The effect of Puccinia jaceae var. solstitialis on the yellow starthistle biological control insects Eustenopus villosus and Chaetorellia succinea

Six insect biocontrol agents have been introduced, with limited success, for managing the invasive plant yellow starthistle (Centaurea solstitialis). In 2003, a recently introduced fungal rust agent, Puccinia jaceae var. solstitialis, was approved for release in California. The presence of the rust in this multi-species complex was evaluated for its effect on performance of the two most common insect biocontrol agents for yellow starthistle, Chaetorellia succinea and Eustenopus villosus. To accomplish this, yellow starthistle was planted in 1 m² plots in monocultures at three densities and in a competition replacement series with wild oat (Avena fatua) in both 2006 and 2007. Twenty seedheads were dissected from each plot to evaluate the effect of P. jaceae on seedhead maturation and insect attack rate. In the replacement series experiment in 2007 and in 2006 and 2007 combined, P. jaceae caused a 35% and 20% increase, respectively, in the proportion of mature seedheads compared to total seedheads. However, there were no significant differences in the density experiment in either year or in the replacement series experiment in 2006. Although P. jaceae appeared to have a slight effect on yellow starthistle seedhead maturation, there was no effect of the rust on seedhead attack rates of either insect biological control, regardless of the experiment or year. These results indicate that P. jaceae does not interact significantly with the insect biological control agents for yellow starthistle.     

Climatic analysis to determine where to collect and release Puccinia jaceae var. solstitialis for biological control of yellow starthistle

Puccinia jaceae var. solstitialis is an autoecious rust fungus that is native to areas of Afro-Eurasia with a Mediterranean climate. An isolate collected near Sivas, Turkey was released for classical biological control of yellow starthistle (YST), which is an invasive alien weed in California, USA. The fungus has been released throughout California, but long-term establishment rates are generally low, apparently because this ecotype is not well adapted to the climate where the weed is most invasive. Using a site with excellent establishment as a target, the Match Climates function in CLIMEX climate modeling software identified similar sites in and around the San Francisco Bay Area, east to the Central Valley and Sierra foothills, and along the coast of Southern California. Similar sites in other states include Walla Walla, Washington, Pendelton, Oregon and Salt Lake City, Utah. A Compare Locations model based primarily on experimentally measured temperature and humidity requirements of the rust produced similar results. Using Sacramento, California, which is in the center of YST distribution, as a target, the Match Climates function predicted that the best locations to search for rust accessions to use in California are near Tunis, Tunisia, Foggia, Italy, Khalkis, Greece, Kayseri, Turkey, and possibly Constantine, Algeria. This generally agrees with the prediction of a Compare Locations model based on the geographic distribution of YST in California. Climatic factors that limit the long-term establishment of the fungus are likely to be summer heat and/or dry stress and short dew periods.     

Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis)

Identifying sources of genetic variation and reconstructing invasion routes for non‐native introduced species is central to understanding the circumstances under which they may evolve increased invasiveness. In this study, we used genome‐wide single nucleotide polymorphisms to study the colonization history of Centaurea solstitialis in its native range in Eurasia and invasions into the Americas. We leveraged this information to pinpoint key evolutionary shifts in plant size, a focal trait associated with invasiveness in this species. Our analyses revealed clear population genomic structure of potential source populations in Eurasia, including deep differentiation of a lineage found in the southern Apennine and Balkan Peninsulas and divergence among populations in Asia, eastern Europe and western Europe. We found strongest support for an evolutionary scenario in which western European populations were derived from an ancient admixture event between populations from eastern Europe and Asia, and subsequently served as the main genetic ‘bridgehead’ for introductions to the Americas. Introductions to California appear to be from a single source region, and multiple, independent introductions of divergent genotypes likely occurred into the Pacific Northwest. Plant size has evolved significantly at three points during range expansion, including a large size increase in the lineage responsible for the aggressive invasion of the California interior. These results reveal a long history of colonization, admixture and trait evolution in C. solstitialis, and suggest routes for improving evidence‐based management decisions for one of the most ecologically and economically damaging invasive species in the western United States.     

