Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm

Hang Zhang; Enliang Liu; Xinzheng Huang; Junfeng Kou; Dong Teng; Beibei Lv; Xiaoqiang Han; Yongjun Zhang

doi:10.3389/fpls.2022.898541

Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm

Front Plant Sci. 2022 Jul 13:13:898541. doi: 10.3389/fpls.2022.898541. eCollection 2022.

Authors

Hang Zhang^{1

2}, Enliang Liu^{3

4}, Xinzheng Huang⁴, Junfeng Kou⁵, Dong Teng², Beibei Lv², Xiaoqiang Han¹, Yongjun Zhang²

Affiliations

¹ Key Laboratory of Oasis Agricultural Pest Management and Plant Protection Resources Utilization, Xinjiang Uygur Autonomous Region, College of Agriculture, Shihezi University, Shihezi, China.
² State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
³ Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China.
⁴ College of Plant Protection, China Agricultural University, Beijing, China.
⁵ Institute of Plant Protection, Cangzhou Academy of Agriculture and Forestry Sciences, Cangzhou, China.

Abstract

When attacked by insect herbivores, plants initiate sophisticated defenses mediated by complex signaling networks and usually release a blend of functional volatiles such as terpenes against infestation. The extra-long staple cotton Gossypium barbadense cultivated worldwide as natural textile fiber crop is frequently exposed to a variety of herbivores, such as cotton bollworm Helicoverpa armigera. However, little is known about insect-induced transcriptional changes and molecular mechanisms underlying subsequent defense responses in G. barbadense. In the current study, transcriptome changes in G. barbadense infested with chewing H. armigera larvae were investigated, and we identified 5,629 differentially expressed genes (DEGs) in the infested cotton leaves compared with non-infested controls. H. armigera feeding triggered complex signaling networks in which almost all (88 out of 90) DEGs associated with the jasmonic acid (JA) pathway were upregulated, highlighting a central role for JA in the defense responses of G. barbadense against target insects. All DEGs involved in growth-related photosynthesis were downregulated, whereas most DEGs associated with defense-related transcript factors and volatile secondary metabolism were upregulated. It was noteworthy that a terpene synthase gene in the transcriptome data, GbTPS1, was strongly expressed in H. armigera-infested G. barbadense leaves. The upregulation of GbTPS1 in qPCR analysis also suggested an important role for GbTPS1 in herbivore-induced cotton defense. In vitro assays showed that recombinant GbTPS1 catalyzed farnesyl pyrophosphate and neryl diphosphate to produce three sesquiterpenes (selinene, α-gurjunene, and β-elemene) and one monoterpene (limonene), respectively. Moreover, these catalytic products of GbTPS1 were significantly elevated in G. barbadense leaves after H. armigera infestation, and elemene and limonene had repellent effects on H. armigera larvae in a dual-choice bioassay and increased larval mortality in a no-choice bioassay. These findings provide a valuable insight into understanding the transcriptional changes reprogramming herbivore-induced sesquiterpene biosynthesis in G. barbadense infested by H. armigera, which help elucidate the molecular mechanisms underlying plant defense against insect pests.

Keywords: GbTPS1; Helicoverpa armigera; extra-long staple cotton; induced defense; sesquiterpene biosynthesis; transcriptome sequencing; β-elemene.