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Comparative transcriptome and histological analyses of wheat in response to phytotoxic aphid Schizaphis graminum and non-phytotoxic aphid Sitobion avenae feeding.
BMC Plant Biol. 2019 Dec 10; 19(1):547.BP

Abstract

BACKGROUND

Infestation of the phytotoxic aphid Schizaphis graminum can rapidly induce leaf chlorosis in susceptible plants, but this effect is not observed with the nonphytotoxic aphid Sitobion avenae. However, few studies have attempted to identify the different defence responses induced in wheat by S. graminum and S. avenae feeding and the mechanisms underlying the activation of chlorosis by S. graminum feeding.

RESULTS

S. graminum feeding significantly reduced the chlorophyll content of wheat leaves, and these effects were not observed with S. avenae. A transcriptomic analysis showed that the expression levels of genes involved in the salicylic acid, jasmonic acid and ethylene signalling defence pathways were significantly upregulated by both S. avenae and S. graminum feeding; however, more plant defence genes were activated by S. graminum feeding than S. avenae feeding. The transcript levels of genes encoding cell wall-modifying proteins were significantly increased after S. graminum feeding, but only a few of these genes were induced by S. avenae. Furthermore, various reactive oxygen species-scavenging genes, such as 66 peroxidase (POD) and 8 ascorbate peroxidase (APx) genes, were significantly upregulated after S. graminum feeding, whereas only 15 POD and one APx genes were induced by S. avenae feeding. The activity of four antioxidant enzymes was also significantly upregulated by S. graminum feeding. Cytological examination showed that S. graminum feeding induced substantial hydrogen peroxide (H2O2) accumulation in wheat leaves. The chlorosis symptoms and the loss of chlorophyll observed in wheat leaves after S. graminum feeding were reduced and inhibited by the scavenging of H2O2 by dimethylthiourea, which indicated that H2O2 plays important role in the induction of chlorosis by S. graminum feeding.

CONCLUSIONS

S. graminum and S. avenae feeding induces the JA, SA and ET signalling pathways, but S. graminum activated stronger plant defence responses than S. avenae. S. graminum feeding triggers strong ROS-scavenging activity and massive H2O2 production in wheat leaves, and the accumulation of H2O2 induced by S. graminum feeding is involved in the activation of chlorosis in wheat leaves. These results enhance our understanding of mechanisms underlying aphid-wheat interactions and provide clues for the development of aphid-resistant wheat varieties.

Authors+Show Affiliations

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People's Republic of China.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People's Republic of China.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People's Republic of China.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People's Republic of China.Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liège, B-5030, Gembloux, Belgium.State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, People's Republic of China. chenjulian@caas.cn.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31823722

Citation

Zhang, Yong, et al. "Comparative Transcriptome and Histological Analyses of Wheat in Response to Phytotoxic Aphid Schizaphis Graminum and Non-phytotoxic Aphid Sitobion Avenae Feeding." BMC Plant Biology, vol. 19, no. 1, 2019, p. 547.
Zhang Y, Fu Y, Fan J, et al. Comparative transcriptome and histological analyses of wheat in response to phytotoxic aphid Schizaphis graminum and non-phytotoxic aphid Sitobion avenae feeding. BMC Plant Biol. 2019;19(1):547.
Zhang, Y., Fu, Y., Fan, J., Li, Q., Francis, F., & Chen, J. (2019). Comparative transcriptome and histological analyses of wheat in response to phytotoxic aphid Schizaphis graminum and non-phytotoxic aphid Sitobion avenae feeding. BMC Plant Biology, 19(1), 547. https://doi.org/10.1186/s12870-019-2148-5
Zhang Y, et al. Comparative Transcriptome and Histological Analyses of Wheat in Response to Phytotoxic Aphid Schizaphis Graminum and Non-phytotoxic Aphid Sitobion Avenae Feeding. BMC Plant Biol. 2019 Dec 10;19(1):547. PubMed PMID: 31823722.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Comparative transcriptome and histological analyses of wheat in response to phytotoxic aphid Schizaphis graminum and non-phytotoxic aphid Sitobion avenae feeding. AU - Zhang,Yong, AU - Fu,Yu, AU - Fan,Jia, AU - Li,Qian, AU - Francis,Frédéric, AU - Chen,Julian, Y1 - 2019/12/10/ PY - 2019/04/22/received PY - 2019/11/19/accepted PY - 2019/12/12/entrez PY - 2019/12/12/pubmed PY - 2020/4/1/medline KW - Chlorosis KW - Cytological KW - Defense responses KW - Hydrogen peroxide KW - Reactive oxygen species scavengers KW - Schizaphis graminum KW - Sitobion avenae KW - Transcriptome KW - Wheat SP - 547 EP - 547 JF - BMC plant biology JO - BMC Plant Biol VL - 19 IS - 1 N2 - BACKGROUND: Infestation of the phytotoxic aphid Schizaphis graminum can rapidly induce leaf chlorosis in susceptible plants, but this effect is not observed with the nonphytotoxic aphid Sitobion avenae. However, few studies have attempted to identify the different defence responses induced in wheat by S. graminum and S. avenae feeding and the mechanisms underlying the activation of chlorosis by S. graminum feeding. RESULTS: S. graminum feeding significantly reduced the chlorophyll content of wheat leaves, and these effects were not observed with S. avenae. A transcriptomic analysis showed that the expression levels of genes involved in the salicylic acid, jasmonic acid and ethylene signalling defence pathways were significantly upregulated by both S. avenae and S. graminum feeding; however, more plant defence genes were activated by S. graminum feeding than S. avenae feeding. The transcript levels of genes encoding cell wall-modifying proteins were significantly increased after S. graminum feeding, but only a few of these genes were induced by S. avenae. Furthermore, various reactive oxygen species-scavenging genes, such as 66 peroxidase (POD) and 8 ascorbate peroxidase (APx) genes, were significantly upregulated after S. graminum feeding, whereas only 15 POD and one APx genes were induced by S. avenae feeding. The activity of four antioxidant enzymes was also significantly upregulated by S. graminum feeding. Cytological examination showed that S. graminum feeding induced substantial hydrogen peroxide (H2O2) accumulation in wheat leaves. The chlorosis symptoms and the loss of chlorophyll observed in wheat leaves after S. graminum feeding were reduced and inhibited by the scavenging of H2O2 by dimethylthiourea, which indicated that H2O2 plays important role in the induction of chlorosis by S. graminum feeding. CONCLUSIONS: S. graminum and S. avenae feeding induces the JA, SA and ET signalling pathways, but S. graminum activated stronger plant defence responses than S. avenae. S. graminum feeding triggers strong ROS-scavenging activity and massive H2O2 production in wheat leaves, and the accumulation of H2O2 induced by S. graminum feeding is involved in the activation of chlorosis in wheat leaves. These results enhance our understanding of mechanisms underlying aphid-wheat interactions and provide clues for the development of aphid-resistant wheat varieties. SN - 1471-2229 UR - https://www.unboundmedicine.com/medline/citation/31823722/Comparative_transcriptome_and_histological_analyses_of_wheat_in_response_to_phytotoxic_aphid_Schizaphis_graminum_and_non_phytotoxic_aphid_Sitobion_avenae_feeding_ DB - PRIME DP - Unbound Medicine ER -