Assessing the biological control of yellow starthistle (Centaurea solstitialis L): prospective analysis of the impact of the rosette weevil (Ceratapion basicorne (Illiger))

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Inheritance of resistance to clopyralid and picloram in yellow starthistle (Centaurea solstitialis L.) is controlled by a single nuclear recessive gene

The noxious weed yellow starthistle (Centaurea solstitialis L.) can be controlled effectively at the seedling stage with foliar application of the auxinic herbicides picloram or clopyralid. Although resistance to these herbicides is rare, a yellow starthistle biotype resistant to picloram and cross-resistant to clopyralid was observed in 1989 near Dayton, WA, in a pasture that had been subjected to intensive picloram selective pressure. Our objective was to determine the mode of inheritance for this resistance trait. Transmission of the resistant phenotype was monitored in reciprocal F(1) crosses between susceptible (SCI) and resistant (RDW) plants, their testcross and pseudo-F(2) progeny. Progeny from all crosses, as well as RDW and SCI seedlings of original populations, were sprayed with picloram or clopyralid to distinguish between susceptible and resistant individuals. All F(1) progeny were susceptible to both herbicides, indicating that the resistance trait was of nuclear origin and recessive in nature. Segregation of the resistant phenotype among pseudo-F(2) and testcross progeny of F(1) genotypes demonstrated monofactorial inheritance (P >.25) for resistance to both herbicides. The conclusion that resistance is conferred by a single recessive allele is consistent with the observation that no other picloram-resistant yellow starthistle populations have been identified in the area since picloram selection pressure was abated.     

Synchytrium solstitiale sp. nov. causing a false rust on Centaurea solstitialis in France

A new species of Synchytrium, S. solstitiale, infecting leaves of Centaurea solstitialis in France, is described and illustrated. Synchytrium solstitiale causes development of orange to red galls on the leaves and petioles of living plants. It differs microscopically from all previously described species of the genus mainly in having larger sporangia and zoospores and resting spores that are formed in succession without an evanescent prosoral stage.     

Phytochemical and Cytogenetic Characterization of Centaurea solstitialis L. (Asteraceae) from Croatia

The cytogenetic characterization of Centaurea solstitialis L. (Asteraceae) showed a chromosome number of 2n = 16. Karyotype is composed by four pairs of metacentric, two pairs of submetacentric and two pairs of subtelocentric chromosomes. Physical mapping of two rDNA probes revealed two loci of 35S and one locus of 5S rRNA genes. Chromomycin fluorochrome banding revealed that all rDNA loci were GC rich. The genome size (2C‐value) of 1.95 pg classes this species in the group of very small genomes. Chemical composition of C. solstitialis volatile oil (VO) from Croatia, studied with gas chromatography–mass spectrometry showed dominant components as it follows: hexadecanoic acid, α‐linolenic acid, germacrene D and heptacosane. Antioxidant capacity, measured by ferric reducing power assay and 2,2‐diphenyl‐1‐picrylhydrazyl methods, as well as inhibition of acetyl‐ and butyrylcholinesterase of VO was lower comparing to a standard solutions. Volatile oil tested with disc diffusion method showed good inhibitory potential against Pseudomonas aeruginosa, Escherichia coli and all tested fungi: Candida albicans, Penicillium funiculosum and Aspergillus fumigatus. The microdilution method showed best activity against Chronobacter sakazakii and A. fumigatus.     

Antiviral and antimicrobial activities of three sesquiterpene lactones from Centaurea solstitialis L. ssp. solstitialis

Three sesquiterpene lactones (centaurepensin=chlorohyssopifolin A, chlorojanerin and 13-acetyl solstitialin A) isolated from the aerial parts of Centaurea solstitialis L. ssp. solstitialis (Asteraceae) were investigated for antimicrobial and antiviral activities. For the antimicrobial activity assessment, both standard and isolated strains of Escherichia coli, Pseudomonas aeruginosa, Enterococcus faecalis, Staphylococcus aureus, Candida albicans and C. parapsilosis were employed by the microdilution method. Herpes simplex type-1, a DNA virus, and Parainfluenza, an RNA virus, were employed for the determination of the antiviral activity of these three sesquiterpene lactones using Vero cell lines. Ampicilline, ofloxocine, ketoconazole, fluconazole, acyclovir and oseltamivir were used as the reference drugs. 13-Acetyl solstitialin A displayed remarkable antibacterial activity against isolated strains of E. faecalis at 1 μg/ml concentration, which was close to the effective concentrations of ampicillin. The same compound also showed significant activity against the DNA virus, being as potent as the reference compound acyclovir at maximum and minimum concentrations of 16–<0.00006 μg/ml. This is the first report showing that 13-acetyl solstitialin A possesses significant antiviral activity.     

