蔗糖对列当科两种根部半寄生植物吸器发生的促进作用

吸器是寄生植物的特征器官,研究影响其发生的因素,有助于了解寄生关系的建立和调控过程。该研究以两种列当科(Orobanchaceae)根部半寄生植物甘肃马先蒿(Pedicularis kansuensis)和松蒿(Phtheirospermum japonicum)为材料,通过皿内培养试验,分析了蔗糖、DMBQ(2,6-二甲氧基-对-苯醌,一种高效的列当科根部半寄生植物吸器诱导化合物)和寄主植物诱导下两种根部半寄生植物吸器发生情况。结果表明：(1)蔗糖显著促进两种根部半寄生植物吸器发生,无寄主存在时,2%蔗糖处理使甘肃马先蒿和松蒿吸器发生率分别提高39.9%和20.2%。(2)蔗糖明显提升寄主植物对两种根部半寄生植物的吸器诱导水平,添加蔗糖后,寄主诱导的甘肃马先蒿单株吸器数和具木质桥的吸器比例分别增加5.7个/株和17.9%,松蒿吸器发生率和具木质桥的吸器比例分别提升76.7%和16.2%。(3)蔗糖对松蒿吸器发生的促进作用与已知吸器诱导化合物DMBQ相当,均能诱导50%以上的植株产生吸器。(4)培养基中添加4%蔗糖对两种根部半寄生植物的吸器诱导效果最好,其中甘肃马先蒿吸器发生率为56%...     

Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolor

Perhaps the most obvious phenotypes associated with chemical signaling between plants are manifested by parasitic species of Orobanchaceae. The development of haustoria, invasive root structures that allow hemiparasitic plants to transition from autotrophic to heterotrophic growth, is rapid, highly synchronous, and readily observed in vitro. Haustorium development is initiated in aseptic roots of the facultative parasite Triphysaria versicolor when exposed to phenolic molecules associated with host root exudates and rhizosphere bioactivity. Morphological features of early haustorium ontogeny include rapid cessation of root elongation, expansion, and differentiation of epidermal cells into haustorial hairs, and cortical cell expansion. These developmental processes were stimulated in aseptic T. versicolor seedlings by the application of exogenous phytohormones and inhibited by the application of hormone antagonists. Surgically dissected root tips formed haustoria if the root was exposed to haustorial-inducing factors prior to dissection. In contrast, root tips that were dissected prior to inducing-factor treatment were unable to form haustoria unless supplemented with indole-3-acetic acid. A transient transformation assay demonstrated that auxin and ethylene-responsive promoters were up-regulated when T. versicolor was exposed to either exogenous hormones or purified haustoria-inducing factors. These experiments demonstrate that localized auxin and ethylene accumulation are early events in haustorium development and that parasitic plants recruit established plant developmental mechanisms to realize parasite-specific functions.     

Progress in parasitic plant biology: host selection and nutrient transfer

Host range varies widely among species of parasitic plants. Parasitic plants realize host selection through induction by chemical molecular signals, including germination stimulants and haustoria-inducing factors (HIFs). Research on parasitic plant biology has provided information on germination, haustorium induction, invasion, and haustorial structures and functions. To date, some molecular mechanisms have been suggested to explain how germination stimulants work, involving a chemical change caused by addition of a nucleophilic protein receptor, and direct or indirect stimulation of ethylene generation. Haustorium initiation is induced by HIFs that are generated by HIF-releasing enzymes from the parasite or triggered by redox cycling between electrochemical states of the inducers. Haustorium attachment is non-specific, however, the attachment to a host is facilitated by mucilaginous substances produced by haustorial hairs. Following the attachment, the intrusive cells of parasites penetrate host cells or push their way through the host epidermis and cortex between host cells, and some types of cell wall-degrading enzymes may assist in the penetration process. After the establishment of host-parasite associations, parasitic plants develop special morphological structures (haustoria) and physiological characteristics, such as high transpiration rates, high leaf conductance, and low water potentials in hemiparasites, for nutrient transfer and resource acquisition from their hosts. Therefore, they negatively affect the growth and development and even cause death of their hosts.     

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.     

