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Transmission of Phloem-Limited Viruses to the Host Plants by Their Aphid Vectors

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Progress in Botany Vol. 82

Part of the book series: Progress in Botany ((BOTANY,volume 82))

Abstract

Plant viruses produce important economic losses in crops worldwide. The study of their transmission by insects has been key in order to develop new strategies to interfere with their spread. Studies on the monitoring of aphid probing behavior by using the electrical penetration graph (EPG) technique allowed to study the different aphid stylet activities in plant tissues associated with the transmission of plant viruses. Aphids produce intermittent intracellular punctures (commonly named as “potential drops”: pds) along the stylet pathway, ultimately reaching the phloem tissues. The phloem-pd has been recently described as the key stylet activity in plant cells associated with the transmission of phloem-limited viruses by aphids. This behavioral pattern represents the first report of a brief intracellular puncture produced by aphids in phloem tissues associated to the transmission of a phloem-limited virus. A single brief phloem-pd (3–5 s) was mandatory to transmit both semipersistently and persistently transmitted, phloem-limited viruses by aphids. Stylet penetration of both sieve elements and companion cells of the host plant during the occurrence of the phloem-pd by M. persicae were confirmed by using confocal laser-scanning microscopy together with CT-microtomography. In this chapter, we revisit the main approaches recently carried out in the field of aphid probing and feeding behavior in association with the transmission of phloem-limited viruses transmitted in either a semipersistent or persistent manner.

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References

  • Agranovsky AA, Koonin EV, Boyko VP, Maiss E, Frötschl R, Lunina NA, Atabekov JG (1994) Beet yellows closterovirus: complete genome structure and identification of a leader papain-like thiol protease. Virology 198(1):311–324

    CAS  PubMed  Google Scholar 

  • Almeida RPP, Backus EA (2004) Stylet penetration behaviors of Graphocephala atropunctata (Signoret) (Hemiptera, Cicadellidae): EPG waveform characterization and quantification. Ann Entomol Soc Am 97(4):838–851

    Google Scholar 

  • Bendix C, Lewis JD (2018) The enemy within: phloem-limited pathogens. Mol Plant Pathol 19(1):238–254

    CAS  PubMed  Google Scholar 

  • Bennett CW (1960) Sugar beet yellows disease in the United States. In: USDA technical bulletin no. 1218. Agricultural Research Service. U.S. Department of Agriculture, Washington, DC, pp 1–63

    Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, New York

    Google Scholar 

  • Blanc S, Drucker M, Uzest M (2014) Localizing viruses in their aphid vectors. Annu Rev Phytopathol 52:403–425

    CAS  PubMed  Google Scholar 

  • Campolo O, Chiera E, Malacrinò A, Laudani F, Fontana A, Albanese GR, Palmeri V (2014) Acquisition and transmission of selected CTV isolates by Aphis gossypii. J Asia Pac Entomol 17(3):493–498

    Google Scholar 

  • Carmo-Sousa M, Moreno A, Plaza M, Garzo E, Fereres A (2016) Cucurbit aphid-borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Ann Appl Biol 169(2):284–297

    CAS  Google Scholar 

  • Chen B, Francki RIB (1990) Cucumovirus transmission by the aphid Myzus persicae is determined solely by the viral coat protein. J Gen Virol 71:939–944

    CAS  Google Scholar 

  • Chen JQ, Martín B, Rahbé Y, Fereres A (1997) Early intracellular punctures by two aphid species on near-isogenic melon lines with and without the virus aphid transmission (Vat) resistance gene. Eur J Plant Pathol 103(6):521–536

    Google Scholar 

  • Chen AYS, Walker GP, Carter D, Ng JCK (2011) A virus capsid protein component mediates virion and transmission by its insect vector. Proc Natl Acad Sci U S A 108(40):16777–16782

    PubMed  PubMed Central  Google Scholar 

  • Collar JL, Avilla C, Fereres A (1997) New correlations between aphid stylet paths and nonpersistent virus transmission. Environ Entomol 26(3):537–544

    Google Scholar 

  • Cornara D, Marra M, Morente M, Garzo E, Moreno A, Saponari M, Fereres A (2020) Feeding behaviour in relation to spittlebug of Xylella fastidiosa. J Pest Sci. https://doi.org/10.1007/s10340-020-01236-4

