Characterization of Transcriptional Responses to Different Aphid Species Reveals Genes that Contribute to Host Susceptibility and Non-host Resistance
Aphids are phloem-feeding insects that cause feeding damage and transmit plant viruses to many crops. While most aphid species are restricted to one or few host plants, some aphids can infest a wide range of plant species. These insects spend a considerable time on non-hosts, where they probe the leaf tissue and secrete saliva, but for unknown reasons are unable to ingest phloem sap. This suggests that aphids interact with non-host plants at the molecular level, but potentially do not suppress plant defences and/or promote the release of nutrients. We compared gene expression of plants during host and non-host interactions with aphids to identify genes involved in immunity. We found significant overlap in the plant responses to aphids regardless of the type of interaction. Despite this, we identified a set of genes specifically affected during host or non-host interactions with specific aphid species. In addition, we showed that several of these genes contribute to host and/or non-host immunity. These findings are important, as they advance our understanding of the plant cellular processes involved in host and non-host responses against insect pests. Understanding mechanisms of host and non-host resistance to plant parasites is essential for development of novel control strategies.
Vyšlo v časopise:
Characterization of Transcriptional Responses to Different Aphid Species Reveals Genes that Contribute to Host Susceptibility and Non-host Resistance. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004918
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004918
Souhrn
Aphids are phloem-feeding insects that cause feeding damage and transmit plant viruses to many crops. While most aphid species are restricted to one or few host plants, some aphids can infest a wide range of plant species. These insects spend a considerable time on non-hosts, where they probe the leaf tissue and secrete saliva, but for unknown reasons are unable to ingest phloem sap. This suggests that aphids interact with non-host plants at the molecular level, but potentially do not suppress plant defences and/or promote the release of nutrients. We compared gene expression of plants during host and non-host interactions with aphids to identify genes involved in immunity. We found significant overlap in the plant responses to aphids regardless of the type of interaction. Despite this, we identified a set of genes specifically affected during host or non-host interactions with specific aphid species. In addition, we showed that several of these genes contribute to host and/or non-host immunity. These findings are important, as they advance our understanding of the plant cellular processes involved in host and non-host responses against insect pests. Understanding mechanisms of host and non-host resistance to plant parasites is essential for development of novel control strategies.
Zdroje
1. Blackman R, Eastop V (2000) Aphids on the world crops. Chichester: Wiley & Sons. 466 p.
2. Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51: 309–330. 16332214
3. Kennedy JS, Booth CO, Kershaw WJS (1959) Host finding by aphids in the field: Aphis fabae scop. (gynoparae) and Brevicoryne brassicae L.; with a re-appraisal of the role of host-finding behaviour in virus spread. Ann Appl Biol 47: 424–444.
4. Alvarez AE, Garzo E, Verbeek M, Vosman B, Dicke M, et al. (2007) Infection of potato plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae. Entomol Exp Appl 125: 135–144.
5. McLean DL (1971) Probing behavior of the pea aphid, Acyrthosiphon pisum. V. comparison of Vicia faba, Pisum sativum, and a chemically defined diet as food sources. Ann Entomol Soc Am 64: 499–503.
