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The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
P.O Box 12, Rehovot 76100, ISRAEL

Tel: 08-9489223 
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Email: orlytal@savion.huji.ac.il

Publications

2019
Yang, R. ; Garcia, D. S. ; Montaño, F. P. ; Da Silva, G. M. ; Zhao, M. ; Guerrero, I. J. ; Rosenberg, T. ; Chen, G. ; Plaschkes, I. ; Morin, S. ; et al. Complete assembly of the genome of an Acidovorax citrulli strain reveals a naturally occurring plasmid in this species. Frontiers in Microbiology 2019, 10. Publisher's VersionAbstract
Acidovorax citrulli is the causal agent of bacterial fruit blotch (BFB), a serious threat to cucurbit crop production worldwide. Based on genetic and phenotypic properties, A. citrulli strains are divided into two major groups: group I strains have been generally isolated from melon and other non-watermelon cucurbits, while group II strains are closely associated with watermelon. In a previous study, we reported the genome of the group I model strain, M6. At that time, the M6 genome was sequenced by MiSeq Illumina technology, with reads assembled into 139 contigs. Here, we report the assembly of the M6 genome following sequencing with PacBio technology. This approach not only allowed full assembly of the M6 genome, but it also revealed the occurrence of a ∼53 kb plasmid. The M6 plasmid, named pACM6, was further confirmed by plasmid extraction, Southern-blot analysis of restricted fragments and obtention of M6-derivative cured strains. pACM6 occurs at low copy numbers (average of ∼4.1 ± 1.3 chromosome equivalents) in A. citrulli M6 and contains 63 open reading frames (ORFs), most of which (55.6%) encoding hypothetical proteins. The plasmid contains several genes encoding type IV secretion components, and typical plasmid-borne genes involved in plasmid maintenance, replication and transfer. The plasmid also carries an operon encoding homologs of a Fic-VbhA toxin-antitoxin (TA) module. Transcriptome data from A. citrulli M6 revealed that, under the tested conditions, the genes encoding the components of this TA system are among the highest expressed genes in pACM6. Whether this TA module plays a role in pACM6 maintenance is still to be determined. Leaf infiltration and seed transmission assays revealed that, under tested conditions, the loss of pACM6 did not affect the virulence of A. citrulli M6. We also show that pACM6 or similar plasmids are present in several group I strains, but absent in all tested group II strains of A. citrulli. Copyright © 2019 Yang, Santos Garcia, Pérez Montaño, da Silva, Zhao, Jiménez Guerrero, Rosenberg, Chen, Plaschkes, Morin, Walcott and Burdman.
2018
Eakteiman, G. ; Moses-Koch, R. ; Moshitzky, P. ; Mestre-Rincon, N. ; Vassão, D. G. ; Luck, K. ; Sertchook, R. ; Malka, O. ; Morin, S. Targeting detoxification genes by phloem-mediated RNAi: A new approach for controlling phloem-feeding insect pests. Insect Biochem Mol Biol 2018, 100, 10-21.Abstract
Many phloem-feeding insects are considered severe pests of agriculture and are controlled mainly by chemical insecticides. Continued extensive use of these inputs is environmentally undesirable, and also leads to the development of insecticide resistance. Here, we used a plant-mediated RNA interference (RNAi) approach, to develop a new control strategy for phloem-feeding insects. The approach aims to silence "key" detoxification genes, involved in the insect's ability to neutralize defensive and toxic plant chemistry. We targeted a glutathione S-transferase (GST) gene, BtGSTs5, in the phloem-feeding whitefly Bemisia tabaci, a devastating global agricultural pest. We report three major findings. First, significant down regulation of the BtGSTs5 gene was obtained in the gut of B. tabaci when the insects were fed on Arabidopsis thaliana transgenic plants expressing dsRNA against BtGSTs5 under a phloem-specific promoter. This brings evidence that phloem-feeding insects can be efficiently targeted by plant-mediated RNAi. Second, in-silico and in-vitro analyses indicated that the BtGSTs5 enzyme can accept as substrates, hydrolyzed aliphatic- and indolic-glucosinolates, and produce their corresponding detoxified conjugates. Third, performance assays suggested that the BtGSTs5 gene silencing prolongs the developmental period of B. tabaci nymphs. Taken together, these findings suggest that BtGSTs5 is likely to play an important role in enabling B. tabaci to successfully feed on glucosinolate-producing plants. Targeting the gene by RNAi in Brassicaceae cropping systems, will likely not eliminate the pest populations from the fields but will significantly reduce their success over the growing season, support prominent activity of natural enemies, eventually allowing the establishment of stable and sustainable agroecosystem.
