Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (20): 4007-4021.doi: 10.3864/j.issn.0578-1752.2024.20.007

• SPECIAL FOCUS: OCCURRENCE AND CONTROL OF MIGRATORY PESTS • Previous Articles     Next Articles

Comparative Analysis of the Toll Receptor Gene Families in Three Species of Rice Planthoppers

ZHONG ZiChun(), WU HongXin, ZHANG Jie, GUO YuJing, HE LiuYan, XU XiaoXia, JIN FengLiang, PANG Rui()   

  1. College of Plant Protection, South China Agricultural University/State Key Laboratory of Green Pesticide, Guangzhou 510642
  • Received:2024-06-22 Accepted:2024-07-20 Online:2024-10-16 Published:2024-10-24
  • Contact: PANG Rui

Abstract:

【Objective】The Toll receptor is one of the key effector factors in the Toll signaling pathway of the innate immune system in insects. This article aims to identify the Toll receptor genes of three types of rice planthoppers (Nilaparvata lugens, Sogatella furcifera, and Laodelphax striatellus), explore the potential functions of the Toll receptor in these three species, and investigate the interspecies differences, so as to provide a theoretical basis for the study of the immune development of rice planthoppers and for the control and prevention of these pests.【Method】Bioinformatics methods were used to identify Toll receptor genes from the genomes of three species of rice planthoppers, and the gene structure and characteristics, physicochemical properties and structural domains of the encoded proteins, chromosome localization and phylogenetic evolutionary relationships were analyzed. Artificial intelligence software AlphaFold 3 was used to predict the three-dimensional structure of Toll receptors and compare it with the known structures and functions of Toll receptors from other species to predict their potential functions and interspecific functional differentiation. Transcriptome data were used to quantitatively analyze the expressions of Toll receptor genes in different tissues and at different developmental stages.【Result】A total of 6, 7, and 6 Toll receptor genes were identified in the genomes of N. lugens, S. furcifera, and L. striatellus, respectively, all of which are distributed on chromosomes 1, 4, and 7, with a clear distribution pattern. The Toll gene family in the three species of rice planthoppers is distributed with one gene on chromosomes 1 and 4, and the rest on chromosome 7. The coding sequence lengths of the Toll receptor genes in the three species of rice planthoppers range from 2 676 to 4 158 bp, with the number of exons ranging from 1 to 7, and the encoded protein sequence lengths range from 891 to 1 385 aa, with molecular weights ranging from 103.31 to 158.25 kDa and theoretical isoelectric points ranging from 5.42 to 6.54. Phylogenetic development analysis showed that the Toll receptor gene family of the three species of rice planthoppers can be divided into six subfamilies, which are homologous to the Toll, Toll6, Toll7, Tollo (Toll8), and Toll9 of other insects. The comparison analysis of the extracellular structures predicted by AlphaFold 3 with those of Toll receptors from other species showed that two Toll receptors in the Toll receptor gene family of S. furcifera were potentially related to virus interactions, one in the Toll receptor gene family of L. striatellus, and none in the Toll receptor gene family of N. lugens. Transcriptome quantitative results showed that the Toll receptor genes in the three species of rice planthoppers were expressed in different tissues and at different developmental stages, suggesting that they may have different functions and participate in different divisions of labor.【Conclusion】A total of 19 Toll receptor genes were identified in three species of rice planthoppers, and their related structures and functions were analyzed and predicted. The study revealed potential differences in the roles played by Toll receptors in the development and immune response, particularly in virus immunity, within the insect body among these three species of rice planthoppers.

Key words: rice planthopper, Toll receptor, immune development, gene family identification

Table 1

Identification and characteristics of Toll gene receptor family members in the three rice planthoppers"