  • D’Arcy CJ (1995) Symptomology and host range of barley yellow dwarf. In: D’Arcy DJ, Burnett PA (eds) Barley yellow dwarf: 40 years of progress. APS, St Paul, pp 9–28

    Google Scholar 

  • Drucker M, Froissart B, Hebrard E, Uzest M, Ravallee M, Esperandieu P, Mani JC, Pugniere M, Roquet F, Fereres A, Blanc S (2002) Intracellular distribution of viral gene products regulates a complex mechanism of Cauliflower mosaic virus acquisition by its aphid vector. Proc Natl Acad Sci U S A 99(4):2422–2427

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esau K (1957) Phloem degeneration in Gramineae affected by the barley yellow-dwarf virus. Am J Bot 44:245–251

    Google Scholar 

  • Esau K (1960) Cytologic and histologic symptoms of beet yellows. Virology 10(1):73–85

    CAS  PubMed  Google Scholar 

  • Esau K (1968) Viruses in plant hosts: form, distribution, and pathologic effects. University of Wisconsin Press, Madison

    Google Scholar 

  • Evert RF, Russin WA, Botha CEJ (1996) Distribution and frequency of plasmodesmata in relation to photoassimilate pathway and phloem loading in the barley leaf. Planta 198:572–579

    CAS  PubMed  Google Scholar 

  • Fereres A (2016) Aphid behavior and the transmission of noncirculative viruses. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. APS, St Paul, pp 31–45

    Google Scholar 

  • Fereres A, Moreno A (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141(2):158–168

    CAS  PubMed  Google Scholar 

  • Fereres A, Raccah B (2015) Plant virus transmission by insects. In: eLS. Wiley, Chichester

    Google Scholar 

  • Field LM, Bass C, Davies TG, Williamson MS, Zhou JJ (2018) Aphid genomics and its contribution to understanding aphids as crop pests. In: van Emden HF, Harrington R (eds) Aphids as crop pests, 2nd edn. CAB International, Wallingford, pp 37–49

    Google Scholar 

  • Foster SP, Paul VL, Slater R, Warren A, Denholm I, Field LM, Williamson MS (2014) A mutation (L1014F) in the voltage-gated sodium channel of the grain aphid, Sitobion avenae, is associated with resistance to pyrethroid insecticides. Pest Manag Sci 70(8):1249–1253

    CAS  PubMed  Google Scholar 

  • Gamalei Y (1989) Structure and function of leaf minor and veins in trees and herbs. A taxonomic review. Trees 3(2):96–110

    Google Scholar 

  • Garret A, Kerlan C, Thomas D (1996) Ultrastructural study of acquisition and retention of potato leafroll luteovirus in the alimentary canal of its aphid vector, Myzus persicae Sulz. Arch Virol 141:1279–1292

    CAS  PubMed  Google Scholar 

  • Garzo E, Fernández-Pascual M, Morcillo C, Fereres A, Gómez-Guillamón ML, Tjallingii WF (2018) Ultrastructure of compatible and incompatible interactions in phloem sieve elements during the stylet penetration by cotton aphids in melon. Int J Insect Sci 25(4):631–642

    CAS  Google Scholar 

  • Gera A, Loebenstein G, Raccah B (1979) Protein coats of two strains of Cucumber mosaic virus affect transmission by Aphis gossypii. Phytopathology 69(4):396–399

    CAS  Google Scholar 

  • Gildow FE (1990) Current status of barley yellow dwarf in the United States: a regional report. In: Burnet PA (ed) World perspectives on barley yellow dwarf. CIMMYT, Mexico, pp 11–20

    Google Scholar 

  • Gildow FE (1999) Luteovirus transmission and mechanisms regulation vector specificity. In: Smith HG, Barker H (eds) The luteoviridae. CAB International, Oxon, pp 88–112

    Google Scholar 

  • Gildow FE, Gray SM (1993) The aphid salivary gland basal lamina as a selective barrier associated with vector-specific transmission of Barley yellow dwarf virus. Phytopathology 83:1293–1302

    Google Scholar 

  • Godfrey LD, Mauk PA (1993) Interactive effects of aphid injury and Beet yellows virus on sugar beet photosynthesis and yield (Abstr.). J Sugar Beet Res 30:95

