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Chromosome-Level Genome Assembly of the Horned-Gall Aphid, Schlechtendalia

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bioRxiv preprint doi: https://doi.org/10.1101/2021.02.17.431348; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

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Chromosome-level genome assembly of the horned-gall aphid, Schlechtendalia chinensis (Hemiptera: Aphididae: Erisomatinae)

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Hong-Yuan Wei1 , Yu-Xian Ye2 , Hai-Jian Huang4, Ming-Shun Chen3, Zi-Xiang Yang1*, Xiao-Ming Chen1*,

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  • Chuan-Xi Zhang2,4*

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  • 1Research Institute of Resource Insects, Chinese Academy of Forestry, Kunming, China

2Institute of Insect Sciences, Zhejiang University, Hangzhou, China 3Department of Entomology, Kansas State University, Manhattan, KS, USA 4State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products; Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, China
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＃Contributed equally. *Correspondence Zi-Xiang Yang, Research Institute of Resource Insects, Chinese Academy of Forestry, Kunming, China. E-mail: [email protected] Xiao-Ming Chen, Research Institute of Resource Insects, Chinese Academy of Forestry, Kunming, China. E-mail: [email protected] Chuan-Xi Zhang, Institute of Insect Sciences, Zhejiang University, Hangzhou, China. E-mail: [email protected] Funding information National Natural Science Foundation of China, Grant/Award number: 31872305, U1402263; The basic research program of Yunnan Province, Grant/Award number: 202001AT070016; The grant for Innovative Team of ‘Insect Molecular Ecology and Evolution’ of Yunnan Province

Abstract

The horned gall aphid Schlechtendalia chinensis, is an economically important insect that induces galls valuable for medicinal and chemical industries. S. chinensis manipulates its host plant to form well-organized horned galls during feeding. So far, more than twenty aphid genomes have been reported; however, all of those are derived from free-living aphids. Here we generated a high-quality genome assembly of S. chinensis, representing the first genome sequence of a galling

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bioRxiv preprint doi: https://doi.org/10.1101/2021.02.17.431348; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

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aphid. The final genome assembly was 280.43 Mb, with 97% of the assembled sequences anchored into thirteen chromosomes. S. chinensis presents the smallest aphid genome size among available aphid genomes to date. The contig and scaffold N50 values were 3.39 Mb and 20.58 Mb, respectively. The assembly included 96.4% of conserved arthropod and 97.8% of conserved Hemiptera single-copy orthologous genes based on BUSCO analysis. A total of 13,437 protein-coding genes were predicted. Phylogenomic analysis showed that S. chinensis formed a single clade between the Eriosoma lanigerum clade and the Aphidini+Macrosiphini aphid clades. In addition, salivary proteins were found to be differentially expressed when S. chinensis underwent host alternation, indicating their potential roles in gall formation and plant defense suppression. A total of 36 cytochrome P450 genes were identified in S. chinensis, considerably fewer compared to other aphids, probably due to its small host plant range. The high-quality S. chinensis genome assembly and annotation provide an essential genetic background for future studies to reveal the mechanism of gall formation and to explore the interaction between aphids and their host plants.

Key words

Schlechtendalia chinensis; PacBio sequencing; Hi-C analysis; Chromosome-level genome assembly; Comparative genomics; Gall formation; Host alternation

1 Introduction

Many aphid species are economically important plant pests that feed on plant sap and also caused damage by transmitting plant viruses. Around 100 aphid species have been identified as significant agricultural pests among the approximately 5,000 known species (Blackman & Eastop, 2017). Up to this point, studies on aphid genomes have mostly focused on the subfamily Aphidinae (International Aphid Genomics Consortium, 2010; Li et al., 2019; Mathers, 2020; Mathers et al., 2017; Mathers, Mugford, et al., 2020; Mathers, Wouters, et al., 2020; Nicholson et al., 2015; Thorpe et al., 2018; Wenger et al., 2016). Genome sequencing efforts of other subfamilies, however, such as Eriosomatinae that are distantly related to Aphidinae are very limited (Julca et. al. 2020; Biallo et al., 2020). Unlike most free-living aphids, the galling species from Eriosomatinae induce the formation of galls on their primary host plant and live in the interior. Galling aphids may serve as good models for the study of unique ecological and behavioral phenomena for insect-plant interaction and

