A species-specific recognition system directs haustorium development in the parasitic plant Triphysaria (Scrophulariaceae)

Parasitic plants use host molecules to trigger developmental programs essential for parasitism. One such program governs the initiation, development, and function of haustoria, parasite-specific organs responsible for attachment and invasion of host tissues. Haustoria development can be initiated by several different molecules produced by appropriate host species. We are interested in understanding how these signals are interpreted by two related facultative parasites, Triphysaria eriantha (Benth.) Chuang and Heckard, and T. versicolor Fischer and C. Meyer, to distinguish their own roots from those of potential hosts. We used an in vitro bioassay to determine what proportion of different Triphysaria populations formed haustoria in the presence and absence of closely related and unrelated host species. We found that the proportion of plants with haustoria was the same whether the plants were grown in isolation or with a conspecific host. In contrast, a significantly higher proportion of plants made haustoria when the host was a congeneric Triphysaria. Plants with haustoria neither enhanced nor inhibited other plants' propensity to form haustoria. Together these results indicate that qualitative differences exist in haustorium-inducing factors exuded by closely related species. The highest proportion of Triphysaria had haustoria when grown with Arabidopsis thaliana (L.) Heynh. Even in this case, however, some Triphysaria failed to develop haustoria. Interestingly, the percentage of haustoria that had vessel elements was higher when connections were made with Arabidopsis than with another Triphysaria. These results demonstrate that host recognition can be manifested at multiple points in haustorium development. Received: 18 December 1996 / Accepted: 14 February 1997     

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%...     

Haustoria in action: Case studies of nitrogen acquisition by woody xylem-tapping hemiparasites from their hosts

Summary This review discusses studies conducted by the author and his colleagues on mistletoes and root hemiparasites native to Western Australia. Morphological characteristics of haustoria are described and their anatomical features are discussed in relation to uptake, transfer, and metabolism of xylem-borne nitrogenous solutes derived from a host. Experimental approaches used include comparisons of xylem sap composition of parasite and host(s), solute pool analyses and enzymatic properties of haustoria, host xylem feeding of¹⁵N-labelled solutes to follow the fate of label in haustoria and body of the parasite, and studies using species-specific nonprotein amino acids to validate successful uptake from hosts or occasional backflow of xylem-borne solutes to a host. Field studies on promiscuous root hemiparasites assess frequencies of exploitation of different hosts.¹⁵N natural abundance assays of host and parasite dry matter demonstrate marked preference bySantalum acuminatum for N₂-fixing as opposed to nonfixing hosts. The ability ofOlax phyllanthi to continue to exploit deep-rooted hosts ranks of importance when xylem water potentials of other hosts go out of sucking range during periods of water stress. Comparisons of xylem sap composition of parasites feeding on different hosts indicate remarkable versatility by haustoria in uptake and utilization of the different major nitrogenous solutes received from these hosts. Solute pools in parasites partly reflect metabolic transformations accentuated by haustoria while also indicating direct throughput from xylem of a host. The review concludes by showing how empirically based modelling techniques can be used to estimate proportional gains of N by parasites from single hosts and repercussions on host growth which accompany such exploitation.Dedicated to Professor Brian E. S. Gunning on the occasion of his 65th birthday     

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     

檀香与不同豆科植物寄生关系的研究

为了解檀香(Santalum album L.)与不同豆科植物的寄生关系,选取11种具有重要经济价值的豆科植物和檀香一起种植,对檀香叶片的光合特征和株高、地径以及寄主植物根系的吸器大小进行了测定。结果表明,檀香的吸器大小、数量在不同寄主之间存在很大差异,不同寄主对檀香的株高、地径也有显著差异。檀香的优良寄主有美洲合欢(Calliandra haematocephala)、苏木(Caesalpinia sappan)、台湾相思(Acacia confusa)、龙牙花(Erythrina corallodendron);一般的寄主植物有马占相思(Acacia mangium)、降香黄檀(Dalbergia odorifera)、黄槐(Cassia surattensis);不适宜的寄主植物有凤凰木(Delonix regia)、海南红豆(Ormosia pinnata)、银合欢(Leucaena leucocephala)、洋紫荆(Bauhinia blakeana)。同时,檀香的株高、地径及光合特征和吸器数量密切相关。因此,檀香种植时应选择适宜的优良寄主植物。     

