An effector from the Huanglongbing-associated pathogen targets citrus proteases

Clark, Kelley; Franco, Jessica; Schwizer, Simon; Pang, Zhe; Hawara, Eva; Liebrand, T.W.H.; Pagliaccia, Deborah; Zeng, Liping; Gurung, Fatta B.; Wang, Pengcheng; Shi, Jinxia; Wang, Yinsheng; Ancona, Veronica; Hoorn, Renier A. L. van der; Wang, Nian; Coaker, Gitta; Ma, Wenbo

doi:10.1038/s41467-018-04140-9

Cited by 141 publications

(136 citation statements)

References 62 publications

(92 reference statements)

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“…SDEs of Las have been explored to understand virulence, survival, and detection (Prasad et al , ; Pagliaccia et al , ; Shi et al , ). Las SDE1 targets citrus papain‐like cysteine proteases, which are induced during infection and known to be plant immune regulators (Clark et al , ). SDE1 also induces starch formation and chlorosis after transient expression in Nicotiana benthamiana (Pitino et al , ).…”

Section: Discussionmentioning

confidence: 99%

“…Unlike most gram‐negative bacteria, Las lacks the type III secretion system, but possesses the general Sec secretion system, which is capable of secreting effectors directly outside bacterial cells (Sugio et al , ). Sec translocon‐dependent effectors (SDEs) are among the most likely Las virulence components (Pagliaccia, et al , ; Clark et al , ). However, the host targets of Las SDEs remain relatively unexplored.…”

Section: Introductionmentioning

confidence: 99%

“…However, the host targets of Las SDEs remain relatively unexplored. One Las SDE, SDE1 (CLIBASIA_05315), is primarily expressed in citrus and acts to inhibit defence‐induced host papain‐like cysteine protease activity (Pagliaccia, et al , ; Clark et al , ).…”

Section: Introductionmentioning

confidence: 99%

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Genome‐wide analyses of Liberibacter species provides insights into evolution, phylogenetic relationships, and virulence factors

Thapa

Francesco

Trinh

et al. 2020

Molecular Plant Pathology

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Candidatus Liberibacter' species are insect-transmitted, phloem-limited α-Proteobacteria in the order of Rhizobiales. The citrus industry is facing significant challenges due to huanglongbing, associated with infection from 'Candidatus Liberibacter asiaticus' (Las). In order to gain greater insight into 'Ca. Liberibacter' biology and genetic diversity, we have performed genome sequencing and comparative analyses of diverse 'Ca. Liberibacter' species, including those that can infect citrus. Our phylogenetic analysis differentiates 'Ca. Liberibacter' species and Rhizobiales in separate clades and suggests stepwise evolution from a common ancestor splitting first into nonpathogenic Liberibacter crescens followed by diversification of pathogenic 'Ca. Liberibacter' species. Further analysis of Las genomes from different geographical locations revealed diversity among isolates from the United States. Our phylogenetic study also indicates multiple Las introduction events in California and spread of the pathogen from Florida to Texas. Texan Las isolates were closely related, while Florida and Asian isolates exhibited the most genetic variation. We have identified conserved Sec translocon (SEC)-dependent effectors likely involved in bacterial survival and virulence of Las and analysed their expression in their plant host (citrus) and insect vector (Diaphorina citri). Individual SEC-dependent effectors exhibited differential expression patterns between host and vector, indicating that Las uses its effector repertoire to differentially modulate diverse organisms. Collectively, this work provides insights into the evolution of 'Ca. Liberibacter' species, the introduction of Las in the United States and identifies promising Las targets for disease management. K E Y W O R D S 'Candidatus Liberibacter' sp., citrus greening disease, HLB, huanglongbing, phylogenomics, SEC effector | 717 THAPA eT Al.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Genome‐wide analyses of Liberibacter species provides insights into evolution, phylogenetic relationships, and virulence factors

Thapa

Francesco

Trinh

et al. 2020

Molecular Plant Pathology

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“…Symptoms of infected trees include leaf mottling, deformed/discolored fruits, premature fruit drop, and premature mortality [2]. It has been suggested that CLas encoded proteins have an inhibitory effect in plant defenses [3,4], but a comprehensive mechanism of infection is still lacking. No effective disease management practice is currently available.…”

Section: Introductionmentioning

confidence: 99%

Functional and comparative genomic analysis of integrated prophage-like sequences inCandidatus Liberibacter asiaticus

Dominguez-Mirazo

Jin

Weitz

2019

Preprint

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Huanglongbing (HLB; yellow shoot disease) is a severe worldwide infectious disease for citrus family plants. The pathogen Candidatus Liberibacter asiaticus (CLas) is an alphaproteobacterium of the Rhizobiaceae family that has been identified as the cause. The virulence of CLas has been attributed, in part, to prophage encoded genes. Prophage and prophage like elements have been identified in 12 of the 15 CLas available genomes, and are classified into three prophage types. Here, we re-examined all 15 CLas genomes using a de novo prediction approach and expanded the number of prophage like elements from 16 to 33. Further, we find that all CLas contain at least one prophage-like sequence. Comparative analysis reveals a prevalent, albeit previously unknown, prophage-like sequence type that is a remnant of an integrated prophage. Notably, this remnant prophage is found in the Ishi-1 CLas strain that had previously been reported as lacking prophages. Our findings provide both a resource and new insights into the evolutionary relationship between phage and CLas pathogenicity.

