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opencc-zeroDec 2020View details →

Unique bacterial composition and assembly in a parasitic plant

How plant-associated microbiota are shaped by, and potentially contribute to the unique ecology and heterotrophic life history of parasitic plants is relatively unknown. Here, we investigate the leaf and root bacterial communities associated with the root holoparasite Orobanche hederae and its host plant Hedera spp. We sequenced the V4 region of the 16S rRNA gene from DNA extracted from leaf and root samples of naturally growing populations of Orobanche and infected and uninfected Hedera. Root bacteria inhabiting Orobanche were less diverse, had fewer co-associations, and displayed increased compositional similarity to leaf bacteria relative to Hedera. Overall, Orobanche bacteria exhibited significant congruency with Hedera root bacteria across sites, but not the surrounding soil. Infection had localized and systemic effects on Hedera bacteria, which included effects on the abundance of individual taxa and root network properties. Collectively, our results indicate that the parasitic plant microbiome is derived but distinct from host plant microbiota, exhibits increased homogenization between shoot and root tissues, and displays far fewer co-associations among individual bacterial members. Host plant infection is accompanied by modest changes of associated microbiota at both local and systemic scales compared with uninfected individuals. The results are a first step towards extending the growing insight into the assembly and function of the plant microbiome to include the ecologically unique but often overlooked guild of heterotrophic plants

opencc-zeroAug 2020View details →

Ethylene signaling mediates host invasion by parasitic plants

Parasitic plants form a specialized organ, a haustorium, to invade host tissues and acquire water and nutrients. To understand the molecular mechanism of haustorium development, we performed a forward genetics screening to isolate mutants exhibiting haustorial defects in the model parasitic plant Phtheirospermum japonicum. We isolated two mutants that show prolonged and sometimes aberrant meristematic activity in the haustorium apex, resulting in severe defects on host invasion. Whole genome sequencing revealed that the two mutants respectively have point mutations in homologs of ETHYLENE RECEPTOR 1 (ETR1) and ETHYLENE INSENSITIVE 2 (EIN2), signaling components in response to the gaseous phytohormone ethylene. Application of the ethylene signaling inhibitors also caused similar haustorial defects, indicating that ethylene signaling regulates cell proliferation and differentiation of parasite cells. Importantly, genetic disruption of host ethylene production also perturbs parasite invasion. We propose that parasitic plants utilize ethylene as a signal to invade host roots.

opencc-zeroJan 2021View details →

Towards genetic modification of plant-parasitic nematodes: Delivery of macromolecules to male germlines and expression of exogenous mRNA in second stage juveniles

Plant-parasitic nematodes are a current and future threat to food security, causing an estimated 100 billion USD in crop losses each year. The most problematic are the obligate sedentary endoparasites (primarily root knot nematodes and cyst nematodes). Progress in understanding their biology is held back by a lack of tools for functional genetics. Forward genetics is largely restricted to studies of natural variation in populations, and reverse genetics is entirely reliant on RNA interference. There is an expectation that the development of functional genetic tools would accelerate progress in plant-parasitic nematology, and hence the development of novel control solutions. Here, we develop some of the foundational biology required to deliver a functional genetic "tool kit" in plant-parasitic nematodes. We characterise the gonads of male Heterodera schachtii and Meloidogyne hapla in the context of spermatogenesis. We test and optimise various methods for the delivery, expression, and/or detection of exogenous nucleic acids in plant-parasitic nematodes. We demonstrate that delivery of macromolecules to cyst and root knot nematode male germlines is difficult but possible. Similarly, we demonstrate the delivery of oligonucleotides to root knot nematode gametes. Finally, we develop a transient expression system in plant-parasitic nematodes by demonstrating the delivery and expression of exogenous mRNA encoding various reporter genes throughout the body of H. schachtii juveniles using lipofectamine-based transfection. We anticipate these developments to be independently useful, and, taken together, will expedite the development of genetic modification protocols for sedentary endoparasitic nematodes, and ultimately catalyze research on a group of nematodes that threaten global food security.

