CASE STUDY 15.4 Plant parasites

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Paul Kriedemann

(Based on material provided by Neil Davidson, Department of Plant Science, University of Tasmania, and Beth Byrne, School of Biological Sciences, Flinders University of South Australia)

Vascular plant parasitism is a worldwide phenomenon with a long evolutionary history. This adaptation has evolved independently in unrelated families, and on numerous occasions. About 3000 species in 13 families of terrestrial plants have representative species that exploit other species in that same family, or in closely related families. These parasitic plants draw water, nutrients and sometimes even photo-assimilate from their hosts. Such adaptation is common in Australia, and is mainly represented by three life forms, mistletoes, dodders and root hemiparasites.

In all cases, parasitic plants rely on their development of an haustorium, that is, an outgrowth of modified root tissue that penetrates host phloem and forms plate-like contact with host xylem. Mistletoes develop a single haustorium on host branches, while root hemiparasites produce many haustoria on roots of other plants. Dodders are leafless aerial parasites with long thread-like stems that produce haustoria at each node. They ramify throughout host-plant canopies and can parasitise a wide range of species, even themselves!

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Figure 1 Well-established mistletoes on a 'struggling' black box (Eucalyptus largiflorens) growing on the upper edge of the Murray River floodplain near Mildura, Victoria (photograph courtesy P.E. Kriedemann)

Mistletoes (Figure 1) grow on branches of eucalypts, acacias and casuarinas throughout mainland Australia (curiously, not in Tasmania). Mistletoe–host relationships are highly specific with a given mistletoe restricted to only a few host species within a given genus. Mistletoe foliage commonly mimics host foliage. This form of mimicry probably confuses herbivores who would otherwise benefit from feeding on mistletoe foliage by virtue of higher nutrient content, and carries an obvious selective advantage.

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Figure 2 Changes in (a) transpiration, (b) stomatal conductance and (c) leaf water potential, of the mistletoe Amyema linophyllum and its host Casuarina obsea at Gingin, Western Australia. Curves are marked 'P' for parasite, and 'H' for host. (Based on Davidson et al. 1989)

Following early studies on mistletoes, Wood (1924) suggested their water use was profligate and subject to little control. Subsequent observations have countered this view, showing that stomatal conductance decreases in response to low humidity and falling leaf moisture content. Furthermore, diurnal patterns of stomatal conductance suggest a co-ordination between host and parasite in response to changing environmental conditions (Ullman et al. 1985). During daytime, mistletoes transpire faster than their host (Figure 2a) due to higher stomatal conductance (Figure 2b). This high stomatal conductance, coupled with a substantial hydraulic resistance to water flow through the haustorium, results in a much lower leaf water potential in parasite compared to that of the host (Figure 2c).

Surprisingly, host–parasite differences in leaf water potential at night-time change little from daytime values despite a 300-fold difference in transpiration rate (Davidson and Pate 1992) and this implies a large increase in haustorial resistance to water flow from day to night. According to Kuo et al. (1989), the haustorial junction of a root hemiparasite (Olax phyllanthi) hydrates at night to a sufficient extent that turgid cells partially close the principal apoplasmic pathway of water movement, forcing water to move through cells rather than between cells (that is, to a symplasmic rather than an apoplasmic pathway). Such a shift in pathway would increase hydraulic resistance and a similar mechanism might apply to mistletoes.

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Table 1

Although mistletoes transpire faster than their hosts, rates of carbon assimilation are about the same. Water use efficiency is therefore lower (Davidson and Pate 1992), and in this respect confirms Wood’s early (1924) assertion. Host–parasite differences in water use efficiency are reflected in carbon isotope signature (Table 1) for Amyema fitzgeraldii growing on Acacia acuminata near Geraldton in Western Australia. Numerically larger values imply lower water use efficiency (Case study 15.3).

Even in xeric environments, mistletoes are more succulent than their hosts, and this succulence confers a greater water-holding capacity on the parasite. Foliage on Amyema linophyllum has more than three times the water-holding capacity of Casuarina obesa, and in this parasite–host relation-ship daytime transpiration draws on parasite water reserves that are recharged during subsequent nights (Whittington and Sinclair 1988). Night-time recharge, combined with lower threshold of leaf water potential for stomatal closure in parasite compared to host, has important implications for diurnal partitioning of water between partners, and especially during water stress.

Water relations of dodders present a different set of issues. Their morphology implies a xerophytic nature and a distinctive hydraulic architecture. Leaves have been reduced to scales, and photosynthetic stems have a thick cuticle with sunken stomata in longitudinal groups of three to seven (McLuckie 1924). These constraints on water loss are complemented by a high concentration of hydrophilic mucilage in vascular conduits that would increase osmotic pressure and contribute towards drought resistance.

