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Xanthomonas diversity, virulence and plant–pathogen interactions

Abstract

Xanthomonas spp. encompass a wide range of plant pathogens that use numerous virulence factors for pathogenicity and fitness in plant hosts. In this Review, we examine recent insights into host–pathogen co-evolution, diversity in Xanthomonas populations and host specificity of Xanthomonas spp. that have substantially improved our fundamental understanding of pathogen biology. We emphasize the virulence factors in xanthomonads, such as type III secreted effectors including transcription activator-like effectors, type II secretion systems, diversity resulting in host specificity, evolution of emerging strains, activation of susceptibility genes and strategies of host evasion. We summarize the genomic diversity in several Xanthomonas spp. and implications for disease outbreaks, management strategies and breeding for disease resistance.

Introduction

Xanthomonas is a Gram-negative bacterial genus in the class Gammaproteobacteria, and contains species causing diseases in more than 400 different plant hosts, such as rice, wheat, citrus, tomato, pepper, cabbage, cassava, banana and bean1,2 (Fig. 1). Outbreaks of Xanthomonas diseases have been reported from multiple hosts worldwide3,4. Banana Xanthomonas wilt, which continues to spread in Central and East African countries, has caused major losses to banana production and threatens the livelihood of millions of farmers, who use it as both a food and a cash crop5,6,7. The genus has undergone changes in nomenclature over the past 25 years based on phenotypic and conventional molecular techniques and, more recently, whole-genome sequencing (WGS)8,9,10. The genus currently comprises more than 35 species11 and is subdivided into subspecies or pathovars. Xanthomonads are characterized by a unique yellow pigment, xanthomonadin12, although some strains do not produce this pigment, such as X. axonopodis pv. manihotis, X. campestris pv. mangiferaindicae and X. campestris pv. viticola13,14,15. Overall, studies have shown extensive genomic diversity among Xanthomonas spp. that can colonize unique ecological niches. For example, X. albilineans and X. oryzae pv. oryzae colonize the vascular tissue of sugarcane and rice, respectively, whereas many other Xanthomonas spp. preferentially colonize mesophyll tissue2,16,17. Additionally, comprehensive ecological studies have identified non-pathogenic Xanthomonas strains, which add to the previously estimated diversity in the genus18. Recombination and horizontal gene transfer contribute to the pathogen population structure and diversity across different Xanthomonas pathosystems19,20,21. Several factors, such as the type III secretion system (T3SS) and associated effectors, lipopolysaccharides, adhesins, transcription factors and TonB-dependent receptors, have been identified that influence host specificity and bacterial pathogenicity in several Xanthomonas spp.22,23,24. Among the widely prevalent and studied xanthomonads are pathovars of X. oryzae, causal agents of bacterial blight and leaf streak of rice; Xanthomonas spp. that cause bacterial spot disease in tomato and pepper; citrus canker caused primarily by X. citri pv. citri; and X. arboricola, pathogenic on stone fruits and nuts — therefore, these taxa will be the focus of this Review.

Fig. 1: Xanthomonas spp. in different plant hosts.
figure1

a | X. oryzae causes bacterial blight in rice. This species encompasses two pathovars, oryzae and oryzicola. b | X. campestris pv. musacearum causes banana Xanthomonas wilt, which can lead to extensive oozing. c | X. citri infects citrus and produces unique pustules in the leaf and fruit tissues. d | X. axonopodis pv. mangiferaindicae causes mango black spot disease. e | Four Xanthomonas spp. are associated with bacterial spot disease in tomato and pepper: X. cynarae pv. gardneri, X. euvesicatoria, X. perforans and X. vesicatoria. Part b courtesy of M. M. Shimwela, Tanzania Agricultural Research Institute, Maruku, Tanzania; part c courtesy of A. M. Gochez, National Agricultural Technology Institute, Argentina; all other images provided by authors (F.F.W and J.B.J).