基因名
Gene name
基因组id
Genome identifier
染色体位置Locus CDS长度
CDS length (bp)
外显子数目
Exon count
正负链
位置
Strand
氨基酸数量
Amino acid count
分子量
Molecular weight (kDa)
等电点
Isoelectric point
不稳定系数
Instability index
染色体
Chromosome
起始位置
<BOLD>S</BOLD>tarting
终止位置
<BOLD>E</BOLD>nding
NlToll1 LOC111055850 Chr1 79753369 79822973 3351 6 + 1116 126.70 5.75 39.62
NlToll2 LOC111062857 Chr4 53973743 53997406 2676 7 + 891 103.31 5.91 38.10
NlToll3 LOC111049148 Chr7 43423988 43538904 3909 2 - 1302 150.69 6.03 47.58
NlToll4 LOC111064393 Chr7 49257891 49263068 3846 2 - 1281 146.01 5.59 38.73
NlToll5 LOC111056049 Chr7 50148873 50196808 3975 2 - 1324 146.42 5.57 46.19
NlToll6 LOC111056401 Chr7 57508998 57767470 3810 2 + 1270 145.31 5.53 44.82
SfToll1 Sfur012514 Chr1 63573403 63639166 3363 6 + 1120 126.92 6.01 41.32
SfToll2 Sfur012217 Chr4 4083510 4099003 2733 7 + 910 107.20 6.54 37.08
SfToll3 Sfur014773 Chr7 10836279 10942139 3888 3 + 1295 145.67 5.44 48.11
SfToll4 Sfur014910 Chr7 25119800 25125233 4158 5 - 1385 158.25 6.03 47.76
SfToll5 Sfur015175 Chr7 26011622 26043098 3864 2 - 1287 146.71 5.55 39.78
SfToll6 Sfur015206 Chr7 27226151 27230098 3918 2 + 1305 148.36 6.06 47.28
SfToll7 Sfur015067 Chr7 27367526 27371473 3918 2 + 1305 148.37 6.06 47.28
LsToll1 Lstr008514 Chr1 48547956 48560133 3087 6 + 1028 116.76 6.05 38.29
LsToll2 Lstr021969 Chr4 1327721 1348391 2724 7 - 907 106.02 5.77 38.55
LsToll3 Lstr001715 Chr7 8226430 8256447 3981 2 - 1326 150.61 6.09 48.13
LsToll4 Lstr001664 Chr7 10019204 10023088 3885 1 - 1294 145.64 5.42 47.44
LsToll5 Lstr000663 Chr7 21157348 21161193 3846 1 - 1281 146.40 5.58 44.05
LsToll6 Lstr000721 Chr7 21612317 21766732 3855 3 - 1284 146.40 5.60 38.63

Fig. 1

Phylogenetic tree of the Toll receptor gene family Yellow branches represent the Toll subfamily, purple branches represent the Toll9 subfamily, green branches represent the subfamily homologous to the D. melanogaster Tollo, red branches represent the Toll6 subfamily, black branches represent the subfamily homologous to the A. aegypti Tollo, and blue branches represent the Toll7 subfamily"

Fig. 2

Chromosome mapping and genomic collinearity of the Toll receptor gene family in three species of rice planthoppers"

Fig. 3

Motif patterns and conserved structural domains of the Toll receptor gene family in three species of rice planthoppers"

Fig. 4

Three-dimensional structure and similarity analysis of Toll receptors in three species of rice planthoppers"

Fig. 5

Heatmap of Toll receptor gene expression at different developmental stages in three species of rice planthoppers"

Fig. 6

Heatmap of the expression levels of Toll receptor genes in different tissues of three species of rice planthoppers"

[1]
汤金仪, 胡伯海, 王建强. 我国水稻迁飞性害虫猖獗成因及其治理对策建议. 生态学报, 1996, 16(2): 167-173.
TANG J Y, HU B H, WANG J Q. Outbreak analysis of rice migratory pests in China and management strategies recommended. Acta Ecologica Sinica, 1996, 16(2): 167-173. (in Chinese)
[2]
刘万才, 刘振东, 黄冲, 陆明红, 刘杰, 杨清坡. 近10年农作物主要病虫害发生危害情况的统计和分析. 植物保护, 2016, 42(5): 1-9, 46.
LIU W C, LIU Z D, HUANG C, LU M H, LIU J, YANG Q P. Statistics and analysis of crop yield losses caused by main diseases and insect pests in recent 10 years. Plant Protection, 2016, 42(5): 1-9, 46. (in Chinese)
[3]
蒯鹏, 娄永根. 稻飞虱生物学、生态学及其防控技术研究进展. 浙江大学学报(农业与生命科学版), 2022, 48(6): 692-700.
KUAI P, LOU Y G. Research advances in biology, ecology and management of rice planthoppers. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(6): 692-700. (in Chinese)
[4]
罗守进. 稻飞虱的研究. 农业灾害研究, 2011, 1(1): 1-13.
LUO S J. Research on rice planthopper. Journal of Agricultural Catastrophology, 2011, 1(1): 1-13. (in Chinese)
[5]
XUE J, ZHOU X, ZHANG C X, YU L L, FAN H W, WANG Z, XU H J, XI Y, ZHU Z R, ZHOU W W, et al. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biology, 2014, 15(12): 521.
[6]
WANG L, TANG N, GAO X L, CHANG Z X, ZHANG L Q, ZHOU G H, GUO D Y, ZENG Z, LI W J, AKINYEMI I A, YANG H M, WU Q F. Genome sequence of a rice pest, the white-backed planthopper (Sogatella furcifera). GigaScience, 2017, 6(1): 1-9.