Defoliation of Centaurea solstitialis Stimulates Compensatory Growth and Intensifies Negative Effects on Neighbors

Efforts to arrest the spread of invasive weeds with herbivory may be hindered by weak effects of the herbivores or strong compensatory responses of the invaders. We conducted a greenhouse experiment to study the effects of defoliation and soil fungi on competition between the invasive weed Centaurea solstitialis and C. solstitialis and Avena barbata, a naturalized Eurasian annual grass, and Nassella pulchra, a native California bunchgrass. Surprisingly, considering the explosive invasion of grasslands by C. solstitialis, Avena and Nassella were strong competitors and reduced the invader’s biomass by 80.2% and 80.1% over all defoliation and soil fungicide treatments, respectively. However, our experiments were conducted in artificial environments where competition was probably accentuated. When fungicide was applied to the soil, the biomass of C. solstitialis was reduced in all treatment combinations, but reduction in the biomass of the invader had no corollary impact on the grasses. There was no overall effect of defoliation on the final biomass of C. solstitialis as the invader compensated fully for severe clipping. In fact, the directional trend of the clipping effect was +6.4% over all treatments after eight weeks. A significant neighbor × soil fungicide × clipping effect suggested that the compensatory response was the strongest without soil fungicide and when C. solstitialis was alone (+ 19%). Our key finding was that the compensatory response of C. solstitialis in all treatments was associated with an increase in the weed’s negative effects on Nassella and Avena – there was a significant decrease in the total biomass of both grasses and the reproductive biomass of Avena in pots with clipped C. solstitialis. Our results were obtained in controlled conditions that may have been conducive to compensatory growth, but they suggest the existence of mechanisms that may allow C. solstitialis, like other Centaurea species, to resist herbivory.     

Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France

Puccinia striiformis f. sp. tritici (PST), a clonal basidiomycete causing yellow rust disease on wheat, has a long record of 'overcoming' cultivar resistance introduced by breeders. Despite the long dispersal capacity of its spores, the French population of PST presents a strong geographical structure, with the presence of a specific pathotype (array of avirulence genes) at high frequencies in the south of France. The genetic diversity underlying this differentiation was analysed by microsatellite and AFLP markers. A total of 213 French isolates belonging to 10 pathotypes collected over a 15-year period were investigated. For each of the 12 microsatellites used, polymorphism resulted from a unique allelic variant associated to the south-specific pathotype. This pathotype was characterized by 40 specific markers over the total of 63 polymorphins detected using 15 AFLP primer combinations. Phylogeographical analysis indicated a strictly clonal structure of the population, and a strong genomic divergence between the northern population and a south-specific clone. Both virulence and molecular data show that the northern French population belongs to the northwestern European population, whereas the southern clone is most likely related to a Mediterranean population, the two subpopulations resulting from the ancient divergence of two clonal lineages. While the virulence complexity in the northern population may be explained by the successive introduction of corresponding resistance genes in cultivars, the maintenance of a simple virulence type in southern France, despite gene flow between the two populations, may be explained in terms of host cultivars repartition and local adaptation to specific host or climatic conditions.     

Dispersal Pathways and Genetic Differentiation among Worldwide Populations of the Invasive Weed Centaurea solstitialis L. (Asteraceae)

