The bright side of parasitic plants: what are they good for?

Parasitic plants are mostly viewed as pests. This is caused by several species causing serious damage to agriculture and forestry. There is however much more to parasitic plants than presumed weeds. Many parasitic plans exert even positive effects on natural ecosystems and human society, which we review in this paper. Plant parasitism generally reduces the growth and fitness of the hosts. The network created by a parasitic plant attached to multiple host plant individuals may however trigger transferring systemic signals among these. Parasitic plants have repeatedly been documented to play the role of keystone species in the ecosystems. Harmful effects on community dominants, including invasive species, may facilitate species coexistence and thus increase biodiversity. Many parasitic plants enhance nutrient cycling and provide resources to other organisms like herbivores or pollinators, which contributes to facilitation cascades in the ecosystems. There is also a long tradition of human use of parasitic plants for medicinal and cultural purposes worldwide. Few species provide edible fruits. Several parasitic plants are even cultivated by agriculture/forestry for efficient harvesting of their products. Horticultural use of some parasitic plant species has also been considered. While providing multiple benefits, parasitic plants should always be used with care. In particular, parasitic plant species should not be cultivated outside their native geographical range to avoid the risk of their uncontrolled spread and the resulting damage to ecosystems.

A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic Pedicularis species.

Despite their ubiquitous distribution and significant ecological roles, soil microorganisms have long been neglected in investigations addressing parasitic plant-host interactions. Because nutrient deprivation is a primary cause of host damage by parasitic plants, we hypothesized that beneficial soil microorganisms conferring nutrient benefits to parasitized hosts may play important roles in alleviating damage. We conducted a pot cultivation experiment to test the inoculation effect of an arbuscular mycorrhizal fungus (Glomus mosseae), a rhizobium (Rhizobium leguminosarum) and their interactive effects, on alleviation of damage to a legume host (Trifolium repens) by two root hemiparasitic plants with different nutrient requirements (N-demanding Pedicularis rex and P-demanding P. tricolor). Strong interactive effects between inoculation regimes and hemiparasite identity were observed. The relative benefits of microbial inoculation were related to hemiparasite nutrient requirements. Dual inoculation with the rhizobium strongly enhanced promotional arbuscular mycorrhizal effects on hosts parasitized by P. rex, but reduced the arbuscular mycorrhizal promotion on hosts parasitized by P. tricolor. Our results demonstrate substantial contribution of arbuscular mycorrhizal and rhizobial symbioses to alleviating damage to the legume host by root hemiparasites, and suggest that soil microorganisms are critical factors regulating host-parasite interactions and should be taken into account in future studies.

Differentiation in fructification percentage between two morphs of Amomum tsaoko (Zingiberaceae).

Amomum tsaoko is a flexistylous ginger. Flexistyly is a unique floral mechanism promoting outcrossing, which is known only in some species of Zingiberaceae till date. This is a pioneer report on flexistyly in A. tsaoko from the aspect of fructification percentage to clarify its influence on reproduction. We observed in 2007 and 2008 that the fructification percentage of the anaflexistyled and the cataflexistyled inflorescence were 14.89 ± 10.35% and 11.31 ± 7.91% respectively, with significant difference (d.f. = 141.920, t = 2.518, P = 0.013 < 0.05). The greatly significant difference between 2007 and 2008 were present in both the flower number (d.f. = 93, t = -2.819, P = 0.006 < 0.01) and the fructification percentage (d.f. = 93, t = -2.894, P = 0.005 < 0.01) of the cataflexistylous inflorescence. Although the two morphs were similar in morphological characteristics, there was some gender differentiation between them, showing a possibility that the anaflexistylous morph might function more as females and the cataflexistylous morph more as males. Reproduction of the cataflexistylous morph was significantly sensitive to change of environmental factors, in contrast to the anaflexistylous morph, thus the yield varied between the abundant year (2008) and the off year (2007).

Host shoot clipping depresses the growth of weedy hemiparasitic Pedicularis kansuensis.

Root hemiparasitic plants show optimal growth when attached to a suitable host by abstracting water and nutrients. Despite the fact that damage to host plants in the wild occurs frequently in various forms (e.g. grazing), effects of host damage on growth and physiological performance of root hemiparasites remain unclear. In this study, host shoot clipping was conducted to determine the influence of host damage on photosynthetic and growth performance of a weedy root hemiparasite, Pedicularis kansuensis, and its interaction with a host, Elymus nutans. Photosynthetic capacity, tissue mineral nutrient content and plant biomass of P. kansuensis were significantly improved when attached to a host plant. Host clipping had no effect on quantum efficiency (ΦPSII), but significantly reduced the growth rate and biomass of P. kansuensis. In contrast, clipping significantly improved photosynthetic capacity and accumulation of potassium in E. nutans. No significant decrease in biomass was observed in clipped host plants. By changing nutrient absorption and allocation, clipping affected the interaction between P. kansuensis and its host. Our results showed that host clipping significantly suppressed the growth of weedy P. kansuensis, but did not affect biomass accumulation in E. nutans. We propose that grazing (a dominant way of causing host damage in the field) may have a potential in the control against the weedy hemiparasite.