In Vitro Haustorium Development in Roots and Root Cultures of the Hemiparasitic Plant Triphysaria Versicolor

Parasitic plants in the Orobanchaceae invade host plant roots through root organs called haustoria. Parasite roots initiate haustorium development when exposed to specific secondary metabolites that are released into the rhizosphere by host plant roots. While molecular approaches are increasingly being taken to understand the genetic mechanism underlying these events, a limitation has been the lack of a transformation system for parasitic plants. Since the haustorium development occurs in roots of Orobanchaceae, root cultures may be suitable material for transient or stable transformation experiments. To this end, root cultures were obtained from explants, and subsequently calluses, from the hemiparasitic plant Triphysaria versicolor. The cultured roots retained their competence to form haustoria when exposed to host roots, host root exudates, or purified haustorium-inducing factors. The root culture haustoria invaded host roots and initiated a vascular continuity between the parasite and host roots. The ontogeny of haustoria development on root cultures was indistinguishable from that on seedlings roots. Root cultures should provide useful material for molecular studies of haustorium development.     

Autotrophy and heterotrophy in root herniparasites

More than 3000 species of flowering plants are at least partially parasitic, acquiring water and solutes from the host via haustoria. More than one third of all parasitic angiosperms - the root hemiparasites - possess green leaves and root systems. In these species there are potentially two opportunities for the capture of water and solutes: an autotrophic or abiotic supply from the external environment, and a heterotrophic or host-derived supply via the haustoria. Most root hemiparasites occur in the Scrophulariaceae, a family also containing autotrophic and holoparasitic plants. Between these two extremes, the root hemiparasites provide an ideal opportunity to investigate the balance between the autotrophic and heterotrophic modes of nutrition in parasitic plants. The tropical hemiparasites within this family are important weeds of cereals and legumes, causing considerable crop losses, and thus fuelling research into the nutritional dependency of these plants on their hosts. These studies have led to some exciting new ideas, particularly with respect to the carbon relations of these plants.     

EXPERIMENTAL INITIATION OF HAUSTORIA IN AGALINIS PURPUREA (SCROPHULARIACEAE)

The initiation and early developmental stages of the haustorium were studied in Agalinis purpurea (Scrophulariaceae). Plants were grown in a 0.9% agar inorganic medium with a 0.5% sucrose supplement. Root exudate collected from Lespedeza sericea induced the initiation of haustoria, with earliest stages evident in 6-12 hr. A 30-min exposure to exudate produced an increased frequency of haustoria and a 24-hr exposure yielded haustorial frequencies equal to the number that were initiated on control plants continuously exposed to root exudate for the 5-day growth period. The early cytological features of haustorial development are described and the possible significance of haustorial initiation in host recognition is discussed.     

檀香幼苗半寄生性初步研究

在不同寄主植物繁殖的基础上,研究了檀香(Santalum album L．)幼苗对寄主植物的半寄生性。檀香种子发芽及幼苗生长初期,并不需要寄主植物的参与,但随后的生长其根系必须寄生于适宜的寄主植物的根上。不同寄主植物对檀香幼苗的生长和吸器的发育影响不同,表现在根寄生吸器的数量、大小和结合的程度上。初步筛选了扶桑(Hibiscus rosa-sinensis)、烂头钵(Phyllanthus reticulatus)等优良的檀香幼苗寄主植物。檀香幼苗根系极不发达,细根缺乏根毛,但其导管非常发达,有利于从寄主根吸收养分和水分。此外还观察了檀香和寄主植物扶桑建立半寄生吸器的过程。     

Polyembryony and twin seedlings in Borassus flabellifer L. (Palmae)

Polyembryony and twin seedlings are noted in Borassus flabellifer L. Both seedlings arising from a seed have an independent hatistorium, cotyledonary sheath, scale leaf and root system. There are instances where twin seedlings are identical in structure and activity; independent plants develop in the same way as normal seedlings. The haustoria of these seedlings are equal in size and activity. Cases are also recorded with disparity in size and activity between twin seedlings. While the haustorium of the bigger seedling is normal, that of the smaller seedling is reduced.     