Santos-Garcia, D. ; Juravel, K. ; Freilich, S. ; Zchori-Fein, E. ; Latorre, A. ; Moya, A. ; Morin, S. ; Silva, F. J. To B or Not to B: Comparative Genomics Suggests as a Source of B Vitamins in Whiteflies. Front Microbiol 2018, 9 2254.Abstract
Insect lineages feeding on nutritionally restricted diets such as phloem sap, xylem sap, or blood, were able to diversify by acquiring bacterial species that complement lacking nutrients. These bacteria, considered obligate/primary endosymbionts, share a long evolutionary history with their hosts. In some cases, however, these endosymbionts are not able to fulfill all of their host's nutritional requirements, driving the acquisition of additional symbiotic species. Phloem-feeding members of the insect family Aleyrodidae (whiteflies) established an obligate relationship with Portiera aleyrodidarum, which provides its hots with essential amino acids and carotenoids. In addition, many whitefly species harbor additional endosymbionts which may potentially further supplement their host's diet. To test this hypothesis, genomes of several endosymbionts of the whiteflies and were analyzed. In addition to , all three species were found to harbor one and one endosymbiont. A comparative analysis of genomes revealed that although all three are capable of synthesizing B vitamins and cofactors, such as pyridoxal, riboflavin, or folate, their genomes and phylogenetic relationship vary greatly. of and belong to the same clade, and display characteristics of facultative endosymbionts, such as large genomes (3 Mb) with thousands of genes and pseudogenes, intermediate GC content, and mobile genetic elements. In contrast, of belongs to a different lineage and displays the characteristics of a primary endosymbiont-a reduced genome (670 kb) with ~400 genes, 32% GC content, and no mobile genetic elements. However, the presence of 274 pseudogenes suggests that this symbiotic association is more recent than other reported primary endosymbionts of hemipterans. The gene repertoire of of is completely integrated in the symbiotic consortia, and the biosynthesis of most vitamins occurs in shared pathways with its host. In addition, endosymbionts have also retained the ability to produce riboflavin, flavin adenine dinucleotide, and folate, and may make a nutritional contribution. Taken together, our results show that hold a pivotal place in whitefly nutrition by their ability to produce B vitamins.
Malka, O. ; Santos-Garcia, D. ; Feldmesser, E. ; Sharon, E. ; Krause-Sakate, R. ; Delatte, H. ; van Brunschot, S. ; Patel, M. ; Visendi, P. ; Mugerwa, H. ; et al. Species-complex diversification and host-plant associations in Bemisia tabaci: A plant-defence, detoxification perspective revealed by RNA-Seq analyses. Mol Ecol 2018, 27, 4241-4256.Abstract
Insect-plant associations and their role in diversification are mostly studied in specialists. Here, we aimed to identify macroevolution patterns in the relationships between generalists and their host plants that have the potential to promote diversification. We focused on the Bemisia tabaci species complex containing more than 35 cryptic species. Mechanisms for explaining this impressive diversification have focused so far on allopatric forces that assume a common, broad, host range. We conducted a literature survey which indicated that species in the complex differ in their host range, with only few showing a truly broad one. We then selected six species, representing different phylogenetic groups and documented host ranges. We tested whether differences in the species expression profiles of detoxification genes are shaped more by their phylogenetic relationships or by their ability to successfully utilize multiple hosts, including novel ones. Performance assays divided the six species into two groups of three, one showing higher performance on various hosts than the other (the lower performance group). The same grouping pattern appeared when the species were clustered according to their expression profiles. Only species placed in the lower performance group showed a tendency to lower the expression of multiple genes. Taken together, these findings bring evidence for the existence of a common detoxification "machinery," shared between species that can perform well on multiple hosts. We raise the possibility that this "machinery" might have played a passive role in the diversification of the complex, by allowing successful migration to new/novel environments, leading, in some cases, to fragmentation and speciation.