    Google Scholar 

  • Gray SM, Gildow FE (2003) Luteovirus-aphid interactions. Annu Rev Phytopathol 41:539–566

    CAS  PubMed  Google Scholar 

  • Hafke JB, van Amerongen JK, Kelling F, Furch ACU, Gaupels F, van Bel AJE (2005) Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol 138:1527–1537

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hafke JB, Höll SB, Kühn C, van Bel AJE (2013) Electrophysiological approach to determine kinetic parameters of sucrose uptake by single sieve elements or phloem parenchyma cells in intact Vicia faba plants. Front Plant Sci 4:274

    PubMed  PubMed Central  Google Scholar 

  • Halbert SC, Voegtlin D (1995) Biology and taxonomy of vectors of barley yellow dwarf viruses. In: D’Arcy CL, Burnett PA (eds) Barley yellow dwarf: 40 years of progress. APS, St Paul, pp 217–258

    Google Scholar 

  • Hardie J (2018) Life cycles and polyphenism. In: van Emden HF, Harrington R (eds) Aphids as crop pests, 2nd edn. CABI, Wallingford, pp 81–97

    Google Scholar 

  • Harris KF, Harris LJ (2001) Ingestion-egestion theory of cuticula-borne virus transmission. In: Harris KF, Smith OP, Duffus JE (eds) Virus-insect-plant interactions. Academic Press, New York, pp 111–132

    Google Scholar 

  • Heathcote GD, Cockbain AJ (1964) Transmission of Beet yellows virus by alatae and apterous aphids. Ann Appl Biol 53(2):259–266

    Google Scholar 

  • Hodges LR, McLean DL (1969) Correlation of transmission of bean yellow mosaic virus with salivation activity of Acrythosiphon pisum (Homoptera: Aphididae). Ann Entomol Soc Am 62:1398–1401

    CAS  PubMed  Google Scholar 

  • Hogenhout S, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359

    CAS  PubMed  Google Scholar 

  • Ingwell LL, Bosque-Pérez NA (2015) The invasive weed Ventenata dubia is a host of barley yellow dwarf virus with implications for an endangered grassland habitat. Weed Res 55:62–70

    Google Scholar 

  • Ingwell LL, Zemetra R, Mallory-Smith C, Bosque-Pérez NA (2014) Arundo donax infection with barley yellow dwarf virus has implications for biofuel production and non-managed habitats. Biomass Bioenergy 66:426–433

    Google Scholar 

  • Jiménez J (2019) Non-circulative virus transmission by aphids: new insights into the mechanisms of transmission and the interference for retention sites in the vector. PhD thesis, Polytechnic University of Madrid

    Google Scholar 

  • Jiménez J, Tjallingii WF, Moreno A, Fereres A (2018) Newly distinguished cell punctures associated with transmission of the semipersistent phloem-limited Beet yellows virus. J Virol 92:e01076–e01018

    PubMed  PubMed Central  Google Scholar 

  • Jiménez J, Arias-Martín M, Moreno A, Garzo E, Fereres A (2020a) Barley yellow dwarf virus can be inoculated during brief intracellular punctures in phloem cells before the sieve element continuous salivation phase. Phytopathology 110(1):85–93

    PubMed  Google Scholar 

  • Jiménez J, Garzo E, Alba-Tercedor J, Moreno A, Fereres A, Walker GP (2020b) The phloem-pd: a distinctive brief sieve element stylet puncture prior to sieve element phase of aphid feeding behavior. Arthropod Plant Interact 14:67–78

    Google Scholar 

  • Johnson DD, Walker GP, Creamer R (2002) Stylet penetration behavior resulting in inoculation of a semipersistently transmitted closterovirus by the whitefly Bemisia argentifolii. Entomol Exp Appl 102(2):115–123

    Google Scholar 

  • Kennedy JS, Booth CO, Kershaw WJS (1961) Host finding by aphids in the field. Ann Appl Biol 49:1–21

    Google Scholar 

  • Killiny N, Harper SJ, Alfaress S, El Mohtar C, Dawson WO (2016) Minor coat and heat-shock proteins are involved in binding of Citrus tristeza virus to the foregut of its aphid vector, Toxoptera citricida. Appl Environ Microbiol 82(21):6294–6302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk M, Temple SR, Summers CG, Wilson LT (1991) Transmission efficiencies of field-collected aphid (Homoptera: Aphididae) vectors of Beet yellows virus. J Econ Entomol 84(2):638–643