MODE OF ATTACHMENT,HAUSTORIUM STRUCTURE,AND HOSTS OF PEDICULARIS CANADENSIS

Piehl, Martin A. (Botanic Garden, Santa Barbara, Calif.) Mode of attachment, haustorium structure, and hosts of Pedicularis canadensis. Amer. Jour. Bot. 50(10): 978–985. Illus. 1963.—Although long known for European members of the genus, parasitism is documented for the first time for the North American Pedicularis canadensis (Scrophulariaceae) from observations made in the field. Every stand examined showed evidence for parasitism, the haustorial connections being established in the seedling stage. The haustoria, which vary somewhat morphologically, produce direct connection between the xylem of the host and that of the parasite. The great diversity of hosts, involving 80 species from 35 families, suggests that connections may be made to essentially any vascular plant with subterranean parts in proximity to those of the parasite, although some species are parasitized much more frequently than others. In addition, haustorial attachments were found to dead parts of vascular plants and, in single instances, to a fungus and small pebbles. Intraspecific parasitism has also been observed.     

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.     

Host range and selectivity of the hemiparasitic plant Thesium chinense (Santalaceae)

Background and Aims

Thesium chinense is a hemiparasitic plant that is common in grassland habitats of eastern Asia. Although the physiology of Thesium has been well studied in attempts to control its weedy habit, there have been few ecological investigations of its parasitic life history. Thesium chinense is thought to parasitize species of Poaceae, but evidence remains circumstantial.

Methods

A vegetation survey was conducted to test whether any plant species occurs significantly more often in plots with T. chinense than expected. In addition, haustorial connections were examined directly by excavating the roots and post-attachment host selectivity was evaluated by comparing the observed numbers of haustoria on different hosts against those expected according to the relative below-ground biomass. Haustorium sizes were also compared among host species.

Key Results

Only two of the 38 species recorded, Lespedeza juncea and Eragrostis curvula, occurred more often in plots with Thesium than expected. In contrast to this, T. chinense parasitized 22 plant species in 11 families, corresponding to 57·9 % of plant species found at the study site. Haustoria were non-randomly distributed among host species, suggesting that there is some post-attachment host selectivity. Thesium chinense generally preferred the Poaceae, although haustoria formed on the Fabaceae were larger than those on other hosts.

Conclusions

This is the first quantitative investigation of the host range and selectivity of hemiparasitic plants of the Santalales. The preference for Fabaceae as hosts may be linked to the greater nutrient availability in these nitrogen-fixing plants.Key words: Haustorium, hemiparasite, host range, host selectivity, Santalaceae, Thesium chinense     

Host-synthesized cysteine protease-specific inhibitor disrupts <Emphasis Type="Italic">Cuscuta campestris</Emphasis> parasitism in tomato

Dodder (Cuscuta campestris) is one of the most important pests of tomato causing severe losses in yield. Cuscutain is a pre-pro-protein produced by dodder that has a cysteine proteinase function essential for normal development of the haustoria and parasitism, which involves the secretion and activation of cuscutain cysteine protease in the host plant tissue. The propeptide subunit of this enzyme has an inhibitory function and restricts the enzymatic activity of cuscutain. Here, we transformed the inhibitory propeptide segment of this enzyme into tomato and examined the tomato resistance to C. campestris. We demonstrate the expression of inhibitory propeptide in transgenic plants and find that it effectively interrupted cuscutain enzyme activity and haustoria development at the endophytic stage. Mature haustoria infecting transgenic hosts showed defects in searching hyphae development and these structures were not elongate, and in most cases no functional haustoria were formed due to inhibitor expression in the transgenic plants after prehaustoria contact. Dodder grown on transgenic lines showed an overall reduction in vigor and fecundity due to defective attachment of haustoria. The increased growth of dodder-challenged transgenic plants relative to controls, demonstrates the efficacy of cysteine protease inhibition in parasite plant control.     