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bioRxiv preprint doi: https://doi.org/10.1101/2021.02.17.431348; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

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coevolution (Moran, 1989; David Wool, 2004). The horned gall aphid, Schlechtendalia chinensis (Hemiptera: Aphididae: Eriosomatinae: Fordini), is one of the most economically valuable insects, since it induces the formation of gallnuts that have been used for medicinal purposes and in chemical industries. The components of gallnuts are useful or essential gradients in producing inks, wine, food, cosmetic antioxidants, and animal feed. These widely uses are due to their high tannin levels which range from 50% to 70% (Zhang, Tang, & Cheng, 2008). The annual yield of gallnuts in China is 8,000-10,000 tons, accounting for >90% of the total yield worldwide (Zhang, Tang, & Cheng, 2008). S. chinensis shows a peculiar complex life cycle involving both sexual and asexual reproduction stages with a host alternation between the Chinese sumac (Rhus chinensis, Anacardiaceae) and mosses (Plagiomnium spp. Mniaceae). In this holocyclic life cycle, a fundatrix produced by a mating female crawls along the trunk and feeds on a new leaf, where it induces the formation of a horned-gall. The fundatrix then continues to feed inside the gall and reproduces fundatrigeniae via parthenogenesis. From here on, the gall grows quickly and forms a highly organized structure. During gall development, drastic morphological rearrangements occur in leaf tissues. For example, the palisade tissues of a gall are reorganized and replaced by parenchym cells (Liu et al., 2014). In autumn, galls become mature and burst to open, alate autumn migrants fly to nearby mosses and reproduce nymphs for overwintering. In the following spring, nymphs develop in the moss into spring migrants that fly back to the primary host, R. chinensis. Here they produce female and male offspring (sexuales) with degenerated mouthparts that allow them to attach themselves to the trunk crevices. After mating, each female reproduces only a fundatrix, starting the next life cycle all over again (Figure 1) (Zhang, Qiao, Zhong & Zhang, 1999; Blackman and Eastop, 2000). Taken together, S. chinensis participates in a series of all-female parthenogenetic generations and only a single sex generation. This unusually life cycle with various morphologically distant aphids at different stages is likely driven by adaptation to different environmental conditions. Unlike most free-living aphids from the Aphidinae taxon, galling aphids have many distinct biological characteristics. The most striking characteristic is that the feeding of most galling aphids does not seriously affect the health of their host plants. In fact, the galls of S. chinensis even provide some benefits to its primary host plant (Chen et al., 2020).
The complexity both in its developmental process and in the structure of its induced galls implies that S. chinensis may have unique gene sets that regulate its development and manipulate its

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bioRxiv preprint doi: https://doi.org/10.1101/2021.02.17.431348; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

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host plants (Takeda et al., 2019; Hirano et al., 2020). The underlying molecular mechanisms for its complex life cycle and ability to parasitize on host plants via apparently harmless galls remain largely unknown. Here we generated a high-quality chromosome-level genome assembly of S. chinensis, representing the first genome sequence of aphids that induces the formation of closed galls, using a combination of Illumina, Pacific Bioscience (PacBio) and Hi-C technologies. Subsequent, gene prediction, functional annotation and phylogenetic analysis were also carried out to determine the relationship between S. chinensis and other aphid species. This reference genome sequence provides information about genomic organization in the Eriosomatinae subfamily and allows comparative genomic studies for a better understanding of genes associated with its own developmental regulation as well as its ability to induce gall formation, living on alternative host plant species and suppress plant defence during parasitism.