Morphological Response of Witchweed (Striga asiatica) to In Vitro Culture

Excised sorghum root segments (5–10 mm in length) werecultured for 50 d in four different liquid media containingmineral salts, vitamins, amino acids, glucose, and IAA. Theroots were removed and the remaining medium was solidified withan equal volume of warm 1–6% water agar. Dry unconditionedor conditioned Striga asiatica seeds were transferred to themedium. Some of the seeds germinated and developed into parasitic-typeseedlings. These seedlings had haustoria, tubercles, dense roothairs, branched shoots, and multiple shoot-borne adventitiousroots. The plumule pole developed into a shoot, but the radiclepole displayed only rudimentary development. On the same media,but which had not previously been used to grow sorghum roots,the seedlings displayed a well-developed radicle-derived rootsystem, but the plumule did not grow. Shoots began to appearon the roots only after 35–50 d of culture. These seedlingshad no haustoria, no tubercles, few or scattered root hairs,no shoot-borne adventitious roots and few shoot branches, andappeared to be non-parasitic-type seedlings. Shoots grew ina medium supplemented with IAA and kinetin, but did not in amedium containing NAA plus IBA. On replacement of glucose andIAA with sucrose and 2,4-D, respectively, Striga seeds germinated,and the heart-shaped embryos dedifferentiated into calli. Thecalli have been maintained by subculturing for over 9 months.The results demonstrated that a host signal, in addition tothose for germination and haustorium formation, is requiredfor further development. Moreover, morphogenesis of culturedS. asiatica is influenced by exogenous growth regulators. Key words: Striga asiatica, parasitic weeds, haustoria, Sorghum bicolor, in vitro culture     

Interactions between hemiparasitic plants and their hosts: The importance of organic carbon transfer

Hemiparasitic plants display a unique strategy of resource acquisition combining parasitism of other species and own photosynthetic activity. Despite the active photoassimilation and green habit, they acquire substantial amount of carbon from their hosts. The organic carbon transfer has a crucial influence on the nature of the interaction between hemiparasites and their hosts which can oscillate between parasitism and competition for light. In this minireview, we summarize methodical approaches and results of various studies dealing with carbon budget of hemiparasites and the ecological implications of carbon heterotrophy in hemiparasites.Key words: haustorium, heterotrophy, parasitic plant, mistletoe, Rhinanthus, Striga, δ¹³CHemiparasitic plants withdraw resources from the vascular system of their hosts through a specialized transfer organ called haustorium.¹ Hemiparasites attack the host''s xylem, in contrast to the holoparasites that infect both phloem and xylem, and as a consequence, hemiparasitic plants have access to water and mineral nutrients but little carbon.¹ Due to their reduced or non-existing root networks, hemiparasitic plants acquire virtually all mineral nutrients and water from the host while organic carbon is provided, at least in part, by their own photosynthetic activity.^2,3 This is in contrast to holoparasitic plants which rely on the host for the supply of both organic and inorganic nutrients. The location of the attachment to the host and the degree of host dependency represent the most important characters defining the three basic functional types within hemiparasitic plants. Root hemiparasites attack host roots but their above-ground appearance is usually not substantially different from that of a non-parasitic plant. This group can be further divided in two—facultative and obligate hemiparasites consisting of plants that are able (at least sometimes) or unable to complete their life cycle without an attachment to the host respectively. Stem hemiparasites are attached to the host stem (usually trunk or branches) and are all obligate parasites, unable to survive without a host.Hemiparasitic plants have an ambiguous relationship with their hosts which, on the one hand, represent exclusive sources of inorganic nutrients but on the other hand, the co-occurrence of these host plants in the hemiparasite vicinity imposes competition for light. The nature and intensity of this competitive relationship varies across different groups and species of hemiparasites. The ability of hemiparasites to acquire organic carbon (largely in the form of xylem-mobile organic and amino acids) is certainly the key factor affecting this interaction since hemiparasites that are capable of efficient organic carbon abstraction should be minimally affected by shading from their host. The fact that hemiparasites can exhibit substantial carbon heterotrophy is now supported by a large number of studies, although a traditional point of view on hemiparasites that highlights the importance of inorganic resources (mainly nitrogen) acquisition is still prevailing. Therefore, we decided to summarize available information on hemiparasite heterotrophy, outline techniques for assessing the proportion of heterotrophy and estimating the overall carbon budget, and discuss possible implications of this phenomenon on hemiparasite ecology.     

