Metabolite changes with induction of Cuscuta haustorium and translocation from host plants

Cuscuta is a stem holoparasitic plant without leaves or roots, parasitizing various types of host plants and causing major problems for certain crops. Cuscuta is known as a generalist and, thus, must have unique parasite strategies to cope with different host plants. For elucidating metabolic responses and mechanisms of parasitization, metabolomic approaches using GC/MS were applied. We compared five stages of Cuscuta japonica: early stage seedlings, with far red light (FR) cue, with contact signal, haustorium induced seedlings by both signals and adult plant parasites on host plants. Sugars, amino acids, organic acids, nucleic acids, and polyols were identified from the polar phase fraction. The apical part contained metabolite profiles different from the haustorium induced part or the basal part. Amino acid and some organic acids were up-regulated for haustorium induction but decreased after parasitization. After attachment to different host plants, metabolite profiles of Cuscuta japonica changed dramatically due to the absorption of specific host plant metabolites such as pinitol. Cuscuta seedlings attached to pinitol rich host plants contained more pinitol and showed different profiles from those attached to plants having less or lacking pinitol.     

Morphological and plant hormonal changes during parasitization by Cuscuta japonica on Momordica charantia

The holostemparasitic plant Cuscuta parasitizes various plants and sucks nutrients from the host stem. We used Cuscuta japonica as the parasite and Momordica charantia as the host plant, and described their interaction. The parasitized Momordica stems started swelling as a hypertrophic response within 3 days after parasitization. Concurrently, the Cuscuta stem grew rapidly and developed bigger scale leaves than usual. Parasitized Momordica stems reduced photosynthetic activity. Histological observation revealed no programmed cell death but an increased number of vascular bundles in the Momordica stem, especially near the Cuscuta hyphae. The defensive response of Momordica mainly involved the SA pathway. Drastic increase of tZ- and DZ-type cytokinins in Momordica stems would play an important role for hypertrophy. Cuscuta had higher cZ endogenously and our results imply that each subtype of CK might play different roles during parasitization process. Comprehensive plant hormone analysis provides new insights into plant interaction studies.     

Host-produced ethylene is required for marked cell expansion and endoreduplication in dodder search hyphae

The genus Cuscuta comprises stem holoparasitic plant species with wide geographic distribution. Cuscuta spp. obtain water, nutrients, proteins, and mRNA from their host plants via a parasitic organ called the haustorium. As the haustorium penetrates into the host tissue, search hyphae elongate within the host tissue and finally connect with the host’s vascular system. Invasion by Cuscuta spp. evokes various reactions within the host plant’s tissues. Here, we show that, when Arabidopsis (Arabidopsis thaliana) is invaded by Cuscuta campestris, ethylene biosynthesis by the host plant promotes elongation of the parasite’s search hyphae. The expression of genes encoding 1-aminocylclopropane-1-carboxylic acid (ACC) synthases, ACC SYNTHASE2 (AtACS2) and ACC SYNTHASE6 (AtACS6), was activated in the stem of Arabidopsis plants upon invasion by C. campestris. When the ethylene-deficient Arabidopsis acs octuple mutant was invaded by C. campestris, cell elongation and endoreduplication of the search hyphae were significantly reduced, and the inhibition of search hyphae growth was complemented by exogenous application of ACC. In contrast, in the C. campestris-infected Arabidopsis ethylene-insensitive mutant etr1-3, no growth inhibition of search hyphae was observed, indicating that ETHYLENE RESPONSE1-mediated ethylene signaling in the host plant is not essential for parasitism by C. campestris. Overall, our results suggest that C. campestris recognizes host-produced ethylene as a stimulatory signal for successful invasion.

Growth of Cuscuta campestris search hyphae is inhibited in ethylene-deficient Arabidopsis mutants, suggesting that host-derived ethylene acts as a stimulatory signal for parasitism by Cuscuta spp.     

<Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> is a susceptible host plant for the holoparasite <Emphasis Type="Italic">Cuscuta </Emphasis>spec

Arabidopsis thaliana and Cuscuta spec. represent a compatible host–parasite combination. Cuscuta produces a haustorium that penetrates the host tissue. In early stages of development the searching hyphae on the tip of the haustorial cone are connected to the host tissue by interspecific plasmodesmata. Ten days after infection, translocation of the fluorescent dyes, Texas Red (TR) and 5,6-carboxyfluorescein (CF), demonstrates the existence of a continuous connection between xylem and phloem of the host and parasite. Cuscuta becomes the dominant sink in this host–parasite system. Transgenic Arabidopsis plants expressing genes encoding the green fluorescent protein (GFP; 27 kDa) or a GFP–ubiquitin fusion (36 kDa), respectively, under the companion cell (CC)-specific AtSUC2 promoter were used to monitor the transfer of these proteins from the host sieve elements to those of Cuscuta. Although GFP is transferred unimpedly to the parasite, the GFP–ubiquitin fusion could not be detected in Cuscuta. A translocation of the GFP–ubiquitin fusion protein was found to be restricted to the phloem of the host, although a functional symplastic pathway exists between the host and parasite, as demonstrated by the transport of CF. These results indicate a peripheral size exclusion limit (SEL) between 27 and 36 kDa for the symplastic connections between host and Cuscuta sieve elements. Forty-six accessions of A. thaliana covering the entire range of its genetic diversity, as well as Arabidopsis halleri, were found to be susceptible towards Cuscuta reflexa.     

Diet mixing in a parasitic plant: adaptation or constraint?

Some herbivores deliberately consume a mixed diet, either to obtain a superior mix of nutrients or to avoid consuming too much of any one toxin. Few studies have examined diet mixing in parasitic plants, which typically have very broad host ranges. We offered the parasitic plant Cuscuta indecora (dodder), a range of mixtures of two hosts (Iva frutescens and Borrichia frutescens) in the greenhouse, and observed correlations between the host community and Cuscuta infection in the field. In the greenhouse, Cuscuta performed better on mixtures with a higher relative abundance of Iva. Cuscuta selectively foraged on whichever host was more abundant (diet switching), the exact opposite of the behavior that would be expected if diet mixing was advantageous. In the field, the intensity of Cuscuta infections was decreased by the presence of non-hosts (grasses), not strongly affected by the presence of intermediate hosts, and increased by the presence of Borrichia. We conclude that Cuscuta does not obtain nutritional benefits from a broad diet, but instead is constrained by its relative lack of mobility to attack hosts of intermediate value. In general, the lack of mobility of parasitic plants compared to herbivores probably selects for broad host ranges in parasitic plants.     

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.     

Like herbivores,parasitic plants are limited by host nitrogen content

Herbivores generally benefit from increased plant nitrogen content, because the nitrogen content of animals is much higher than that of plants. Consequently, high plant nitrogen alleviates the profound stoichiometric imbalance that herbivores face in their diets. Parasitic plants provide the opportunity to test this generalization for consumers across kingdoms. We fertilized two microhabitats in a California salt marsh that were dominated by Salicornia virginica or a mixture of S. virginica and Jaumea carnosa. The nitrogen content of both host plants and of the holoparasite Cuscuta salina (dodder) increased in fertilized plots in both microhabitats. Cuscuta preferred to attack Jaumea, although Jaumea had lower nitrogen content than Salicornia. When host nitrogen content was altered by fertilizing plots, however, the percent cover of the parasite doubled. Although parasitic plants and their hosts have similar tissue nitrogen contents, suggesting no stoichiometric imbalance between host and consumer, parasitic plants do not feed on host tissue, but on host xylem and phloem, which are very low in nitrogen. Consequently, parasitic plants face the same dietary stoichiometric constraints as do herbivores, and both herbivores and holoparasitic plants may respond positively to increases in host nitrogen status.     

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%...     