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2 Materials and Methods 2.1 Sample collection

S. chinensis samples were collected in October, 2019, from fresh mature galls on R. chinensis, in

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Wufeng county (30°10′ N，110°52′ E，960 m above sea level), Hubei Province, China. Winged and

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wingless fundatrigeniae in a gall were treated as the same clone. Fundatrigeniae contained within a gall were poured onto a petri dish after dissecting the gall. Impurities such as waxes were removed manual. The fundatrigeniae were then transferred to Eppendorf tubes. Samples were separated into groups with each group containing about 20 individuals. The samples were immediately frozen in liquid nitrogen for 2 hours and then stored at -80℃ for later genome, RNA-seq and Hi-C analyses respectively.
In addition to the original samples, a colony was established through artificial cultivation for other genetic studies. To establish a colony, autumn migrants of S. chinensis were collected from mature galls and transferred to a nursery of the moss Plagiomnium maximoviczii, which were maintained in a greenhouse. In the following year, spring migrants (sexuparae) were collected from the mosses and cultivated in lab. Aphids were transferred to host trees after fundatrix emergence for gall induction. Aphid samples of different stages including fundatrix, fundatrigeniae, autumn migrants, overwinter nymphs, and spring migrants as well as male and female sexuales were collected separately. All aphid samples were immediately frozen in liquid nitrogen for two hours and then stored at -80℃ until further analysis.

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2.2 Genomic sequencing

Genomic DNA was isolated from aphid samples using a DNeasy Blood & Tissue Extraction Kit (Qiagen Inc., Valencia, CA, USA) by following the manufacturer's instructions. After the measurement of quality and quantity, the DNA samples were used for making a paired-end sequencing library (150 bp in length). The library was sequenced using the Illumina NovaSeq6000 plantform. In addition, a 20 kb library was constructed and sequenced using the PacBio RSII platform at Annoroad Gene Technology Co., Ltd. (Beijing, China).
Hi-C libraries were also constructed from aphid samples according to the Proximo Hi-C procedure and its quality and concentration were determined via an Agilent 2100 Bioanalyzer and qPCR. Briefly, aphid samples were mixed with 1% formaldehyde for 10 min at room temperature and the nuclei were extracted and permeabilized. After the quality of the library was ascertained, different libraries were pooled to achieve required concentrations for Illumina sequencing (Rao et al., 2014).
RNA samples were extracted from the fundatrix, the fundatrigeniae, autumn migrants, nymphs, spring migrants (sexuparae), male and female sexuales, respectively, following the standard protocols provided by the manufacturer. RNA quantity, purity and integrity were determined by a NanoPhotometer and the Agilent 2100 Bioanalyzer. cDNA libraries were built following the chain specific method. The libraries were initially quantified with qubit 2.0 fluorometer and diluted to 1.5 ng/ul. Different libraries were pooled according to the requirements of effective concentration and target data volume for Illumina sequencing.

2.3 Genome assembly

We selected a k-mer length of 19 bases and used Illumina paired end reads for k-mer analysis to estimate the genome size and generate k-mer distribution as described by Jellyfish and GenomeScope (Ranallo-Benavidez, Jaron, & Schatz, 2020). We used PacBio sequencing to assembly genome using Wtdbg2. Long reads were used to fix base errors in sequences generated by noisy long reads using NextPolish (Hu, Fang, Su, & Liu, 2019). Pilon was used to improve the draft assembly from Illumina reads (Walker et al., 2014). Finally, HaploMerger2 was used to remove the heterozygosity (Huang, Kang, & Xu, 2017).
Haploid contigs were scaffolded using the 3D de novo assembly (3D-DNA) software
(Dudchenko et al., 2017). Hi-C sequences were aligned with the draft genome assembly using

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Juicer. An initial assembly was generated via a 3D-DNA analysis. The initial assembly was validated using JBAT Juicebox, resulting in a finally chromosome-level genome assembly.

