The genome of the rice planthopper egg parasitoid wasps Anagrus nilaparvatae casts light on the chemo- and mechanosensation in parasitism

Abstract

Background Mymaridae is an ancient insect group and is a basal lineage of the superfamily Chalcidoidea. Species of Mymaridae have great potential for biological control. Anagrus nilaparvatae, a representative species of Mymaridae, is ideal for controlling rice planthopper due to its high rate of parasitism and ability to find hosts efficiently in paddy ridges and fields. Results Using both PacBio single-molecule real-time and Illumina sequencing, we sequenced and assembled the whole genome of A. nilaparvatae, a first for the family Mymaridae. The assembly consists of 394 scaffolds, totaling 488.8 Mb. The assembly is of high continuity and completeness, indicated by the N50 value of 25.4 Mb and 98.2% mapping rate of Benchmarking Universal Single-Copy Orthologs. In total, 16,894 protein-coding genes in the genome were annotated. A phylogenomic tree constructed for A. nilaparvatae and other 12 species of Hymenoptera confirmed that the family Mymaridae is sister to all remaining chalcidoids. The divergence time between A. nilaparvatae and the other seven Chalcidoidea species was dated at ~ 126.9 Mya. Chemoreceptor and mechanoreceptor genes are important in explaining parasitic behavior. We identified 17 odorant binding proteins, 11 chemosensory proteins, four Niemann-Pick type C2 proteins, 88 olfactory receptors, 12 gustatory receptors, 22 ionotropic receptors and 13 sensory neuron membrane proteins in the genome of A. nilaparvatae, which are associated with the chemosensory functions. Strikingly, there is only one pickpocket receptors and nine transient receptor potential genes in the genome that have a mechanosensory function. Conclusions We obtained a high-quality genome assembly for A. nilaparvatae using PacBio single-molecule real-time sequencing, which provides phylogenomic insights for its evolutionary history. The small numbers of chemo- and mechanosensory genes in A. nilaparvatae indicate the species-specific host detection and oviposition behavior of A. nilaparvatae might be regulated by relatively simple molecular pathways.

Genome Assembly and Comparative Analysis of the Egg Parasitoid Wasp Trichogramma dendrolimi Shed Light on the Composition and Evolution of Olfactory Receptors and Venoms

“…A previous phylogeny study based on transcriptomes found that Mymaridae and Trichogrammatidae, two small egg parasitoids, were placed as sister groups of all remaining Chalcidoidea, indicating that small body size and egg parasitoidism were possible ancestral traits of this super family [ 79 ]. Compared with the previous estimation by Ma et al [ 80 ], the range of the estimated age of the divergence between T. pretiosum and three other Trichogramma species increased from 6.4 Mya to 16.9 Mya.…”

Transcriptome Analysis and Identification of Chemosensory Genes in Baryscapus dioryctriae (Hymenoptera: Eulophidae)

“…A total of 155 ORs were identified in B. dioryctriae, which is close to the number of ORs in M. mediator (169) [58] and A. mellifera (170) [59] but less than that in N. vitripennis (301) [60]. The different numbers of OR genes in wasps may be affected by species specificity and sequencing technology and depth [20,27]. In Hymenopteran species, a large expansion event of the OR gene family has been found, and gene gain and loss events are common in bees, wasps, and ants [61].…”

“…CSPs are soluble carrier proteins that function in a manner similar to OBPs in chemical signal reception in insects [50]. A total of nine CSPs were identified in B. dioryctriae, which is close to the number of CSPs in C. cunea (11) [51], A. nilaparvatae (11) [20] and Aphidius gifuensis (12) [52], but less than that in D. longicaudata (19) [23]. Previous studies have shown that some insect CSPs are expressed exclusively in non-sensory organs (legs, heads, thoraxes, midguts, ovaries, fat body and even the female pheromone glands, etc.)…”

“…NPC2s are considered small soluble proteins and are critical for cholesterol transport in humans [56], while in Hymenoptera insects, they are odorant carrier proteins, similar to OBPs and CSPs in the olfactory system [57]. A total of three NPC2 genes were identified in B. dioryctriae, which was fewer than the total of ten members of the NPC2 family known in most Hymenopteran species [20], such as A. nilaparvatae (4), Microplitis demolitor (8) and Fopius arisanus (10) [20]. Previous related studies on Hymenoptera insects revealed that NPC2s are generally specifically expressed in antennae, including MmedNPC2 of Microplitis mediator [57] and McinNPC2 of Macrocentrus cingulum 57.…”

“…In Hymenoptera, an enormous number of chemosensory genes from various species have been reported, and most of them have been identified through antennal transcriptomes. According to our statistics from Insectbase 2.0 [18] and the NCBI (National Center for Biotechnology Information (nih.gov)) (accessed on 10 September 2022), chemosensory genes from approximately 4 superfamilies, 18 families and 89 species have been identified, such as Trichogramma pretiosum [19], Anagrus nilaparvatae [20,21], Aenasius bambawalei [22] and Diachasmimorpha longicaudata [23]. In the past five years, an increasing number of studies have investigated the function of chemosensory genes.…”