The hemibiotrophic lifestyle of Colletotrichum species

Colletotrichum species infect several economically important crop plants. To establish a compatible parasitic interaction, a specialized infection cell, the melanized appressorium, is differentiated on the cuticle of the host. After penetration, an infection vesicle and primary hyphae are formed. These structures do not kill the host cell and show some similarities with haustoria formed by powdery mildews and rust fungi. Therefore, this stage of infection is called biotrophic. Later in the infection process, necrotrophic secondary hyphae spread within and kill the host tissue. The lifestyle of Colletotrichum species is called hemibiotrophic, as biotrophic and necrotrophic developmental stages are sequentially established. As most Colletotrichum species are accessible to molecular techniques, genes can be identified and functionally characterized. Here we demonstrate that Agrobacterium tumefaciens-mediated transformation is a well-suited method for tagging of genes mediating compatibility in the Colletotrichum graminicola–maize interaction.     

Habitat requirements and host selectivity of Thesium species (Santalaceae)

The aim of this study was to identify the habitat requirements and host specificity of three root parasites in the genus Thesium (T. linophyllon, T. bavarum and T. ebracteatum). We conducted a vegetation survey and tested whether some plant species occur significantly more often in plots with Thesium spp. than expected, thereby representing potential hosts of the parasites. To test if the potential hosts are the species to which Thesium is physically attached, we also conducted an excavating and sowing experiment. We found a positive association with surrounding species for T. linophyllon, but not for the other two species. The number of haustoria of T. linophyllon attached to roots of host species was significantly affected by the number of roots of the surrounding species and by their identity (species, family and plant group). Thesium was, however, attached to 94% of all species occurring in the plots. We suggest that Thesium spp. do not specifically select hosts, but rather occur in microhabitats with specific conditions. This conclusion is also supported by the fact that there were differences in the microhabitats with and without Thesium and that germination of Thesium in the sowing experiment was higher in pots without any host. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164 , 394–408.     

Haustorial Development and Growth Benefit to Seedlings of the Root Hemiparasitic Tree Nuytsia floribunda(Labill.) R.Br. in Association with Various Hosts

Dry matter gains and haustorial production of pot-cultured seedlingsof Nuytsia floribunda were assessed after a 12 month periodof association singly with each of a range of potential woodyhost species. One species,Adenanthos cygnorum , of similar sizeto most parasitized hosts, served as measure of response ofNuytsia in a non-benefiting situation. Rated on this basis,all 23 parasitized hosts elicited greater mean dry weights ofNuytsia than when on Adenanthos, and seven of these instanceswere highly significant. Numbers and weights of penetratingand presumably functional haustoria formed on a host were broadlycorrelated with growth benefit to Nuytsia, but there were notableinstances of unusually poor or great benefit from a host relativeto the complement of haustoria involved. Experiments in whichhaustoria-bearing associations of Nuytsia partnered with nodulatedAcacia hosts (Acacia acuminata and A. cyclops) were fed¹⁵N₂showedsignificant transfer of¹⁵N to the parasite, but failed to determinewhether the label had been acquired through haustoria or directlyby Nuytsia roots following turnover of nodule and root residuesof the host in the rooting medium. A parallel study using theunusual non-protein amino acid, djenkolic acid, as a markerof benefit from the djenkolic acid-containing host A. cyclops,showed appearance and progressive build-up of the compound infoliage of Nuytsia over a 6 month period after partnering thespecies in pot culture. Presence of the compound at final harvestin xylem sap of both partners but not in soil solution of thecultures strongly indicated xylem transfer via haustoria asthe principal avenue for N benefit to the parasite. Resultsare discussed in relation to a recent evaluation of haustorialstructure and functioning of N. floribunda. Copyright 2000 Annalsof Botany Company Root hemiparasite, Nuytsia, Loranthaceae, growth benefit, haustorial production, nitrogen transfer from hosts     

The double cloak of invisibility: phenotypic plasticity and larval decoration in a geometrid moth,Synchlora frondaria,across three diet treatments