Although water can move in either direction along dodder stems, there is a limit on distance travelled. Stems seldom grow longer than about 50 cm beyond a given haustorium and may reflect a maximum distance for cost-effective transport of water and nutrients within their thread-like stems. Extension growth to new hosts then depends upon an anastomosing network of stems, aided by autoparasitism.

Root hemiparasites such as Olax spp., Exocarpos spp. and Leptomeria spp., in contrast to dodder and mistletoes, are equipped with many haustoria and are able to parasitise a large number of different individuals or host species in their vicinity. Moreover, they express very different water relations from those of mistletoes which have just one haustorium per plant. These more generalist root parasites enjoy the luxury of making ephemeral haustorial contact with hosts, and then severing those links if host water relations are unfavourable to themselves. For example, Olax phyllanthi (Table 1) may have as many as 1000 active haustoria attached to a wide range of host species, but these organs of extraction senesce during periods of low rainfall (Pate et al. 1990). Senescence probably occurs for those haustoria attached to a host whose water potentials are out of range (more negative than the parasite). Root hemiparasites thereby avoid a scenario where water potential gradients are reversed, and water moves from parasite to host.

Unlike mistletoes, both transpiration and CO2 assimilation by Olax phyllanthi are lower than corresponding rates by host plants. Host and parasite return similar values for carbon isotope signature (Table 1), but water use efficiency is not necessarily comparable because a large proportion of carbon present in Olax is derived heterotrophically from its host plants and would dilute any 13C enrichment due to Olax itself. Indeed, d13C and C:N ratio studies indicated as much as 51–63% heterotrophic acquisition of carbon by Olax under field conditions (Tennakoon and Pate 1996).

Striga, an herbaceous root hemiparasite of annual crops, provides an even more extreme case of host exploitation. One species, Striga hermonthica, transpires 10 times faster than the annuals it parasitises. Photosynthetic pigments are present at about 40% of host levels, and stomata are insensitive to either light or water stress. This extraordinarily low water use efficiency impacts severely on host water relations and reduces yield dramatically. A second species, S. gesnerioides, transpires more slowly but is almost devoid of chlorophyll and is thus heavily dependent on host-plant photoassimilate. In this case, almost 70% of imported carbon is expended on haustorium respiration which in turn sustains uptake of carbon, nitrogen and mineral nutrients. Diversion of such large quantities of resources from the host plant (Vigna unguiculata, cowpea) reduces host plant growth by 75% (Graves et al. 1992).

In a reversal of host–parasite relations more equitable for horticulture where parasite rather than host plant is put to human use, quandong (Santalum acuminatum) operates as a root hemiparasite on a wide range of host species. Quandong is native to southern Australia with potential for commercial cropping in arid areas with poor-quality water (Sedgley 1984). Mainly recognised as an indigenous arid-zone plant, quandong can access water from host plants via a fleshy haustorium rich in starch (Figure 3). Reminiscent of the high resistance to hydraulic flow in mistletoe haustoria discussed above, an interrupted zone in quandong–host connections (Figure 3) is characteristic in members of the Santalaceae family and would increase resistance to flow between host and parasite because vascular connections are reduced to a few xylem elements.

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Figure 3 A hand section and schematic drawing of a qauandong (Santalum acuminatum) haustorium showing (left to right) quandong root, interrupted zone, vascular tissue, parenchyma tissue and host root in cross-section. Scale bar = 250 µm. (Original illustration courtesy B.R. Byrne)

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Figure 4 Quandong (Santalum acuminatum) grows much faster in association with a compatible host plant such as Atriplex nummularia. Present data come from container plants in a greenhouse experiment at Flinders University of South Australia. Similar responses occur under field conditions where quandong can access a wide range of host plants. (Original data courtesy B.R. Byrne)

In greenhouse trials at Flinders University (Byrne et al. 1997) height growth in quandong was greatly enhanced by a parasitic association with Atriplex nummularia (Figure 4). Other host species such as Templetonia retusa, Myoporum parvifolium and Acacia cyclops proved less effective.

In field trials at Aldinga and Middleback (South Australia) gradients in water potential and osmotic potential between host and parasite ensure a flow of xylem contents from host to parasite. Leaf extracts from quandong averaged total solute concentrations of around 1315 mM compared with host plants at only 735 mM. While chloride, sodium and potassium ions all contributed to this host–parasite difference, an unusual organic solute was largely responsible, namely mannitol. Leaf extracts from quandong growing at Middle-back contained up to 366 mM mannitol, and contributed to generation of leaf osmotic pressures of between 3.5 and 4 MPa, compared with host tree osmotic pressures of around 2 MPa. Host tree foliage was devoid of mannitol.