Xanthomonas spp. use the T3SS, encoded by the hrp cluster, to translocate proteins referred to as type III secreted effectors (T3SEs) into plant host cells25,26. Xanthomonas T3SEs are generally called Xops (Xanthomonas outer proteins), except for AvrBs1, AvrBs2 and AvrBs3, which are traditionally associated with their respective avirulence phenotype, recognized by corresponding R proteins from hosts, resulting in effector-triggered immunity (ETI)26. Currently, 53 Xop families are known, with an alphabetical nomenclature from XopA to XopBA (Overview of T3SEs in Xanthomonas Resource). These effectors have important roles in host colonization and pathogenicity. Improved genomic databases, population and genome-wide association studies, and machine-learning approaches have improved the identification of Xops and their interactions with the plant hosts, when the phenotype is indistinct27,28. The T3SS contributes significantly towards suppression of host defences and disease progression, and there has been considerable progress in our understanding of the contribution of other pathogenicity factors, such as cell wall-degrading enzymes secreted by the type II secretion system (T2SS), type IV secreted effectors, the type VI secretion system (T6SS) and associated effectors, adhesins, lipopolysaccharides, small RNAs and regulators, such as Rpf, HrpG, HrpX, HpaR, Clp, Zur, FhrR and RsmA29,30,31,32,33,34,35. Not all of these other secretion systems and factors are directly involved in virulence of the pathogen but they can affect pathogen fitness34.

Understanding plant–microorganism interactions within an ecological context has been key in developing new knowledge to enhance overall plant health. Recent studies of Xanthomonas spp. have integrated the host, pathogen and microbial community influencing disease development, making it a model system to study plant pathogenic bacteria. In this Review, we will cover recent insights into Xanthomonas spp. virulence factors, diversity and their evolution. We will highlight the genomic diversity in Xanthomonas spp., examine current understanding in pathogenomics and discuss mechanisms of host evasion.

Xanthomonas genomics and diversity

Starting with the sequencing of two Xanthomonas spp. in the early 2000s (ref.36), there are now more than 1,400 Xanthomonas genomes representing all named Xanthomonas spp. publicly available in the National Center for Biotechnology Information (NCBI) database. A typical Xanthomonas genome is ~5 Mb with a GC content well over 60% and encodes >4,000 genes1,37,38. The exception is X. albilineans, which has a reduced genome of ~3.7 Mb (refs39,40). This species has undergone genome erosion with an estimated loss of more than 500 genes, but the drivers of this gene loss are unclear39,41.

Xanthomonas diversity can be categorized at multiple levels, including genetic diversity within populations and species, and functional or ecological diversity, which describes their roles in plant microbiomes. Our understanding of Xanthomonas diversity is mainly based on population and species-level data, described by analyses of single genes, several housekeeping genes and whole genomes. Recent studies targeting microbial communities have revealed ecologically diverse lineages within Xanthomonas spp. and novel pathogenic and non-pathogenic species.

Population and species diversity

Advances in omics tools have revealed more of the Xanthomonas diversity and identified mechanisms of speciation and evolution42,43. Strains of X. arboricola pv. juglandis are increasingly reported from various parts of Europe and population studies have found unprecedented genetic diversity, with non-pathogenic strains cohabiting with pathogenic strains in several plants18,44,45. Genomic comparisons found that several non-pathogenic strains of X. arboricola and X. cannabis carried only four T3SS-associated regulatory genes (hrpG, hrpX, hpaS and hpaR2) and orthologues of six T3SEs, compared with 24 orthologues found in pathogenic strains45,46.

High genome plasticity has been shown in several Xanthomonas spp., suggesting mechanisms for bacterial adaptability and response to selection. Comparison of bacterial spot-causing xanthomonads in tomato and pepper showed genome-wide recombination of X. perforans with X. euvesicatoria19,47,48. A host-driven population shift was observed in X. oryzae pv. oryzae. Six different groups with distinct genotypic characteristics evolved after introduction of plants with the Xa4 resistance locus in the Philippines49. A total of 386 full-length insertion sequences was found in a single genome of X. oryzae, indicating high genome plasticity of individual strains50. Insertion sequences are reported to have an important role in genome instability and loss of gene function, as exemplified by the insertion sequence-mediated inactivation of the gumM gene, which is involved in xanthan production, and thus abrogated the production of this extracellular polysaccharide in X. oryzae51. Plasmids are another source of genomic variability and Xanthomonas diversity, and a chimeric (hybrid) plasmid was reported in an X. citri pv. citri strain carrying four copies of the same type of effectors52 in a single plasmid53. Similarly, mobile elements including integrative and conjugative elements, which typically function as conjugative transposons, have been reported to carry copper resistance genes in the pathogenic X. arboricola strain CFBP 7179 (ref.18).