doi: 10.1093/gigascience/giw004 pmid: 28369349
[7]
CUI T, BAI Q, YU W Q, GUO D Y, BAN Y W, CHEN K, RAZA A, ZHOU G H, WU Q F. Chromosome-level genome assembly and population genomic analysis provide novel insights into the immunity and evolution of Sogatella furcifera. Genomics, 2023, 115(6): 110729.
[8]
HU Q L, YE Y X, ZHUO J C, HUANG H J, LI J M, ZHANG C X. Chromosome-level assembly, dosage compensation and sex-biased gene expression in the small brown planthopper Laodelphax striatellus. Genome Biology and Evolution, 2022, 14(11): evac160.
[9]
BAO Y Y, QU L Y, ZHAO D, CHEN L B, JIN H Y, XU L M, CHENG J A, ZHANG C X. The genome- and transcriptome-wide analysis of innate immunity in the brown planthopper Nilaparvata lugens. BMC Genomics, 2013, 14: 160.
[10]
李有志, 方继朝. 水稻害虫: 研究进展与展望. 昆虫学报, 2024, 67(4): 443-455.
LI Y Z, FANG J C. Rice pests: Research progresses and prospects. Acta Entomologica Sinica, 2024, 67(4): 443-455. (in Chinese)
[11]
ZHANG H J, LIN Y P, LIU M, LIANG X Y, JI Y N, TANG B Z, HOU Y M. Functional conservation and division of two single-carbohydrate- recognition domain C-type lectins from the nipa palm hispid beetle Octodonta nipae (Maulik). Developmental and Comparative Immunology, 2019, 100: 103416.
[12]
HULTMARK D. Drosophila immunity: Paths and patterns. Current Opinion in Immunology, 2003, 15(1): 12-19.
[13]
LEULIER F, PARQUET C, PILI-FLOURY S, RYU J H, CAROFF M, LEE W J, MENGIN-LECREULX D, LEMAITRE B. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunology, 2003, 4(5): 478-484.
[14]
ZAMBON R A, NANDAKUMAR M, VAKHARIA V N, WU L P. The Toll pathway is important for an antiviral response in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(20): 7257-7262.
[15]
RAMIREZ J L, DIMOPOULOS G. The Toll immune signaling pathway control conserved anti-dengue defenses across diverse Ae. aegypti strains and against multiple dengue virus serotypes. Developmental and Comparative Immunology, 2010, 34(6): 625-629.
[16]
FERREIRA A G, NAYLOR H, ESTEVES S S, PAIS I S, MARTINS N E, TEIXEIRA L. The Toll-dorsal pathway is required for resistance to viral oral infection in Drosophila. PLoS Pathogens, 2014, 10(12): e1004507.
[17]
HE Y J, LU G, QI Y H, ZHANG Y, ZHANG X D, HUANG H J, ZHUO J C, SUN Z T, YAN F, CHEN J P, ZHANG C X, LI J M. Activation of Toll immune pathway in an insect vector induced by a plant virus. Frontiers in Immunology, 2021, 11: 613957.
[18]
IMLER J L, ZHENG L B. Biology of Toll receptors: Lessons from insects and mammals. Journal of Leukocyte Biology, 2004, 75(1): 18-26.
[19]
齐小浪, 杜娟, 李尚伟, 黄海. 昆虫Toll与IMD信号通路研究进展. 山地农业生物学报, 2022, 41(2): 44-50.
QI X L, DU J, LI S W, HUANG H. Research progress of insect Toll and lMD signal pathways. Journal of Mountain Agriculture and Biology, 2022, 41(2): 44-50. (in Chinese)
[20]
NUSSLEIN-VOLHARD C, LOHS-SCHARDIN M, SANDER K, CREMER C. A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature, 1980, 283(5746): 474-476.
[21]
ELDON E, KOOYER S, D’EVELYN D, DUMAN M, LAWINGER P, BOTAS J, BELLEN H. The Drosophila 18 wheeler is required for morphogenesis and has striking similarities to Toll. Development, 1994, 120(4): 885-899.
[22]
TAKEDA K, AKIRA S. Toll-like receptors in innate immunity. International Immunology, 2005, 17(1): 1-14.