2.4 Chromosome staining

Salivary glands were dissected from fundatrigeniae of S. chinensis in a phosphate-buffer saline (PBS) solution (137 mM NaCl, 2.68 mM KCl, 8.1 mM Na2HPO4 and 1.47 mM KH2PO4 at pH 7.4) under a stereomicroscope (COIC, Chongqing, China). The samples were fixed in 4% paraformaldehyde (Sangon Biotech, Shanghai, China) for 1 h and washed with PBS three times. Then the samples were triturated mechanically, and 20 ml DAPI solution (Abcam, Cambridge, USA) was added to stain the chromosomes. Fluorescence images were examined and photographed under a Leica confocal laser-scanning microscope (Leica, Heidelberg, Germany).

2.5 Gene annotation

Repetitive sequences were identified based on homology and de novo approaches. For the homology-based approach, RepeatMasker was used to screen the S. chinensis genome against the Hemiptera ch repeat database, set this parameter to RepeatMasker -pa 4 -e ncbi -species Hemiptera ch -dir. Repeatmodeler identifies repetitive sequences based on de novo approaches prediction (Flynn et al., 2020). Statistical results of RepeatMasker and Repeatmodeler analyses were combined.
Gene structure predictions were performed using homology-based, de novo, and RNA-seq assisted methods. For the homology-based method, gene structures were predicted based on

homology to those from Eriosoma lanigerum, Acyrthosiphon pisum, Myzus persicae, Aphis glycines,

Rhopalosiphum maidis (Birney, Michele, & Durbin, 2004). For de novo prediction, Augustus was first used for Augustus training, then for RNA-seq data to make hint files, and finally run to perform gene prediction (Stanke et al., 2006; Blanco, Parra & Guigó, 2007). In addition, GeneMark-ET, BRAKER, Maker and SNAP were also applied separately to generate ab initio gene predictions. For the RNA-seq assisted method, RNA-seq data were alignedto the S. chinensis genome using PASA. Finally, gene prediction results were integrated by EVidenceModeler (Haas et al., 2008). We aligned the genes to seven functional databases to annotate genes in the S. chinensis genome. The databases used in the study were NCBI Non-Redundant Protein Sequence (Nr), Non-Redundant Nucleotide Sequence Database (Nt), SwissProt, Cluster of Orthologous Groups for eukaryotic complete genomes (KOG), The Integrated Resource of Protein Domains and Functional

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Sites (InterPro), Conserved Domain Database (CDD), Gene Ontology (GO), Kyoto Encyclopedia of Genes and Genomes, Orthology database (KEGG) and evolutionary genealogy of genes: Non-supervised Orthologous Groups (eggNOG). A localized Blast2GO database was built first and then GO annotation was processed via Blast2GO. KAAS of KEGG was used to annotate S. chinensis genome sequence quickly, and the pattern of BBH was chosen.

2.6 Non-coding RNA identification

Transfer RNAs (tRNAs) were identified using the tRNAscan-SE program (set to default parameters, the same as below unless specific notes). RNAmmer was used to identify 5S/ 8S, 16S/ 18S and 23S/ 28S rRNA. Ribosomal RNAs (rRNAs), microRNAs (miRNAs) and small nuclear RNAs (snRNAs) were identified based on the Rfam database (12.2) (Kalvari et al., 2017).

2.7 Phylogenetic analysis

We constructed phylogenetic trees using whole-genome sequences of S. chinensis and whole-genome sequences of other ten aphid species including Cinara cedri, E. lanigerum, Ap.

glycines, Ap. gossypii, R. maidis, R. padi, Ac. pisum, Diuraphis noxia, M. cerasi and M. persicae.

