Current Science

Open Access Open Access  Restricted Access Subscription Access

Genome Organization and Comparative Evolutionary Mitochondriomics of Rice Earhead Bug Leptocorisa oratoria (Fabricius)


Affiliations
1 ICAR-National Rice Research Institute, Cuttack 753 006, India
2 ICAR-Research Complex for the Eastern Region, Farming System Research Centre for Hill and Plateau Region, Ranchi 834 010, India
3 World Biodiversity Association Onlus, C/o Museo Civico di Storia Naturale, Lungadige Porta Vittoria 9, 37129 Verona, Italy
 

The rice earhead bug, Leptocorisa oratoria (Fabricius, 1794) is a critical rice pest in India. No mitochondrial genome of L. oratoria has been sequenced earlier, and the mitochondrial data are crucial for phylogenetic and population genetic studies of this significant rice pest. In the present study, the genome of L. oratoria is 17,584 bp long with 73.57% AT content. We observed tandem repeat in the control region. Analyses from genetic distance, sliding window and Ka/Ks ratio revealed a purifying selection of 13 protein-coding genes, with cox1 and nad2 reporting the lowest and highest rate of evolution respectively. Phylogenetic analysis was reconstructed using 65 pentatomid mitogenomes with Bayesian inference and maximum likelihood methods. The results help differentiate the Coreoidea superfamily from Lygaeoidea, Aradoidea and Pentatomoidea. There were two topologies at the family level, i.e. one clade formed with Coreidae + Rhopalidae + Alydidae, and the rest of the families of Pentatomomorpha for­med in separate clades. Further, L. oratoria produced an independent subclade from the earlier reported Leptocorisa sp. genome. This study provides a source mitogenome for L. oratoria species to study population demography, individual differences and phylogeography of hemipterans.

Keywords

Mitogenome, Next Generation Sequencing, Population Genetics, Phylogeny, Rice Earhead Bug.
User
Notifications
Font Size

  • Rao, J. and Prakash, A., Bio-deterioration of paddy seed quality due to insects and mites and its control using botanicals. Final report of ICAR Ad-hoch Scheme, Central Rice Research Institute, Cuttack, India, 1995.

  • Aktera, U. S., Islam, K. S., Jahan, M., Rahman, M. S., Talukder, F. U. and Hasan, M. A., Extent of damage of rice bug (Leptocorisa acuta) and its control with insecticides. Acta Sci. Malays., 2020, 4(2), 82–87; doi:10.26480/asm.02.2020.82.87.

  • Rai, A. B., Singh, J. and Rai, L., Evaluation of gundhi bug, Lepto corisavaricornis (F.) damage in rice. In International Symposium on Rice Research, Hyderabad, 1990.

  • Gupta, K. and Kumar, A., Field efficacy of certain insecticides against rice gundhi bug (Leptocorisa acuta (Thonberg)) under agro-climatic condition of Allahabad, India. Int. J. Curr. Microbiol. Appl. Sci., 2017, 6(8), 343–345.

  • Nugaliyadde, L., Dissanayake, N., Mitrasena, J. and Wijesundera, D. S., Advances of pest and disease management of rice in Sri Lanka: a review. In Annual Symposium of the Department of Agriculture, Sri Lanka, 2000, vol. 2, pp. 409–422.

  • Jahn, G. C., Domingo, I., Liberty, M., Almazan, P. and Pacia, J., Effect of rice bug Leptocoris aoratorius (Hemiptera: Alydidae) on rice yield, grain quality and seed viability. J. Econ. Entomol., 2004, 97(6), 1923–1927; https://doi.org/10.1093/jee/97.6.1923.

  • Lessinger, A. C. et al., The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Mol. Biol., 2000, 9(5), 521–529; https://doi.org/10.1046/j.1365-2583.2000.00215.x.

  • Lewis, J. A., Huq, A., Liu, W. and Jacob, A., Induction of gene expression by intracellular interferon-: abrogation of the species specificity barrier. Virology, 1995, 212(2), 438–450; https://doi.org/10.1006/viro.1995.1501.

