce witches’ broom formation. Concentrations of cytokinins were highest in dwarf mistletoe shoots, less in mistletoe-infected branches, and not detectable in uninfected branches. Whether cytokinins in dwarf mistletoe shoots were produced by the parasite or whether they originated from infected branches was not determined.
Uninfected stem tissues from Picea mariana and tissues infected by Arceuthobium pusillum were assayed for abscisic acid (ABA), indole-3-acetic acid (IAA), zeatin, and zeatin riboside (Livingston and others 1984). Zeatin was not detected in the analysis, but concentrations of zeatin riboside and IAA were generally higher for infected tissues than for uninfected tissues tested from April to October. However, ABA levels were consistently lower for infected tissues throughout the test period. The authors concluded that increases in cytokinins and IAA, in conjunction with decreases in ABA, altered the growth substance composition and resulted in sink formation, stem swellings, and loss of apical dominance by infected branches.
The concentration of nitrogen is generally higher in all mistletoes than in their hosts (Lamont 1983b). Knutson (1979) considered nitrogen a critical element in hostparasite physiology. The element is absorbed as ammonium and organic nitrogen rather than as nitrate. Greenham and Leonard (1965) made comparative hostparasite analyses of 22 amino acids in 6 mistletoes, including 4 dwarf mistletoes. Mistletoes generally had higher concentrations of both free and bound amino acids than their hosts, although the amino acid composition of the mistletoes closely resembled that of the host. Arceuthobium abietinum contained gamma aminobutyric acid, but its host, Abies concolor, did not. Shoots of all mistletoes tested contained asparagine, but most hosts did not. McDowell (1964) also found that Arceuthobium campylopodum had a similar amino acid composition to that of its host (Pinus ponderosa), except cysteic acid was present only in the dwarf mistletoe and glycine only in the host. Asparagine was the primary amino acid transferred from host to parasite in A. oxycedri (Rey and others 1991), and glutamine was present in the parasite only after periods of active growth (Evstigneeva and Aseeva 1967). Arceuthobium oxycedri was able to synthesize valine and isoleucine (Kagan and others 1964).
Blakely (1959) unsuccessfully attempted in vitro propagation of seeds of Arceuthobium douglasii on callus-tissue cultures of Pseudotsuga menziesii. In a few cases, callus cultures of infected P. menziesii tissues were grown in vitro, but these were short-lived. Bonga (1968, 1972, 1974) attempted to culture A. pusillum on various media, but was unable to maintain cultures beyond seed germination and modified holdfast development.
The physiological processes causing reduced growth rates and eventual host mortality due to infection by dwarf mistletoes have not been adequately defined. The available information, however, allows us to speculate on some aspects of the interaction (Knutson 1979). The dwarf mistletoes initiate disease by penetrating the host and producing hormones (probably mostly cytokinins). These hormones cause increased translocation of nutrients to the dwarf mistletoe at the expense of the host’s uninfected parts. This change is shown by the increased size of infected branches and increased ratio of branch to main stem biomass (Wanner and Tinnin 1986). The higher transpiration rates of dwarf mistletoe shoots and their higher cytoplasmic osmotic concentrations cause disproportionately higher rates of water and absorbed nutrient movement from the host to infected sites. This shift establishes a sourcesink relationship. In addition, the concomitant loss of sugars, amino acids, and amines to the parasite also severely affects the host. As more and more nutrients are transferred from the host to infected branches and dwarf mistletoe shoots, main stem growth steadily declines. When there is insufficient foliage on a tree to sustain minimal photosynthetic capacity, growth ceases and death follows. Mortality is often hastened by secondary infestations of insects, such as bark beetles, when the tree is in decline.
The witches’ brooms formed by most dwarf mistletoes cause greater losses of nutrients and water from the host than do the dwarf mistletoe plants themselves. This difference has been demonstrated by growth rates of broomed and non-broomed trees with the same infection ratings (Hawksworth 1961a); diameter growth rates of non-broomed trees was 4 to 6 times greater than that of comparable broomed hosts. Trees also recover vigor following broom removal, which is taken as further evidence of the debilitating effects of witches’ brooms on tree growth and vitality (Hawksworth and Johnson 1989a, Lightle and Hawksworth 1973, Scharpf and others 1987).
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