The aphid genome sequence and gene structure annotation files were downloaded from the NCBI genome database, and genes containing mRNA information were retained and the tail CDS was modified. Finally, the protein and CDS sequences of all genes were obtained. The obtained protein sequences were filtered and analyzed by all vs all blast. Homologous genes were clustered using OrthoMCl (Li, Stoeckert & Roos, 2003). The coding sequences of homologous single copy genes were extracted. Multi-sequence alignments of homologous single copy genes were performed using

MAFFT (Katoh, Misawa, Kuma, & Miyata, 2002; Katoh & Standley, 2013). Protein sequence

alignments were converted to codon sequence alignments and conserved blocks were extracted from the alignments using Gblocks. The extracted codon sequence alignments of all homologous single copy genes were integrated for phylogenetic trees using RAxML (Castresana, 2000). The branch length of homologous genes was analyzed using PAML, and then compared with the standard tree to eliminate abnormal genes. Then the tree was built using RAxML again (Stamatakis, 2014). By providing the root number and multiple sequence alignment results with calibration point information, the species divergence time can be calculated using mcmctree (a part of the PAML software), and the divergence time within the evolutionary tree can be obtained with 95% confidence (Yang, 2007). The nodal dates of Ac. pisum and M. cerasi were 42.4-48.0 MYA, and

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those of Ac. pisum and Ap. gossypii were 34-60 MYA.

2.8 Gene family expansion and contraction

We used CAFÉ to analyze the gene family expansion and contraction by comparing our data with

those from 10 other aphids (C. cedri, E. lanigerum, Ap. glycines, Ap. gossypii, R. maidis, R. padi, Ac. pisum, D. noxia, M. cerasi and M. persicae). Briefly, the quantitative information of gene

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  • Phylogenetics of Buchnera Aphidicola Munson Et Al., 1991

    Phylogenetics of Buchnera Aphidicola Munson Et Al., 1991

    Türk. entomol. derg., 2019, 43 (2): 227-237 ISSN 1010-6960 DOI: http://dx.doi.org/10.16970/entoted.527118 E-ISSN 2536-491X Original article (Orijinal araştırma) Phylogenetics of Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae) based on 16S rRNA amplified from seven aphid species1 Farklı yaprak biti türlerinden izole edilen Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae)’nın 16S rRNA’ya göre filogenetiği Gül SATAR2* Abstract The obligate symbiont, Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae) is important for the physiological processes of aphids. Buchnera aphidicola genes detected in seven aphid species, collected in 2017 from different plants and altitudes in Adana Province, Turkey were analyzed to reveal phylogenetic interactions between Buchnera and aphids. The 16S rRNA gene was amplified and sequenced for this purpose and a phylogenetic tree built up by the neighbor-joining method. A significant correlation between B. aphidicola genes and the aphid species was revealed by this phylogenetic tree and the haplotype network. Specimens collected in Feke from Solanum melongena L. was distinguished from the other B. aphidicola genes on Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) with a high bootstrap value of 99. Buchnera aphidicola in Myzus spp. was differentiated from others, and the difference between Myzus cerasi (Fabricius, 1775) and Myzus persicae (Sulzer, 1776) was clear. Although, B. aphidicola is specific to its host aphid, certain nucleotide differences obtained within the species could enable specification to geographic region or host plant in the future. Keywords: Aphid, genetic similarity, phylogenetics, symbiotic bacterium Öz Obligat simbiyont, Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae), yaprak bitlerinin fizyolojik olaylarının sürdürülmesinde önemli bir rol oynar.
  • Anatomical Investigations of the Male Reproductive System of Selected Species of Macrosiphini

    Anatomical Investigations of the Male Reproductive System of Selected Species of Macrosiphini

