Transcriptional up-regulation of host-specific terpene metabolism in aphid-induced galls of Pistacia palaestina

Author:

Davidovich-Rikanati Rachel1,Bar Einat1,Hivert Gal12,Huang Xing-Qi34,Hoppen-Tonial Carolina56,Khankin Vered7,Rand Karin18,Abofreih Amal7,Muhlemann Joelle K39,Marchese José Abramo5,Shotland Yoram7,Dudareva Natalia34,Inbar Moshe8,Lewinsohn Efraim12ORCID

Affiliation:

1. Institute of Plant Sciences, Newe Ya’ar Research Center, Agricultural Research Organization, The Volcani Center, Ramat Yishay, 30095, Israel

2. Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel

3. Department of Biochemistry, Purdue University, West Lafayette, IN 47907-1165, USA

4. Purdue Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA

5. Department of Agronomy, Federal University of Technology - Paraná, Pato Branco, 85503-390, Brazil

6. Department of Agronomy, Federal Institute of Paraná, Palmas, 85555-000, Brazil

7. Department of Chemical Engineering, Shamoon College of Engineering, Beer Sheva, 84100, Israel

8. Department of Evolutionary & Environmental Biology, University of Haifa, Mount Carmel, Haifa, 3498838, Israel

9. The James Hutton Institute, UK

Abstract

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.

Funder

Israel Science Foundation

United States - Israel Binational Science Foundation

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Physiology

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