doi: 10.1093/intimm/dxh186 pmid: 15585605
[23]
CHRISTOPHIDES G K, ZDOBNOV E, BARILLAS-MURY C, BIRNEY E, BLANDIN S, BLASS C, BREY P T, COLLINS F H, DANIELLI A, DIMOPOULOS G, et al. Immunity-related genes and gene families in Anopheles gambiae. Science, 2002, 298(5591): 159-165.
[24]
EVANS J D, ARONSTEIN K, CHEN Y P, HETRU C, IMLER J L, JIANG H, KANOST M, THOMPSON G J, ZOU Z, HULTMARK D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology, 2006, 15(5): 645-656.
[25]
TANAKA H, ISHIBASHI J, FUJITA K, NAKAJIMA Y, SAGISAKA A, TOMIMOTO K, SUZUKI N, YOSHIYAMA M, KANEKO Y, IWASAKI T, SUNAGAWA T, YAMAJI K, ASAOKA A, MITA K, YAMAKAWA M. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochemistry and Molecular Biology, 2008, 38(12): 1087-1110.
[26]
ALTINCICEK B, KNORR E, VILCINSKAS A. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Developmental and Comparative Immunology, 2008, 32(5): 585-595.
[27]
GERARDO N M, ALTINCICEK B, ANSELME C, ATAMIAN H, BARRIBEAU S M, DE VOS M, DUNCAN E J, EVANS J D, GABALDÓN T, GHANIM M, et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biology, 2010, 11(2): R21.
[28]
KAMBRIS Z, HOFFMANN J A, IMLER J, CAPOVILLA M. Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expression Patterns, 2002, 2(3/4): 311-317.
[29]
NIE L, CAI S Y, SHAO J Z, CHEN J. Toll-like receptors, associated biological roles, and signaling networks in non-mammals. Frontiers in Immunology, 2018, 9: 1523.

doi: 10.3389/fimmu.2018.01523 pmid: 30034391
[30]
NAKAMOTO M, MOY R H, XU J, BAMBINA S, YASUNAGA A, SHELLY S S, GOLD B, CHERRY S. Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity, 2012, 36(4): 658-667.
[31]
HE Y, LU G, XU B, MAO Q, QI Y, JIAO G, WENG H, TIAN Y, HUANG H, ZHANG C, CHEN J, LI J. Maintenance of persistent transmission of a plant arbovirus in its insect vector mediated by the Toll-dorsal immune pathway. Proceedings of the National Academy of Sciences of the United States of America, 2024, 121(14): e2315982121.
[32]
JIA D, LUO G, GUAN H, YU T, SUN X, DU Y, WANG Y, CHEN H, WEI T. Arboviruses antagonize insect Toll antiviral immune signaling to facilitate the coexistence of viruses with their vectors. PLoS Pathogens, 2024, 20(6): e1012318.
[33]
赖坤龙, 王海峰, 徐钟天, 崔娜. 稻飞虱传播水稻病毒机制的研究进展. 福建农林大学学报(自然科学版), 2021, 50(5): 577-587.
LAI K L, WANG H F, XU Z T, CUI N. Advance in the mechanism of rice virus transmission by planthopper. Journal of Fujian Agriculture and Forestry University (Natural Science Edition), 2021, 50(5): 577-587. (in Chinese)
[34]
MA W H, XU L, HUA H X, CHEN M Y, GUO M J, HE K, ZHAO J, LI F. Chromosomal-level genomes of three rice planthoppers provide new insights into sex chromosome evolution. Molecular Ecology Resources, 2021, 21(1): 226-237.
[35]
GASTEIGER E, HOOGLAND C, GATTIKER A, DUVAUD S, WILKINS M R, APPEL R D, BAIROCH A. Protein identification and analysis tools on the ExPASy server//The Proteomics Protocols Handbook. Totowa, NJ: Humana Press, 2005: 571-607.
[36]
KATOH K, STANDLEY D M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 2013, 30(4): 772-780.