寄生植物对寄主植物的化学识别

植物间寄生关系的研究近年来受到了广泛的重视。大量的研究表明,寄主释放的次生物质对植物间寄生关系的建立和维持起了重要的调节作用。寄主植物的次生物质对寄生植物的化学防御和昆虫授粉等生态功能起重要的作用,寄主植物次生物质对寄生植物生理与生态的调节作用是受寄生植物基因调节的。更为重要的是寄主植物释放的次生物质成为寄生植物的种子萌发和吸器发生的异源识别物质。能够刺激寄生植物种子萌发的次生物质主要是倍半萜和氢醌类物质,而诱导吸器发生的物质则是酚酸、醌和黄酮类化合物,诱导吸器发生的核心结构是对苯醌。这些异源识别物质大多是寄主植物释放的化感抑制物质,显示寄生植物在化学防御方面要比寄主植物高级。异源识别化合物的活性与其氧化潜力显著相关。由于寄生植物中存在一抑制异源识别物质诱导吸器发生的调节过程,因此吸器的产生与寄生植物根部接触异源识别物质的浓度与时间呈正相关关系,这一调节过程对寄生植物准确识别寄主并寄生其上是十分重要的。对寄生植物和寄主植物间的化学识别关系的揭示有助于人们防治有害寄生植物和开发利用有价值的寄生植物资源。     

Correlations between Haustoria Formation and Parasitic Development in Orthocarpus purpurascens (Scrophulariaceae)

Three lines of evidence correlate the parasitic performane ofOrthocarpus purpuruscens Benth. with numbers of haustoria produced:(i) the pattern of variation in numbers of haustoria producedin agar culture with different chemical stimuli correspondsclosely to the variation pattern of parasite vigour producedby a range of host plants; (ii) the progeny of plants demonstratingvigorous growth with hosts produce significantly more haustoriathan progeny from parents exhibiting weak parasitic development;(iii) conversely, seedlings that produce high numbers of haustoriain agar culture grow significantly better when transplantedwith hosts than do seedlings with low numbers of haustoria.Haustoria-forming potential is heritable, but highly influencedby environmental factors. Potential number of haustoria is aproduct of the concentration and/or quality of haustoria inducingstimuli, and the parasite's individual ability to respond. Intra-populationdifferences in parasitic development appear to be largely dueto the quantity rather than the quality of substrates receivedfrom host plants. haustoria, Orthocarpus purpurarcens, parasitic development     

N-P fertilization did not reduce AMF abundance or diversity but alter AMF composition in an alpine grassland infested by a root hemiparasitic plant

Fertilization has been shown to have suppressive effects on arbuscular mycorrhizal fungi (AMF) and root hemiparasites separately in numerous investigations, but its effects on AMF in the presence of root hemiparasites remain untested. In view of the contrasting nutritional effects of AMF and root hemiparasites on host plants, we tested the hypothesis that fertilization may not show strong suppressive effects on AMF when a plant community was infested by abundant hemiparasitic plants. Plants and soil samples were collected from experimental field plots in Bayanbulak Grassland, where N and P fertilizers had been applied for three continuous years for control against a spreading root hemiparasite, Pedicularis kansuensis. Shoot and root biomass of each plant functional group were determined. Root AMF colonization levels, soil spore abundance, and extraradical hyphae length density were measured for three soil depths (0-10 cm, 10-20 cm, 20-30 cm). Partial 18S rRNA gene sequencing was used to detect AMF diversity and community composition. In addition, we analyzed the relationship between relative abundance of different AMF genera and environmental factors using Spearman's correlation method. In contrast to suppressive effects reported by many previous studies, fertilization showed no significant effects on AMF root colonization or AMF species diversity in the soil. Instead, a marked increase in soil spore abundance and extraradical hyphae length density were observed. However, fertilization altered relative abundance and AMF composition in the soil. Our results support the hypothesis that fertilization does not significantly influence the abundance and diversity of AMF in a plant community infested by P. kansuensis.     

Evolution of the secondary haustoria to a primary haustorium in the parasiticScrophulariaceae/Orobanchaceae

In the parasiticScrophulariaceae andOrobanchaceae, two types of contact organs exist: secondary and primary haustoria. Secondary haustoria are lateral organs, developing in large numbers and only when the seedling is fully established. In contrast, a primary haustorium represents the first developmental stage of the seedling itself. In the root system of the parasiticLesquereuxia syriaca (=Siphonostegia syriaca) there are only secondary haustoria, but a few of them apparently develop in a terminal position. This is achieved by transferring the haustorial initiation region closer to the root apex. One can interpret this as a transformation of the apical meristem into a meristematic haustorial tissue. On the condition that an extreme shortening (abbrevation) of the primary root could happen, we discuss the transformation of the terminal secondary into a primary haustorium.     

