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Zhang, C.-X.

Publications and source records attributed to Zhang, C.-X..

8 recordsLinked to original sources

Sex-determination cascade orchestrates male-male pheromone synthesis in the bean bug

Volatile pheromones are vital for insect intraspecific communication, yet the genetic basis of homosexual recognition remains elusive. In the bean bug Riptortus pedestris, we show that two previously identified aggregation pheromone components, (E)-2-hexenyl-(Z)-3-hexenoate (E2HZ3H) and (E)-2-hexenyl-(E)-2-hexenoate (E2HE2H), serve as key chemosensory cues for male-male recognition during mate selection. Their biosynthesis is governed by the sex-determination cascade Rpfmd-Rpdsx. The male-specific isoform Rpdsx_M promotes pheromone production in males and induces ectopic synthesis in females upon knockdown of the feminizing switch gene Rpfmd. Knockdown of Rpdsx_M in males abolishes both compounds, prompting wild-type males to court them as if they were females. Metathoracic gland cells act as the production hub. Behaviourally, E2HZ3H or E2HE2H disrupt mating when applied to females: males avoid such females. E2HZ3H reduces female mobility in the presence of the male-derived primary aggregation pheromone tetradecyl isobutyrate (14:iBu), whereas E2HE2H shows no obvious such effect. These differential effects ensure mating accuracy. The discovery of volatile pheromones functioning in male-male recognition and of their synthesis being governed by the sex-determination cascade updates our understanding of mating accuracy in insect chemical communication.

animal behavior and cognition↗

Augment rice ANNEXIN expression to counter planthopper NlAnnexin-like5 as an anti-virulence strategy against a major crop pest

The brown planthopper (BPH) is the most devastating insect pest in rice, posing a serious threat to global rice production. One attractive control strategy would be based on the understanding of the virulence mechanisms of BPH at the molecular level and then designing targeted methods to neutralize such mechanisms. Salivary proteins of BPH are important players in mediating rice-BPH interactions. Here, we describe a pivotal role of a watery saliva protein, NlAnnexin-like5 (NlANX5), in the rice-BPH interaction. RNA interference (RNAi) of NlANX5 greatly compromised BPH feeding performance and survival rate on rice plants. NlANX5-RNAi BPH triggered a rapid calcium ion influx in rice cells. The feeding and survival defects of NlANX5-RNAi BPH can be restored in NlANX5-expressing transgenic rice plants. NlANX5 targets rice annexin (OsANN) proteins, including OsANN2 and OsANN8. Further analysis with NlANX5 and OsANN2 as well as OsANN8 showed that NlANX5 displaces OsANN2 and OsANN8 from the rice cell membrane. The osann2 osann8 mutant rice plants are hypersusceptible to BPH infestation. In contrast, enhanced expression of OsANN2 and OsANN8 gene resulted in robust rice resistance against BPH. This study highlights a successful example of identifying and augmenting the expression of the host targets of a major BPH virulence effector as a promising anti-virulence strategy against an important crop pest. Significance StatementInsect pests pose a serious biotic threat to crop production worldwide. Understanding how insect pests attack plants could inspire innovative pest control measures to enhance global food security. The brown planthopper (BPH; Nilaparvata lugens St[a]l) is the most devastative insect pest in rice. In this study, we discovered that BPH secretes a salivary protein, NlAnnexin-like5 (NlANX5), to target rice host annexins that are associated with calcium fluxes and activation of multiple rice defense pathways. This knowledge led to employing enhanced expression of rice annexin-encoding genes to successfully defeat the virulence function of NlANX5. Results have significant implications in the development of anti-virulence breeding strategies against BPH.

plant biology↗

Brochosomes as an antireflective camouflage coating for leafhoppers

In nature, insects face immense predation pressure, where visual cues play a vital role in predators locating them. To counter this threat, insects employ a variety of nano- and microstructures on their cuticular layer to manipulate and interact with light, enhancing anti-reflective properties and providing camouflage or reducing detectability by predators. Leafhoppers have a unique extra-cuticular coating called brochosome, yet its anti-reflective functions and protein composition remain unclear. Our study demonstrates strong anti-reflective properties of brochosomes, effectively reducing reflectance on the cuticle surface, especially in the ultraviolet spectrum, to improve evasion from visual predators. Furthermore, we identify four novel structural proteins of the brochosome (BSM) for the first time. Inhibiting their synthesis by RNAi alters brochosome morphology, impacting the optical properties of the cuticle surface. Evolutionary origin analysis of BSM suggests that brochosomes likely originated from a process involving duplication-divergence. Our study reveals that leafhoppers employ a unique camouflage strategy by secreting brochosomes as anti-reflection nano-coatings, enabling them to evade natural predators and contributing to their evolutionary success.

ecology↗

Diversity and adaptability of RNA viruses in rice planthopper, Laodelphax striatellus

Although a large number of insect-specific viruses (ISVs) have recently been discovered from hematophagous insect, studies on ISV diversity and their association with phytophagous insect hosts were still insufficient. A systematic RNA virome investigation was performed for an important plant virus vector, small brown planthopper (SBPH), Laodelphax striatellus. A total number of 22 RNA viruses (including 17 novel viruses) belonging to various families were successfully identified and characterized. Subsequent analysis indicated that the overall RNA virus transcripts per million (TPM) in SBPH was relatively consistent throughout various different developmental stages of the insects, although the titers of individual viruses differ among different insect tissues, suggesting a delicate balance between ISVs and insect hosts. Moreover, analysis of virus-derived small interfering RNA (siRNA) demonstrated that siRNA mediated antiviral immune response of SBPH was activated in response to the replication of the discovered RNA viruses. Additionally, evaluation for potential cross-species ability of SBPH-ISVs showed that certain SBPH ISVs could successfully infect and replicate in another two rice planthoppers, the brown planthopper and the white-backed planthopper, through microinjection. In conclusion, the RNA virome and their adaptability in SBPH revealed in this study will contribute to a better understanding of the intimate relationship between ISVs and the host insects.

