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Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina.
J Exp Bot. 2022 01 13; 73(2):555-570.JE

Abstract

Galling insects gain food and shelter by inducing specialized anatomical structures in their plant hosts. Such galls often accumulate plant defensive metabolites protecting the inhabiting insects from predation. We previously found that, despite a marked natural chemopolymorphism in natural populations of Pistacia palaestina, the monoterpene content in Baizongia pistaciae-induced galls is substantially higher than in leaves of their hosts. Here we show a general up-regulation of key structural genes in both the plastidial and cytosolic terpene biosynthetic pathways in galls as compared with non-colonized leaves. Novel prenyltransferases and terpene synthases were functionally expressed in Escherichia coli to reveal their biochemical function. Individual Pistacia trees exhibiting chemopolymorphism in terpene compositions displayed differential up-regulation of selected terpene synthase genes, and the metabolites generated by their gene products in vitro corresponded to the monoterpenes accumulated by each tree. Our results delineate molecular mechanisms responsible for the formation of enhanced monoterpene in galls and the observed intraspecific monoterpene chemodiversity displayed in P. palaestina. We demonstrate that gall-inhabiting aphids transcriptionally reprogram their host terpene pathways by up-regulating tree-specific genes, boosting the accumulation of plant defensive compounds for the protection of colonizing insects.

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Authors+Show Affiliations

Davidovich-Rikanati R
Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel.
Bar E
Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel.
Hivert G
Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel. Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel.
Huang XQ
Department of Biochemistry, Purdue University, West Lafayette, IN 47907-1165, USA. Purdue Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA.
Hoppen-Tonial C
Department of Agronomy, Federal University of Technology - Paraná, Pato Branco, 85503-390, Brazil. Department of Agronomy, Federal Institute of Paraná, Palmas, 85555-000, Brazil.
Khankin V
Department of Chemical Engineering, Shamoon College of Engineering, Beer Sheva, 84100, Israel.
Rand K
Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel. Department of Evolutionary & Environmental Biology, University of Haifa, Mount Carmel, Haifa, 3498838, Israel.
Abofreih A
Department of Chemical Engineering, Shamoon College of Engineering, Beer Sheva, 84100, Israel.
Muhlemann JK
Department of Biochemistry, Purdue University, West Lafayette, IN 47907-1165, USA. The James Hutton Institute, UK.
Marchese JA
Department of Agronomy, Federal University of Technology - Paraná, Pato Branco, 85503-390, Brazil.
Shotland Y
Department of Chemical Engineering, Shamoon College of Engineering, Beer Sheva, 84100, Israel.
Dudareva N
Department of Biochemistry, Purdue University, West Lafayette, IN 47907-1165, USA. Purdue Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA.
Inbar M
Department of Evolutionary & Environmental Biology, University of Haifa, Mount Carmel, Haifa, 3498838, Israel.
Lewinsohn E
Institute of Plant Sciences, Newe Ya'ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel. Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel.

MeSH

AnimalsAphidsPistaciaPlant TumorsTerpenesUp-Regulation

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

34129033

Citation

Davidovich-Rikanati, Rachel, et al. "Transcriptional Up-regulation of Host-specific Terpene Metabolism in Aphid-induced Galls of Pistacia Palaestina." Journal of Experimental Botany, vol. 73, no. 2, 2022, pp. 555-570.
Davidovich-Rikanati R, Bar E, Hivert G, et al. Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina. J Exp Bot. 2022;73(2):555-570.
Davidovich-Rikanati, R., Bar, E., Hivert, G., Huang, X. Q., Hoppen-Tonial, C., Khankin, V., Rand, K., Abofreih, A., Muhlemann, J. K., Marchese, J. A., Shotland, Y., Dudareva, N., Inbar, M., & Lewinsohn, E. (2022). Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina. Journal of Experimental Botany, 73(2), 555-570. https://doi.org/10.1093/jxb/erab289
Davidovich-Rikanati R, et al. Transcriptional Up-regulation of Host-specific Terpene Metabolism in Aphid-induced Galls of Pistacia Palaestina. J Exp Bot. 2022 01 13;73(2):555-570. PubMed PMID: 34129033.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina. AU - Davidovich-Rikanati,Rachel, AU - Bar,Einat, AU - Hivert,Gal, AU - Huang,Xing-Qi, AU - Hoppen-Tonial,Carolina, AU - Khankin,Vered, AU - Rand,Karin, AU - Abofreih,Amal, AU - Muhlemann,Joelle K, AU - Marchese,José Abramo, AU - Shotland,Yoram, AU - Dudareva,Natalia, AU - Inbar,Moshe, AU - Lewinsohn,Efraim, PY - 2021/05/14/received PY - 2021/06/11/accepted PY - 2021/6/16/pubmed PY - 2022/1/28/medline PY - 2021/6/15/entrez KW - Baizongia pistaciae KW - Pistacia palaestina KW - extended phenotype KW - gall-forming insects KW - monoterpene biosynthesis KW - plant defense compounds KW - prenyl transferases KW - terpene metabolism KW - terpene synthases SP - 555 EP - 570 JF - Journal of experimental botany JO - J Exp Bot VL - 73 IS - 2 N2 - Galling insects gain food and shelter by inducing specialized anatomical structures in their plant hosts. Such galls often accumulate plant defensive metabolites protecting the inhabiting insects from predation. We previously found that, despite a marked natural chemopolymorphism in natural populations of Pistacia palaestina, the monoterpene content in Baizongia pistaciae-induced galls is substantially higher than in leaves of their hosts. Here we show a general up-regulation of key structural genes in both the plastidial and cytosolic terpene biosynthetic pathways in galls as compared with non-colonized leaves. Novel prenyltransferases and terpene synthases were functionally expressed in Escherichia coli to reveal their biochemical function. Individual Pistacia trees exhibiting chemopolymorphism in terpene compositions displayed differential up-regulation of selected terpene synthase genes, and the metabolites generated by their gene products in vitro corresponded to the monoterpenes accumulated by each tree. Our results delineate molecular mechanisms responsible for the formation of enhanced monoterpene in galls and the observed intraspecific monoterpene chemodiversity displayed in P. palaestina. We demonstrate that gall-inhabiting aphids transcriptionally reprogram their host terpene pathways by up-regulating tree-specific genes, boosting the accumulation of plant defensive compounds for the protection of colonizing insects. SN - 1460-2431 UR - https://www.unboundmedicine.com/medline/citation/34129033/Transcriptional_up_regulation_of_host_specific_terpene_metabolism_in_aphid_induced_galls_of_Pistacia_palaestina_ L2 - https://academic.oup.com/jxb/article-lookup/doi/10.1093/jxb/erab289 DB - PRIME DP - Unbound Medicine ER -