opencc-zeroDec 2015View details →

Data from: Population structure of a vector-borne plant parasite

Parasites are among the most diverse groups of life on Earth, yet complex natural histories often preclude studies of their speciation processes. The biology of parasitic plants facilitates in situ collection of data on both genetic structure and the mechanisms responsible for that structure. Here, we studied the role of mating, dispersal and establishment in host race formation of a parasitic plant. We investigated the population genetics of a vector-borne desert mistletoe (Phoradendron californicum) across two legume host tree species (Senegalia greggii and Prosopis velutina) in the Sonoran desert using microsatellites. Consistent with host race formation, we found strong host-associated genetic structure in sympatry, little genetic variation due to geographic site and weak isolation by distance. We hypothesize that genetic differentiation results from differences in the timing of mistletoe flowering by host species, as we found initial flowering date of individual mistletoes correlated with genetic ancestry. Hybrids with intermediate ancestry were detected genetically. Individuals likely resulting from recent, successful establishment events following dispersal between the host species were detected at frequencies similar to hybrids between host races. Therefore, barriers to gene flow between the host races may have been stronger at mating than at dispersal. We also found higher inbreeding and within-host individual relatedness values for mistletoes on the more rare and isolated host species (S. greggii). Our study spanned spatial scales to address how interactions with both vectors and hosts influence parasitic plant structure with implications for parasite virulence evolution and speciation.

opencc-zeroDec 2017View details →

Data from: Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity

Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called "polydnaviruses." Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant–herbivore interactions than ever considered.

opencc-zeroDec 2017View details →

Data from: Host cues mediate growth and establishment of oak mistletoe (Phoradendron leucarpum, Viscaceae), an aerial parasitic plant.

The oak mistletoe (Phoradendron leucarpum, Viscaceae) is well-documented to exhibit preference for a few potential host species in a given locality, even when many potential host species are present. In trying to explain this distribution, we examined the mechanisms by which mistletoe seedlings recognize potentially suitable hosts in the Piney Woods ecoregion of east Texas. An initial survey of patterns of infection on the campus of Sam Houston State University revealed that water oak (Quercus nigra) was host to nearly half of the mistletoes observed, despite comprising less than 15% of trees surveyed. Field experiments demonstrated that light, host physiochemistry, and volatiles released from potential host trees serve as cues affecting the viability and establishment of mistletoe seedlings. These results provoked further study in controlled laboratory settings, in which it was demonstrated that chemical compounds in the bark of local host trees (compared to trees that serve as hosts elsewhere, but not in our survey) induce significantly although slightly greater seedling viability. Establishment of haustoria depended only on the presence of these chemicals, regardless of host species. Importantly, we demonstrated that three common monoterpenes, limonene, β-myrcene, and β-phellandrene induce a positive growth response of mistletoe radicles. These results taken together suggest a model to explain local host preference in P. leucarpum, in which covariation between mistletoe fruit maturity and monoterpene production by hosts determines the distribution of successful haustorial establishment.

opencc-zeroDec 2018View details →

Data from: Sequential horizontal gene transfers from different hosts in a widespread Eurasian parasitic plant, Cynomorium coccineum

Premise of the study: Parasites with large geographic ranges, and different hosts in parts of their range, might acquire horizontally-transferred genes (HGTs), which might sometimes leave a footprint of gradual host and range expansion. Cynomorium coccineum, the only member of the Saxifragales family Cynomoriaceae, is a root holoparasite that occurs in water-stressed habitats from western China to the Canary Islands. It parasitizes at least ten angiosperm families from different orders, some of them only in parts of its range. This parasite therefore offers an opportunity to trace HGTs as long as parasite/host pairs can be obtained and sequenced. Methods: By sequencing mitochondrial, plastid, and nuclear loci from parasite/host pairs from throughout the parasite's range and with prior information from completely assembled mitochondrial and plastid genomes, we detected ten HGTs of five mitochondrial genes. Key Results: The ten HGTs appear to have occurred sequentially as C. coccineum expanded from East to West. Molecular-clock models yield Cynomorium stem ages between 66 and 156 Myr, with relaxed clocks converging on 66–67 Myr. Chinese Sapindales, probably Nitraria, were the first source of transferred genes, followed by Iranian and Mediterranean Caryophyllales. The most recently acquired gene appears to come from a Tamarix host in the Iberian Peninsula. Conclusion: Data on HGTs that have accumulated over the past 15 years, along with this discovery of multiple HGTs within a single widespread species, underline the need for more whole-genome data from parasite/host pairs to investigate if and how transferred copies coexist with, or replace, native functional genes. In compliance with data protection regulations, you may request that we remove your personal registration details at any time. (Use the following URL: https://www.editorialmanager.com/ajb/login.asp?a=r) Please contact the publication office if you have any questions.