Intraspecific diversity and host specialization are apparent in X. citri pv. citri, which exhibits three pathotypes: A, A* and Aw. These three pathotypes have a varying host range: pathotype A has a wide host range, whereas A* only infects Citrus aurantifolia, C. latifolia and C. macrophylla, and Aw affects C. aurantifolia and C. macrophylla54. Aw also induces a hypersensitive response in grapefruit54,55. The effector AvrGf1 found in Aw was identified as a host-limiting factor that determined the hypersensitive response in grapefruit56. Although deletion of this gene in Aw resulted in no hypersensitive response, the mutated strain was unable to grow to levels similar to an A-type strain, thus suggesting the presence of additional host-limiting factor(s) in distinct lineages. A recent WGS study of 95 X. citri pv. citri strains predicted that the diversification of these strains occurred approximately 1,700–5,700 years ago57. This diversification coincides with the spread of citrus cultivars in Asia, much later than the origin of citrus, suggesting that the pathotypes evolved as a result of cross-infection by dispersal rather than by host-driven speciation57. Unlike X. citri pv. citri diversification, a host-driven population shift was observed in X. oryzae pv. oryzae in response to the introduction of resistant plants49.

Diversity in the phytobiome

Comprehensive studies of Xanthomonas diversity and epidemiology should take into account the total microbial population. An analysis of the leaf microbiomes of 3,024 rice accessions adapted to a wide variety of agro-ecosystems in China and Philippines, two major rice production areas, found that the leaf microbiome converged to a few central taxa that strongly regulated the microbial networks58. Xanthomonas was among the most abundant genera within these microbiomes. Another study investigated the seed microbiomes of five genotypes of rice and found that Xanthomonas was one of the abundant genera shared by all of the genotypes59, indicating that they form part of the major core of endophytic bacteria. However, the role of Xanthomonas spp. as dominant endophytes in healthy, asymptomatic rice seeds is not well understood. This type of study begins to unravel the ecological roles of Xanthomonas spp. within the host microbiome (Box 1).

Virulence mechanisms

Evolution of Xanthomonas-associated secretion systems

WGS of diverse Xanthomonas spp. enabled studying the evolution of the Xanthomonas core genome. Phylogenomic analysis of the core genome indicates two major groups within Xanthomonas, and at least five clades within group 2 (Fig. 2). WGS has also provided insights into the evolution of secretion systems, their associated virulence factors and their ancestral acquisition patterns (Fig. 2). The T3SS cluster, also known as the Hrp (hypersensitive response and pathogenicity) cluster, which belongs to the Hrp2 family in the genus Xanthomonas, has been extensively studied. For all group 2 species except X. campestris, acquisition of the Hrp2 cluster occurred in their common ancestor60. X. campestris pv. campestris independently acquired Hrp2, as suggested by the chromosomal location of its T3SS cluster, which differs from the other group 2 species46. A different genetic organization, different genomic content and high divergence at the sequence level of the Hrp2 cluster in group 1 species compared with group 2 species indicated independent acquisition in group 1 (ref.60). Some species and strains that are scattered throughout the phylogenetic tree seem to have lost the Hrp2 cluster. Gene flow in the Hrp2 cluster was observed between X. arboricola strains belonging to clade A and X. dyei and X. hortorum60.

Fig. 2: Diversity of Xanthomonas spp. and lineages and their virulence genes.
figure2

We determined the phylogenetic distribution of Xanthomonas spp. based on the core alignment of 198,114 nucleotide sequences using the Roary pipeline171. Whole-genome sequences of type strains or completely sequenced genomes representing the Xanthomonas spp. available in the National Center for Biotechnology Information (NCBI) database were used for phylogenetic reconstruction. The presence of virulence-associated secretion systems is shown. The xps type II secretion system (T2SS) is conserved in all Xanthomonas spp. The type III secretion system (T3SS) is found in most strains, except X. maliensis and X. sacchari. X. hyacinthi, X. theicola and X. albilineans have an atypical T3SS. Of the group 1 strains, only X. translucens carries the full T3SS. X. pisi and X. dyei have more than one core gene of the T3SS. T6SS, type VI secretion system.