Signaling Organogenesis in Parasitic Angiosperms: Xenognosin Generation, Perception, and Response

Abstract Parasitic strategies within the angiosperms generally succeed by tightly coupling developmental transitions with host recognition signals in a process referred to as xenognosis. Within the Scrophulariaceae, Striga asiatica is among the most studied and best understood parasitic member with respect to the processes of host recognition. Specific xenognosins regulate seed germination, the development of the host attachment organ, the haustorium, and several later stages of host-parasite integration. Here we discuss the signals regulating the development of the haustorium, the critical vegetative/parasitic transition in the life cycle of this obligate parasite. We provide evidence for the localized production of H₂O₂ at the Striga root tip and suggest how this oxidant is used to exploit host peroxidases and cell wall pectins to generate a simple benzoquinone signal. This benzoquinone xenognosin proves to be both necessary and sufficient for haustorial induction in cultured seedlings. Furthermore, evidence is provided that benzoquinone binding to a redox active site completes a ``redox circuit' to mediate signal perception. This redox reaction regulates the time-dependent expression of specific marker genes critical for the development of the mature host attachment organ. These studies extend the emerging series of events necessary for the molecular regulation of organogenesis within the parasitic plants and suggest novel signaling features and molecular mechanisms that may be common across higher plants.     

Physiological and ecological warnings that dodders pose an exigent threat to farmlands in Eastern Africa

Invasive holoparasitic plants of the genus Cuscuta (dodder) threaten African ecosystems due to their rapid spread and attack on various host plant species. Most Cuscuta species cannot photosynthesize and hence rely on host plants for nourishment. After attachment through a peg-like organ called a haustorium, the parasites deprive hosts of water and nutrients, which negatively affects host growth and development. Despite their rapid spread in Africa, dodders have attracted limited research attention, although data on their taxonomy, host range, and epidemiology are critical for their management. Here, we combine taxonomy and phylogenetics to reveal the presence of field dodder (Cuscuta campestris) and C. kilimanjari (both either naturalized or endemic to East Africa), in addition to the introduction of the giant dodder (C. reflexa), a south Asian species, in continental Africa. These parasites have a wide host range, parasitizing species across 13 angiosperm orders. We evaluated the possibility of C. reflexa to expand this host range to tea (Camelia sinensis), coffee (Coffea arabica), and mango (Mangifera indica), crops of economic importance to Africa, for which haustorial formation and vascular-bundle connections in all three crops revealed successful parasitism. However, only mango mounted a successful postattachment resistance response. Furthermore, species distribution models predicted high habitat suitability for Cuscuta spp. across major tea- and coffee-growing regions of Eastern Africa, suggesting an imminent risk to these crops. Our findings provide relevant insights into a poorly understood threat to biodiversity and economic wellbeing in Eastern Africa, and provide critical information to guide development of management strategies to avert Cuscuta spp. spread.

Microscopy and habitat suitability modeling provide an early warning that dodder’s invasion in Eastern Africa poses a threat to important cash crops.     

Taste input from tarsal sensilla is related to egg‐laying behavior in Papilio hospiton

In herbivorous insects, host selection involves various sensory modalities (sight, smell, taste), but the contact chemoreceptors capable of detecting stimuli both from host and non‐host plants play an important role in the final steps of oviposition behavior. Female butterflies scratch and drum the leaf surface and taste the compounds present in plant saps with their tarsal chemosensilla. We assumed that tarsal taste sensitivity may be related to the breadth of host selection in ovipositing females of Papilio hospitonGéné (Lepidoptera: Papilionidae). The spike activity of tarsal taste basiconic sensilla was recorded in response to stimulation with NaCl, bitter compounds, and carbohydrates, with the aim of characterizing the gustatory receptor neurons (GRNs) and of comparing the response patterns in the light of differences in acceptability of host plants. Then we studied the sensitivity of GRNs to saps of the host plants Ferula communis L., Peucedanum paniculatumLoisel, Pastinaca latifolia (Duby) DC. (all Apiaceae), and Ruta lamarmorae Bacch., Brullo et Giusso (Rutaceae), and evaluated the relationship between taste sensitivity and oviposition preference. The results indicate that (1) each sensillum houses sugar‐, bitter‐, and salt‐sensitive cells; (2) the spike activity of the gustatory neurons in response to plant saps produces a different response pattern across all active GRNs; and (3) the number of eggs laid on each plant is highest on F. communis and lowest on R. lamarmorae. These results suggest that the varying activity of the tarsal GRNs may affect host plant acceptability and that ovipositing females of P. hospiton seem to be able to discriminate between host plants.     