6. Troncoso AJ, Vargas RR, Tapia DH, Olivares-Donoso R, Niemeyer HM (2005) Host selection by the generalist aphid Myzus persicae (Hemiptera: Aphididae) and its subspecies specialized on tobacco, after being reared on the same host. Bull Entomol Res 95: 23–28. 15705211
7. Louis J, Shah J (2013) Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Front Plant Sci 4: 213. doi: 10.3389/fpls.2013.00213 23847627
8. Pegadaraju V, Louis J, Singh V, Reese JC, Bautor J, et al. (2007) Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. Plant J 52: 332–341. 17725549
9. Louis J, Leung Q, Pegadaraju V, Reese J, Shah J (2010) PAD4-dependent antibiosis contributes to the ssi2-conferred hyper-resistance to the green peach aphid. MPMI 23: 618–627. doi: 10.1094/MPMI-23-5-0618 20367470
10. Kettles GJ, Drurey C, Schoonbeek H-j, Maule AJ, Hogenhout SA (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198: 1178–1190. doi: 10.1111/nph.12218 23528052
11. Kim JH, Lee BW, Schroeder FC, Jander G (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54: 1015–1026. doi: 10.1111/j.1365-313X.2008.03476.x 18346197
12. Prince DC, Drurey C, Zipfel C, Hogenhout SA (2014) The leucine-rich repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the cytochrome P450 PHYTOALEXIN DEFICIENT3 contribute to innate immunity to aphids in Arabidopsis. Plant Physiol 164: 2207–2219. doi: 10.1104/pp.114.235598 24586042
13. Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. MPMI 27: 747–756. doi: 10.1094/MPMI-01-14-0018-R 24654979
14. Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I (2014) GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc Natl Acad Sci U S A 111: 8919–8924. doi: 10.1073/pnas.1407687111 24927572
15. Dogimont C, Bendahmane A, Chovelon V, Boissot N (2010) Host plant resistance to aphids in cultivated crops: genetic and molecular bases, and interactions with aphid populations. C R Biol 333: 566–573. doi: 10.1016/j.crvi.2010.04.003 20541167
16. Moloi MJ, van der Westhuizen AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol 163: 1118–1125. 17032617
17. Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, et al. (2008) Towards global understanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31: 1097–1115. doi: 10.1111/j.1365-3040.2008.01823.x 18433442
18. Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant Cell Environ 35: 430–440. doi: 10.1111/j.1365-3040.2011.02395.x 21736590
19. Mai VC, Bednarski W, Borowiak-Sobkowiak B, Wilkaniec B, Samardakiewicz S, et al. (2013) Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisum infestation. Phytochem 93: 49–62. doi: 10.1016/j.phytochem.2013.02.011 23566717
20. Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99: 517–522. 11756663
21. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, et al. (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2. ra45 doi: 10.1126/scisignal.2000448 19690331
22. Stam R, Mantelin S, McLellan H, Thilliez G (2014) The role of effectors in nonhost resistance to filamentous plant pathogens. Front Plant Sci 5: 582. doi: 10.3389/fpls.2014.00582 25426123
23. Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16: 117–125. doi: 10.1016/j.tplants.2011.01.001 21317020
24. Balciunas JK, Burrows DW, Purcell MF (1994) Field and laboratory host ranges of the Australian weevil, Oxyops vitiosa, a potential biological control agent of the paperbark tree, Melaleuca quinquenervia. Biol Control 4: 351–360.
25. Pratt C, Pope T, Powell G, Rossiter J (2008) Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two coccinellid species. J Chem Ecol 34: 323–329. doi: 10.1007/s10886-007-9421-z 18270780
26. Louda SM, Rand TA, Russell FL, Arnett AE (2005) Assessment of ecological risks in weed biocontrol: Input from retrospective ecological analyses. Biol Control 35: 253–264. 15881011
27. Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, et al. (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459: 1136–1140. doi: 10.1038/nature08066 19506555
28. Chen Y, Aung K, Rolčík J, Walicki K, Friml J, et al. (2014) Inter-regulation of the unfolded protein response and auxin signaling. Plant J 77: 97–107. doi: 10.1111/tpj.12373 24180465
29. Kanter U, Usadel B, Guerineau F, Li Y, Pauly M, et al. (2005) The inositol oxygenase gene family of Arabidopsis is involved in the biosynthesis of nucleotide sugar precursors for cell-wall matrix polysaccharides. Planta 221: 243–254. 15660207
30. Siddique S, Endres S, Atkins JM, Szakasits D, Wieczorek K, et al. (2009) Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytol 184: 457–472. doi: 10.1111/j.1469-8137.2009.02981.x 19691674
31. Endres S, Tenhaken R (2011) Down-regulation of the myo-inositol oxygenase gene family has no effect on cell wall composition in Arabidopsis. Planta 234: 157–169. doi: 10.1007/s00425-011-1394-z 21394467
32. Siddique S, Endres S, Sobczak M, Radakovic ZS, Fragner L, et al. (2014) Myo-inositol oxygenase is important for the removal of excess myo-inositol from syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytol 201: 476–485.