Although the T3SS is considered the primary secretion system responsible for virulence, the contribution of other secretion systems, including the T2SS and T6SS, towards pathogenesis or overall pathogen fitness has been shown in X. euvesicatoria, X. citri pv. citri and X. oryzae pv. oryzae30,61,62,63. These two systems have been implicated in the secretion of several cell wall-degrading enzymes. The T2SS Xps cluster is conserved in the Xanthomonas genus. Furthermore, the T2SS Xcs cluster is present in all clade C, D and E strains and in most clade A and B strains, but is absent from X. populi, X. fragarie and X. oryzae strains. X. arboricola, X. vasicola, X. oryzae pv. oryzicola and X. bromi had partial Xcs clusters. The Xcs cluster is absent from group 1 strains, with the exception of X. translucens (Fig. 2). The T6SS is important for interactions with both prokaryotic and eukaryotic neighbours, including manipulation of virulence in animal pathogens64,65. In plant pathogens, there is little evidence for its direct interaction with the plant hosts but it influences interactions with other members of the plant microbiota35,63. The presence of the T6SS across different clades warrants attention to its role in xanthomonads. Based on the gene content and phylogeny, three different T6SSs are described in Xanthomonas. T6SS-I is present in some of the clade B strains, including X. oryzae, X. vasicola, species belonging to the X. euvesicatoria complex, X. axonopodis and X. phaseoli. X. maliensis is an exception as it has the complete T6SS-I cluster as well as partial clusters of T6SS-II and T6SS-III63,66. T6SS-II is present only in three species surveyed here: X. hortorum, X. oryzae and X. fragarie. T6SS-III is present in clade C, X. euvesicatoria and sister species, X. citri pv. citri and related species, and X. phaseoli from clade B (Fig. 2).

T3SS-dependent Xanthomonas outer proteins

T3SEs modulate host physiology to obtain nutrients, facilitate infection and/or evade host immune responses67. Putative identification of T3SEs has relied on homology-based searches largely driven by phenotypic observations, followed by functional reporter assays to confirm translocation of the candidate effectors into the plant cell68,69. These reporter assays take advantage of our understanding of molecular signals, including secretion and translocation signals found in T3SEs (ref.68). More recently, machine-learning approaches have been developed that rely on multiple criteria for the identification of novel effectors, such as secretion signals at the amino-terminus of T3SEs, amino acid composition, conserved motifs, structural disorder, regulation by HrpX and HrpG, GC content, codon use and homology to known and validated T3SEs (refs27,70). Such a machine-learning approach identified seven novel T3SEs in X. euvesicatoria 85-10 as a representative genome and the method could be used to predict effectors from other Gram-negative bacteria that have a T3SS (ref.27).

T3SEs are integral to Xanthomonas pathogenicity, and are determinants of host specificity and pathogen fitness (Fig. 3). Xanthomonas effectors have evolved to target different components of the pathogen or damage-associated molecular pattern (P/DAMP)-triggered immunity (PTI/DTI) pathway1,71. The T3SEs XopACXcc, XopYXoo, XopAAXoo and XopNXe target receptor-like cytoplasmic kinases, members of the receptor-like kinase superfamily. XopQXoo, XopXXoo, XopZXoo and XopNXoo inhibit DTI72. XopAUXe, a catalytically active protein kinase, promotes disease development by manipulating MAPK signalling through phosphorylation and activation of the immunity-associated MKK2 (ref.73). Examples of effectors that inhibit PTI include XopPXoo, XopLXe and XopSXe74,75. Effectors such as AvrXv4, XopJXe and XopDXe interfere with the host ubiquitin proteasomal system76. XopBXe interferes with vesicle trafficking, interferes with cell wall-bound invertases and prevents sugar-mediated defence signals77. XopDXe, XopDXcc8004, XopJXe and XopAH (also known as AvrXccC) interfere with hormone signalling pathways involved in plant defences or disease susceptibility78. Effectors eliciting ETI have conventionally been identified as avirulence genes, and examples with known direct or indirect targets include XopJ4 (AvrXv4), XopH (AvrBs1.1), XopAG (AvrGf2), AvrXccC and AvrRxv26,79. T3SEs also function as ETI suppressors. Examples include AvrBsT, which is involved in suppression of AvrBs1-mediated ETI80, and XopQXe (ref.81).

