Abstract
A recent electrical penetration graph (EPG) study identified a unique intracellular puncture that is associated with inoculation of the semipersistently transmitted, phloem-limited Beet yellows virus (BYV, Closterovirus) by the aphid Myzus persicae. This new aphid EPG pattern (named phloem-pd) always occurs shortly before phloem sieve element phase (PSEP) and has a similar voltage drop as PSEP, both of which are less than the voltage drop of standard-pds. Structure of pd subphase II-2 differs between phloem-pds and standard-pds. The objective of this study was to determine the type of phloem cell penetrated during phloem-pds. Stylets of M. persicae feeding on sugar beet (Beta vulgaris) were fixed in situ by cryofixation during phloem-pds, standard-pds and PSEP waveform E1. The cell penetrated by the stylet tips was then identified by confocal laser-scanning microscopy and micro-computed tomography. Sieve elements (SEs) or companion cells (CCs) were penetrated during phloem-pds, whereas cells other than SEs or CCs (mesophyll, bundle sheath cells and possibly phloem parenchyma) were penetrated during standard-pds. SEs were penetrated during waveform E1. The implications of these findings for inoculation of other phloem-limited viruses that currently are thought to be inoculated primarily during waveform E1 are discussed.
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Alba-Tercedor J, Hunter WB (2014) From the sample preparation to the volume rendering images of small animals: A step by step example of a procedure to carry out the micro-CT study of the leafhopper insect Homalodisca vitripennis (Hemiptera: Cicadellidae). In: BrukermicroCT (ed) Bruker Micro-CT Users Meeting, Kontich, Belgium, pp 260–288 (ISBN: 9789081678100; ISSN: 2033-8031)
Brady J (1965) A simple technique for making very fine, durable dissecting needles by sharpening tungsten wire electrolytically. Bull World Health Organ 32(1):143–144
Chen JQ, Martin 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 103:521–536. https://doi.org/10.1023/A:1008610812437
Chen AYS, Walker GP, Carter D, Ng JCK (2011) A virus capsid component mediates virion retention and transmission by its insect vector. PNAS 108:16777–16782. https://doi.org/10.1073/pnas.1109384108
Cornara D, Garzo E, Morente M, Moreno M, Alba-Tercedor J, Fereres A (2018) EPG combined with micro-CT and video recording reveals new insights on the feeding behavior of Philaenus spumarius. PLoS ONE. https://doi.org/10.1371/journal.pone.0199154
IBM Corp (2017) Released 2017. IBM SPSS Statistics for Macintosh, Version 25.0. Armonk, NY: IBM Corp
Esau K (1969) Viruses in plant hosts: form, distribution, and pathologic effects. Science 165(3888):53–54. https://doi.org/10.1126/science.165.3888.53-a
Fereres A (2016) Aphid behavior and the transmission of noncirculative viruses. In: Brown JK (ed) Vector-mediated transmission of plant pathogens. APS Press, St. Paul, pp 31–45
Fereres A, Raccah B (2015) Plant Virus transmission by insects. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0000760.pub3
Gamalei Y (1989) Structure and function of leaf minor and veins in trees and herbs. A taxonomic review. Trees 3:96–110. https://doi.org/10.1007/BF01021073
Garzo E, Fernández-Pascual M, Morcillo C, Fereres A, Gómez-Guillamón 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. https://doi.org/10.1111/1744-7917.12447
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. https://doi.org/10.1104/pp.104.05851
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. https://doi.org/10.3389/fpls.2013.00274
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. https://doi.org/10.1016/B978-012327681-0/50009-1
Haugland RP (2005) The handbook. A guide to fluorescent probes and labeling technologies, 10th edn. Invitrogen Corporation, Carlsbad, p 1126
Hogenhout S, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359. https://doi.org/10.1146/annurev.phyto.022508.092135
Jiang YX, de Blas C, Barrios L, Fereres A (2000) Correlation between whitefly (Homoptera: Aleyrodidae) feeding behavior and transmission of Tomato yellow leaf curl virus. Ann Entomol Soc Am 93:573–579. https://doi.org/10.1603/0013-8746(2000)093%5b0573:CBWHAF%5d2.0.CO;2
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. https://doi.org/10.1128/JVI.01076-18
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 102:115–123. https://doi.org/10.1046/j.1570-7458.2002.00931.x
López-Abella D, Bradley RHE, Harris KF (1988) Correlation between stylet paths made during superficial probing and the ability of aphids to transmit nonpersistent viruses. In: Harris KF (ed) Advances in disease vector research. Praeger Publishers, New York, pp 251–285
Maluta NKP, Garzo E, Moreno A, Navas-Castillo J, Fiallo-Olivé E, Spotti J, Fereres A (2017) Stylet penetration activities of the whitefly Bemisia tabaci associated with inoculation of the crinivirus Tomato chlorosis virus. J Gen Virol 98(6):1515–1520. https://doi.org/10.1099/jgv.0.000783
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 78:2701–2705. https://doi.org/10.1099/0022-1317-78-10-2701
Medina-Ortega KJ, Walker GP (2015) Faba bean forisomes can function in defence against generalist aphids. Plant, Cell Environ 38:1167–1177. https://doi.org/10.1111/pce.12470
Moreno A, Garzo E, Fernandez-Mata G, Kassem M, Aranda MA, Fereres A (2011) Aphids secrete watery saliva into plant tissues from the onset of stylet penetration. Entomol Exp Appl 139(2):145–153. https://doi.org/10.1111/j.1570-7458.2011.01117.x