  • Zhang, D. X., Szymura, J. M. and Hewitt, G. M., Evolution and structural conservation of the control region of insect mitochondrial DNA. J. Mol. Evol., 1995, 40(4), 382–391; https://doi.org/10.1007/BF00164024.

  • Shao, R., Campbell, N. J. and Barker, S. C., Numerous gene rear-rangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera). Mol. Biol. Evol., 2001, 18(5), 858–865; https://doi.org/10.1093/oxfordjournals.molbev.a003867.

  • Choudhary, J. S., Naaz, N., Prabhakar, C. S., Rao, M. S. and Das, B., The mitochondrial genome of the peach fruit fly, Bactrocera zonata (Saunders) (Diptera: Tephritidae): Complete DNA sequence, genome organization, and phylogenetic analysis with other tephritids using next generation DNA sequencing. Gene, 2015, 569(2), 191–202; https://doi.org/10.1016/j.gene.2015.05.066.

  • Taanman, J. W., The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta, 1999, 1410(2), 103–123; https://doi.org/10.1016/S0005-2728(98)00161-3.

  • Boore, J. L., Animal mitochondrial genomes. Nucleic Acids Res., 1999, 27, 1767–1780; doi:10.1093/nar/27.8.1767.

  • Cameron, S. L., Beckenbach, A. T., Dowton, M. P. and Whiting, M. F., Evidence from mitochondrial genomics on interordinal relationships in insects. Arthropod Syst. Phylogen., 2006, 64(1), 27–34.

  • Ashlock, P. D. and Slater, A., Family Lygaeidae Schilling, 1829 (= Infericornes Amyot and Serville, 1843; Myodochidae Kirkaldy, 1899; Geocoridae Kirkaldy, 1902): the seed bugs and chinch bugs. In Catalog of the Heteroptera, or True Bugs of Canada and the Continental United States, CRC Press, Boca Raton, Florida, 2019, pp. 167–245.

  • Schuh, R. T. and Slater, J. A., True Bugs of the Eorld (Hemiptera: Heteroptera): Classification and Natural History, Cornell University Press, Ithaca, New York, 1995, pp. 609–610.

  • Chilana, P., Sharma, A. and Rai, A., Insect genomic resources: status, availability and future. Curr. Sci., 2012, 102(4), 571–580.

  • Ribeiro, F. J. et al., Finished bacterial genomes from shotgun sequence data. Genome Res., 2012, 22(11), 2270–2277; http://www.genome.org/cgi/doi/10.1101/gr.141515.112.

  • Kirkness, E. F. et al., Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl. Acad. Sci. USA, 2010, 107(27), 12168–12173; https://doi.org/10.1073/pnas.1003379107.

  • Knaus, B. J., Cronn, R., Liston, A., Pilgrim, K. and Schwartz, M. K., Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore. BMC Ecol., 2011, 11(1), 1–4; https://doi.org/10.1186/1472-6785-11-10.

  • Ma, P. F., Guo, Z. H. and Li, D. Z., Rapid sequencing of the bamboo mitochondrial genome using Illumina technology and parallel episodic evolution of organelle genomes in grasses. PLoS ONE, 2012, 7(1), e30297; https://doi.org/10.1371/journal.pone.0030297.

  • Coates, B. S., Assembly and annotation of full mitochondrial genomes for the corn rootworm species, Diabrotica virgifera virgifera and Diabrotica barberi (Insecta : Coleoptera : Chrysomelidae), using next generation sequence data. Gene, 2014, 542(2), 190–197; https://doi.org/10.1016/j.gene.2014.03.035.

  • Barrion, A. T. and Litsinger, J. A., Dichogaster nr. Curgensis Michaelsen (Annelida : Octochaetidae): an earthworm pest of terraced rice in the Philippine Cordilleras. Crop Prot., 1997, 16(1), 89–93; https://doi.org/10.1016/S0261-2194(96)00058-0.

  • Govindharaj, G. P. et al., Genome organization and comparative evolutionary mitochondriomics of brown planthopper, Nilaparvata lugens biotype 4 using next generation sequencing (NGS). Life, 2022, 12(9), 1289; https://doi.org/10.3390/life12091289.

  • Bernt, M. et al., MITOS: improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol., 2013, 69(2), 313–319; https://doi.org/10.1016/j.ympev.2012.08.023.

