Abstract
In this study, 15 closely related barley genotypes were analyzed for the abundance of three β-1,3-glucanase transcripts immediately before and during infestation by the bird cherry-oat aphid (Rhopalosiphum padi L.). The barley lines are doubled haploid lines in backcross (BC) generations BC1 and BC2 from a cross between cultivar Lina and a wild barley accession. Previously, they have been characterized as susceptible (S) or resistant (R) to R. padi based on their ability to support nymphal growth. Here we also tested whether resistance was manifested as reduced aphid settling on the plants. Indeed, aphid numbers were lower on R than on S lines in all cases where there were significant differences between R and S lines. The choice of β-1,3-glucanase sequences is based on earlier results comparing two S and two R genotypes, suggesting that at least two of the three studied sequences are susceptibility factors. The comparisons of transcript abundance in plants with aphids showed for two of the β-1,3-glucanase sequences that there were several cases where an S genotype had significantly higher abundance than an R genotype, and in no case did an R line have significantly higher abundance than an S line. Thus, there was some support for the idea that β-1,3-glucanase sequences are susceptibility factors in the interaction between barley and R. padi.
Similar content being viewed by others
References
Anderson VA, Haley SD, Peairs FB, van Eck L, Leach JE, Lapitan NLV (2014) Virus-induced gene silencing suggests (1,3;1,4)-β-glucanase is a susceptibility factor in the compatible Russian wheat aphid–wheat interaction. MPMI 27:913–922
Blackman RL, Eastop VF (2007) Taxonomic issues. In: van Emden H, Harrington R (eds) Aphids as crop pests. CABI, Wallingford, pp 1–29
Botha AM, Swanefelder ZH, Lapitan NLV (2010) Transcript profiling of wheat genes expressed during feeding by two different biotypes of Diuraphis noxia. Environ Entomol 39:1206–1231
Delp G, Gradin T, Åhman I, Jonsson LMV (2009) Microarray analysis of the interaction between the aphid Rhopalosiphum padi and host plants reveals both differences and similarities between susceptible and partially resistant barley lines. Mol Genet Genomics 281:233–248
Forslund K, Pettersson J, Bryngelsson T, Jonsson L (2000) Aphid infestation induces PR-proteins differently in barley susceptible or resistant to the bird cherry-oat aphid (Rhopalosiphum padi). Physiol Plant 110:496–502
Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F, Van Bel AJE, Kogel KH, Kehr J (2008) Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J Exp Bot 59:3297–3306
Giordanengo P, Brunissen L, Rusterucci C, Vincent C, Van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain JL (2010) Compatible plant–aphid interactions: how aphids manipulate plant responses. CR Biol 333:516–523
Hamada AM, Jonsson LMV (2013) Thiamine treatments alleviate aphid infestations in barley and pea. Phytochemistry 94:135–141
Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146:1810–1820
Hoj PB, Hartman DJ, Morrice NA, Doan DNP, Fincher GB (1989) Purification of (1 → 3)-β-glucan endohydrolase isoenzyme II from germinated barley and determination of its primary structure from a cDNA clone. Plant Mol Biol 13:31–42
Li YF, Zhu R, Xu PL (2005) Activation of the gene promoter of barley β-1,3-glucanase isoenzyme GIII is salicylic acid (SA)-dependent in transgenic rice plants. J Plant Res 118:215–221
Mehrabi S, Åhman I, Jonsson LMV (2014) Transcript abundance of resistance—and susceptibility—related genes in a barley breeding pedigree with partial resistance to the bird cherry-oat aphid (Rhopalosiphum padi L.). Euphytica 198:211–222
Painter RH (1951) The mechanisms of resistance. Insect resistance in crop plants. Macmillan Company, New York, pp 23–84
Park SJ, Huang YH, Ayoubi P (2006) Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 223:932–947
Reddy SK, Weng YQ, Rudd JC, Akhunova A, Liu SY (2013) Transcriptomics of induced defense responses to greenbug aphid feeding in near isogenic wheat lines. Plant Sci 212:26–36
Riedell WE, Kieckhefer RW, Haley SD, Langham MAC, Evenson PD (1999) Winter wheat responses to bird cherry-oat aphids and barley yellow dwarf virus infection. Crop Sci 39:158–163
Riedell WE, Kieckhefer RW, Langham MAC, Hesler LS (2003) Root and shoot responses to bird cherry-oat aphids and barley yellow dwarf virus in spring wheat. Crop Sci 43:1380–1386
Saheed SA, Cierlik I, Larsson KAE, Delp G, Bradley G, Jonsson LMV, Botha CEJ (2009) Stronger induction of callose deposition in barley by Russian wheat aphid than bird cherry-oat aphid is not associated with differences in callose synthase or β-1,3-glucanase transcript abundance. Physiol Plant 135:150–161
Smith CM (2005a) Antixenosis—adverse effects of resistance on arthropod behavior. Plant resistance to arthropods. Molecular and conventional approaches. Springer, Dordrecht, pp 19–63
Smith CM (2005b) Antibiosis—adverse effects of resistance on arthropod biology. Plant resistance to arthropods. Molecular and conventional approaches. Springer, Dordrecht, pp 65–99
van der Westhuizen AJ, Qian XM, Botha AM (1998) β-1,3-Glucanases in wheat and resistance to the Russian wheat aphid. Physiol Plant 103:125–131
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162
Wang J, Xu PL, Fincher GB (1992) Purification, characterization and gene structure of (1 → 3)-β-glucanase isoenzyme GIII from barley (Hordeum vulgare). Eur J Biochem 209:103–109
Xu PL, Wang J, Fincher GB (1992) Evolution and differential expression of the (1 → 3)-β-glucan endohydrolase-encoding gene family in barley, Hordeum vulgare. Gene 120:157–165
Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431
Acknowledgments
The authors thank Lantmännen Lantbruk for providing the plant material and Velemir Ninkovic, SLU Uppsala for providing bird cherry-oat aphids at the start of the study. This study had financial support from the Royal Physiographic Society in Lund via a stipend from the Nilsson Ehle-donations to SM, funding from the Swedish Research Council Formas to IÅ and faculty funding to LJ.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Robert Glinwood.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mehrabi, S., Åhman, I. & Jonsson, L.M.V. The constitutive expression and induction of three β-1,3-glucanases by bird cherry-oat aphid in relation to aphid resistance in 15 barley breeding lines. Arthropod-Plant Interactions 10, 101–111 (2016). https://doi.org/10.1007/s11829-016-9415-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-016-9415-2