doi: 10.1093/molbev/mst010 pmid: 23329690
[37]
MINH B Q, SCHMIDT H A, CHERNOMOR O, SCHREMPF D, WOODHAMS M D, VON HAESELER A, LANFEAR R. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 2020, 37(5): 1530-1534.

doi: 10.1093/molbev/msaa015 pmid: 32011700
[38]
LETUNIC I, BORK P. Interactive tree of life (iTOL) v6: Recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Research, 2024, 52(W1): W78-W82.
[39]
CHEN C J, WU Y, LI J W, WANG X, ZENG Z H, XU J, LIU Y L, FENG J T, CHEN H, HE Y H, XIA R. TBtools-II: A “one for all, all for one” bioinformatics platform for biological big-data mining. Molecular Plant, 2023, 16(11): 1733-1742.
[40]
WANG Y P, TANG H B, DEBARRY J D, TAN X, LI J P, WANG X Y, LEE T H, JIN H Z, MARLER B, GUO H, KISSINGER J C, PATERSON A H. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 2012, 40(7): e49.
[41]
EMMS D M, KELLY S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biology, 2019, 20(1): 238.
[42]
BAILEY T L, WILLIAMS N, MISLEH C, LI W W. MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research, 2006, 34: W369-W373.

doi: 10.1093/nar/gkl198 pmid: 16845028
[43]
ABRAMSON J, ADLER J, DUNGER J, EVANS R, GREEN T, PRITZEL A, RONNEBERGER O, WILLMORE L, BALLARD A J, BAMBRICK J, et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature, 2024, 630(8016): 493-500.
[44]
KOCIC G, HADZI-DJOKIC J, COLIC M, VELJKOVIC A, TOMOVIC K, ROUMELIOTIS S, SMELCEROVIC A, LIAKOPOULOS V. The role of nucleases cleaving TLR3, TLR7/8 and TLR9 ligands, dicer RNase and miRNA/piRNA proteins in functional adaptation to the immune escape and xenophagy of prostate cancer tissue. International Journal of Molecular Sciences, 2022, 24(1): 509.
[45]
MORENO-EUTIMIO M A, LÓPEZ-MACÍAS C, PASTELIN-PALACIOS R. Bioinformatic analysis and identification of single-stranded RNA sequences recognized by TLR7/8 in the SARS-CoV-2, SARS-CoV, and MERS-CoV genomes. Microbes and Infection, 2020, 22(4/5): 226-229.
[46]
STÖVEN S, ANDO I, KADALAYIL L, ENGSTRÖM Y, HULTMARK D. Activation of the Drosophila NF-κB factor Relish by rapid endoproteolytic cleavage. EMBO Reports, 2000, 1(4): 347-352.
[47]
ZHU J J, JIANG F, WANG X H, YANG P C, BAO Y Y, ZHAO W, WANG W, LU H, WANG Q S, CUI N, et al. Genome sequence of the small brown planthopper, Laodelphax striatellus. GigaScience, 2017, 6(12): 1-12.

doi: 10.1093/gigascience/gix109 pmid: 29136191
[48]
BRAY N L, PIMENTEL H, MELSTED P, PACHTER L. Near-optimal probabilistic RNA-Seq quantification. Nature Biotechnology, 2016, 34(5): 525-527.