  • Lowe, T. M. and Eddy, S. R., tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res., 1997, 25(5), 955–964; https://doi.org/10.1093/nar/25.5.955.

  • Grant, J. R. and Stothard, P., The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res., 2008, 36(2), W181–W184; https://doi.org/10.1093/nar/gkn179.

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 2013, 30(12), 2725–2729; https://doi.org/10.1093/molbev/mst197.

  • Choudhary, J. S., Naaz, N., Lemtur, M., Das, B., Singh, A. K., Bhatt, B. P. and Prabhakar, C. S., Genetic analysis of Bactrocerazonata (Diptera : Tephritidae) populations from India based on cox1 and nad1 gene sequences. Mitochondrial DNA Part A, 2018, 29(5), 727–736; https://doi.org/10.1080/24701394.2017.1350952.

  • Perna, N. T. and Kocher, T. D., Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J. Mol. Evol., 1995, 41(3), 353–358; https://doi.org/10.1007/BF0018-6547.

  • Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009, 25(11), 1451–1452; https://doi.org/10.1093/bioinformatics/btp187.

  • Katoh, K. and Standley, D. M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol., 2013, 30(4), 772–780; https://doi.org/10.1093/molbev/mst010.

  • Talavera, G. and Castresana, J., Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol., 2007, 56(4), 564–577; https://doi.org/10.1080/10635150701472164.

  • Bu, R. et al., Tillage and straw-returning practices effect on soil dissolved organic matter, aggregate fraction and bacteria community under rice-rice-rapeseed rotation system. Agric. Ecosyst. Environ., 2020, 287, 106681; https://doi.org/10.1016/j.agee.2019.106681.

  • Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. and Calcott, B., PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol., 2017, 34(3), 772–773; https://doi.org/10.1093/molbev/msw260.

  • Guindon, S. and Gascuel, O., A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 2003, 52(5), 696–704; https://doi.org/10.1080/10635150390235520.

  • Huelsenbeck, J. P. and Ronquist, F., MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics, 2001, 17(8), 754–755.

  • Letunic, I. and Bork, P., Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res., 2019, 47(W1), W256–W259; https://doi.org/10.1093/nar/gkz239.

  • Crease, T. J., The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene, 1999, 233(1–2), 89–99; https://doi.org/10.1016/S0378-1119(99)00151-1.

  • Yuan, M. L., Zhang, Q. L., Guo, Z. L., Wang, J. and Shen, Y. Y., The complete mitochondrial genome of Corizus tetraspilus (Hemiptera: Rhopalidae) and phylogenetic analysis of Pentatomomorpha. PLoS ONE, 2015, 10(6), e0129003; https://doi.org/10.1371/journal.pone.0129003.

  • Zhang, K. J. et al., The complete mitochondrial genomes of two rice planthoppers, Nilaparvata lugens and Laodelphax striatellus: conserved genome rearrangement in Delphacidae and discovery of new characteristics of atp8 and tRNA genes. BMC Genomics, 2013, 14(1), 1–2; https://doi.org/10.1186/1471-2164-14-417.

  • Anant, A. K. et al., Genetic dissection and identification of candidate genes for brown planthopper, Nilaparvata lugens (Delphacidae: Hemiptera) resistance in farmers’ varieties of rice in Odisha. Crop Prot., 2021, 144, 105600; https://doi.org/10.1016/j.cropro.2021.10-5600.

  • Cha, S. Y. et al., The complete nucleotide sequence and gene organization of the mitochondrial genome of the bumblebee, Bombus ignitus (Hymenoptera: Apidae). Gene, 2007, 392(1–2), 206–220; https://doi.org/10.1016/j.gene.2006.12.031.

  • Jiang, S. T., Hong, G. Y., Yu, M., Li, N., Yang, Y., Liu, Y. Q. and Wei, Z. J., Characterization of the complete mitochondrial genome of the giant silkworm moth, Eriogyna pyretorum (Lepidoptera: Saturniidae). Int. J. Biol. Sci., 2009, 5(4), 351; doi:10.7150/ijbs.5.351.