The natural history of introduced species is often unclear due to a lack of historical records. Even when historical information is readily available, important factors of the invasions such as genetic bottlenecks, hybridization, historical relationships among populations and adaptive changes are left unknown. In this study, we developed a set of nuclear, simple sequence repeat markers and used these to characterize the genetic diversity and population structure among native (Eurasian) and non-native (North and South American) populations of Centaurea solstitialis L., (yellow starthistle). We used these data to test hypotheses about the invasion pathways of the species that were based on historical and geographical records, and we make inferences about historical relationships among populations and demographic processes following invasion. We confirm that the center of diversity and the native range of the species is likely the eastern Mediterranean region in the vicinity of Turkey. From this region, the species likely proceeded to colonize other parts of Europe and Asia via a slow, stepwise range expansion. Spanish populations were the primary source of seed to invade South America via human-mediated events, as was evident from historical records, but populations from the eastern Mediterranean region were also important. North American populations were largely derived from South America, but had secondary contributors. We suggest that the introduction history of non-native populations from disparate parts of the native range have allowed not just one, but multiple opportunities first in South America then again in North America for the creation of novel genotypes via intraspecific hybridization. We propose that multiple intraspecific hybridization events may have created especially potent conditions for the selection of a noxious invader, and may explain differences in genetic patterns among North and South America populations, inferred differences in demographic processes, as well as morphological differences previously reported from common garden experiments.     

Laboratory and field experimental evaluation of host plant specificity of Aceria solstitialis, a prospective biological control agent of yellow starthistle

Centaurea solstitialis (yellow starthistle, Asteraceae) is an invasive annual weed in the western USA that is native to the Mediterranean Region and is a target for classical biological control. Aceria solstitialis is an eriophyid mite that has been found exclusively in association with Ce. solstitialis in Italy, Greece, Turkey and Bulgaria. The mite feeds on leaf tissue and damages bolting plants, causing stunting, witch’s broom and incomplete flower development. Field experiments and laboratory no-choice and two-way choice experiments were conducted to assess host plant specificity of the mite in Bulgaria. Mites showed the highest degree of host specificity in the field and lowest in the no-choice experiments. In the field, highest densities of mites occurred on Ce. solstitialis and Ce. cyanus (bachelor’s button), and either no mites or trace numbers occurred on the other test plants: Ce. diffusa (diffuse knapweed), Carthamus tinctorius (safflower) and Cynara scolymus (artichoke). In no-choice experiments, mites persisted for 60 days on Ce. diffusa, Ce. cyanus, Ce. solstitialis, Ca. tinctorius and Cy. scolymus, whereas in two-way choice experiments mites persisted on 25% of Cy. scolymus plants for 60 days and did not persist on Ca. tinctorius beyond 40 days. The eight other species of plants that were tested in the laboratory were less suitable for the mite. These results suggest that although A. solstitialis can persist on some nontarget plants for as long as 60 days in the laboratory, it appears to be much more specific under natural conditions, and warrants further evaluation as a prospective biological control agent.     

Comparison of the effect of elevated CO2 on an invasive species (Centaurea solstitialis) in monoculture and community settings

The ongoing increase in atmospheric CO₂ concentration ([CO₂]) is likely to change the species composition of plant communities. To investigate whether growth of a highly invasive plant species, Centaurea solstitialis (yellow starthistle), was affected by elevated [CO₂], and whether the success of this species would increase under CO₂ enrichment, I grew the species in serpentine soil microcosms, both as a monoculture and as a component of a grassland community. Centaurea grown in monoculture responded strongly to [CO₂] enrichment of 350 mol mol^–1, increasing aboveground biomass production by 70%, inflorescence production by 74%, and midday photosynthesis by an average of 132%. When grown in competition with common serpentine grassland species, Centaurea responded to CO₂ enrichment with similar but nonsignificant increases (+69% aboveground biomass, +71% inflorescence production), while total aboveground biomass of the polyculture increased by 28%. Centaurea's positive CO₂ response in monoculture and parallel (but non-significant) response in polyculture provoke questions about possible consequences of increasing CO₂ for more typical California grasslands, where the invader already causes major problems.     

Effect of leaf age and nitrogen fertilisation on sporulation of crown rust (Puccinia coronata var. lolii) on perennial ryegrass (Lolium perenne L.)

Individual leaves of perennial ryegrass cv. Aberystwyth S23 of two leaf ages and at two levels of nitrogen fertilisation were point inoculated with Puccinia coronata f.sp. coronata in a growth chamber. In general, there was no significant difference in the lifespan of inoculated versus control leaves. However, the higher rate of nitrogen extended leaf lifespan more markedly in rusted than in control leaves. Uredospore production varied according to leaf age: colonies on juvenile leaves produced three times as many spores as those on mature leaves.     