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

³²P 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.     

Spatial analysis of root hemiparasitic shrubs and their hosts: a search for spatial signatures of above- and below-ground interactions

Root hemiparasitic plants take up resources from the roots of neighbouring plants, which they use for fuelling their own growth. While taking up resources from the hosts below-ground, they may simultaneously compete with the hosts for sunlight. Suppression caused by the parasitism could result in openings in the vegetation structure and increased mortality levels. On the other hand, the root hemiparasites may also be constrained by the hosts, restricting the parasites to a limited number of locations within a community. These vegetation alterations and location restrictions can be referred to as spatial signatures of the root hemiparasites. In order to search for such spatial signatures, we investigated a population of a predominant Acacia species in Australia co-occurring with established root hemiparasitic shrubs, using intensity estimates of the Acacia and dead shrubs to be indicators of parasite populations. We find evidence that the root hemiparasitic shrubs, like herbaceous root hemiparasites, prefer growing at distances from neighbouring plants that fulfil resource requirements both below-ground and above-ground. Assuming that root hemiparasites are limited by their hosts, we present an optimal host density and distance to host hypothesis (‘Goldilocks hypothesis’) to account for such a vegetation pattern. Although mortality appeared to primarily result from intraspecific competition and shoot parasitism, the root parasitism could explain some of the mortality in open areas. It is likely that both processes occur simultaneously. In spite of differing annual and perennial life strategies among root hemiparasites, root parasitism across systems may follow these two general processes in the formation of vegetation patterns.     

Modelling the Population Dynamics of Root Hemiparasitic Plants Along a Productivity Gradient

Root hemiparasitic plants interact with their host plants through parasitism and competition. The interactions can be divided into aboveground and belowground interactions. Because both groups of plants are autotrophic, they compete for light aboveground. Belowground interactions are more complex. The host plants compete for resources in the soil and the hemiparasitic plants prey on the host plants through haustoria, using the hosts as the main source of water and nutrients. In this paper, we modeled the relationship between these two plant types, extending the well-known Rosenzweig-MacArthur predator-prey model to cover both light competition and intra-specific parasitism among hemiparasites. We included a realistic relationship of carrying capacity to environmental productivity and followed model behavior on a productivity gradient. The model shows that, at very low productivities, there are only a few poor hosts and hemiparasites have no chance to persist. As productivity increases, there is a range of productivity where both plant types coexist. A further increase in productivity gets the system out of the coexistence range, and only host plants survive. This final prediction successfully explains patterns observed in empirical data, contrary to the results of an earlier, oversimplified model of the explored interaction. Comparison of various models demonstrates that the model is able to reproduce the decline of hemiparasites with increasing productivity only when competition for light is included.     

Nutritional studies of Hemiparasitic Orthocarpus (Scrophulariaceae)

Excised shoot tips from Orthocarpus attenautus and O. purpurascenswere cultured in vitro to ascertain whether the stem tips ofthese hemiparasites require complex organic substances for theirdevelopment, and to determine if the capacity for haustoriaformation is retained by the resulting plantlets. Explants consistedof the apical meristem plus the four smallest leaf primordia,having a volume of less than 0.5 mm3. A variety of mineral media,sucrose concentrations, root extract, soil extract, yeast extract,and malt extract were tested for effects on growth. Both speciescompleted development in sterile culture on simple media. Orthocarpusattenuatus grew best on Knop‘s minerals with Ball’smicroelements + 0.1 g ferric citrate 1–1+ 1% (w/v) sucrose,while MurashigeSkoog‘s minerals+ 2% sucrose provided thebest growth of the media tested for O. purpurascens. Haustoriaformed on the roots of all plantlets chemically induced by cottonstring. The mean number of haustoria per plantlet was abouthalf that of control plants raised from seed. Growth of intactO. Purpurascens seedlings was also compared on mineral agar,mineral agar supplemented with yeast extract, and in soil culturessupplemented with yeast extract and a host. While yeast extracthas variable effects on the growth of shoot tip explants andintact plants raised under axenic conditions, it is highly stimulatoryto the autotrophic growth of intact plants in soil culture.