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Research paper | Open Access

Investigation of the mechanism of adult-stage resistance to barley yellow dwarf virus associated with a wheat–Thinopyrum intermedium translocation

Xindong Wanga,b,1, Wei Ronga,1, Yan Liuc,1, Xifeng Wangc, Zengyan Zhanga( )
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Jiangxi Academy of Forestry, Nanchang 330013, Jiangxi, China
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

1 Authors contributed equally to this work.

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

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Abstract

Barley yellow dwarf virus (BYDV) can infect wheat (Triticum aestivum L.), leading to yield loss. Among four BYDV strains (GAV, GPV, PAV, and RMV) identified in China, BYDV-GAV is the prevailing isolate. YW642, a wheat–Thinopyrum intermedium translocation line, is resistant to BYDV isolates at both seedling and adult stages. Zhong 8601 is the wheat recurrent parent of YW642 and is susceptible to BYDV. In this study, we investigated the adult-stage resistance mechanism of YW642, measured BYDV titer and hydrogen peroxide (H2O2) in adult-stage leaves of YW642 and Zhong 8601 inoculated with BYDV-GAV, and identified transcriptional differences between YW642 and Zhong 8601 using microarray-based comparative transcriptomics. Enzyme-linked immunosorbent assay and H2O2 assay showed that both BYDV titer and H2O2 content were markedly lower in YW642 than in Zhong 8601 at 21, 28, 35, and 40days post-inoculation (dpi). The transcriptomic comparison revealed that many types of genes were significantly up-regulated at 35dpi in adult-stage leaves of YW642 compared to Zhong 8601. The important up-regulated genes associated with the adult-stage resistance encoded 15 resistance-like proteins, pathogenesis-related proteins (such as defensin and lipid transfer proteins), protein kinase homologs, transcription factors, reactive oxygen species scavenging-related proteins, and jasmonic acid and gibberellic acid biosynthesis enzymes. These results suggest that precise expression regulation of these proteins plays a crucial role in adult-stage resistance of YW642 against BYDV infection.

Keywords

Reactive oxygen speciesPhytohormoneBarley yellow dwarf virusResistance at adult stageDefense-associated genes

References

[1]

X. Huang, M.S. Röder, Molecular mapping of powdery mildew resistance genes in wheat: a review, Euphytica 137 (2004) 203-223.
Crossref Google Scholar
[2]
C.J. D'Arcy, Symptomology and host range of barley yellow dwarf, in: C.J. D'Arcy, P.A. Burnett (Eds.), Barley Yellow Dwarf: 40 Years of Progress, APS Press, St. Paul, Minnesota, USA 1995, pp. 9–28.
[3]

S.J. McKirdy, R.A.C. Jones, Effect of sowing time on barley yellow dwarf virus infection in wheat: virus incidence and grain yield losses, Aust. J. Agric. Res. 12 (1997) 105-109.
Crossref Google Scholar
[4]

D.A.J. Herbert, E.L. Stromberg, G.F. Chappel, S.M. Malone, Reduction of yield components by barley yellow dwarf infection in susceptible winter wheat and winter barley in Virginia, J. Prod. Agric. 12 (1999) 105-109.
Crossref Google Scholar
[5]

W.E. Riedell, R.W. Kieckhefer, S.D. Haley, M.A.C. Langham, P.D. Evenson, Winter wheat responses to bird cherry-oat aphids and barley yellow dwarf virus infection, Crop Sci. 39 (1999) 158-163.
Crossref Google Scholar
[6]

K.L. Perry, F.L. Kolb, B. Sammons, C. Lawson, G. Cisar, H. Ohm, Yield effects of barley yellow dwarf virus in soft red winter wheat, Phytopathology 90 (2000) 1043-1048.
Crossref Google Scholar
[7]

P.M. Banks, J.L. Davidson, H. Bariana, P.J. Larkin, Effects of barley yellow dwarf virus on the yield of winter wheat, Aust. J. Agric. Res. 46 (1995) 935-946.
Crossref Google Scholar
[8]

W.F. Rochow, Biological properties of four isolates of BYDV, Phytopathology 59 (1969) 1580-1589.
Google Scholar
[9]

W.F. Rochow, Comparative diagnosis of BYDV by serological and aphid transmission test, Plant Dis. Rep. 63 (1979) 426-430.
Google Scholar
[10]