Arbuscular mycorrhizal fungi: potential biocontrol agents against the damaging root hemiparasite Pedicularis kansuensis?

Spatial expansion of root hemiparasitic Pedicularis kansuensis in Bayanbulak Grassland of Xinjiang Uygur Autonomous Region (China) has caused great loss of herbage yield and has threatened the local livestock industry. Current management practices using manual eradication and chemical control have been proved problematic. Arbuscular mycorrhizal (AM) fungi have been suggested to be potential biocontrol agents against a number of plant pests, but experimental evidence is lacking against weedy P. kansuensis. In this study, we tested the hypothesis that inoculation with AM fungi will cause growth depression in P. kansuensis and reduce its damage to host plants. Based on the confirmation of AM status and host community of the hemiparasite in the field, a pot cultivation experiment was conducted to test the influence of an AM fungus (Glomus mosseae) on growth of P. kansuensis and the parasitized host (Elymus nutans). AM colonization was observed in roots of P. kansuensis, but the levels were much lower than those of its adjacent host species. A negative correlation between AM levels and the numbers of haustoria was detected for the field samples of the hemiparasite. Strong suppression of haustorium formation, a significant reduction in plant dry weight (DW), as well as marked reduction in the survival rate of P. kansuensis after inoculation with AM fungi was observed. In contrast, inoculation with G. mosseae increased root DW and whole plant DW of parasitized host plants. Our findings demonstrated significantly repressive effects of AM fungi on growth performance of P. kansuensis with and without the presence of a host. The potential of AM fungi as biocontrol agents against the damaging hemiparasite was confirmed.

Nutrient requirements differ in two Pedicularis species in the absence of a host plant: implication for driving forces in the evolution of host preference of root hemiparasitic plants.

BACKGROUND AND AIMS: Facultative root hemiparasitic plants generally have a wide host range, but in most cases show an obvious host preference. The reasons for the marked difference in growth performance of hemiparasites when attached to different hosts are not fully understood. In this study, the hypothesis was tested that hemiparasites showing a preference for different hosts have different nutrient requirements. METHODS: Two facultative root hemiparasitic Pedicularis species (P. rex and P. tricolor) with a different host dependency and preference were used to test their responses to inorganic solutes. The effects of nitrogen, phosphorus and potassium on growth of the hemiparasitic plants not attached to a host were determined, using an orthogonal design in pot cultivation under greenhouse conditions. Variables including biomass, shoot nutrient concentration, root:shoot (R:S) ratios and the number of haustoria were measured. KEY RESULTS: As in autotrophic plants, nutrient deficiency reduced dry weight (DW) and nutrient concentrations in the root hemiparasites. Nitrogen and phosphorus significantly influenced growth of both Pedicularis species, while potassium availability influenced only shoot DW of P. rex. Nitrogen had far more effect on growth of P. rex than on P. tricolor, while phosphorus deficiency caused more marked growth depression in P. tricolor than in P. rex. Pedicularis rex grew faster than P. tricolor in a range of nutrient supplies. Different patterns of biomass allocation between the two Pedicularis species were observed. While P. rex invested more into roots (particularly fine rootlets) than P. tricolor, the number of haustoria produced by P. rex was relatively much lower than that produced by P. tricolor, which had a much smaller root system. CONCLUSIONS: The two Pedicularis species differ in nutrient requirements and biomass allocation. Distinct interspecific traits in growth and nutrient requirements can be driving forces for the differential interactions between hemiparasites and their hosts.

Direct and indirect influences of arbuscular mycorrhizal fungi on phosphorus uptake by two root hemiparasitic Pedicularis species: do the fungal partners matter at low colonization levels?