Abstract 1. Crypsis is one of the main defences that insects use to avoid predators, and both the juveniles and adults of many geometrid moths are remarkable in their ability to blend into different host backgrounds. The larvae of Synchlora frondaria have two methods to achieve crypsis: phenotypic plasticity in colouration that enable them to hide more effectively on their host plants, and a self‐decorating behaviour whereby the larvae camouflage themselves with materials from their host plants. 2. Larvae of Synchlora frondaria reared on three different host plants showed systematic differences in relative growth rate, survivorship and larval colouration. 3. Larval colouration varied across diet treatments in a way that was consistent with diet‐induced phenotypic plasticity, and larvae also exhibited characteristic decorating behaviour on all three hosts. 4. Larvae showed highest survivorship on Heterotheca subaxillaris (Asteraceae), and had significantly higher relative growth rates on H. subaxillaris (Asteraceae) and Lantana camara (Verbenaceae) than on Bejaria racemosa (Ericaceae). 5. Synchlora frondaria provides an example of a species where both decorating behaviour and phenotypic plasticity in larval colouration produce a cryptic form that is remarkably responsive to its background.     

Comparative haustorium morphology and vegetative reproduction in the Old World genus Scurrula L. (Loranthaceae) from the Central Nepal Himalayas

In a comparative morphological study of haustoria in the four Scurrula species occurring in the Annapurna Conservation Area (ACA) of Nepal, only one basic type of haustorium was found, regardless of host and elevation, namely a primary haustorium (leading to a wood rose) with epicortical root. The endophytic system of the primary haustorium, however, showed differences, which allowed classification into (1) flanging endophyte, (2) flanging endophyte with radial shaft, and (3) sinker endophyte. Scurrula elata and Scurrula gracilifolia showed marked differences in haustorium morphology on different hosts. Scurrula elata is most successful in establishing over a wide range of hosts due to its specific haustorium morphology and endophyte system. Epicortical roots of the genus Scurrula resemble those of other Old World Loranthaceae morphologically and functionally, but differ significantly from New World species. Vegetative reproduction by means of epicortical roots, which develop secondary haustoria and shoots, is very common in all four Scurrula species. The number of root-borne shoots produced by secondary haustoria varied among Scurrula species, depending on the age of the mistletoes as well as the length and vigour of the roots.     

檀香吸器维管组织的个体发育

为了解檀香吸器维管组织的发育过程,采用激光共聚焦显微镜、光学显微镜和透射电镜观察檀香吸器维管组织的个体发育。结果表明,檀香维管组织的分化分为两个时期:入侵前和入侵后。吸器维管组织发育始于盘状吸器时期,起源于吸器基部具有分生能力的细胞,后分为两束。侵入前无向顶的分化,处于吸器基部。侵入后随吸管深入寄主根与寄主根维管束连通,形成具有吸收功能的维管组织。成熟吸器维管组织呈倒烧瓶结构,仅处于吸器烧瓶核心两边,由木质部组成而无韧皮部。檀香的吸器维管组织发育有两个因素诱导,一个是遗传因素,另一个为寄主。这些为檀香半寄生性特性研究提供了形态解剖学基础。     

Genetic variation in a phylogenetic context: Responses of two specialized leaf beetles (Coleoptera: Chrysomelidae) to host plants of their congeners

This work explores the possibility that constraints on genetic variation guide host shifts and are responsible for the evolutionary conservatism of host affiliation in phytophagous insects. To this end, we used full- and half-sib breeding designs to screen two species of the North American bettle genus Ophraella for genetic variation in larval and adult feeding responses to several host plants of other species of Ophraella. All the plants are in the family Asteraceae. In O. conferta, we observed effectively no feeding response, and hence no genetic variation in response, to three of five test plant species; only those plants related to the species' natural hosts evoked genetically variable responses. In O. artemisiae, adults displayed genetic variation in response to a congener of the natural host, but not to two distantly related plants. However, significant variation among full-sib broods in larval feeding suggests the existence of nonadditive genetic variance in feeding response to all five species of test plants—although survival was very low on most of them. The results suggest that patterns of presence versus apparent absence of detectable genetic variation may be related to the chemical similarity of plants to the insects' natural hosts, but not evidently to the phylogenetic history of host affiliation within the genus. Almost all genetic correlations in responses to host plants were not significantly different from zero; the few significant correlations were positive, and negative correlations that might explain host specificity were not found. Our data do not explain why exclusive shifts to new hosts should occur, but the apparent lack of genetic variation in responses to some plants suggests that the direction of host shifts is genetically constrained.     