G.H. Zhou, S.X. Zhang, Y.T. Qian, Identification and application of four strains of wheat yellow dwarf virus, Sci. Agric. Sin. 20 (1987) 7-12 (in Chinese with English abstract).
Crossref Google Scholar
[11]

Y. Liu, B. Sun, X.F. Wang, C.L. Zheng, G.H. Zhou, Three digoxigenin-labeled cDNA probes for specific detection of the natural population of barley yellow dwarf viruses in China by dot-blot hybridization, J. Virol. Methods 145 (2007) 22-29.
Crossref Google Scholar
[12]

N. Li, Z. Chen, Y. Liu, Y. Liu, X.P. Zhou, J.X. Wu, Development of monoclonal antibodies and serological assays specific for barley yellow dwarf virus GAV strain, Virol. J. 12 (2015) 136-144.
Crossref Google Scholar
[13]

L. Ayala, M. Van Ginkel, M. Khairallah, B. Keller, M. Henry, Expression of Thinopyrum intermedium-derived barley yellow dwarf virus resistance in elite bread wheat backgrounds, Phytopathology 91 (2001) 55-62.
Crossref Google Scholar
[14]

Z.Y. Zhang, Z.S. Lin, Z.Y. Xin, Research progress in BYDV resistance genes derived from wheat and its wild relatives, J. Genet. Genomics 36 (2009) 567-573.
Crossref Google Scholar
[15]

H. Sharma, B. Gill, J. Uyemoto, High levels of resistance in Agropyron species to barley yellow dwarf and wheat streak mosaic viruses, J. Phytopathol. 110 (1984) 143-147.
Crossref Google Scholar
[16]

Z.Y. Xin, R.I.S. Brettell, Z.M. Cheng, R. Waterhouse, P. Appels, M. Banks, G.H. Zhou, X. Chen, P.J. Larkin, Characterization of a potential source of barley yellow dwarf virus resistance for wheat, Genome 30 (1988) 250-257.
Crossref Google Scholar
[17]

Z.Y. Xin, H.J. Xu, X. Chen, Z.S. Lin, G.H. Zhou, Y.T. Qian, Z.M. Chen, P.J. Larkin, P.M. Banks, R. Apples, B. Clarke, R.I.S. Brettell, Development of common wheat germplasm resistant to barley yellow dwarf virus by biotechnology, Sci. China B 34 (1991) 1055-1062.
Google Scholar
[18]

P.J. Larkin, P.M. Banks, E.S. Lagudah, R. Appels, X. Chen, Z.Y. Xin, H.W. Ohm, R.A. McIntosh, Disomic Thinopyrum intermedium addition lines in wheat with barley yellow dwarf virus resistance and with rust resistances, Genome 38 (1995) 385-394.
Crossref Google Scholar
[19]

H. Sharma, L. Ohm, R. Goulart, R. Lister, R. Appels, O. Benlhabib, Introgression and characterization of barley yellow dwarf virus resistance from Thinopyrum intermedium into wheat, Genome 38 (1995) 406-413.
Crossref Google Scholar
[20]

O.R. Crasta, M.G. Francki, D.B. Bucholtz, H.C. Sharma, J. Zhang, R.C. Wang, H.W. Ohm, J.M. Anderson, Identification and characterization of wheat-wheatgrass translocation lines and localization of barley yellow dwarf virus resistance, Genome 43 (2000) 698-706.
Crossref Google Scholar
[21]

P.M. Banks, P.J. Larkin, H.S. Bariana, E.S. Lagudah, R. Appels, P.M. Waterhouse, R.I.S. Brettel, X. Chen, H.J. Xu, Z.Y. Xin, Y.T. Qian, X.N. Zhou, Z.M. Cheng, G.H. Zhou, The use of cell culture for subchromosomal introgressions of barley yellow dwarf virus resistance from Thinopyrum intermedium to wheat, Genome 38 (1995) 395-405.
Crossref Google Scholar
[22]

Z.Y. Xin, Z.Y. Zhang, X. Chen, Z.S. Lin, Y.Z. Ma, H.J. Xu, P.M. Banks, P.J. Larkin, Development and characterization of common wheat–Thinopyrum intermedium translocation lines with resistance to barley yellow dwarf virus, Euphytica 119 (2001) 161-165.
Crossref Google Scholar
[23]