doi: 10.1038/nbt.3519 pmid: 27043002
[49]
吴洪鑫, 许亚婷, 康泽泓, 杨荣蓉, 陆永跃, 金丰良, 许小霞. 红火蚁Serpin家族基因鉴定及其在绿僵菌侵染下的表达模式分析. 环境昆虫学报, 2022, 44(6): 1541-1552.
WU H X, XU Y T, KANG Z H, YANG R R, LU Y Y, JIN F L, XU X X. Genome-wide identification of Serpin gene family in Solenopsis invicta and expression analysis in response to Metarhizium anisopliae. Journal of Environmental Entomology, 2022, 44(6): 1541-1552. (in Chinese)
[50]
SHMUELI A, SHALIT T, OKUN E, SHOHAT-OPHIR G. The Toll pathway in the central nervous system of flies and mammals. Neuromolecular Medicine, 2018, 20: 419-436.

doi: 10.1007/s12017-018-8515-9 pmid: 30276585
[51]
HASHIMOTO C, HUDSON K L, ANDERSON K V. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell, 1988, 52(2): 269-279.
[52]
MCILROY G, FOLDI I, AURIKKO J, WENTZELL J S, LIM M A, FENTON J C, GAY N J, HIDALGO A. Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nature Neuroscience, 2013, 16(9): 1248-1256.
[53]
SEPPO A, MATANI P, SHARROW M, TIEMEYER M. Induction of neuron-specific glycosylation by Tollo/Toll-8, a Drosophila Toll-like receptor expressed in non-neural cells. Development, 2003, 130(7): 1439-1448.
[54]
BALLARD S L, MILLER D L, GANETZKY B. Retrograde neurotrophin signaling through Tollo regulates synaptic growth in Drosophila. Journal of Cell Biology, 2014, 204(7): 1157-1172.
[55]
WARD A, HONG W, FAVALORO V, LUO L. Toll receptors instruct axon and dendrite targeting and participate in synaptic partner matching in a Drosophila olfactory circuit. Neuron, 2015, 85(5): 1013-1028.
[56]
NARBONNE-REVEAU K, CHARROUX B, ROYET J. Lack of an antibacterial response defect in Drosophila Toll-9 mutant. PLoS ONE, 2011, 6(2): e17470.
[57]
WU S, ZHANG X, CHEN X, CAO P, BEERNTSEN B T, LING E. BmToll9, an arthropod conservative Toll, is likely involved in the local gut immune response in the silkworm Bombyx mori. Developmental and Comparative Immunology, 2010, 34(2): 93-96.
[58]
MORGAN M M, MAHOWALD A P. Multiple signaling pathways establish both the individuation and the polarity of the oocyte follicle in Drosophila. Archives of Insect Biochemistry and Physiology, 1996, 33(3/4): 211-230.
[59]
WANG Z, NIE K, LIANG Y, NIU J, YU X, ZHANG O, LIU L, SHI X, WANG Y, FENG X, ZHU Y B, WANG P H, CHENG G. A mosquito salivary protein-driven influx of myeloid cells facilitates flavivirus transmission. The EMBO Journal, 2024, 43(9): 1690-1721.
[60]
ZHAO W, LU L X, YANG P C, CUI N, KANG L, CUI F. Organ-specific transcriptome response of the small brown planthopper toward rice stripe virus. Insect Biochemistry and Molecular Biology, 2016, 70: 60-72.

doi: 10.1016/j.ibmb.2015.11.009 pmid: 26678499
[61]
何晓婵, 徐红星, 郑许松, 杨亚军, 高广春, 潘建红, 陆强, 吕仲贤. 水稻黑条矮缩病毒对非介体稻飞虱——白背飞虱适应性的影响. 中国水稻科学, 2011, 25(6): 654-658.
HE X C, XU H X, ZHENG X S, YANG Y J, GAO G C, PAN J H, LU Q, Z X. Effects of rice black-streaked dwarf virus on ecological fitness of non-vector planthopper Sogatella furcifera. Chinese Journal of Rice Science, 2011, 25(6): 654-658. (in Chinese)
[62]
万贵钧. 病毒和磁场对稻飞虱发育、生殖及行为的影响研究[D]. 南京: 南京农业大学, 2015.
WAN G J. Effects of virus and magnetic field on the development, reproduction and behaviour of rice planthopper[D]. Nanjing: Nanjing Agricultural University, 2015. (in Chinese)
[63]
CARDOSO-JAIME V, TIKHE C V, DONG S Z, DIMOPOULOS G. The role of mosquito hemocytes in viral infections. Viruses, 2022, 14(10): 2088.
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