Arabinogalactan protein-rich cell walls,paramural deposits and ergastic globules define the hyaline bodies of rhinanthoid Orobanchaceae haustoria

Background and Aims

Parasitic plants obtain nutrients from their hosts through organs called haustoria. The hyaline body is a specialized parenchymatous tissue occupying the central parts of haustoria in many Orobanchaceae species. The structure and functions of hyaline bodies are poorly understood despite their apparent necessity for the proper functioning of haustoria. Reported here is a cell wall-focused immunohistochemical study of the hyaline bodies of three species from the ecologically important clade of rhinanthoid Orobanchaceae.

Methods

Haustoria collected from laboratory-grown and field-collected plants of Rhinanthus minor, Odontites vernus and Melampyrum pratense attached to various hosts were immunolabelled for cell wall matrix glycans and glycoproteins using specific monoclonal antibodies (mAbs).

Key Results

Hyaline body cell wall architecture differed from that of the surrounding parenchyma in all species investigated. Enrichment in arabinogalactan protein (AGP) epitopes labelled with mAbs LM2, JIM8, JIM13, JIM14 and CCRC-M7 was prominent and coincided with reduced labelling of de-esterified homogalacturonan with mAbs JIM5, LM18 and LM19. Furthermore, paramural bodies, intercellular deposits and globular ergastic bodies composed of pectins, xyloglucans, extensins and AGPs were common. In Rhinanthus they were particularly abundant in pairings with legume hosts. Hyaline body cells were not in direct contact with haustorial xylem, which was surrounded by a single layer of paratracheal parenchyma with thickened cell walls abutting the xylem.

Conclusions

The distinctive anatomy and cell wall architecture indicate hyaline body specialization. Altered proportions of AGPs and pectins may affect the mechanical properties of hyaline body cell walls. This and the association with a transfer-like type of paratracheal parenchyma suggest a role in nutrient translocation. Organelle-rich protoplasts and the presence of exceptionally profuse intra- and intercellular wall materials when attached to a nitrogen-fixing host suggest subsequent processing and transient storage of nutrients. AGPs might therefore be implicated in nutrient transfer and metabolism in haustoria.     

Constraints on host use by a parasitic plant

Consumers do not always utilize all suitable hosts. Understanding why parasitic plants do not always parasitize potentially suitable hosts requires a better understanding of the constraints that limit host use by parasitic plants. In Texas salt marshes, the parasitic plant Cuscuta indecora rarely parasitizes three hosts that support vigorous growth in the greenhouse. We identified three constraints on host use by C. indecora. First, a mismatch between the phenology of C. indecora and some suitable hosts meant that these hosts were not abundant when C. indecora was growing most vigorously, and therefore were underutilized. Second, C. indecora preferentially parasitized tall plants versus short ones, causing relatively short species to be underutilized. Third, C. indecora overwinters in some perennial hosts but has to reinfect annual hosts each year, causing annuals and perennials that do not support overwintering to be underutilized. In combination, these constraints, which reflect the general lack of mobility of parasitic plants relative to herbivores, remove half of the potential host species from the actual diet of C. indecora, and therefore likely represent a major limitation on the success of this parasite. Similar constraints are likely to limit the realized host range of many parasitic plants and select for generalized diet preferences.     

Is palatability of a root-hemiparasitic plant influenced by its host species?

Palatability of parasitic plants may be influenced by their host species, because the parasites take up nutrients and secondary compounds from the hosts. If parasitic plants acquired the full spectrum of secondary compounds from their host, one would expect a correlation between host and parasite palatability. We examined the palatability of leaves of the root-hemiparasite Melampyrum arvense grown with different host plants and the palatability of these host plants for two generalist herbivores, the caterpillar of Spodoptera littoralis and the slug Arion lusitanicus. We used 19 species of host plants from 11 families that are known to contain a wide spectrum of anti-herbivore compounds. Growth of M. arvense was strongly influenced by the host species. The palatability of the individual host species for the two herbivores differed strongly. Both A. lusitanicus and S. littoralis discriminated also between hemiparasites grown with different host plants. There was no correlation between the palatability of a host species and that of the parasites grown on that host, i.e., hemiparasites grown on palatable host species were not more palatable than those grown on unpalatable hosts. We suggest an interacting pattern of specific effects of chemical anti-herbivore defences and indirect effects of the hosts on herbivores through effects on growth and tissue quality of the parasites.