Z.Y. Zhang, Z.Y. Xin, Y.Z. Ma, X. Chen, Q.F. Xu, Z.S. Lin, Mapping of a BYDV resistance gene from Thinopyrum intermedium in wheat background by molecular markers, Sci. China C 42 (1999) 663-668.
Crossref Google Scholar
[24]

X.D. Wang, Y. Liu, L. Chen, D. Zhao, X.F. Wang, Z.Y. Zhang, Wheat resistome in response to barley yellow dwarf virus infection, Funct. Integr. Genomics 13 (2013) 155-165.
Crossref Google Scholar
[25]

M.A. López, G. Bannenberg, C. Castresana, Controlling hormone signaling is a plant and pathogen challenge for growth and survival, Curr. Opin. Plant Biol. 11 (2008) 420-427.
Crossref Google Scholar
[26]

J.D. Jones, J.L. Dangl, The plant immune system, Nature 444 (2006) 323-329.
Crossref Google Scholar
[27]

C.M. Pieterse, A. Leon-Reyes, S. van der Ent, S.C. van Wees, Networking by small-molecule hormones in plant immunity, Nat. Chem. Biol. 5 (2009) 308-316.
Crossref Google Scholar
[28]

R. Desikan, M.K. Cheng, A. Clarke, S. Golding, M. Sagi, R. Fluhr, Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum, Funct. Plant Biol. 31 (2004) 913-920.
Crossref Google Scholar
[29]

L.J. Quan, B. Zhang, W. Shi, H.Y. Li, Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network, Plant Biol. 50 (2008) 2-18.
Crossref Google Scholar
[30]

D.H. Lee, C.B. Lee, Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzymes activity assays, Plant Sci. 159 (2000) 75-85.
Crossref Google Scholar
[31]

G. Wingsle, J.E. Hallgren, Influence of SO2 and NO2 exposure on glutathione, superoxide dismutase and glutathione reductase activities in Scots pine needles, J. Exp. Bot. 44 (1993) 463-470.
Crossref Google Scholar
[32]

J.S. Zhang, C.J. Li, J. Wei, M.B. Kirkham, Protoplasmic factors, antioxidants responses, and chilling resistance in maize, Plant Physiol. Biol. Chem. 382 (1995) 1123-1131.
Google Scholar
[33]

K. Hahlborck, P. Bednarek, I. Ciolkowski, B. Hamberger, A. Heise, H. Liedgens, E. Logemann, T. Nürnberger, E. Schmelzer, I.E. Somssich, J. Tan, Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14569-14576.
Crossref Google Scholar
[34]

F.M. Ausubel, Are innate immune signaling pathways in plants and animals conserved, Nat. Immunol. 6 (2005) 973-979.
Crossref Google Scholar
[35]

T. Boller, G. Felix, A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors, Annu. Rev. Plant Biol. 60 (2009) 379-406.
Crossref Google Scholar
[36]

Z.Q. Fu, X. Dong, Systemic acquired resistance: turning local infection into global defense, Annu. Rev. Plant Biol. 64 (2013) 839-863.
Crossref Google Scholar
[37]

I.E. Somssich, K. Hahlbrock, Pathogen defence in plants-a paradigm of biological complexity, Trends Plant Sci. 3 (1998) 86-90.
Crossref Google Scholar
[38]

Y. Zhu, C.M. Schluttenhoffer, P. Wang, F. Fu, J. Thimmapuram, J.K. Zhum, S.Y. Lee, D.J. Yun, T. Mengiste, Cyclin-dependent kinase8 differentially regulates plant immunity to fungal pathogens through kinase-dependent and -independent functions in Arabidopsis, Plant Cell 26 (2014) 4149-4170.
Crossref Google Scholar
[39]

M.D. Bolton, J.A. Kolmer, W.W. Xu, D.F. Garvin, Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways, Mol. Plant-Microbe Interact. 21 (2008) 1515-1527.
Crossref Google Scholar
[40]

M.M. Xin, X.F. Wang, H.R. Peng, Y.Y. Yao, C.J. Xie, Y. Han, Z.F. Ni, Q.X. Sun, Transcriptome comparison of susceptible and resistant wheat in response to powdery mildew infection, Genomics Proteomic Bioinformatics 10 (2012) 94-106.
Crossref Google Scholar
[41]

M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, M.A. Harris, D.P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J.C. Matese, J.E. Richardson, M. Ringwald, G.M. Rubin, G. Sherlock, Gene ontology: tool for the unification of biology. The Gene Ontology Consortium, Nat. Genet. 25 (2000) 25-29.
Crossref Google Scholar
[42]