    Bulletin of Insectology 61 (1): 179, 2008 ISSN 1721-8861 Anatomical investigations of the male reproductive system of selected species of Macrosiphini Karina WIECZOREK Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, Katowice, Poland Abstract Histological sections and whole mount preparations of five species of Macrosiphini [Impatientinum asiaticum Nevsky, Hypero- myzus (Hyperomyzus) pallidus Hille Ris Lambers, Myzus (Myzus) cerasi (F.), Rhopalomyzus (Judenkoa) loniceare (Siebold) and Uroleucon obscurum (Koch)] were examined. Key words: Hemiptera, Aphidoidea, Aphididae, Macrosiphini, male reproductive system. In previous research on the structure of the male repro- References ductive system of aphids, about 70 species from various subfamilies have been described, mainly Lachninae BLACKMAN R. L., 1987.- Reproduction cytogenetics and de- (Wojciechowski, 1977), Chaitophorinae (Wieczorek and velopment, pp 163-191. In: Aphids, their biology, natural Wojciechowski, 2004), and Calaphidinae (Głowacka et. enemies and control (MINKS A. K., HARREWIJN P., Ed).- El- sevier, Amsterdam, The Netherland. al., 1974; Wieczorek and Wojciechowski, 2001; Wiec- BOCHEN K., KLIMASZEWSKI S. M., WOJCIECHOWSKI W., zorek, 2006). 1975.- Budowa męskiego układu rozrodczego Macrosipho- In contrast, Aphidinae are the largest and most diverse niella artemisiae (B.De Fonsc.) i M. millefolli (De Geer) group of aphids whose male reproductive system is least (Homoptera, Aphididae).- Acta Biologica Uniwersytet Slaski studied. In Pterocommatini the structure of the male re- w Katowicach, 90: 73-81. productive system has been analysed in Pterocomma GŁOWACKA E., KLIMASZEWSKI S. M., SZELEGIEWICZ H., WOJ- populeum (Kaltenbach) (Wieczorek and Wo- CIECHOWSKI W., 1974.- Uber den Bau des mannlichen Fort- jciechowski, 2005) and Pterocomma salicis (L.) (Wiec- pflanzungssystems der Aphiden (Homoptera, Aphidoidea).- zorek and Mróz, 2006), in Aphidini in Rhopalosiphum Annales Universitas Mariae Curie-Skłodowska, 29C: 133-138.
  • Woolly Apple Aphid Generalist Predator Feeding Behavior Assessed Through Video Observation in an Apple Orchard

    Woolly Apple Aphid Generalist Predator Feeding Behavior Assessed Through Video Observation in an Apple Orchard

    J Insect Behav https://doi.org/10.1007/s10905-019-09722-z Woolly Apple Aphid Generalist Predator Feeding Behavior Assessed through Video Observation in an Apple Orchard Robert J. Orpet & David W. Crowder & Vincent P. Jones Received: 19 February 2019 /Revised: 21 June 2019 /Accepted: 28 June 2019 # Springer Science+Business Media, LLC, part of Springer Nature 2019 Abstract Generalist predators are considered effective larvae and earwigs differ in their feeding behavior in biological control agents in many agroecosystems. the field, and provide new evidence that ants may hinder However, characterizing the behavior of different gen- aphid biological control by antagonizing earwigs. eralist predator species in realistic field settings is diffi- cult due to challenges associated with directly observing Keywords Biological control . Eriosoma lanigerum . predation events in the field. Here we video recorded Forficula auricularia . formicidae . intraguild predation woolly apple aphid (Erisoma lanigerum) (Hemiptera: Aphididae) colonies to directly observe the feeding behavior of their generalist predators during the day Introduction and night. To observe European earwigs (Forficula auricularia) (Dermaptera: Forficulidae), which are Pest consumption in agroecosystems generally increases thought to be key woolly apple aphid predators but were when different predator taxa complement each other by not present at our study location, we released earwigs feeding at different times or in different locations into the study area. Across 1413 h of video recorded (Straub et al. 2008). However, if niche overlap occurs, over 4 weeks, earwigs made the most attacks on woolly intraguild predation can disrupt biological control of apple aphid colonies, but coccinellid larvae spent more pests (Rosenheim 1998;Straubetal.2008).
  • Effect of Imidacloprid Foliar Treatment and Banana Leaf Age on Pentalonia Nigronervosa (Hemiptera, Aphididae) Survival