    Google Scholar 

  • Limburg DD, Mauk PA, Godfrey LD (1997) Characteristics of Beet Yellows Closterovirus transmission to sugar beets by Aphis fabae. Phytopathology 87(7):766–771

    CAS  PubMed  Google Scholar 

  • Loxdale HD, Edwards O, Tagu D, Vorburger C (2018) Population genetic issues: new insights using conventional molecular markers. In: van Emden HF, Harrington R (eds) Aphids as crop pests, 2nd edn. CABI, Wallingford, pp 50–80

    Google Scholar 

  • Martín B, Collar JL, Tjallingii WF, Fereres A (1997) Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J Gen Virol 78(10):2701–2705

    PubMed  Google Scholar 

  • Mauck KE, Chesnais Q, Shapiro LR (2018) Evolutionary determinants of host and vector manipulation by plant viruses. Adv Virus Res 101:189–250

    PubMed  Google Scholar 

  • Mauck KE, Kenney J, Chesnais Q (2019) Progress and challenges in identifying molecular mechanisms underlying host and vector manipulation by plant viruses. Curr Opin Insect Sci 33:7–18

    PubMed  Google Scholar 

  • McLean DK, Kinsey MG (1964) A technique for electronically recording aphid feeding and salivation. Nature 202:1358–1359

    Google Scholar 

  • Medina-Ortega KJ, Walker G (2015) Faba bean forisomes can function in defence against generalist aphids. Plant Cell Environ 38(6):1167–1177

    PubMed  Google Scholar 

  • Moreno A, Tjallingii WF, Fernández-Mata G, Fereres A (2012) Differences in the mechanism of inoculation between a semi-persistent and non-persistent aphid-transmitted plant virus. J Gen Virol 93(3):662–667

    CAS  PubMed  Google Scholar 

  • Murant AF, Roberts IM, Elnagar S (1976) Association of virus-like particles with the foregut of the aphid Cavariella aegopodii transmitting the semi-persistent viruses Anthriscus yellows and Parsnip yellow fleck. J Gen Virol 31:47–57

    Google Scholar 

  • Normand RA, Pirone TP (1968) Differential transmission of strains of Cucumber mosaic virus by aphids. Virology 36(4):538–544

    CAS  PubMed  Google Scholar 

  • Oerke EC (2006) Crop losses to pests. J Agric Sci 144(1):31–43

    Google Scholar 

  • Palacios I, Drucker M, Blanc S, Leite S, Moreno A, Fereres A (2002) Cauliflower mosaic virus is preferentially acquired from the phloem by its aphid vectors. J Gen Virol 83:3163–3171

    CAS  PubMed  Google Scholar 

  • Peng HC, Walker GP (2018) Sieve element occlusion provides resistance against Aphis gossypii in TGR-1551 melons. Insect Sci 27(1):33–48

    PubMed  PubMed Central  Google Scholar 

  • Peremyslov VV, Andreev IA, Prokhnevsky AI, Duncan GH, Taliansky ME, Dolja VV (2004) Complex molecular architecture of beet yellows virus particles. PNAS 101(4):5030–5035

    CAS  PubMed  Google Scholar 

  • Pirone TP, Blanc S (1996) Helper-dependent vector transmission of plant viruses. Annu Rev Phytopathol 34(1):227–247

    CAS  PubMed  Google Scholar 

  • Powell G (1991) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Ann Appl Biol 119(2):313–321

    Google Scholar 

  • Powell G (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. J Gen Virol 86(10):469–472

    CAS  PubMed  Google Scholar 

  • Powell G, Pirone T, Hardie J (1995) Aphid stylet activities during potyvirus acquisition from plants and an in vitro system that correlate with subsequent transmission. Eur J Plant Pathol 101(4):411–420

    Google Scholar 

  • Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51(1):309–330

    CAS  PubMed  Google Scholar 

  • Power AG, Seaman AJ, Gray SM (1991) Aphid transmission of Barley yellow dwarf virus: inoculation access periods and epidemiological implications. Phytopathology 81(5):545–548

    Google Scholar 

  • Prado E, Tjallingii WF (1994) Aphid activities during sieve elements punctures. Entomol Exp Appl 72(2):157–165