  • Song, N. and Liang, A. P., Complete mitochondrial genome of the small brown planthopper, Laodelphax striatellus (Delphacidae: Hemiptera), with a novel gene order. Zool. Sci., 2009, 26(12), 851–860; https://doi.org/10.2108/zsj.26.851.

  • Chen, M. M. et al., Complete mitochondrial genome of the Atlas moth, Attacus atlas (Lepidoptera: Saturniidae) and the phylogenetic relationship of Saturniidae species. Gene, 2014, 545(1), 95–101; https://doi.org/10.1016/j.gene.2014.05.002.

  • Hua, J., Li, M., Dong, P., Cui, Y., Xie, Q. and Bu, W., Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics, 2008, 9(1), 1–5; https://doi.org/10.1186/1471-2164-9-610.

  • Hou, W. R. et al., A complete mitochondrial genome sequence of Asian black bear Sichuan subspecies (Ursus thibetanus mupinensis). Int. J. Biol. Sci., 2007, 3(2), 85; doi:10.7150/ijbs.3.85.

  • Hong, G., Jiang, S., Yu, M., Yang, Y., Li, F., Xue, F. and Wei, Z., The complete nucleotide sequence of the mitochondrial genome of the cabbage butterfly, Artogeia melete (Lepidoptera: Pieridae). Acta Biochim. Biophys. Sin., 2009, 41(6), 446–455; https://doi.org/10.1093/abbs/gmp030.

  • Lv, L., Peng, X., Jing, S., Liu, B., Zhu, L. and He, G., Intraspecific and interspecific variations in the mitochondrial genomes of Nilaparvata (Hemiptera: Delphacidae). J. Econ. Entomol., 2015, 108(4), 2021–2029; https://doi.org/10.1093/jee/tov122.

  • Thao, M. L., Baumann, L. and Baumann, P., Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evol. Biol., 2004, 4(1), 1–3; https://doi.org/10.1186/1471-2148-4-25.

  • Zhu, Y. J., Zhou, G. L., Fang, R., Ye, J. and Yi, J. P., The complete sequence determination and analysis of Lymantria dispar (Lepidoptera: Lymantriidae) mitochondrial genome. Plant Quarantine, 2010, 24(4), 6–11.

  • Valero, M. C., Ojo, J. A., Sun, W., Tamò, M., Coates, B. S. and Pittendrigh, B. R., The complete mitochondrial genome of Anoplocnemis curvipes F. (Coreinea, Coreidae, Heteroptera), a pest of fresh cowpea pods. Mitochondrial DNA, Part B, 2017, 2(2), 421–423; https://doi.org/10.1080/23802359.2017.1347829.

  • Huang, Y. X. and Qin, D. Z., First mitogenome for the tribe Saccharosydnini (Hemiptera: Delphacidae: Delphacinae) and the phylogeny of three predominant rice planthoppers. Eur. J. Entomol., 2018, 30, 115.

  • Ohtsuki, T., Kawai, G. and Watanabe, K., The minimal tRNA: unique structure of Ascaris suum mitochondrial tRNASerUCU having a short T arm and lacking the entire D arm. FEBS Lett., 2002, 514(1), 37–43; https://doi.org/10.1016/S0014-5793(02)02328-1.

  • Sheffield, N. C., Song, H., Cameron, S. L. and Whiting, M. F., Nonstationary evolution and compositional heterogeneity in beetle mitochondrial phylogenomics. Syst. Biol., 2009, 58(4), 381–394; https://doi.org/10.1093/sysbio/syp037.

  • Zhao, Q., Wang, J., Wang, M. Q., Cai, B., Zhang, H. F. and Wei, J. F., Complete mitochondrial genome of Dinorhynchus dybowskyi (Hemiptera: Pentatomidae: Asopinae) and phylogenetic analysis of Pentatomomorpha species. J. Insect Sci., 2018, 18(2), 44; https://doi.org/10.1093/jisesa/iey031.

  • Lee, W., Kang, J., Jung, C., Hoelmer, K., Lee, S. H. and Lee, S., Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of hemipteran suborders. Mol. Cells, 2009, 28(3), 155–165; https://doi.org/10.1007/s10059-009-0125-9.