    Effect of Imidacloprid Foliar Treatment and Banana Leaf Age on Pentalonia Nigronervosa (Hemiptera, Aphididae) Survival

    NewRobson Zealand et al.—Imidacloprid Journal of Crop effect and Horticulturalon Pentalonia Science, nigronervosa 2007, Vol. 35: 415–422 415 0014–0671/07/3504–0415 © The Royal Society of New Zealand 2007 Effect of imidacloprid foliar treatment and banana leaf age on Pentalonia nigronervosa (Hemiptera, Aphididae) survival JACQUELINE D. ROBSON of aphids and does not become systemic within the MARK G. WRIGHT* plant. From these results, it is likely that management 3050 Maile Way, Room 310 of banana aphid using imidacloprid under field Department of Plant and Environmental conditions will be effective on old leaves and new Protection Sciences leaves that are sprayed, but leaves emerging after University of Hawaii at Manoa sprays will not be completely protected from aphids. Honolulu, HI 96822, United States Regular scouting for aphids should be implemented email: [email protected] in support of imidacloprid applications. RODRIGO P. P. ALMEIDA Keywords banana bunchy top virus; pest 137 Mulford Hall management; Provado; vector Department of Environmental Science, Policy and Management University of California, Berkeley INTRODUCTION CA 94720, United States Pentalonia nigronervosa Coq. (Hemiptera, Aphididae), the banana aphid, is the vector of Abstract Pentalonia nigronervosa, the banana Banana bunchy top virus (BBTV) (Magee 1927; aphid, is the vector of Banana bunchy top virus Hu et al. 1996), the causal agent of banana bunchy to banana. This virus is the etiological agent of top disease (BBTD). This disease was first detected banana bunchy top disease, a limiting factor in in Hawaii, United States in 1989 (Conant 1992), many banana growing regions, including Hawaii, and despite eradication and control efforts, has since United States.
  • Ipm of Vector Aphids

    Ipm of Vector Aphids

    IPM OF VECTOR APHIDS Hajimu Takada Laboratory of Entomology, Faculty of Agriculture Kyoto Prefectural University, Kyoto, Japan ABSTRACT The following tactics are described for control of aphids as virus vectors; chemical con- trol (repellents, feeding deterrents, alarm pheromone, insecticides), physical control (mulch, fleece, netting) and biological control (insect parasitoids and predators). No tactic is able to protect plants completely against virus infections when used alone, except for certain fleeces. Multiple tactics must be used to build integrated pest management programs (IPM). INTRODUCTION Azadirachtin This paper reviews recent work on tactics This triterpenoid, isolated from the neem for controlling vector aphids to protect plants against tree (Azadirachta indica), reduced probing activity virus infection. I hope it will contribute to the by R. padi and Sitobion avenae on winter barley development of an effective strategy against the treated with concentrations of <500 ppm. The effect viruses, which cause serious damage to tropical lasted for at least four days after application (West crops. Such viruses include banana bunchy top virus and Mordue 1992). The reduction in probing activ- (BBTV) and papaya ringspot virus (PRSV). ity would diminish the probability of BYDV trans- mission by these aphids. CHEMICAL CONTROL Alarm Pheromone (-)-Polygodial Applying the alarm pheromone (E)-beta- This compound, isolated from water-pep- farnesene has not been effective, because it makes per (Polygonum hydropiper), is a sesquiterpenoid the aphids more active, and might increase transmis- which is highly repellent to aphids (Asakawa et al. sion of viruses. However, a spray application of 1988, Griffiths et al. 1989). Extraction of (-)- carbamate or organic phosphate, at one-tenth of the polygodial from the plant yielded material for a field recommended dose, in combination with the phero- trial to test the level of protection against barley mone, was successful in controlling aphids on ice- yellow dwarf virus (BYDV), transmitted by the berg lettuce (Ester et al.
  • Aphids (Hemiptera, Aphididae)

    Aphids (Hemiptera, Aphididae)

