Abstract

The gram-negative bacterial genus Liberibacter includes economically important pathogens, such as ‘Candidatus Liberibacter asiaticus’ that cause citrus greening disease (or Huanglongbing, HLB) and ‘Ca. Liberibacter solanacearum’ (Lso) that cause zebra chip disease in potato. Liberibacter pathogens are fastidious bacteria transmitted by psyllids. Pathogen manipulation of the host’ and vector’s immune system for successful colonization is hypothesized to be achieved by Sec translocon-dependent effectors (SDE). In previous work, we identified hypothetical protein effector 1 (HPE1), an SDE from Lso, that acts as a suppressor of the plant’s effector-triggered immunity (ETI)-like response. In this study, using a yeast two-hybrid system, we identify binding interactions between tomato RAD23 proteins and HPE1. We further show that HPE1 interacts with RAD23 in both nuclear and cytoplasmic compartments in planta. Immunoblot assays show that HPE1 is not ubiquitinated in the plant cell, but rather the expression of HPE1 induced the accumulation of other ubiquitinated proteins. A similar accumulation of ubiquitinated proteins is also observed in Lso infected tomato plants. Finally, earlier colonization and symptom development following Lso haplotype B infection are observed in HPE1 overexpressing plants compared to wild-type plants. Overall, our results suggest that HPE1 plays a role in virulence in Lso pathogenesis, possibly by perturbing the ubiquitin-proteasome system via direct interaction with the ubiquitin-like domain of RAD23 proteins.

Highlights

  • The bacterial genus Liberibacter includes several economically important pathogens, such as ‘Candidatus Liberibacter asiaticus’ (Las), ‘Ca. L. americanus’, and ‘Ca. L. africanus’ that cause citrus greening disease, as well as ‘Ca. L. solanacearum’ (Lso), the causal agent of Zebra chip disease in potato and other diseases

  • After first 45 amino acids oscfrSeeonliyncg0u2pgt0o8258×4100(6Finigduivrideu1aAl y)e.aSstoclylocn0e2s,gw0e85id8e4n0tifiisedR1A6 Dclo2n3ees,haavminegmthbreeer of the RADIATION SENSITIVE23 (RAD23) protdeififnerenfat min-iflryamtehinastertinsecqluuednecess. tOhfrteheeseo, 1th4 eclronetos mhaadtiodenptircoaltecoindisn,g sReAquDen2c3esa, (Solyc03g117780), RAwhDic2h3wce(rSeofelrytco0h4egre0a0s7H1P2E01),InatenrdactRinAg CDlo2n3ed1 ((HSIoCl1y)c. 0B2LAg0ST6x3a1n3a0ly)s[is2a5g]a.inHstItChe1 encodes the N-termittnoomathlaetuofibrresiftqe4rue5niatcmiengi-nelonikoamecideds(oSoomflaSnaouliymnc0l(y2Ucgo0pB8eLr5s8i)c4u0om(fFiiRTgAuAGreD2.142A)3)re.evS(oeFalyliecgd0u2tghr0ae8t 5H18BI4C0)1,iscaoRrdAreoDspm2o3nae,dinas that is assumed to inmteermabcetrwofitthhe RthAeD236Sproptreointefaamsiolymtheatcionmclupdleesxth[r2ee6]o.thBeerctoamuasteo RprAoteDin2s3, RsAeDrv23eas as the principal shut(Stloelypc0r3ogt1e1i7n78f0o),rRAuDbi2q3cu(iStoinlyact0e4dg00t7a1r2g0e),tasntdoR2A6DS23pdr(oSotelyacs0o2gm06e3,13a0n)d[25i]s

  • The subcellular localization of HPE1B and of SlRAD23e were evaluated by Because HPE1B and SlRAD23e colocalized in planta, we investigated the binding of the two proteins by bi-molecule fluorescence complementation (BiFC)

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Summary

Introduction

The bacterial genus Liberibacter includes several economically important pathogens, such as ‘Candidatus Liberibacter asiaticus’ (Las), ‘Ca. L. americanus’, and ‘Ca. L. africanus’ that cause citrus greening disease (or Huanglongbing, HLB), as well as ‘Ca. L. solanacearum’ (Lso), the causal agent of Zebra chip disease in potato and other diseases. Manipulations of the metabolism and immune response by these pathogens have been reported in the infected plant hosts, and insect vectors through multi-omic approaches in the past decade. In response to Liberibacter infections, psyllid vectors show dramatic changes in the expression of genes involved in the citric acid cycle, stress-resistance, and the immune system [10,11]. How these pathogens with simple genomes (~1.2 Mb) manipulate their plant hosts and insect vectors remains unclear

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