K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method, Methods 25 (2001) 402-408.
Crossref Google Scholar
[43]

X. Hu, S. Neill, W. Cai, Z. Tang, Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension-cultured cells of Panax ginseng, Physiol. Plant. 118 (2003) 414-421.
Crossref Google Scholar
[44]

C. Riedel, A. Habekuss, E. Schliephake, R. Niks, I. Broer, F. Ordon, Pyramiding of Ryd2 and Ryd3 conferring tolerance to a German isolate of barley yellow dwarf virus-PAV (BYDV-PAV-ASL-1) leads to quantitative resistance against this isolate, Theor. Appl. Genet. 123 (2011) 69-76.
Crossref Google Scholar
[45]

T. Oikawa, M. Koshioka, K. Kojima, H. Yoshida, M. Kawata, A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice, Plant Mol. Biol. 55 (2004) 687-700.
Crossref Google Scholar
[46]

A. Schilmiller, G.A. Howe, Systemic signaling in the wound response, Curr. Opin. Cell Biol. 8 (2005) 369-377.
Crossref Google Scholar
[47]

B. Balaji, D.B. Bucholtz, J.M. Anderson, Barley yellow dwarf virus and cereal yellow dwarf virus quantification by real-time polymerase chain reaction in resistant and susceptible plants, Phytopathology 93 (2003) 1386-1392.
Crossref Google Scholar
[48]

X.D. Liu, Z.Y. Zhang, Y. Liu, Z.Y. Xin, Molecular evidence of barley yellow dwarf virus replication/movement suppressed by the resistance gene Bdv2, Acta Genet. Sin. 32 (2005) 942-947.
Google Scholar
[49]

V.I. Nicaise, Crop immunity against viruses: outcomes and future challenges, Front. Plant Sci. 5 (2014) 660.
Crossref Google Scholar
[50]

J.L.M. Soosaar, T.M. Burch-Smith, S.P. Dinesh-Kumer, Mechanisms of plant resistance to viruses, Nat. Rev. Microbiol. 3 (2005) 789-798.
Crossref Google Scholar
[51]

J.M. Andrew, C. Carole, I.B. Margaret, Sources of natural resistance to plant viruses: status and prospects, Mol. Plant Pathol. 8 (2007) 223-231.
Crossref Google Scholar
[52]

A. Caverzan, A. Bonifacio, F.E. Carvalho, C.M. Andrade, G. Passaia, M. Schünemann, S. Maraschin Fdos, M.O. Martins, F.K. Teixeira, R. Rauber, R. Margis, J.A. Siveira, M. Margis-Pinheiro, The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice, Plant Sci. 214 (2014) 74-87.
Crossref Google Scholar
[53]

F. Myouga, C. Hosoda, T. Unezawa, H. Jizumi, T. Kuromori, R. Motohashi, Y. Shono, N. Nagata, M. Ikeuchi, K. Shinozaki, A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis, Plant Cell 20 (2008) 3148-3162.
Crossref Google Scholar
[54]

M.H. Cui, S.H. Ok, K.S. Yoo, K.W. Jung, S.D. Yoo, J.S. Shin, An Arabidopsis cell growth defect factor-related protein, CRS, promotes plant senescence by increasing the production of hydrogen peroxide, Plant Cell Physiol. 54 (2013) 155-167.
Crossref Google Scholar
[55]

B. Le Martret, M. Poage, K. Shiel, G.D. Nugent, P.J. Dix, Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance, Plant Biotechnol. J. 9 (2011) 661-673.
Crossref Google Scholar
[56]

S. Van der Ent, S.C. Van Wees, C.M. Pieterse, Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes, Phytochemistry 70 (2009) 581-588.
Crossref Google Scholar
The Crop Journal
Volume 6 Issue 4,
August 2018
Pages 394-405
DOI: 10.1016/j.cj.2018.02.002
Cite this article:
Wang X, Rong W, Liu Y, et al. Investigation of the mechanism of adult-stage resistance to barley yellow dwarf virus associated with a wheat–Thinopyrum intermedium translocation. The Crop Journal, 2018, 6(4): 394-405. https://doi.org/10.1016/j.cj.2018.02.002

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Received: 19 July 2017
Revised: 22 February 2018
Accepted: 07 March 2018
Published: 27 March 2018
© 2018 "Crop Science Society of China and Institute of Crop Science, CAAS".

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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