Transcriptomic and functional analyses reveal the molecular mechanisms underlying Fe-mediated tobacco resistance to potato virus Y infection

Chuantao Xu; Huiyan Guo; Rui Li; Xinyu Lan; Yonghui Zhang; Qiang Xie; Di Zhu; Qing Mu; Zhiping Wang; Mengnan An; Zihao Xia; Yuanhua Wu

doi:10.3389/fpls.2023.1163679

Transcriptomic and functional analyses reveal the molecular mechanisms underlying Fe-mediated tobacco resistance to potato virus Y infection

Front Plant Sci. 2023 Mar 30:14:1163679. doi: 10.3389/fpls.2023.1163679. eCollection 2023.

Authors

Chuantao Xu^{1

2}, Huiyan Guo¹, Rui Li¹, Xinyu Lan¹, Yonghui Zhang², Qiang Xie², Di Zhu³, Qing Mu³, Zhiping Wang¹, Mengnan An¹, Zihao Xia¹, Yuanhua Wu¹

Affiliations

¹ Liaoning Key Laboratory of Plant Pathology, College of Plant Protection, Shenyang Agricultural University, Shenyang, China.
² Luzhou City Company of Sichuan Province Tobacco Company, Luzhou, China.
³ Guizhou Qianxinan Prefectural Tobacco Company, Xingyi, China.

Abstract

Potato virus Y (PVY) mainly infects Solanaceous crops, resulting in considerable losses in the yield and quality. Iron (Fe) is involved in various biological processes in plants, but its roles in resistance to PVY infection has not been reported. In this study, foliar application of Fe could effectively inhibit early infection of PVY, and a full-length transcriptome and Illumina RNA sequencing was performed to investigate its modes of action in PVY-infected Nicotiana tabacum. The results showed that 18,074 alternative splicing variants, 3,654 fusion transcripts, 3,086 long non-coding RNAs and 14,403 differentially expressed genes (DEGs) were identified. Specifically, Fe application down-regulated the expression levels of the DEGs related to phospholipid hydrolysis, phospholipid signal, cell wall biosynthesis, transcription factors (TFs) and photosystem I composition, while those involved with photosynthetic electron transport chain (PETC) were up-regulated at 1 day post inoculation (dpi). At 3 dpi, these DEGs related to photosystem II composition, PETC, molecular chaperones, protein degradation and some TFs were up-regulated, while those associated with light-harvesting, phospholipid hydrolysis, cell wall biosynthesis were down-regulated. At 9 dpi, Fe application had little effects on resistance to PVY infection and transcript profiles. Functional analysis of these potentially critical DEGs was thereafter performed using virus-induced gene silencing approaches and the results showed that NbCat-6A positively regulates PVY infection, while the reduced expressions of NbWRKY26, NbnsLTP, NbFAD3 and NbHSP90 significantly promote PVY infection in N. benthamiana. Our results elucidated the regulatory network of Fe-mediated resistance to PVY infection in plants, and the functional candidate genes also provide important theoretical bases to further improve host resistance against PVY infection.

Keywords: Fe; Illumina RNA sequencing; PVY; full-length transcriptome; virus-induced gene silencing.

Grants and funding

This research was funded by the Planning and Management Project of Sichuan Company for controlling plant vector-borne viruses, grant number SCYC202214, and the Science and Technology Project of Guizhou Qianxinan Prefectural Company for controlling plant vector-borne viruses, grant number 2022-01.