BACKGROUND AND AIMS: Because most parasitic plants do not form mycorrhizal associations, the nutritional roles of arbuscular mycorrhizal (AM) fungi in them have hardly been tested. Some facultative root hemiparasitic Pedicularis species form AM associations and hence are ideal for testing both direct and indirect effects of AM fungi on their nutrient acquisition. The aim of this study was to test the influence of AM inoculation on phosphorus (P) uptake by Pedicularis rex and P. tricolor. METHODS: (32)P labelling was used in compartmented pots to assess the contribution of the AM pathway and the influence of AM inoculation on P uptake from a host plant into the root hemiparasites. Laboratory isolates of fungal species (Glomus mosseae and G. intraradices) and the host species (Hordeum vulgare 'Fleet') to which the two Pedicularis species showed obvious responses in haustorium formation and growth in previous studies were used. KEY RESULTS: The AM colonization of both Pedicularis spp. was low (<15 % root length) and only a very small proportion of total plant P (<1 %) was delivered from the soil via the AM fungus. In a separate experiment, inoculation with AM fungi strongly interfered with P acquisition by both Pedicularis species from their host barley, almost certainly because the numbers of haustoria formed by the parasite were significantly reduced in AM plants. CONCLUSIONS: Roles of AM fungi in nutrient acquisition by root parasitic plants were quantitatively demonstrated for the first time. Evidence was obtained for a novel mechanism of preventing root parasitic plants from overexploiting host resources through AM fungal-induced suppression of the absorptive structures in the parasites.

Inoculation with arbuscular mycorrhizal fungi suppresses initiation of haustoria in the root hemiparasite Pedicularis tricolor.

BACKGROUND AND AIMS: Plant parasitism and arbuscular mycorrhizal (AM) associations have many parallels and share a number of regulatory pathways. Despite a rapid increase in investigations addressing the roles of AM fungi in regulating interactions between parasitic plants and their hosts, few studies have tested the effect of AM fungi on the initiation and differentiation of haustoria, the parasite-specific structures exclusively responsible for host attachment and nutrient transfer. In this study, we tested the influence of AM fungi on haustorium formation in a root hemiparasitic plant. METHODS: Using a facultative root hemiparasitic species (Pedicularis tricolor) with the potential to form AM associations, the effects of inoculation were tested with two AM fungal species, Glomus mosseae and Glomus intraradices, on haustorium initiation in P. tricolor grown alone or with Hordeum vulgare 'Fleet' (barley) as the host plant. This study consisted of two greenhouse pot experiments. KEY RESULTS: Both AM fungal species dramatically suppressed intraspecific haustorium initiation in P. tricolor at a very low colonization level. The suppression over-rode inductive effects of the parasite's host plant on haustoria production and caused significant growth depression of P. tricolor. CONCLUSIONS: AM fungi had strong and direct suppressive effects on haustorium formation in the root hemiparasite. The significant role of AM fungi in haustorium initiation of parasitic plants was demonstrated for the first time. This study provides new clues for the regulation of haustorium formation and a route to development of new biocontrol strategies in management of parasitic weeds.

Root hemiparasitism in Malania oleifera (Olacaceae), a neglected aspect in research of the highly valued tree species.

Malania oleifera (Olacaceae) is a valued tree species, mostly because its seeds have high precious fatty acid content (particularly nervonic acid). However, seedling mortality rates are often high and regeneration of this tree has been problematic, which greatly hinders its utilization at a large scale. Cultivation difficulties of some tree species in the family Olacaceae have been attributed to their root hemiparasitic habit. Prompted by field observations and the taxonomic proximity of M. oleifera to root hemiparasites in Olacaceae, we hypothesized that tuberous structures observed on the roots of M. oleifera are parasitic organs known as haustoria. To test this hypothesis, we collected root samples from M. oleifera plants of various ages and growth conditions, investigated the morphological and anatomical features of tuberous structures and their connections to neighboring roots. Our analyses confirmed that M. oleifera are root hemiparasites. To the best of our knowledge, this is the first empirical report on root hemiparasitism in M. oleifera. Because life strategies of root hemiparasitic plants differ greatly from autotrophic plants, the root hemiparasitic habit needs to be taken into account for successful seedling regeneration of M. oleifera. This study establishes the foundation for investigations into a long-neglected but essential aspect in research of these highly valued tree species.

Antimicrobial activity of four species of Berberidaceae.

Ethanolic extracts of the stems and leaves of Nandina domestica, Mahonia fortunei, Mahonia bealei and Berberis thunbergii were tested for their antibacterial and antifungal activity. Most of the extracts have been proved to be active against Gram(+) bacteria.

Long-Distance Dispersal after the Last Glacial Maximum (LGM) Led to the Disjunctive Distribution of Pedicularis kansuensis (Orobanchaceae) between the Qinghai-Tibetan Plateau and Tianshan Region.