opencc-zeroJul 2019View details →

Data from: A native parasitic plant and soil microorganisms facilitate a native plant co-occurrence with an invasive plant

Invasive plants often interact with antagonists that include native parasitic plants and pathogenic soil microbes, which may reduce fitness of the invaders. However, to date, most of the studies on the ecological consequences of antagonistic interactions between invasive plants and the resident biota focused only on pairwise interactions. A full understanding of invasion dynamics requires studies that test the effects of multiple antagonists on fitness of invasive plants and co-occurring native plants. Here, we used an invasive plant Mikania micrantha, a co-occurring native plant Coix lacryma-jobi, and a native holoparasitic plant Cuscuta campestris to test whether parasitism on M. micrantha interacts with soil fungi and bacteria to reduce fitness of the invader and promote growth of the co-occurring native plant. In a factorial set up, M. micrantha and C. lacryma-jobi were grown together in pots in the presence versus absence of parasitism on M. micrantha by C. campestris, and in the presence versus absence of full complements of soil bacteria and fungi. Fungicide and bactericide were used to suppress soil fungi and bacteria, respectively. Findings show that heavy parasitism by C. campestris caused the greatest reduction in M. micrantha biomass when soil fungi and bacteria were suppressed. In contrast, the co-occurring native plant C. lacryma-jobi experienced the greatest increase in biomass when grown with heavily parasitized M. micrantha and in the presence of a full complement of soil fungi and bacteria. Taken together, our results suggest that selective parasitism on susceptible invasive plants by native parasitic plants and soil microorganisms may diminish competitive ability of invasive plants and facilitate native plant co-existence with invasive plants.

opencc-zeroDec 2012View details →

Data from: The impact of spatial scale and habitat configuration on patterns of trait variation and local adaptation in a wild plant parasite

Theory indicates that spatial scale and habitat configuration are fundamental for coevolutionary dynamics and how diversity is maintained in host–pathogen interactions. Yet, we lack empirical data to translate the theory to natural host–parasite systems. In this study, we conduct a multiscale cross-inoculation study using the specialist wild plant pathogen Podosphaera plantaginis on its host plant Plantago lanceolata. We apply the same sampling scheme to a region with highly fragmented (Åland) and continuous (Saaremaa) host populations. Although theory predicts higher parasite virulence in continuous regions, we did not detect differences in traits conferring virulence among the regions. Patterns of adaptation were highly scale dependent. We detected parasite maladaptation among regions, and among populations separated by intermediate distances (6.0–40.0 km) within the fragmented region. In contrast, parasite performance did not vary significantly according to host origin in the continuous landscape. For both regions, differentiation among populations was much larger for genetic variation than for phenotypic variation, indicating balancing selection maintaining phenotypic variation within populations. Our findings illustrate the critical role of spatial scale and habitat configuration in driving host–parasite coevolution. The absence of more aggressive strains in the continuous landscape, in contrast to theoretical predictions, has major implications for long-term decision making in conservation, agriculture, and public health.

FIGURE 7 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 7. Micrographs of Hemicycliophora thienemanni, H. conida, Hemicaloosia graminis from turfgrasses in NC and SC. All scale bars =20µm. A. Female esophageal region of H. thienemanni. B. Vulva region of H. thienemanni. C. Female tail of H. thienemanni. D. Female esophageal region of H. conida. E,F. Vulva region of H. conida. G. Female esophageal region of Hemicaloosia graminis. H. Vulva region of Hemicaloosia graminis. I. Female tail of Hemicaloosia graminis. J. Male esophageal region of Hemicaloosia graminis. K. Male tail of Hemicaloosia graminis.

FIGURE 4 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 4. Micrographs of Belonolaimus longicaudatus and Dolichodorus heterocephalus from turfgrasses in NC and SC. All scale bars=20µm. A. Pharyngeal region of B. longicaudatus. B. Vulva region of B. longicaudatus. C. Female tail of B. longicaudatus. D,E. Male tails of B. longicaudatus. F. Pharyngeal region of D. heterocephalus. G. Vulval region of D. heterocephalus. H. Female tail of D. heterocephalus. I. Male tails of D. heterocephalus.