Fig. 3: Xanthomonas spp. effectors and their modes of action to trigger or suppress host defence responses.
figure3

a | Effectors involved in suppression of pathogen or damage-associated molecular pattern (P/DAMP)-triggered immunity can interact with receptor-like kinases (RLKs) or interfere with downstream signalling pathways. Some effectors can interfere with hormone signalling pathways, cytoskeleton remodelling or sugar-mediated defences during early pathogenesis. b | Avirulence genes and their products interact with specific host components in the cytoplasm, nucleus or chloroplast and trigger effector-triggered immunity (ETI). Xanthomonas spp. have evolved some effectors that can suppress the ETI response by direct or indirect interaction with the ETI components, or by modulating hormone signalling pathways. These effectors contribute to effector-triggered susceptibility. Please see Supplementary Box 1 for details on functions of individual effectors. CWDE, cell wall-degrading enzyme; P, phosphorylation; ROS, reactive oxygen species; T3SE, type III secreted effector; T3SS, type III secretion system; Ub, ubiquitination; WT, wild type; Xop, Xanthomonas outer protein.

Several functional methods exist to characterize effectors in terms of their direct or indirect molecular targets in the host and their mode of action69,82,83, including mutagenesis of the effector(s) and host interactor, Agrobacterium tumefaciens-mediated transient expression, yeast two-hybrid assays and pull-down assays. Two additional approaches, the protoplast transient expression assay84 and the recently developed pathogen-free protoplast-based assay in Arabidopsis thaliana85, were used to identify effectors that target specific host signalling pathways. For example, effectors from X. euvesicatoria 85-10 that interfere with PTI signalling mediated by Flg22, a highly conserved PAMP present in flagellin, were identified by expressing them in the attenuated Pseudomonas syringae pv. tomato DC3000∆CEL strain85. Another method used to study Xanthomonas spp. effectors included using yeast as a heterologous system for expression of effectors and identifying effectors that affect cell growth and viability86. Recent technological advances in imaging tools enabled quantitative image-based phenotyping to study spatio-temporal dimensions of disease development for the vascular pathogen of cassava, X. axonopodis pv. manihotis, and to understand the contribution of individual effectors by time-resolved imaging87.

TAL effectors

Xanthomonas spp. have evolved a distinct family of T3SEs known as transcription activation-like effectors (TALEs)52, which increase plasticity in adaption of the bacteria to host plants. They have a rearrangeable repetitive domain that controls the ability to bind promoters of host susceptibility genes in a sequence-specific manner88,89,90. There is an uneven distribution of genes encoding TALEs among Xanthomonas spp. In some Xanthomonas spp., such as X. gardneri, X. campestris36, X. euvesicatoria91 and X. perforans43, TALEs are not found in all strains, whereas TALEs are prevalent in X. oryzae, with X. oryzae pv. oryzicola strain BLS256 carrying a record 27 genes37.

Various TALE-associated susceptibility genes, defined here as host genes associated with some aspect of disease or pathogen population, have been identified. A prominent example of TALEs and their cognate susceptibility are TALEs of X. oryzae pv. oryzae and SWEET genes of rice, which are responsible for a pronounced phenotype in bacterial blight of rice (Box 2). Eight major TALEs are known in X. oryzae pv. oryzae that target one of three SWEET alleles of the clade III SWEET members; host targets that are convergently activated by multiple TALEs are referred to as susceptibility hubs92,93,94. In the absence of SWEET gene expression, bacteria fail to effectively colonize rice leaves. The TALE PthXo1 occurs in a subset of strains in the Asian lineage of X. oryzae pv. oryzae89 and targets SWEET11, a sugar transporter gene that is essential for the early stage of rice grain filling95. Some rice cultivars have a recessive resistance allele (xa13), which interferes with PthXo1 function at the SWEET11 promoter89,96 (Fig. 4). Loss of function at a particular SWEET allele and consequential loss of bacterial virulence can be overcome by the presence of major TALEs that target other SWEET genes97,98. African lineage strains of X. oryzae pv. oryzae have evolved in apparent isolation from Asian lineage strains and have a distinct set of major TALEs that target SWEET14, which encodes a low-affinity sugar transporter93,94,99,100.