Host plant selection behaviour of Chilo partellus and its implication for effectiveness of a trap crop

Female lepidopterans can display a hierarchy of preference among potential host species, a trait thought to arise from the balance between attractants and deterrents to which the insects respond. Host plant ranking by moths and larvae of Chilo partellus Swinhoe (Lepidoptera: Crambidae), an important pest of cereals in Africa, was investigated, and whether eggs deposited on specific host plants yield larvae of particular host preferences. Trap plants are used in management of this pest. However, any ‘disagreement’ in host ranking between moths and larvae could potentially reduce effectiveness of trap crops as larvae emigrate to the main crop from the parent’s preferred trap plant. We also investigated whether host plant preference is influenced by the diet upon which larvae fed as part of an integrated assessment of the relationship between host plant selection and learning in C. partellus. Five host plants (all Poaceae) were used: maize (Zea mays L.), sorghum (Sorghum bicolor Moench), Napier grass (Pennisetum purpureum Schumach), and two varieties of signal grass [Brachiaria brizantha (A. Rich.) Stapf], viz., local (henceforth signal grass) and improved (‘Mulato’). In multiple choice tests, C. partellus female moths preferentially oviposited on Napier grass, followed by sorghum, maize, and signal grass, and least preferred ‘Mulato’. Larvae however equally orientated and settled on leaf cuts of maize, sorghum, signal grass, and Napier grass, but least preferred ‘Mulato’. Moreover, eggs from specific host plants did not yield larvae of particular host preferences. Furthermore, oviposition preference was not altered by the larval food. These results imply only a slight ‘disagreement’ in host ranking behaviour between moths and larvae, which is beneficial for trap cropping as larvae would not ‘reject’ the trap plant and appreciably disperse to the neighboring plants. Moreover, absence of larval learning behaviour indicates that regardless of the larval food C. partellus moths would still be attracted to the selected trap plant.     

Das Phloem der Haustorien vonCuscuta

Summary Haustoria ofCuscuta odorata R. & P. andC. grandiflora H.B.K. show continuous traces of sieve elements, connecting the phloem of the host with that of theCuscuta shoot. The continuity of this haustorial phloem is discernible by callose fluorescence after staining with aniline blue. The fine structural criteria for sieve tubes are analyzed electronmicroscopically, with special respect to sieve pores, P-protein, and a distinct wall-standing smooth surfaced ER. Within the central part of the haustorium sieve tubes are elongated, while the elements abutting the phloem of theCuscuta shoot are nearly isodiametric in shape. Both elements are associated with rather large companion cells, derived from an unequal division.

     

Ferulic acid is a putative surrender signal to stimulate programmed cell death in grapevines after infection with Neofusicoccum parvum

An apoplectic breakdown from grapevine trunk diseases (GTDs) has become a serious challenge to viticulture as a consequence of drought stress. We hypothesize that fungal aggressiveness is controlled by a chemical communication between the host and colonizing fungus. We introduce the new concept of a ‘plant surrender signal’ accumulating in host plants under stress and facilitating the aggressive behaviour of the strain Neofusicoccum parvum (Bt-67) causing Botryosphaeriaceae-related dieback in grapevines. Using a cell-based experimental system (Vitis cells) and bioactivity-guided fractionation, we identify trans-ferulic acid, a monolignol precursor, as a ‘surrender signal’. We show that this signal specifically activates the secretion of the fungal phytotoxin fusicoccin A aglycone. We show further that this phytotoxin, mediated by 14-3-3 proteins, activates programmed cell death in Vitis cells. We arrive at a model showing a chemical communication facilitating fusicoccin A secretion that drives necrotrophic behaviour during Botryosphaeriaceae–Vitis interaction through trans-ferulic acid. We thus hypothesize that channelling the phenylpropanoid pathway from this lignin precursor to the trans-resveratrol phytoalexin could be a target for future therapy.     