  • Li, H., Liu, H., Shi, A., Štys, P., Zhou, X. and Cai, W., The complete mitochondrial genome and novel gene arrangement of the unique-headed bug Stenopirates sp. (Hemiptera: Enicocephalidae). PLoS ONE, 2012, 7(1), e29419; https://doi.org/10.1371/journal.pone.0029419.

  • Castellana, S., Vicario, S. and Saccone, C., Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein-coding genes. Genome Biol. Evol., 2011, 3, 1067–1079; https://doi.org/10.1093/gbe/evr040.

  • Wang, Y., Chen, J., Jiang, L. Y. and Qiao, G. X., Hemipteran mitochondrial genomes: features, structures and implications for phylogeny. Int. J. Mol. Sci., 2015, 16(6), 12382–12404; https://doi.org/10.3390/ijms160612382.

  • Zhao, L., Wei, J., Zhao, W., Chen, C., Gao, X. and Zhao, Q., The complete mitochondrial genome of Pentatoma rufipes (Hemiptera, Pentatomidae) and its phylogenetic implications. ZooKeys, 2021, 1042, 51; doi:10.3897/zookeys.1042.62302.

  • Johnson, K. P. et al., Phylogenomics and the evolution of hemipteroid insects. Proc. Natl. Acad. Sci. USA, 2018, 115(50), 12775–12780; https://doi.org/10.1073/pnas.1815820115.


Abstract Views: 83

PDF Views: 58




  • Genome Organization and Comparative Evolutionary Mitochondriomics of Rice Earhead Bug Leptocorisa oratoria (Fabricius)

Abstract Views: 83  |  PDF Views: 58

Authors

Guru-Pirasanna-Pandi Govindharaj
ICAR-National Rice Research Institute, Cuttack 753 006, India
M. Annamalai
ICAR-National Rice Research Institute, Cuttack 753 006, India
Jaipal Singh Choudhary
ICAR-Research Complex for the Eastern Region, Farming System Research Centre for Hill and Plateau Region, Ranchi 834 010, India
G. Basana-Gowda
ICAR-National Rice Research Institute, Cuttack 753 006, India
Totan Adak
ICAR-National Rice Research Institute, Cuttack 753 006, India
Naiyar Naaz
ICAR-Research Complex for the Eastern Region, Farming System Research Centre for Hill and Plateau Region, Ranchi 834 010, India
Naveenkumar Patil
ICAR-National Rice Research Institute, Cuttack 753 006, India
Enrico Ruzzier
World Biodiversity Association Onlus, C/o Museo Civico di Storia Naturale, Lungadige Porta Vittoria 9, 37129 Verona, Italy
Prakash Chandra Rath
ICAR-National Rice Research Institute, Cuttack 753 006, India

Abstract


The rice earhead bug, Leptocorisa oratoria (Fabricius, 1794) is a critical rice pest in India. No mitochondrial genome of L. oratoria has been sequenced earlier, and the mitochondrial data are crucial for phylogenetic and population genetic studies of this significant rice pest. In the present study, the genome of L. oratoria is 17,584 bp long with 73.57% AT content. We observed tandem repeat in the control region. Analyses from genetic distance, sliding window and Ka/Ks ratio revealed a purifying selection of 13 protein-coding genes, with cox1 and nad2 reporting the lowest and highest rate of evolution respectively. Phylogenetic analysis was reconstructed using 65 pentatomid mitogenomes with Bayesian inference and maximum likelihood methods. The results help differentiate the Coreoidea superfamily from Lygaeoidea, Aradoidea and Pentatomoidea. There were two topologies at the family level, i.e. one clade formed with Coreidae + Rhopalidae + Alydidae, and the rest of the families of Pentatomomorpha for­med in separate clades. Further, L. oratoria produced an independent subclade from the earlier reported Leptocorisa sp. genome. This study provides a source mitogenome for L. oratoria species to study population demography, individual differences and phylogeography of hemipterans.

Keywords


Mitogenome, Next Generation Sequencing, Population Genetics, Phylogeny, Rice Earhead Bug.

References





DOI: https://doi.org/10.18520/cs%2Fv125%2Fi4%2F407-415