    A peer-reviewed open-access journal BioRisk 4(1): 435–474 (2010) Aphids (Hemiptera, Aphididae). Chapter 9.2 435 doi: 10.3897/biorisk.4.57 RESEARCH ARTICLE BioRisk www.pensoftonline.net/biorisk Aphids (Hemiptera, Aphididae) Chapter 9.2 Armelle Cœur d’acier1, Nicolas Pérez Hidalgo2, Olivera Petrović-Obradović3 1 INRA, UMR CBGP (INRA / IRD / Cirad / Montpellier SupAgro), Campus International de Baillarguet, CS 30016, F-34988 Montferrier-sur-Lez, France 2 Universidad de León, Facultad de Ciencias Biológicas y Ambientales, Universidad de León, 24071 – León, Spain 3 University of Belgrade, Faculty of Agriculture, Nemanjina 6, SER-11000, Belgrade, Serbia Corresponding authors: Armelle Cœur d’acier ([email protected]), Nicolas Pérez Hidalgo (nperh@unile- on.es), Olivera Petrović-Obradović ([email protected]) Academic editor: David Roy | Received 1 March 2010 | Accepted 24 May 2010 | Published 6 July 2010 Citation: Cœur d’acier A (2010) Aphids (Hemiptera, Aphididae). Chapter 9.2. In: Roques A et al. (Eds) Alien terrestrial arthropods of Europe. BioRisk 4(1): 435–474. doi: 10.3897/biorisk.4.57 Abstract Our study aimed at providing a comprehensive list of Aphididae alien to Europe. A total of 98 species originating from other continents have established so far in Europe, to which we add 4 cosmopolitan spe- cies of uncertain origin (cryptogenic). Th e 102 alien species of Aphididae established in Europe belong to 12 diff erent subfamilies, fi ve of them contributing by more than 5 species to the alien fauna. Most alien aphids originate from temperate regions of the world. Th ere was no signifi cant variation in the geographic origin of the alien aphids over time.
  • Managing Floral Resources in Apple Orchards for Pest Control: Ideas, Experiences and Future Directions

    Managing Floral Resources in Apple Orchards for Pest Control: Ideas, Experiences and Future Directions

    insects Review Managing Floral Resources in Apple Orchards for Pest Control: Ideas, Experiences and Future Directions Annette Herz 1,*, Fabian Cahenzli 2, Servane Penvern 3, Lukas Pfiffner 2, Marco Tasin 4 and Lene Sigsgaard 5 1 Julius Kühn-Institut, Institute for Biological Control, Heinrichstr. 243, 64287 Darmstadt, Germany 2 Department of Crop Sciences, Research Institute of Organic Agriculture (FiBL), Ackerstrasse 113, 5070 Frick, Switzerland 3 INRA, Centre de Recherche PACA, UR Ecodeveloppement, 84914 Avignon, France 4 Department of Plant Protection Biology—Unit of Integrated Plant Protection, Swedish University of Agricultural Science, P.O. Box 102, SE-230 53 Alnarp, Sweden 5 Department of Plant and Environmental Sciences, University of Copenhagen (UCPH), Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark * Correspondence: [email protected] Received: 31 May 2019; Accepted: 6 August 2019; Published: 11 August 2019 Abstract: Functional biodiversity is of fundamental importance for pest control. Many natural enemies rely on floral resources to complete their life cycle. Farmers need to ensure the availability of suitable and sufficient floral biodiversity. This review summarizes 66 studies on the management of floral biodiversity in apple orchards, published since 1986. Approaches followed different degrees of intervention: short-term practices (mowing regime and weed maintenance, cover crops), establishment of durable ecological infrastructures (perennial flower strips, hedgerows) and re-design of the crop system (intercropping, agroforestry). Although short-term practices did not always target the nutrition of natural enemies by flowering plants, living conditions for them (alternative prey, provision of habitat) were often improved. Perennial flower strips reliably enhanced natural enemies and techniques for their introduction continuously developed.