    Google Scholar 

  • Price WC (1966) Flexuous rods in phloem cells of lime plants infected with Citrus tristeza virus. Virology 29(2):285–294

    CAS  PubMed  Google Scholar 

  • Scheller HV, Shukle RH (1986) Feeding behavior and transmission of Barley yellow dwarf virus by Sitobion avenae on oats. Entomol Exp Appl 40(2):189–195

    Google Scholar 

  • Song Q, Zheng YJ, Xue Y, Sheng WG, Zhao MR (2017) An evolutionary deep neural network for predicting morbidity of gastrointestinal infections by food contamination. Neurocomputing 226:16–22

    Google Scholar 

  • Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43(1):83–116

    CAS  PubMed  Google Scholar 

  • Sylvester ES (1956) Beet yellows virus transmission by the green peach aphid. J Econ Entomol 49(6):789–800

    Google Scholar 

  • Tjallingii WF (1978) Electronic recording of penetration behavior by aphids. Entomol Exp Appl 24(3):721–730

    Google Scholar 

  • Uzest M, Blanc S (2016) Molecular mechanisms involved in noncirculative virus–vector interactions. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. APS, St Paul, pp 59–72

    Google Scholar 

  • Uzest M, Gargani D, Drucker M, Hebrard E, Garzo E, Candresse T, Fereres A, Blanc S (2007) A protein key to plant virus transmission at the tip of the insect vector stylet. PNAS 104(46):17959–17964

    CAS  PubMed  Google Scholar 

  • van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26(1):125–149

    Google Scholar 

  • van Bel AJE, Kempers R (1997) The pore/plasmodesm unit; key element in the interplay between sieve element and companion cell. Prog Bot 58:278–291

    Google Scholar 

  • van Bel AJE, van Rijen HVM (1993) Microelectrode-recorded development of the symplastic autonomy of the sieve elements/companion cells complex in the stem phloem of Lupinus luteus L. Planta 192(2):165–175

    Google Scholar 

  • van Hemden HF (2018) Host-plant resistance. In: van Emden HF, Harrington R (eds) Aphids as crop pests, 2nd edn. CAB International, Wallingford, pp 515–532

    Google Scholar 

  • Visser JH, Piron PGM, Hardie J (1996) The aphid’s peripheral perception of plant volatiles. Entomol Exp Appl 80(1):35–38

    CAS  Google Scholar 

  • Watson MA (1938) Further studies on the relationship between Hyoscyamus virus 3 and the aphid Myzus persicae (Sulz.) with special reference to the effects of fasting. Proc R Soc Lond B 125:144–170

    Google Scholar 

  • Wayadande AC, Nault LR (1993) Leafhopper probing behavior associated with chlorotic dwarf virus transmission. Phytopathology 83:522–526

    Google Scholar 

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Authors and Affiliations

  1. Instituto de Ciencias Agrarias – Consejo Superior de Investigaciones Científicas (ICA-CSIC), Madrid, Spain

    Jaime Jiménez, Aránzazu Moreno & Alberto Fereres

  2. Department of Entomology and Nematology, University of Florida, Gainesville, FL, USA

    Jaime Jiménez

Authors
  1. Jaime Jiménez
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  2. Aránzazu Moreno
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  3. Alberto Fereres
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Correspondence to Jaime Jiménez .

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Editors and Affiliations

  1. Department of Molecular Biology and Biochemistry, University of Málaga, Málaga, Spain

    Francisco M. Cánovas

  2. Department of Biology, Technical University of Darmstadt, Darmstadt, Germany

    Ulrich Lüttge

  3. Pollen Biotechnology of Crop Plants Group, Centro de Investigaciones Biologicas (CIB) CSIC Madrid, Madrid, Spain

    María-Carmen Risueño

  4. Chair for Forest Growth and Yield Science, School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Bayern, Germany

    Hans Pretzsch

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Jiménez, J., Moreno, A., Fereres, A. (2020). Transmission of Phloem-Limited Viruses to the Host Plants by Their Aphid Vectors. In: Cánovas, F.M., Lüttge, U., Risueño, MC., Pretzsch, H. (eds) Progress in Botany Vol. 82. Progress in Botany, vol 82. Springer, Cham. https://doi.org/10.1007/124_2020_47

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