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 93:662–667. https://doi.org/10.1099/vir.0.037887-0
Ng JCK, Zhou JS (2015) Insect vector-plant virus interactions associated with non-circulative, semi-persistent transmission: current perspectives and future challenges. Curr Opin Virol 15:48–55. https://doi.org/10.1016/j.coviro.2015.07.006
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. https://doi.org/10.1099/0022-1317-83-12-3163
Peng HC, Walker GP (2018) Sieve element occlusion provides resistance against Aphis gossypii in TGR-1551 melons. Insect Sci. https://doi.org/10.1111/1744-7917.12610
Powell G (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. J Gen Virol 86(2):469–472. https://doi.org/10.1099/vir.0.80632-0
Powell G, Pirone T, Hardie J (1995) Aphid stylet activities during Potyvirus acquisition from plants and an in vitro system that correlates with subsequent transmission. Eur J Plant Pathol 101:411–420. https://doi.org/10.1007/BF01874855
Prado E, Tjallingii WF (1994) Aphid activities during sieve element punctures. Entomol Exp Appl 72:157–165. https://doi.org/10.1111/j.1570-7458.1994.tb01813.x
Price WC (1966) Flexuous rods in phloem cells of lime plants infected with Citrus Tristeza Virus. Virol 29:285–294. https://doi.org/10.1016/0042-6822(66)90035-3
Scheller HV, Shukle RH (1986) Feeding behavior and transmission of Barley yellow dwarf virus by Sitobion avenae on oats. Entomol Exp Appl 40:189–195. https://doi.org/10.1007/BF00349215
Sylvester ES (1956) Beet yellows virus transmission by the green peach aphid. J Econ Entomol 49:789–800
Tjallingii WF (1978) Electronic recording of penetration behavior by aphids. Entomol Exp Appl 24:521–530. https://doi.org/10.1111/j.1570-7458.1978.tb02836.x
Tjallingii WF (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomol Exp Appl 38:177–186. https://doi.org/10.1111/j.1570-7458.1985.tb03516.x
Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57(4):739–745. https://doi.org/10.1093/jxb/erj088
Tjallingii WF, Gabrys B (1999) Anomalous stylet punctures of phloem sieve elements by aphids. Physiol Entomol 91:97–103. https://doi.org/10.1046/j.1570-7458.1999.00470.x
Tjallingii WF, Hogen Esch TH (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18:317–328. https://doi.org/10.1111/j.1365-3032.1993.tb00604.x
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 2:2. https://doi.org/10.1073/pnas.0706608104
van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant, Cell Environ 26(1):125–149. https://doi.org/10.1046/j.1365-3040.2003.00963.x
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. https://doi.org/10.1007/978-3-642-60458-4_11
van Bel AJE, van Rijen HVM (1993) Microelectrode-recorded development of the symplastic autonomy of the sieve elements/companion cell complex in the stem phloem of Lupinus luteus L. Planta 192:165–175. https://doi.org/10.1007/BF00194449
van Helden M, Tjallingii WF (2000) Experimental design and analysis in EPG experiments with emphasis on plant resistance research. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behaviour. Thomas Say Publications, Lanham, MD, pp 144–171
Walker GP, Medina-Ortega KJ (2012) Penetration of faba bean sieve elements by pea aphid does not trigger forisome dispersal. Entomol Exp Appl 144:326–335. https://doi.org/10.1111/j.1570-7458.2012.01297.x
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 125:144–170. https://doi.org/10.1098/rspb.1938.0018
Acknowledgements
Authors especially thank James Ng lab for providing material and for their advice during the development of the experiments. Authors also thank Maria del Carmen Risueño Almeida (Biological Research Center, CIB—Madrid, Spain) and David Carter (Center for Plant Cell Biology, UCR) for their contribution to the analysis of the CLSM images. Special thanks to the staff at Bruker-micro-CT for their support, patience and effectiveness, and for their constant improvements to the software, including new options that we requested. This paper benefitted from sub-award agreement S15192.01 between Kansas State University (KSU) and the University of Granada, as part of the USDA-NIFA award 2014-70016-23028 to Susan J. Brown (KSU). This work was funded by the project AGL2013-47603-C2-2-R from the Spanish Ministry of Economy, Industry and Competitiveness (fellowship BES-2014-067806). The present manuscript is part of Jaime Jiménez PhD Thesis at Universidad Politécnica de Madrid.
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Supplementary material 1—For micro-CT scanning, samples were glued with cyanocrilate to the tip of a 200 µm diameter nylon fishing line (3) (A, B, C), inserted in a piece of plasticine (4) at the end of the sample holder (5) (A, D) and protected with a plastic straw tube (6) to prevent possible movements in the scanning process due to the cooling process by ventilation (E) (in A, arrows point to the gold-wire (2) glued with silver paint to the dorsum of the aphid (1) used to monitor the aphid feeding behavior by electrical penetration graphs (EPG) technique) (PDF 1107 kb)
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Jiménez, J., Garzo, E., Alba-Tercedor, J. et al. The phloem-pd: a distinctive brief sieve element stylet puncture prior to sieve element phase of aphid feeding behavior. Arthropod-Plant Interactions 14, 67–78 (2020). https://doi.org/10.1007/s11829-019-09708-w
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DOI: https://doi.org/10.1007/s11829-019-09708-w