microbiology↗

Rapid intracellular acidification is a novel plant defense response countered by the brown planthopper

The brown planthopper (BPH) is the most destructive insect pest in rice. Through a stylet, BPH secrets a plethora of salivary proteins into rice phloem cells as a crucial step of infestation. However, how various salivary proteins function in rice cells to promote insect infestation is poorly understood. Among them, one of the salivary proteins is predicted to be a carbonic anhydrase (NlCA). The survival rate of the NlCA-RNA interference (RNAi) BPH insects was extremely low on rice, indicating a vital role of this salivary protein in BPH infestation. We generated NICA transgenic rice plants and found that NlCA expressed in rice plants could restore the ability of NlCA-RNAi BPH to survive on rice. Next, we produced rice plants expressing the ratiometric pH sensor pHusion and found that NlCA-RNAi BPH induced rapid intracellular acidification of rice cells during feeding. Further analysis revealed that both NlCA-RNAi BPH feeding and artificial of lowering intracellular pH activated plant defense responses, and that NICA-mediated intracellular pH stabilization is linked to diminished defense responses, including reduced callose deposition at the phloem sieve plates and suppressed defense gene expression. Given the importance of pH homeostasis across the kingdoms of life, discovery of NICA-mediated intracellular pH modulation uncovered a new dimension in the interaction between plants and piecing/sucking insect pests. The crucial role of NICA for BPH infestation of rice suggests that NICA is a promising target for chemical or trans-kingdom RNAi-based inactivation for BPH control strategies in plants. HighlightsO_LIRapid intracellular acidification is a novel plant defense response. C_LIO_LIBrown planthopper delivers into rice tissues a major virulence protein, carbonic anhydrase (NlCA), critical for survival. C_LIO_LINlCA counters intracellular acidification to suppress plant defense. C_LIO_LIResults implicate existence of pH-responsive regulators of defense responses in the rice-brown planthopper interaction. C_LI In briefThe brown planthopper (BPH) is the most devasting insect pest in rice. Jiang et al. discovered that BPH secretes a salivary carbonic anhydrase (NICA) to regulate the intracellular pH of the rice cell to facilitate its feeding and survival on rice plants and that NICA-counters host intracellular pH acidification to diminished defense responses. These findings uncovered that intracellular pH homeostasis is a previously uncharacterized battleground in plant-insect interactions, but also open a door to future discovery of pH-responsive intracellular regulators of defense responses, which could add a new research dimension in the study of plant-biotic interactions.

plant biology↗

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

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 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.

genomics↗

Whole genome sequencing of 358 brown planthoppers uncovers the landscape of their migration and dispersal worldwide

The brown planthopper (BPH), Nilaparvata lugens, is a serious migratory rice pest, which is distributed in the broad area of the tropical and temperate Asian-Pacific region. However, we know little about key aspects regarding its evolution such as how they diverged and dispersed worldwide. By resequencing and analyzing 358 BPH genomes from 92 populations across the world, we uncover the genetic relationships among their worldwide populations and the history of their global dispersal. We recovered five genetic groups representing the major population structures. Of these, Australian BPHs were shown large genetic divergence with Asian BPHs; two distinct groups have formed in South and Southeast/East Asia that show strong genetic admixture in the southwest border regions of China and west Thailand with Myanmar; two local populations in Bangladesh and Fujian province of China, respectively, unexpectedly separated with surrounding populations. We also find the genetic similarity and closely phylogenetic relationships between majority of East Asian BPHs and Indo-china peninsula BPHs, indicating that Southeast Asia mainland is the major insect sources and overwintering sites for East Asia. Our study provides important molecular evidence to address BPH evolution and other key aspects of its biology such as insecticides resistance and rice varieties virulence.

evolutionary biology↗

Identification of a female determinant gene for the sexual determination of a hemipteran insect, the brown planthopper

The sex determination mechanism for hemipteran species remains poorly understood. During the sex determination of the brown planthopper (BPH), Nilaparvata lugens, one species of Hemiptera, the functions of doublesex (Nldsx) and NlTra-2 (NlTra-2) genes were identified in our previous studies. Here, we identify an upstream gene for Nldsx in the sex determination cascade, NlFmd, which acts as female determinant gene for N. lugens. The sex-specific transcript of NlFmd (NlFmd-F) encodes an arginine/serine-, and proline-rich protein that is essential for female development. The knockdown of NlFmd resulted in the development of pseudomales, with sex-specific alternative Nldsx processing, and maternal RNA interference (RNAi) against NlFmd generates male-only progeny. Moreover, homologous genes for NlFmd have also been identified in two rice planthopper species, the white-backed planthopper (WBPH, Sogotalla furcifera) and the small brown planthopper (SBPH, Laodelphax striatellus), and these genes appear to be involved in the sex determination cascades for these species. Our data suggest that the sex determination cascade in Delphacidae is conserved.

molecular biology↗