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C. Hoppen - Federal Institute of Paraná, Department of Agronomy, Palmas, Brazil
J. Muhlemann - Purdue University, West Lafayette, Department of Biochemistry, West Lafayette, Indiana, United States of America
J. A. Marchese -
Federal University of Technology - Paraná, Department of Agronomy, Pato Branco, Brazil
Y. Shotland -
Shamoon College of Engineering, Department of Chemical Engineering, Beer Sheva, Israel
N. Dudareva -
Purdue University, West Lafayette, Department of Biochemistry, West Lafayette, Indiana, United States of America,
M. Inbar -
University of Haifa, Mount Carmel, Department of Evolutionary & Environmental Biology, Haifa, Israel

Galls are modified plant organs conferring colonizing organisms a steady food source and protection against biotic and abiotic challenges. Galls frequently accumulate many specialized compounds of plant origin often protecting the invader organisms at the host's expense. The galling aphid Baizongia pistaciae L. induces banana-like galls on buds of the Mediterranean tree Pistacia palaestina Boiss. (Anacardiaceae). These galls accumulate high levels of monoterpenes protecting the colonizing aphids from natural enemies. Gall monoterpenes are not merely transported from adjacent or distal tissues, but galls possess enhanced monoterpene biosynthetic capacity as compared to intact non-colonized leaves. In this study, we examined galls transcriptomes from two individual trees growing in different locations in Northern Israel (Carmel Mt. and Schania) to ascertain if the enhanced ability to biosynthesize monoterpenes in galls is transcriptionally regulated. Our results indicate that the expression levels of key genes in both the plastidial and cytosolic terpene biosynthetic pathways were significantly higher in aphid-induced galls as compared to intact non-colonized leaves. PpGPPS.SSU, a gene likely encoding for the small subunit of geranyl diphosphate synthase, an enzyme providing geranyl diphosphate, the key substrate for monoterpene biosynthesis was upregulated in galls by more than a 10 fold. Furthermore, four novel members of the Tps (terpene synthase) gene family exhibited up to 100 fold upregulation in gall tissues as compared to non-colonized leaves. These genes were functionally evaluated in E. coli to test for their biochemical function. PpTPS53788 was upregulated in both trees and encoded an enzyme mainly producing (+) α-pinene and lower levels of (+) β-pinene from geranyl diphosphate in vitro. PpTPS27344 was upregulated only in the "Carmel" tree and encoded an enzyme exclusively producing (+)-limonene in vitro. PpTPS809 (upregulated in "Carmel") and PpTPS32115 (upregulated in "Schania") mainly produced α-thujene, (-) sabinene and γ-terpinene. Interestingly, the aphid-gall mediated upregulation of specific sets of TPS genes in individual trees and the products they produce in vitro can partially explain the intraspecific chemodiversity in monoterpene compositions observed among galls and leaves of individual P. palaestina trees. Our results demonstrate a transcriptional takeover of key genes in the terpene pathway as part of the galling habit by which aphids clearly recruit and manipulate plant chemistry for their own defense.

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The galling aphids Baizongia pistacia transcriptionally manipulate plant terpene metabolism resulting in augmented levels of defensive monoterpenes in galls (#126)

C. Hoppen - Federal Institute of Paraná, Department of Agronomy, Palmas, Brazil
J. Muhlemann - Purdue University, West Lafayette, Department of Biochemistry, West Lafayette, Indiana, United States of America
J. A. Marchese -
Federal University of Technology - Paraná, Department of Agronomy, Pato Branco, Brazil
Y. Shotland -
Shamoon College of Engineering, Department of Chemical Engineering, Beer Sheva, Israel
N. Dudareva -
Purdue University, West Lafayette, Department of Biochemistry, West Lafayette, Indiana, United States of America,
M. Inbar -
University of Haifa, Mount Carmel, Department of Evolutionary & Environmental Biology, Haifa, Israel

Galls are modified plant organs conferring colonizing organisms a steady food source and protection against biotic and abiotic challenges. Galls frequently accumulate many specialized compounds of plant origin often protecting the invader organisms at the host's expense. The galling aphid Baizongia pistaciae L. induces banana-like galls on buds of the Mediterranean tree Pistacia palaestina Boiss. (Anacardiaceae). These galls accumulate high levels of monoterpenes protecting the colonizing aphids from natural enemies. Gall monoterpenes are not merely transported from adjacent or distal tissues, but galls possess enhanced monoterpene biosynthetic capacity as compared to intact non-colonized leaves. In this study, we examined galls transcriptomes from two individual trees growing in different locations in Northern Israel (Carmel Mt. and Schania) to ascertain if the enhanced ability to biosynthesize monoterpenes in galls is transcriptionally regulated. Our results indicate that the expression levels of key genes in both the plastidial and cytosolic terpene biosynthetic pathways were significantly higher in aphid-induced galls as compared to intact non-colonized leaves. PpGPPS.SSU, a gene likely encoding for the small subunit of geranyl diphosphate synthase, an enzyme providing geranyl diphosphate, the key substrate for monoterpene biosynthesis was upregulated in galls by more than a 10 fold. Furthermore, four novel members of the Tps (terpene synthase) gene family exhibited up to 100 fold upregulation in gall tissues as compared to non-colonized leaves. These genes were functionally evaluated in E. coli to test for their biochemical function. PpTPS53788 was upregulated in both trees and encoded an enzyme mainly producing (+) α-pinene and lower levels of (+) β-pinene from geranyl diphosphate in vitro. PpTPS27344 was upregulated only in the "Carmel" tree and encoded an enzyme exclusively producing (+)-limonene in vitro. PpTPS809 (upregulated in "Carmel") and PpTPS32115 (upregulated in "Schania") mainly produced α-thujene, (-) sabinene and γ-terpinene. Interestingly, the aphid-gall mediated upregulation of specific sets of TPS genes in individual trees and the products they produce in vitro can partially explain the intraspecific chemodiversity in monoterpene compositions observed among galls and leaves of individual P. palaestina trees. Our results demonstrate a transcriptional takeover of key genes in the terpene pathway as part of the galling habit by which aphids clearly recruit and manipulate plant chemistry for their own defense.

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