Quaternary climate fluctuations have profoundly affected the current distribution patterns and genetic structures of many plant and animal species in the Qinghai-Tibetan Plateau (QTP) and adjacent mountain ranges, e.g. Tianshan (TSR), Altay, etc. In this greater area disjunct distributions are prominent but have nevertheless received little attention with respect to the historical processes involved. Here, we focus on Pedicularis kansuensis to test whether the current QTP and TSR disjunction is the result of a recent Holocene range expansion involving dispersal across arid land bridge(s) or a Pleistocene range fragmentation involving persistence in refugia. Two chloroplast DNA spacers were sequenced for 319 individuals from 34 populations covering the entire distribution range of this species in China. We found a total of 17 haplotypes of which all occurred in the QTP, and only five in the TSR. Overall genetic diversity was high (HT = 0.882, HS = 0.559) and higher in the QTP than in the TSR. Genetic differentiation among regions and populations was relatively low (GST = 0.366) and little evidence for a phylogeographic pattern emerged. The divergence times for the four main lineages could be dated to the early Pleistocene. Surprisingly, the two ubiquitous haplotypes diverged just before or around the Last Glacial Maximum (LGM) and were found in different phylogenetic lineages. The Species Distribution Model suggested a disappearance of P. kansuensis from the TSR during the LGM in contrast to a relatively constant potential distribution in the QTP. We conclude that P. kansuensis colonized the TSR after the LGM. The improbable long-distance dispersal by wind or water across arid land seed flow may well have had birds or men as vector.

Two sympatric root hemiparasitic Pedicularis species differ in host dependency and selectivity under phosphorus limitation.

Parasitic biology of Pedicularis L. (Orobanchaceae) has been underinvestigated despite its wide distribution and potential ecological significance. To better understand the parasitic aspects of the root hemiparasites, host-parasite interactions were investigated with two sympatric Pedicularis species, Pedicularis rex C. B. Clarke and Pedicularis tricolor Hand.-Mazz., at two developmental stages. Plant DW, shoot phosphorus (P) content, root:shoot ratio and number of haustoria were measured in Pedicularis grown with either a host plant or a plant of its own species in pot experiments. In addition, effects of parasitism and intraspecific competition on growth and biomass allocation in four host species belonging to three major functional groups (grasses, legumes and forbs) were investigated. The two Pedicularis species showed obvious host preference, but preferred different host species. Interactions between Pedicularis and their hosts depended on both species identity and developmental stages of the partners. Overall, P. rex showed much weaker host dependency and less damage to hosts than P. tricolor. Interspecific variations were observed among different host species in their responses to intraspecific competition and parasitism. We concluded that different Pedicularis-host pairs showed different interaction patterns. Sympatric Pedicularis may have differential influence on plant community structure and productivity.

Arbuscular mycorrhizal fungi may serve as another nutrient strategy for some hemiparasitic species of Pedicularis (Orobanchaceae).

As an important component of plant kingdom, parasitic plants have intrigued many scientists with their heterotrophic strategy. Numerous investigations have been carried out for a better understanding of interactions between parasitic plants and their hosts. Nevertheless, studies on parasitic plants from a mycorrhizal perspective are lacking, largely because of the notion that parasitic plants do not form mycorrhizal associations. Although long being regarded as nonmycorrhizal, some Pedicularis species are recently found to be heavily colonized by mycorrhizal fungi. Because the precise information about parasitism of Chinese Pedicularis has been lacking, we surveyed both the mycorrhizal status and parasitism of 29 Pedicularis species from the northwest of Yunnan Province, China, to test the hypothesis that some Pedicularis may be mycorrhizal and parasitic simultaneously. The majority of studied species were found to be parasitic as well as mycorrhizal. In some cases, parasitic organs and arbuscular mycorrhizal fungi (AMF) were detected in the same rootlets. The results suggest that some Pedicularis species may have another nutrient strategy (e.g., mycotrophy) besides being parasitic. Also, the findings indicate that host plants as well as AMF should be taken into account in cultivation of Pedicularis species.

Mycorrhizal and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province, China.

Colonization of mycorrhizal and root endophytic fungi in 14 Pedicularis species from northwest of Yunnan Province, southwest China, was examined. These species included: Pedicularis gracilis Wall., Pedicularis longipes Maxim., Pedicularis axillaris Franch., Pedicularis cephalantha Franch., Pedicularis tenuisecta Franch., Pedicularis tapaoensis Tsoong, Pedicularis likiangensis Franch., Pedicularis dichotoma Bonati, Pedicularis yui Li, Pedicularis rhinanthoides Schrenk, Pedicularis rex C.B. Clarke, Pedicularis longiflora Rudolph., Pedicularis siphonantha Don, and Pedicularis oxycarpa Franch., among which nine are endemic to China (one to Yunnan). Three types of potentially beneficial fungi associated with roots of these species were observed, namely, arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and dark septate endophytic fungi (DSEF), with DSEF as the most common colonizers. An unexpected high colonization level was detected in this hemiparasitic genus. Of the 19 sampling sites examined, 10 gave colonization frequency of above 50% and 6 showed a colonization index of above 50. Heavy colonization suggested a significant ecological role of these fungi and their potential to be applied to successful cultivation of these intractable plants.