Xylem–xylem connections exist (Figure 3) and would enable movement between host and parasite, but phloem connections have not been observed. A meagre translocation of 14C-labelled assimilates from host plant to parasite reported by Byrne et al. (1997) presumably takes an indirect route. Because quandong is photosynthetically competent, host plant dependence is largely confined to water and inorganic nutrients, although secondary metabolites with insecticidal value have been detected in quandong fruit from plants growing in association with Melia azedarach, a known source of the natural insecticide azadirachtin.

Concluding remarks

Plant parasites do not exploit their hosts in an uncontrolled fashion. Instead, parasite physiology is beautifully adapted for coordination with nutrient and water relations of the host plant. For example, water potential differences between host and parasite are remarkably constant over a wide range of environmental conditions, and are maintained by a transpiration-driven reduction in parasite water potential coupled with a high fluid phase resistance in the haustorium. This difference is maintained at night-time via adjustments in haustorium resistance. A high moisture capacitance of succulent parasite foliage provides a buffer against desiccation when host plants are water stressed.

Water and nutrients are both critical currencies in host–parasite relations, but carbon acquisition may well prove more pervasive in sustaining parasitic habits as discussed here. In particular, perennial parasites need to retain a healthy host for their own survival as individuals, so that parasites with a low capacity for autotrophic carbon gain must also adapt with failsafe mechanisms for reproduction and species preservation in the event of their host dying prematurely. Such parasites impose greatest demand on host plants and include dwarf mistletoes that infect pine plantations, dodders in the genus Cuscata that act as vectors for viruses in pasture and grain crops, and herbaceous root hemiparasitic weeds such as Striga spp. that commonly parasitise legume and grain crops. Host responses to virulent parasites include loss of photosynthetic capacity, reduced fecundity and bizzare growth patterns such as ‘witches broom’ as observed on conifers. Evolution of such highly successful life forms once again emphasises adaptive plasticity in vascular plants and they offer rich ground for research into mechanisms responsible for host–parasite interactions on growth and reproductive development.

References

Byrne, B.R., Tyerman, S.D. and Loveys, B.R. (1997). ‘The transfer of compounds from host plants to the hemiparasite Santalum acuminatum’, Proceedings 41st Annual ASBMB and 37th Annual ASPP Conferences, Melbourne, 29 September–
2 October 1997, Abstract P1–44.

Davidson, N.J. and Pate, J.S. (1992). ‘Water relations of the mistletoe Amyema fitzgeraldii and its host Acacia acuminata’, Journal of Experimental Botany, 43, 1549–1555.

Davidson, N.J., True, K.C. and Pate, J.S. (1989). ‘Water relations of the parasite:host relationship between the mistletoe Amyema linophyllum (Fenzl) Tieghem and Casuarina obesa Miq.’, Oecologia, 80, 321–330.

Graves, J.D., Press, M.C., Smith, S. and Stewart, G.R. (1992). ‘The carbon economy of the association between cowpea and the parasitic angiosperm Striga gesnerioides’, Plant, Cell and Environment, 15, 283–288.

Kuo, J., Pate, J.S. and Davidson, N.J. (1989). ‘Ultrastructure of the haustorial interface and apoplastic continuum between host and the root hemiparasite Olax phyllanthi (Labill.) R. Br. (Olacaceae)’, Protoplasma, 150, 27–39.

McLuckie, J. (1924). ‘Studies in parasitism. I. A contribution to the physiology of the genus Cassytha’, Proceedings of the Linnean Society of New South Wales, 49, 55–78.

Pate, J.S., Davidson, N.J., Kuo, J. and Milburn, J.A.M. (1990). ‘Water relations of the root hemiparasite Olax phyllanthi (Libill) R. Br. (Olacaceae) and its multiple hosts’, Oecologia, 84, 186–193.

Sedgley, M. (1984). ‘Australia’s first commercial fruit?’, Australian Horticulture, 82, 52–59.

Tennakoon, K.U. and Pate, J.S. (1996). ‘Heterotrophic gain of carbon from hosts by the xylem tapping root hemiparasite Olax phyllanthi (Olacaceae)’, Oecologia, 105, 369–376.

Ullman, I., Lange, O.L., Ziegler, H., Ehleringer, J., Schulze, E.-D. and Cowan, I.R. (1985). ‘Diurnal course in leaf conductance and transpiration of mistletoes and their hosts in Central Australia’, Oecologia, 67, 577–587.

Whittington, J. and Sinclair, R. (1988). ‘Water relations of the mistletoe Amyema miquelii and its host Eucalyptus fasciculosa’, Australian Journal of Botany, 36, 329–356.

Wood, J.G. (1924). ‘The relationship between distribution, structure, and transpiration of arid South Australian plants’, Transactions of the Royal Society of South Australia, 48, 226–235.

 

 

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