2017
Santos-Garcia, D. ; Silva, F. J. ; Morin, S. ; Dettner, K. ; Kuechler, S. M. The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution. Genome Biology and Evolution 2017, 9 2893 - 2910. Publisher's VersionAbstract
Hemipteran insects are well-known in their ability to establish symbiotic relationships with bacteria. Among them, heteropteran insects present an array of symbiotic systems, ranging from the most common gut crypt symbiosis to the more restricted bacteriome-associated endosymbiosis, which have only been detected in members of the superfamily Lygaeoidea and the family Cimicidae so far. Genomic data of heteropteran endosymbionts are scarce and have merely been analyzed from the Wolbachia endosymbiont in bed bug and a few gut crypt-associated symbionts in pentatomoid bugs. In this study, we present the first detailed genomic analysis of a bacteriome-associated endosymbiont of a phytophagous heteropteran, present in the seed bug Henestaris halophilus (Hemiptera: Heteroptera: Lygaeoidea). Using phylogenomics and genomics approaches, we have assigned the newly characterized endosymbiont to the Sodalis genus, named as Candidatus Sodalis baculum sp. nov. strain kilmister. In addition, our findings support the reunification of the Sodalis genus, currently divided into six different genera. We have also conducted comparative analyses between 15 Sodalis species that present different genome sizes and symbiotic relationships. These analyses suggest that Ca. Sodalis baculum is a mutualistic endosymbiont capable of supplying the amino acids tyrosine, lysine, and some cofactors to its host. It has a small genome with pseudogenes but no mobile elements, which indicates middle-stage reductive evolution. Most of the genes in Ca. Sodalis baculum are likely to be evolving under purifying selection with several signals pointing to the retention of the lysine/tyrosine biosynthetic pathways compared with other Sodalis.
2016
Zidon, R. ; Tsueda, H. ; Morin, E. ; Morin, S. Projecting pest population dynamics under global warming: the combined effect of inter- and intra-annual variations. Ecological Applications 2016, 26, 1198-1210. Publisher's VersionAbstract
AbstractThe typical short generation length of insects makes their population dynamics highly sensitive not only to mean annual temperatures but also to their intra-annual variations. To consider the combined effect of both thermal factors under global warming, we propose a modeling framework that links general circulation models (GCMs) with a stochastic weather generator and population dynamics models to predict species population responses to inter- and intra-annual temperature changes. This framework was utilized to explore future changes in populations of Bemisia tabaci, an invasive insect pest-species that affects multiple agricultural systems in the Mediterranean region. We considered three locations representing different pest status and climatic conditions: Montpellier (France), Seville (Spain), and Beit-Jamal (Israel). We produced ensembles of local daily temperature realizations representing current and future (mid-21st century) climatic conditions under two emission scenarios for the three locations. Our simulations predicted a significant increase in the average number of annual generations and in population size, and a significant lengthening of the growing season in all three locations. A negative effect was found only in Seville for the summer season, where future temperatures lead to a reduction in population size. High variability in population size was observed between years with similar annual mean temperatures, suggesting a strong effect of intra-annual temperature variation. Critical periods were from late spring to late summer in Montpellier and from late winter to early summer in Seville and Beit-Jamal. Although our analysis suggested that earlier seasonal activity does not necessarily lead to increased populations load unless an additional generation is produced, it is highly likely that the insect will become a significant pest of open-fields at Mediterranean latitudes above 40° during the next 50 years. Our simulations also implied that current predictions based on mean temperature anomalies are relatively conservative and it is better to apply stochastic tools to resolve complex responses to climate change while taking natural variability into account. In summary, we propose a modeling framework capable of determining distinct intra-annual temperature patterns leading to large or small population sizes, for pest risk assessment and management planning of both natural and agricultural ecosystems.
