FKBP-type peptidyl-prolyl cis-trans isomerase interacts with the movement protein of tomato leaf curl New Delhi virus and impacts viral replication in Nicotiana benthamiana

Ho-Hsiung Chang; Chia-Hwa Lee; Chung-Jan Chang; Fuh-Jyh Jan

doi:10.1111/mpp.13181

FKBP-type peptidyl-prolyl cis-trans isomerase interacts with the movement protein of tomato leaf curl New Delhi virus and impacts viral replication in Nicotiana benthamiana

Mol Plant Pathol. 2022 Apr;23(4):561-575. doi: 10.1111/mpp.13181. Epub 2022 Jan 4.

Authors

Ho-Hsiung Chang¹, Chia-Hwa Lee^{1

2}, Chung-Jan Chang^{1

3}, Fuh-Jyh Jan^{1

2

4}

Affiliations

¹ Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan.
² Ph.D. Program in Microbial Genomics, National Chung Hsing University and Academia Sinica, Taichung and Taipei, Taiwan.
³ Department of Plant Pathology, University of Georgia, Griffin, Georgia, USA.
⁴ Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung, Taiwan.

Abstract

Begomoviruses belonging to the family Geminiviridae are plant-infecting DNA viruses. Begomoviral movement protein (MP) has been reported to be required for virus movement, host range determination, and symptom development. In the present study, the FK506-binding protein (FKBP)-type peptidyl-prolyl cis-trans isomerase (NbFKPPIase) of Nicotiana benthamiana was identified by a yeast two-hybrid screening system using the MP of tomato leaf curl New Delhi virus (ToLCNDV) oriental melon (OM) isolate (MP^OM ) as bait. Transient silencing of the gene encoding NbFKPPIase increased replication of three test begomoviruses, and transient overexpression decreased viral replication, indicating that NbFKPPIase plays a role in defence against begomoviruses. However, infection of N. benthamiana by ToLCNDV-OM or overexpression of the gene encoding MP^OM drastically reduced the expression of the gene encoding NbFKPPIase. Fluorescence resonance energy transfer analysis revealed that MP^OM interacted with NbFKPPIase in the periphery of cells. Expression of the gene encoding NbFKPPIase was induced by salicylic acid but not by methyl jasmonate or ethylene. Moreover, the expression of the gene encoding NbFKPPIase was down-regulated in response to 6-benzylaminopurine and up-regulated in response to gibberellin or indole-3-acetic acid, suggesting a role of NbFKPPIase in plant development. Transcriptome analysis and comparison of N. benthamiana transient silencing and overexpression of the gene encoding MP^OM led to the identification of several differentially expressed genes whose functions are probably associated with cell cycle regulation. Our results indicate that begomoviruses could suppress NbFKPPIase-mediated defence and biological functions by transcriptional inhibition and physical interaction between MP and NbFKPPIase to facilitate infection.

Keywords: begomovirus; movement protein; peptidyl-prolyl cis-trans isomerase; replication; tomato leaf curl New Delhi virus (ToLCNDV).

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Begomovirus* / genetics
Nicotiana / genetics
Peptidylprolyl Isomerase
Plant Diseases
Solanum lycopersicum*
Tacrolimus Binding Proteins
Virus Replication

Substances

Tacrolimus Binding Proteins
Peptidylprolyl Isomerase

Supplementary concepts

Tomato leaf curl New Delhi virus