1 Introduction
Numerous aphid species are economically important plant pests that feed
on plant sap. Many plant-feeding aphids can also transmit plant viruses.
Around 100 out of approximately 5,000 known aphid species are
significant agricultural pests due to their feeding damages and/or
disease transmission (Blackman & Eastop, 2020). Currently, studies on
aphid genomes have mainly 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 on species from other
subfamilies that are distantly related to Aphidinae is relatively
limited (Julca et al., 2020; Biallo et al., 2020). Unlike most
free-living aphids, galling aphids can induce gall formation on their
primary host plants and then live in galls. Galling aphids may are ideal
models to study unique ecological and behavioral phenomena underlying
insect-plant interactions and their coevolution (Moran, 1989; Wool,
2004). So far, only two galling aphids have been sequenced and assembled
(Eriosoma lanigerum and Hormaphis cornu ). The aphidE. lanigerum often causes bark deformation and cancer-like
swelling on the roots, trunk or brunches of apple, and sometimes induces
the formation of leaf-rosette galls on American elm (Ulmus
americana ) (Blackman and Eastop, 2020). The aphid, H. cornu ,
induces a gall on the underside of leaves of witch hazel,Hamamelis virginiana (Kurosu et al., 1992). The galls induced byE. lanigerum and H. cornu are quite different from the
completely closed galls induced by Schlechtendalia chinensis ,
which has peculiar strategies to adapt to a closed environment that has
extremely high levels of CO2 honeydew, and other aphid
metabolites (Chen et al., 2020).
The horned gall aphid,S.
chinensis (Hemiptera: Aphididae:
Eriosomatinae:
Fordini), is one of the most economically valuable insects. Gallnuts
induced by the aphids are valuable for medicinal purposes and in
chemical industries. The components in gallnuts, such as tannins, are
important gradients for producing inks, wine, food, cosmetic
antioxidants, and animal feed. High levels of tannins (50- 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 over 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 of the genus
(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 can produce wingless
fundatrigeniae in galls via parthenogenesis. In autumn, wingless
fundatrigeniae will produce winged fundatrigeniae named autumn migrants.
When galls become mature and burst open, the alate autumn migrants will
fly to nearby mosses and produce nymphs for overwintering. In the
following spring, nymphs on mosses will develop into spring winged
migrants, which then fly back to the primary host, R. chinensisand produce both female and male offspring called sexuales. After
mating, each female reproduces only one fundatrix, starting the cycle
again (Figure 1) (Zhang, Qiao, Zhong & Zhang, 1999; Blackman and
Eastop, 2020). This representing an unusual life cycle with comprising
various morphologically distinct aphid forms at different stages, and
its evolution was likely driven by the adaptation to different
environmental conditions. Unlike most free-living aphids from the
Aphidinae taxon, galling aphids exhibit diverse biological
characteristics. For example, most galling aphid species do not
seriously affect the health of their host plants. In some cases, the
galls are thought to be beneficial to host plants (Chen et al., 2020).
For S. chinensis , the complexities in its developmental process
and the structure of its induced galls imply that it may possess unique
gene sets that regulate its development and manipulate its host plants
(Takeda et al., 2019; Hirano et al., 2020). The molecular mechanisms
underlying its complex life cycle remain largely unknown. Galls are
produced through the insect-driven dramatic reprogramming of plant cell
biology. Previous studies have shown that gall induction is highly
species-specific, and that different galling insects deliver unique sets
of effectors into plant tissues, resulting in gall formation (Zhao et
al., 2015; Aljbory et al., 2018). The underlying mechanisms of the
parasitic ability of galling aphids on host plants via apparently
harmless galls remain unknown so far. To understand the genetic basis of
the complex lifestyle, a high-quality chromosome-level genome assembly
of S. chinensis accomplished, representing the first genome
sequence of aphids that induces the formation of completely closed
galls. Phylogenetic relationship between S. chinensis and closely
related species was analyzed to better understand the unique biological
characteristics of S. chinensis .