Malka, O. ; Shekhov, A. ; Reichelt, M. ; Gershenzon, J. ; Vassão, D. G. ; Morin, S. Glucosinolate Desulfation by the Phloem-Feeding Insect Bemisia tabaci. Journal of Chemical Ecology 2016, 42, 230–235. Publisher's VersionAbstract
Glucosinolates are plant secondary defense metabolites confined nearly exclusively to the order Brassicales. Upon tissue rupture, glucosinolates are hydrolyzed to various bioactive breakdown products by the endogenous plant enzyme myrosinase. As the feeding of chewing insect herbivores is associated with plant tissue damage, these insects have developed several independent strategies for coping with the glucosinolate-myrosinase defense system. On the other hand, our knowledge of how phloem-feeding insects interact with the glucosinolate-myrosinase system is much more limited. In fact, phloem feeders might avoid contact with myrosinase altogether so their susceptibility to intoxication by glucosinolate hydrolysis products is unclear. Previous studies utilizing Arabidopsis thaliana plants accumulating high levels of aliphatic- or indolic-glucosinolates indicated that both glucosinolate groups have moderate negative effects on the reproductive performance of Bemisia tabaci, a generalist phloem-feeding insect. To get a deeper understanding of the interaction between B. tabaci and glucosinolate-defended plants, adults were allowed to feed on artificial diet containing intact glucosinolates or on Brussels sprout and A. thaliana plants, and their honeydew was analyzed for the presence of possible metabolites. We found that B. tabaci is capable of cleaving off the sulfate group of intact glucosinolates, producing desulfoglucosinolates that cannot be activated by myrosinases, a mechanism described to date only in several chewing insect herbivores. The presence of desulfated glucosinolates in the honeydew of a generalist phloem-feeder may indicate the necessity to detoxify glucosinolates, likely due to some level of cellular damage during feeding, which results in glucosinolate activation, or as a mechanism to circumvent the non-enzymatic breakdown of indolic glucosinolates.
Roditakis, E. ; Morin, S. ; Baixeras, J. Is Bactra bactrana (Kennel, 1901) a novel pest of sweet peppers?. Bulletin of Entomological Research 2016, 106, 161-167. Publisher's VersionAbstract
This is the first report of Bactra bactrana (Kennel, 1901) (Lepidoptera: Tortricidae) attacking a major solanaceous crop, sweet pepper Capsicum annuum L. The infestation was detected in two greenhouses at the area of Tympaki (Southern Crete, Greece). The moth larvae caused typical symptoms of a fruit borer with numerous small holes on the surface of the peppers and extensive damage on the inside of the fruit as a result of the feeding activity. Unknown factors facilitated this major shift in host range since B. bactrana is typically a stem borer of sedges. In addition, the pest status of B. bactrana is currently under question, as in both cases the infestations by the moth were associated with significant yield losses. B. bactrana was moderately controlled with chemicals registered for Lepidoptera management in sweet pepper due to the boring nature of the infestation. Some comparative taxonomic notes are provided to facilitate accurate pest discrimination of related Bactra species. Finally, biological attributes of the species are summarized and are discussed from pest control and ecological perspectives. Because Bactra species have been used in augmentative releases for the control of sage, the implications of our findings on the release of biocontrol agents are placed in perspective.