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“…In addition, P. infestans secretes Kazal-like serine protease inhibitors, including the EPI1 and EPI10 proteins that inhibit tomato subtilase P69B(Tian et al, 2004; Tian et al, 2005). More recently, a study on the pathogenicity of Huanglongbing uncovered the Candidatus Liberibacter asiaticus effector SDE1 that directly interacts with and inhibits citrus PLCP activity(Clark et al, 2018). In another case, the cyst nematode Heterodera schachtii effector protein 4E02 repurposes a PLCP from its role in defense by targeting it to distinct plant cell compartments without inhibibiting its activity(Pogorelko et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Cleavage of a pathogen apoplastic protein by plant subtilases activates immunity

Wang

Xing

Wang

et al. 2019

Preprint

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19The plant apoplast is a harsh environment in which hydrolytic enzymes, 20 especially proteases, accumulate during pathogen infection. However, the 21 defense functions of most apoplastic proteases remains largely elusive. Here, we 22 show that a newly identified small cysteine-rich secreted protein PC2 from the 23 potato late blight pathogen Phytophthora infestans induces immunity in Solanum 24 plant species only after cleavage by plant apoplastic subtilisin-like proteases, 25 such as tomato P69B. A minimal 61-amino-acid core peptide carrying two key 26 cysteines and widely conserved among most oomycete species is sufficient for 27 2 PC2 activity. Kazal-like protease inhibitors, such as EPI1 produced by P. 28 infestans can prevent PC2 cleavage and dampen PC2 elicited host immunity. 29 This study reveals that cleavage of pathogen proteins to release immunogenic 30 peptides is an important function of apoplastic proteases but that pathogens 31 interfere with these functions using protease inhibitor effectors. 32 83 colonization, adapted microbial pathogens deliver protease inhibitors into the 84 host apoplast to counteract host defense. For example, fungal apoplastic effector 85 Pit2 secreted by U. maydis inhibits a set of apoplastic maize cysteine proteases 86 implicated in maize defense and contributes to the virulence of U. maydis in 87 4 maize(Mueller et al., 2013; Misas Villamil et al., 2019). In Phytophthora, a well-88 characterized group of intercellular proteins are the extracellular cystatin-like 89 protease inhibitors (EPIC). P. infestans EPIC1 binds to tomato PLCP Rcr3 and 90 C14 and inhibits their activity in the tomato apoplast(Kaschani et al., 2010). 91EPIC2B is a more robust cysteine protease inhibitor with stronger inhibitory 92 activity against Rcr3 and Pip1(Dong et al., 2014). Beside Phytophthora EPIC2B 93 and fungal Avr2, Gr-Vap1 from cyst nematode and Cip1 from Pseudomonas 94 bacteria pathogen also target these tomato proteases (Misas Villamil et al., 2019), 95 indicating that different pathogens have independently evolved divergent 96 effectors to inhibit plant protease during co-evolution. In addition, P. infestans 97 secretes Kazal-like serine protease inhibitors, including the EPI1 and EPI10 98 proteins that inhibit tomato subtilase P69B (Tian et al., 2004; Tian et al., 2005). 99More recently, a study on the pathogenicity of Huanglongbing uncovered the 100 Candidatus Liberibacter asiaticus effector SDE1 that directly interacts with and 101 inhibits citrus PLCP activity (Clark et al., 2018). In another case, the cyst 102 nematode Heterodera schachtii effector protein 4E02 repurposes a PLCP from 103 its role in defense by targeting it to distinct plant cell compartments without 104 inhibibiting its activity (Pogorelko et al., 2019). These studies illustrate a 105 concerted interaction between the host proteases and the pathogen protease 106 inhibitors, which dictates the success of pathogen colonization. 107

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An effector from the Huanglongbing-associated pathogen targets citrus proteases

Cited by 141 publications

References 62 publications

Genome‐wide analyses of Liberibacter species provides insights into evolution, phylogenetic relationships, and virulence factors

Genome‐wide analyses of Liberibacter species provides insights into evolution, phylogenetic relationships, and virulence factors

Functional and comparative genomic analysis of integrated prophage-like sequences inCandidatus Liberibacter asiaticus

Cleavage of a pathogen apoplastic protein by plant subtilases activates immunity

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