Does legume nitrogen fixation underpin host quality for the hemiparasitic plant Rhinanthus minor?

The high quality of leguminous hosts for the parasitic plantRhinanthus minor (in terms of growth and fecundity), comparedwith forbs (non-leguminous dicots) has long been assumed tobe a function of the legume's ability to fix atmospheric nitrogen(N) from the air and the potential for direct transfer of compatibleamino compounds to the parasite. Using associations betweenRhinanthus minor and Vicia faba (Fabaceae) that receive N eitherexclusively via symbiotic associations with rhizobia supplyingorganic N fixed from N₂ or exclusively through the supply ofinorganic nitrate to the substrate, the underlying reasons forthe quality of legumes as hosts for this parasite are unravelled.It is shown that sole dependence of the host, V. faba, on Nfixation results in lower growth of the attached parasite thanwhen the host is grown in a substrate supplied exclusively withinorganic N. In contrast, the host plants themselves achieveda similar biomass irrespective of their N source. The physiologicalbasis for this is investigated in terms of N and abscisic acid(ABA) partitioning, haustorial penetration, and xylem sap aminoacid profiles. It is concluded that legume N fixation does notunderpin the quality of legumes as hosts for Rhinanthus butrather the well-developed haustorium formed by the parasite,coupled with the lack of defensive response of the host tissuesto the invading haustorium and the presence of sufficient nitrogenouscompounds in the xylem sap accessible to the parasite haustoria,would appear to be the primary factors influencing host qualityof the legumes. Key words: ABA, haustorium, legume, nitrogen fixation, nodules, parasitic plant Received 14 November 2007; Revised 7 January 2008 Accepted 8 January 2008     

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。     

Adaptation of the parasitic plant lifecycle: germination is controlled by essential host signaling molecules

Parasitic plants are plants that connect with a haustorium to the vasculature of another, host, plant from which they absorb water, assimilates, and nutrients. Because of this parasitic lifestyle, parasitic plants need to coordinate their lifecycle with that of their host. Parasitic plants have evolved a number of host detection/host response mechanisms of which the germination in response to chemical host signals in one of the major families of parasitic plants, the Orobanchaceae, is a striking example. In this update review, we discuss these germination stimulants. We review the different compound classes that function as germination stimulants, how they are produced, and in which host plants. We discuss why they are reliable signals, how parasitic plants have evolved mechanisms that detect and respond to them, and whether they play a role in host specificity. The advances in the knowledge underlying this signaling relationship between host and parasitic plant have greatly improved our understanding of the evolution of plant parasitism and are facilitating the development of more effective control measures in cases where these parasitic plants have developed into weeds.

Root parasitic plants grow on the roots of other plants and germinate only in the presence of that host, on which they completely depend, through the perception of host presence signaling molecules called germination stimulants.

Outstanding questions

• Have we overlooked the role of germination stimulants in facultative parasites?
• What is the biological relevance of the observation that many plant species produce and secrete a range of different strigolactones?
• Have parasitic plants evolved mechanisms to compensate for low phosphorus availability, a condition that stimulates their germination?
• What is the contribution of the HTL strigolactone receptors to host specificity in parasitic plants or does downstream signaling play a role?
• What other, nonstrigolactone, germination stimulants can parasitic plants respond to and does this require adaptation in the HTL receptors?
• What is the role of germination and underlying mechanism in the rapid adaptation of (orobanchaceous) parasitic plants to a new host?