Identification of Autophagy-Related Genes in the Potato Psyllid, Bactericera cockerelli and Their Expression Profile in Response to 'Candidatus Liberibacter Solanacearum' in the Gut.

Xiao-Tian Tang,Cecilia Tamborindeguy

doi:10.3390/insects12121073

Abstract

Simple SummaryIn North America, the bacterial plant pathogen ‘Candidatus Liberibacter solanacearum’ (Lso) infects solanaceous plants. Currently, Lso haplotypes, LsoA and LsoB are transmitted by potato psyllid, Bactericera cockerelli (Šulc). Because these bacteria are transmitted in a circulative and persistent manner, the gut of the psyllid is the first organ they encounter and could be a barrier to its transmission. Therefore, it is important to understand the molecular mechanisms involved in Lso acquisition and transmission. This study explored if an autophagic response was triggered in response to LsoA and/or LsoB in the gut of the adult potato psyllid. The results showed that Lso may induce the autophagic response in the adult psyllid gut since the majority of autophagy-related genes (ATGs) are sensitive and responsive to the exposure or infection of both LsoA and LsoB. Therefore, this study represents a stepping-stone towards understanding the molecular mechanisms involved in Lso transmission.Autophagy, also known as type II programmed cell death, is a cellular mechanism of “self-eating”. Autophagy plays an important role against pathogen infection in numerous organisms. Recently, it has been demonstrated that autophagy can be activated and even manipulated by plant viruses to facilitate their transmission within insect vectors. However, little is known about the role of autophagy in the interactions of insect vectors with plant bacterial pathogens. ‘Candidatus Liberibacter solanacearum’ (Lso) is a phloem-limited Gram-negative bacterium that infects crops worldwide. Two Lso haplotypes, LsoA and LsoB, are transmitted by the potato psyllid, Bactericera cockerelli and cause damaging diseases in solanaceous plants (e.g., zebra chip in potatoes). Both LsoA and LsoB are transmitted by the potato psyllid in a persistent circulative manner: they colonize and replicate within psyllid tissues. Following acquisition, the gut is the first organ Lso encounters and could be a barrier for transmission. In this study, we annotated autophagy-related genes (ATGs) from the potato psyllid transcriptome and evaluated their expression in response to Lso infection at the gut interface. In total, 19 ATGs belonging to 17 different families were identified. The comprehensive expression profile analysis revealed that the majority of the ATGs were regulated in the psyllid gut following the exposure or infection to each Lso haplotype, LsoA and LsoB, suggesting a potential role of autophagy in response to Lso at the psyllid gut interface.

Highlights

With the exception of ATG4a, at least one putative homolog to the Drosophila autophagy-related genes (ATGs) was identified in the B. cockerelli transcriptome; those included serine/threonine protein kinase ULK2 (BcATG1), BcATG2-BcATG5, Beclin1 (BcATG6), BcATG7, gamma-aminobutyric acid receptor-associated protein (BcATG8), BcATG9, BcATG10, BcATG12, BcATG13, beclin 1-associated autophagy-related key regulator (BcATG14), BcATG16, RB1-inducible coiled-coil protein 1-like (BcATG17), WD repeat domain phosphoinositide-interacting proteins (BcATG18), and BcATG101
Take S. flexneri for example, after bacterial uptake into host cells, the bacterial peptidoglycans can be detected by nucleotide-binding oligomerization domain (NOD)-like receptors (NLRs), which can further interact with Atg16L1 and recruit other autophagy proteins to initiate autophagosome biogenesis in response to bacterial invasion [49]
We annotated autophagy-related genes in the potato psyllid and we evaluated their expression in the gut following Liberibacter solanacearum’ (Lso) exposure or infection

Summary

Introduction

Autophagy, which means “self-eating”, is a conserved cellular degradation process that serves to deliver cytoplasmic proteins and organelles to lysosomes for degradation [1]. It plays important roles in many biological processes, such as maintaining homeostasis and preventing nutritional and metabolic-mediated stresses in eukaryotic organisms ranging from yeast to insects and mammals [2]. Autophagy is an important component in the innate immune defense against infection by viral, bacterial, and fungal pathogens in animals [3]. In the last two decades, a series of autophagy-related genes (ATGs) have been characterized from lower (e.g., yeast) to higher eukaryotes (e.g., mammals and insects) [4,5,6]

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