The nitrogen-dependent GABA pathway of tomato provides resistance to a globally invasive fruit fly

Hao Li; Yuan Zhang; Hu Li; Gadi V P Reddy; Zhihong Li; Fajun Chen; Yucheng Sun; Zihua Zhao

doi:10.3389/fpls.2023.1252455

The nitrogen-dependent GABA pathway of tomato provides resistance to a globally invasive fruit fly

Front Plant Sci. 2023 Dec 7:14:1252455. doi: 10.3389/fpls.2023.1252455. eCollection 2023.

Authors

Hao Li^#^{1

2}, Yuan Zhang^#^{1

2}, Hu Li¹, Gadi V P Reddy³, Zhihong Li^{1

2}, Fajun Chen⁴, Yucheng Sun⁵, Zihua Zhao^{1

2}

Affiliations

¹ Department of Plant Biosecurity & Ministry of Agriculture and Rural Affairs (MARA) Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing, China.
² Sanya Institute of China Agricultural University, Sanya, China.
³ Department of Entomology, Louisiana State University, Baton Rouge, LA, United States.
⁴ Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing, China.
⁵ National Key Lab Integrated Management Pest Insects, Institute of Zoology, Chinese Academy Science, Beijing, China.

^# Contributed equally.

Abstract

Introduction: The primary metabolism of plants, which is mediated by nitrogen, is closely related to the defense response to insect herbivores.

Methods: An experimental system was established to examine how nitrogen mediated tomato resistance to an insect herbivore, the oriental fruit fly (Bactrocera dorsalis). All tomatoes were randomly assigned to the suitable nitrogen (control, CK) treatment, nitrogen excess (NE) treatment and nitrogen deficiency (ND) treatment.

Results: We found that nitrogen excess significantly increased the aboveground biomass of tomato and increased the pupal biomass of B. dorsalis. Metabolome analysis showed that nitrogen excess promoted the biosynthesis of amino acids in healthy fruits, including γ-aminobutyric acid (GABA), arginine and asparagine. GABA was not a differential metabolite induced by injury by B. dorsalis under nitrogen excess, but it was significantly induced in infested fruits at appropriate nitrogen levels. GABA supplementation not only increased the aboveground biomass of plants but also improved the defensive response of tomato.

Discussion: The biosynthesis of GABA in tomato is a resistance response to feeding by B. dorsalis in appropriate nitrogen, whereas nitrogen excess facilitates the pupal weight of B. dorsalis by inhibiting synthesis of the GABA pathway. This study concluded that excess nitrogen inhibits tomato defenses in plant-insect interactions by inhibiting GABA synthesis, answering some unresolved questions about the nitrogen-dependent GABA resistance pathway to herbivores.

Keywords: Bactrocera dorsalis; interaction; nitrogen; plant defense; primary metabolism; γ-aminobutyric acid.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Key R&D Program of China [Grant No. 2021YFC2600400] and the Sanya Institute of China Agricultural University (Grant No. SYND-2021-29). This work was also supported by the China National Tobacco Corporation of Science and Technology Major Project (Grant No. 110202101049[LS-09]), and the Key Project of Science and Technology Plan of Yunnan Company of China National Tobacco Corporation (Grant No. 2022530000241019).