Pollinator Interactions with Yellow Starthistle (Centaurea solstitialis) across Urban,Agricultural, and Natural Landscapes

Pollinator-plant relationships are found to be particularly vulnerable to land use change. Yet despite extensive research in agricultural and natural systems, less attention has focused on these interactions in neighboring urban areas and its impact on pollination services. We investigated pollinator-plant interactions in a peri-urban landscape on the outskirts of the San Francisco Bay Area, California, where urban, agricultural, and natural land use types interface. We made standardized observations of floral visitation and measured seed set of yellow starthistle (Centaurea solstitialis), a common grassland invasive, to test the hypotheses that increasing urbanization decreases 1) rates of bee visitation, 2) viable seed set, and 3) the efficiency of pollination (relationship between bee visitation and seed set). We unexpectedly found that bee visitation was highest in urban and agricultural land use contexts, but in contrast, seed set rates in these human-altered landscapes were lower than in natural sites. An explanation for the discrepancy between floral visitation and seed set is that higher plant diversity in urban and agricultural areas, as a result of more introduced species, decreases pollinator efficiency. If these patterns are consistent across other plant species, the novel plant communities created in these managed landscapes and the generalist bee species that are favored by human-altered environments will reduce pollination services.     

Genetic control of durable resistance to yellow rust (Puccinia striiformis) in the wheat cultivar Hybride de Bersée

The wheat cultivar Hybride de Bersee is described as possessing durable resistance to yellow rust. Some races of Puccinia striiformis can infect it at the seedling stage but not severely in the field. Using euploid and aneuploid stocks of Bersee it was shown that a large part of this resistance was controlled by chromosome 5BS-7BS, the effect being detectable in seedlings and at later growth stages. Measurements of spore production from infected seedlings showed that the line ditelosomic for the 5BS arm of the chromosome was more resistant than the line ditelosomic for the 7BS arm under environments favouring high spore production, but more susceptible under environments favouring low spore production. Thus both arms of the chromosome could contribute to resistance in appropriate environments. Chromosome 5BS-7BS did not carry the factors controlling the race-specific resistance to race 37 E132 of P. striiformis. The possibility of exploiting the resistance carried by chromosome 5BS-7BS in wheat breeding programmes is discussed.     

Supplemental risk evaluations of Puccinia jaceae var. solstitialis for biological control of yellow starthistle

Additional tests of native North American Cirsium species, Saussurea americana, and modern safflower cultivars (Carthamus tinctorius) were requested by regulators and specific interest groups during the risk assessment of foreign isolates of Puccinia jaceae var. solstitialis for biological control of yellow starthistle (YST, Centaurea solstitialis) in the United States. These tests supplement an earlier, extensive host range determination that established P. jaceae from YST as generally host specific and potentially useful for biological control. The additional research was in response to potential hazards identified in an earlier study, changes in safflower cultivars, and concern that P. jaceae might cause a safflower seedling disease similar to hypocotyl infections from infestation by Puccinia carthami teliospores. S. americana, a close relative of yellow starthistle, had not been tested previously. All tests were conducted in a containment greenhouse. Foliage of 19 Cirsium species, 11 safflower cultivars, and S. americana was inoculated with urediniospores and subjected to a 16-h dew period at 18–20 °C. Neither the Cirsium species nor S. americana became infected after foliar inoculations. Compared to foliar infections by P. carthami from safflower in California, only minor infections developed from inoculations with P. jaceae. These were similar to infections observed in earlier studies, and it was not possible to maintain P. jaceae under optimal greenhouse conditions on safflower foliage. Quantitative teliospore inoculations with P. jaceae did not cause infection on safflower hypocotyls, even though large cankers occurred on plants inoculated with P. carthami teliospores. Clear microscopic evidence of infection also was observed in hypocotyls inoculated with P. carthami. These data suggest that native (including rare, threatened, or endangered) Cirsium spp., modern safflower cultivars, and S. americana are not likely to be adversely affected by the use of P. jaceae for biological control of YST. Results from these studies substantiate previous findings and were incorporated in a proposal for permission to use P. jaceae for YST control in California.