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, 2020).
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 on
other subfamilies that are distantly related to Aphidinae are very
limited (Julca et al., 2020; Biallo et al., 2020). Unlike most
free-living aphids, galling aphids induce the formation of galls on
their primary host plants and live in the galls. Galling aphids may
serve as good models for the study of unique ecological and behavioral
phenomena for insect-plant interaction and coevolution (Moran, 1989;
Wool, 2004). Up to now, galling aphids whose genomes have been sequenced
include Eriosoma lanigerum and Hormaphis corn . The aphidE. lanigerum often causes bark deformation and cancer-like
swellings on roots, trunk or brunches of apple, and sometimes induces
leaf-rosette galls on American elm (Ulmus americana ) (Blackman
and Eastop, 2020). Another aphid H. corn induces a gall which has
an ostiole on the underside of the leaf (Kurosu et al., 1992). The galls
induced by E. lanigerum and H. corn are quite different to
the completely closed gall since its aphids have peculiar strategies to
adapt the specific characteristics such as high CO2concentration, honeydew treatment and nutrition exchange of the closed
internal environment (Chen et al., 2020).
The horned gall aphid,Schlechtendalia
chinensis (Hemiptera: Aphididae:
Eriosomatinae:
Fordini), is one of the most economically valuable insects. Its gallnuts
are valuable for medicinal purposes and in chemical industries. Some of
the gallnuts components such as tannins are useful in producing inks,
wine, food, cosmetic antioxidants, and animal feed. High levels of
tannins ranged from 50 to 70% have been found in horned galls (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 has a 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 mated female
crawls along the trunk and feeds on a new leaf, where it induces the
formation of a horned-gall. The fundatrix produces wingless
fundatrigeniae via parthenogenesis in gall. In autumn, wingless
fundatrigeniae produce winged fundatrigeniae named autumn migrants. When
galls become mature and burst open, alate autumn migrants fly to nearby
mosses and produce nymphs for overwintering. In the following spring,
nymphs on mosses develop into spring migrants that fly back to the
primary host, R. chinensis and produce female and male offspring
(sexuales). After mating, each female reproduces only a fundatrix,
starting the cycle again (Figure 1) (Zhang, Qiao, Zhong & Zhang, 1999;
Blackman and Eastop, 2020). This unusual 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 formation of galls can provide
some benefits to the 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 host plants
(Takeda et al., 2019; Hirano et al., 2020). The underlying molecular
mechanisms for its complex life cycle remain largely unknown. Galls
result from dramatic reprogramming of plant cell biology driven by
insect molecules. Previous studies have shown that gall induction is
highly, species-specific and different galling insects deliver unique
sets of effectors into plant tissues, resulting in gall formation (Zhao
et al., 2015; Alibory et al., 2018). The underlying mechanisms for the
ability of the galling aphid to parasitize on host plants via apparently
harmless galls remained unknown either. To understand the genetic basis
of the complex lifestyle, we generated a high-quality chromosome-level
genome assembly of S. chinensis , representing the first genome
sequence of aphids that induces the formation of completely closed
galls. In addition, we analyzed the phylogenetic relationship betweenS. chinensis and closely related species to give a better
understanding of the unique biological characteristics of S.
chinensis , such as suppressing plant defense and inducing gall
formation.