FIGURE 1 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 1. Micrographs of Pratylenchus penetrans, Tylenchorhynchus claytoni and Filenchus cylindricus from turfgrasses in NC and SC. Scale bars: A, B, J=50 μm; C-I, K-M=20μm. A,B. Entire body of P. penetrans. C. Pharyngeal region of P. penetrans. D,E. Female tails of P. penetrans. F. Male tail of P. penetrans. G. Pharyngeal region of T. claytoni. H. Female tail of T. claytoni. I. Male tail of T. claytoni. J. Entire body of F. cylindricus. K. Pharyngeal region of F. cylindricus. L. Vulval region of F. cylindricus. M. Female tail of F. cylindricus.

FIGURE 6 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 6. Micrographs of Hemicriconemoides chitwoodi, H. wessoni, Paratylenchus goldeni and Aphelenchoides myceliophagus from turfgrasses in NC and SC. Scale bars: A, D=50µm; B, C, E–M=20µm. A. Entire body of H. chitwoodi. B. Pharyngeal region of H. chitwoodi. C. Vulva and tail region of H. chitwoodi. D. Entire body of H. wessoni. E. Pharyngeal region of H. wessoni. F. Vulva and tail region of H. wessoni. G. Pharyngeal region of P. g o l d e n i. H. Vulva and tail region of P. goldeni. I. Pharyngeal region of A. myceliophagus. J. Vulval region of A. myceliophagus. K. Pharyngeal region of A. myceliophagus. L. Female tail of A. myceliophagus. M. Male tail of A. myceliophagus.

FIGURE 3 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 3. Micrographs of J2 of Meloidogyne graminis, M. naasi, Heterodera sp. and Cactodera sp. from turfgrasses in NC and SC. Scale bars: A, E, I, L=50µm; B–D, F–H, J, K, M–O=20µm. A. Entire body of M. graminis. B. Pharyngeal region of M. graminis. C,D. Tail of M. graminis. E. Entire body of M. naasi. F. Pharyngeal region of M. naasi. G,H. Tails of M. naasi. I. Entire body of H. sp. J. Pharyngeal region of H. sp. K. Tail of H. sp. L. Entire body of C. sp. M. Pharyngeal region of C. sp. N,O. Tails of C. sp.

FIGURE 2 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 2. Micrographs of Hoplolaimus galeatus, Scutellonema brachyurum and Helicotylenchus dihystera from turfgrasses in NC and SC. All scale bars =20 μm. A. Pharyngeal region of H. galeatus. B. Vulval region of H. galeatus. C. Female tail of H. galeatus. D,E. Male tails of H. galeatus. F. Pharyngeal region of S. brachyurum. G. Vulval region of S. brachyurum. H. Female tail of S. brachyurum. I. Pharyngeal region of H. dihystera. J. Vulva and tail region of H. dihystera.

FIGURE 5 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 5. Micrographs of Mesocriconema curvatum, M. xenoplax, M. sphaerocephala and Ogma floridense from turfgrasses in NC and SC. All scale bars=20µm. A. Pharyngeal region of M. curvatum. B. Pharyngeal region of M. xenoplax. C. Pharyngeal region of M. sphaerocephala. D,G. Female tail of M. xenoplax. E. Pharyngeal region of O. floridense. F. Female tail of M. curvatum. H. Female tail of M. sphaerocephala. I. Body with anastomoses of M. sphaerocephala. J. Vulva and tail region of O. floridense.

FIGURE 9 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 9. Micrographs of Paratrichodorus allius, Paratrichodorus minor from turfgrasses in NC and SC (Scale bars: A=100µm; B-F= 20µm). A. Female entire body of P. allius. B. Female esophageal region of P. allius. C. Female tail region of P. allius. D. Female esophageal region of P. m i n o r. E. Vulva and tail region of P. m i n o r. F. Female tail region of P. m i n o r.

FIGURE 8 in Taxonomy and morphology of plant-parasitic nematodes associated with turfgrasses in North and South Carolina, USA

FIGURE 8. Micrographs of Xiphinema americana, X. bakeri, X. chambersi, Longidorus paralongicaudatus from turfgrasses in NC and SC. All scale bars =20µm. A. Female esophageal region of X. americana. B. Vulva region of X. americana. C,H. Female esophageal region of X. bakeri. D. Vulva region of X. bakeri. E. Female esophageal region of X. chambersi. F. Vulva region of X. chambersi. G. Female tail region of X. americana. I. Female tail region of X. bakeri. J. Female tail region of X. chambersi. K. Female esophageal region of L. paralongicaudatus. L. Vulva region of L. paralongicaudatus. M,N. Female tail region of L. paralongicaudatus.