33. Berger S, Bell E, Sadka A, Mullet JE (1995) Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol Biol 27: 933–942. 7766883
34. Liu Y, Ahn J- E, Datta S, Salzman RA, Moon J, et al. (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol 139: 1545–1556. 16258019
35. Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13: 1025–1034. 11340179
36. Hundertmark M, Hincha DK (2008) LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9: 118. doi: 10.1186/1471-2164-9-118 18318901
37. Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis thaliana. Plant Physiol 154: 373–390. doi: 10.1104/pp.110.158964 20668063
38. Battaglia M, Covarrubias AA (2013) Late Embryogenesis Abundant (LEA) proteins in legumes. Front Plant Sci 4: 190. doi: 10.3389/fpls.2013.00190 23805145
39. Dang NX, Popova AV, Hundertmark M, Hincha DK (2014) Functional characterization of selected LEA proteins from Arabidopsis thaliana in yeast and in vitro. Planta 240: 325–336. doi: 10.1007/s00425-014-2089-z 24841476
40. Liu Y, Wang L, Xing X, Sun L, Pan J, et al. (2013) ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 54: 944–959. doi: 10.1093/pcp/pct047 23543751
41. Salleh FM, Evans K, Goodall B, Machin H, Mowla SB, et al. (2012) A novel function for a redox-related LEA protein (SAG21/AtLEA5) in root development and biotic stress responses. Plant Cell Environ 35: 418–429. doi: 10.1111/j.1365-3040.2011.02394.x 21736589
42. Mowla SB, Cuypers A, Driscoll SP, Kiddle G, Thomson J, et al. (2006) Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant (LEA)-like protein in oxidative stress tolerance. Plant J 48: 743–756. 17092320
43. Knepper C, Savory EA, Day B (2011) Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion1. Plant Physiol 156: 286–300. doi: 10.1104/pp.110.169656 21398259
44. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251–275. 15012264
45. Shapiro AD, Zhang C (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol 127: 1089–1101. 11706189
46. Maffei ME, Mithöfer A, Boland W (2007) Insects feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochem 68: 2946–2959. 17825328
47. Chaouch S, Queval G, Noctor G (2012) AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant J 69: 613–627. doi: 10.1111/j.1365-313X.2011.04816.x 21985584
48. de Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis-aphid interactions. Bioessays 29: 871–883. 17691101
49. Kerchev P, Karpińska B, Morris J, Hussain A, Verrall S, et al. (2013) Vitamin C and the abscisic acid-insensitive 4 transcription factor are important determinants of aphid resistance in Arabidopsis. Antioxid Redox Signal 18: 2091–2105. doi: 10.1089/ars.2012.5097 23343093
50. Macedo TB, Higley LG, Ni X, Quisenberry SS (2003) Light activation of Russian wheat aphid-elicited physiological responses in susceptible wheat. J Econ Entomol 96: 194–201. 12650362
51. Velez-Ramirez AI, van Ieperen W, Vreugdenhil D, Millenaar FF (2011) Plants under continuous light. Trends Plant Sci 16: 310–318. doi: 10.1016/j.tplants.2011.02.003 21396878
52. L'Haridon F, Besson-Bard A, Binda M, Serrano M, Abou-Mansour E, et al. (2011) A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. PLoS Pathog 7: e1002148. doi: 10.1371/journal.ppat.1002148 21829351
53. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, et al. (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180–1183. 16293760
54. Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, et al. (2010) VirtualPlant: A software platform to support systems biology research. Plant Physiol 152: 500–515. doi: 10.1104/pp.109.147025 20007449
55. Mewes HW, Frishman D, Güldener U, Mannhaupt G, Mayer K, et al. (2002) MIPS: a database for genomes and protein sequences. Nucleic Acids Res 30: 31–34. 11752246
56. Takemoto D, Jones DA, Hardham AR (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33: 775–792. 12609049
57. Jaouannet M, Morris JA, Hedley PE, Bos JIB. Data from: Characterization of Arabidopsis transcriptional responses to different aphid species reveals genes that contribute to host susceptibility and non-host resistance. Dryad Digital Repository. doi: 10.5061/dryad.18b29
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 5
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Human Cytomegalovirus miR-UL112-3p Targets TLR2 and Modulates the TLR2/IRAK1/NFκB Signaling Pathway
- Paradoxical Immune Responses in Non-HIV Cryptococcal Meningitis
- Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance
- Fob1 and Fob2 Proteins Are Virulence Determinants of via Facilitating Iron Uptake from Ferrioxamine