An Essential Role of Mitochondrial α-Ketoglutarate Dehydrogenase E2 in the Basal Immune Response Against Bacterial Pathogens in Tomato.

Qiaomei Ma,Ping Wang,Golam Jalal Ahammed,Kai Shi,Yaru Liu,Hanmo Fang,Wenshan Zai

doi:10.3389/fpls.2020.579772

Abstract

Plants intensely modulate respiration when pathogens attack, but the function of mitochondrial respiration-related genes in plant–bacteria interaction is largely unclear. Here, the functions of α-ketoglutarate dehydrogenase (α-kGDH) E2 subunit and alternative oxidase (AOX) were investigated in the interaction between tomato and the virulent bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pst). Pst inoculation suppressed the transcript abundance of α-kGDH E2, but enhanced AOX expression and salicylic acid (SA) accumulation. Gene silencing and transient overexpression approaches revealed that plant susceptibility to Pst was significantly reduced by silencing α-kGDH E2 in tomato, but increased by overexpressing α-kGDH E2 in Nicotiana benthamiana, whereas silencing or overexpressing of AOX1a did not affect plant defense. Moreover, silencing octanoyltransferase (LIP2), engaged in the lipoylation of α-kGDH E2, significantly reduced disease susceptibility and hydrogen peroxide accumulation. Use of transgenic NahG tomato plants that cannot accumulate SA as well as the exogenous SA application experiment evidenced that α-kGDH E2 acts downstream of SA defense pathway. These results demonstrate tomato α-kGDH E2 plays a negative role in plant basal defense against Pst in an AOX-independent pathway but was associated with lipoylation and SA defense pathways. The findings help to elucidate the mechanisms of mitochondria-involved plant basal immunity.

Highlights

Plants growing in diverse environments are constantly challenged by a wide range of microbial pathogens and herbivorous insects that often result in growth inhibition and crop yield losses, leading to a significant risk to global agriculture
The salicylic acid (SA) biosynthesis- and signaling-related genes, including phenylalanine ammonia-lyase (PAL2/4/6), enhanced disease susceptibility 1 (EDS1), peptidyl arginine deiminase 4 (PAD4), non-expresser of pathogenesis-related gene 1 (NPR1), and PR family members, are up-regulated in response to Pst inoculation, which were reported in a previous independent study (Yang et al, 2015)
Other seven genes clustered in another group were down-regulated in response to Pst inoculation, including tricarboxylic acid (TCA) cycle-related genes α-ketoglutarate dehydrogenase (α-kGDH) E2, lipoyl synthase (LIP1), octanoyltransferase (LIP2) and mitochondrial β-ketoacylacyl carrier protein synthase, mitochondrial electron transport chain (miETC)-related genes cytochrome c oxidase subunit (COX1), and AOX1c, as well as SA biosynthesis-related gene isochorismate synthase (ICS)

Summary

Introduction

Plants growing in diverse environments are constantly challenged by a wide range of microbial pathogens and herbivorous insects that often result in growth inhibition and crop yield losses, leading to a significant risk to global agriculture. Many studies have suggested that leaf respiration is one of the most important metabolic processes in immune response (Colombatti et al, 2014). Plants have acquired a sophisticated immune system to mitigate the adverse effects of pathogen attack, i.e., effector-triggered immunity (ETI) and pattern-triggered immunity (PTI). ETI usually occurs in incompatible plant– pathogen interactions, in which plant Resistance (R) proteins detect the presence of avirulent pathogen effectors that are delivered inside plant cells (Jones and Dangl, 2006). PTI often occurs in the compatible plant–pathogen interaction, which relies on the recognition of pathogen/damage-associated molecular patterns by cell surface pattern recognition receptors (Couto and Zipfel, 2016). For the susceptible host plants, PTI effectively repels most virulent pathogens, contributing to basal immunity (Couto and Zipfel, 2016)

Methods

Results

Conclusion