Fig. 4: Role of Xanthomonas TALEs in plant susceptibility and resistance.
figure4

a | The repeat regions of the transcription activation-like effectors (TALEs) bind to the effector binding elements (EBEs) in the host and transcribe a host susceptibility gene for pathogenicity92,96. b | Several mechanisms underlie host resistance: (i) a modified EBE (red) avoids TALE binding and, thus, the susceptibility gene is not transcribed, resulting in host resistance96,98; (ii) the host carries resistance instead of a susceptibility gene under control of the promoter targeted by the TALE — this set-up tricks the pathogen into activating transcription of a resistance gene when the TALE binds to the executor EBE, leading to host resistance107,111,172; and (iii) the host uses recognition by nucleotide binding, leucine-rich repeat (NLR) protein of the TALE to trigger ETI107,108,109. c | In response, pathogens have evolved mechanisms to evade host resistance and induce pathogenicity: (i) variable copies of TALEs can bind to different EBEs, transcribing the same susceptibility gene; (ii) Xanthomonas spp. can use modified repeat variable di-residues (RVDs) to bind the modified EBE and the susceptibility gene is successfully transcribed to cause disease173; (iii) Xanthomonas spp. can modify the RVDs to avoid binding to the EBE and activating the executor gene, which leads to host susceptibility174; and (iv) interfering TALEs (iTALEs) lack the activation domain, and thus interfere with the function of NLR proteins109. AAD, acidic activation domain; NLS, nuclear localization signals.

Bacterial leaf streak is a wheat disease caused by X. translucens pv. undulosa, and one of eight genes encoding TALEs in the bacterial genome is associated with lesion length and the specific induction of the gene encoding 9-cis-epoxycarotenoid dioxygenase (NCED), causing a rise in the levels of the phytohormone abscisic acid101. A second TALE gene of X. translucens pv. undulosa with an unknown host target gene has been associated with virulence102. Lateral organ boundaries 1 (CsLOB1), a member of the plant-specific lateral organ boundaries domain (LBD) family of transcription factor genes, is targeted for expression by several TALEs of X. citri pv. citri and X. fuscans pv. aurantifolii, the causal agents of citrus canker103,104. Loss of the ability to induce CsLOB1 either by loss of the relevant TALE or modification of the effector binding site in the CsLOB1 promoter by genome editing leads to loss of the typical canker symptoms103,105,106.

TALE-mediated ETI involving nucleotide binding, leucine-rich repeat (NLR) resistance genes has been identified in tomato and rice107,108,109. Remarkably, the rice NLR gene, Xa1, was identified some time ago but research failed to identify the corresponding elicitor110. XA1, in fact, recognizes several TALEs, and most strains of X. oryzae have several TALEs. However, TALE-triggered resistance by XA1 is masked by sets of truncated TALEs, the iTALEs, which interfere with Xa1 function and occur in most strains of X. oryzae109. For example, the iTALE Tal2h suppresses recognition mediated by rice Xa1. Similar findings have been reported for the NLR gene Xo1 of the American heirloom rice variety Carolina Gold Select40,108. TALE-mediated ETI can also be triggered by host genes that combine an effector binding site with a gene encoding a toxic gene product or a so-called executor gene111 (Fig. 4).

Other factors associated with fitness and virulence

A previous review has discussed in detail virulence factors such as extracellular polysaccharides, lipopolysaccharides, adhesins, substrates of virulence-associated secretion systems, including T1SS and T2SS, and the regulatory network, including RpfC, RpfG, RpfF, RavS, RavR, ColS, ColR, PhoP, PhoQ, Clp, Zur, FhrR, HrpX, HrpG and HpaR, and post-transcriptional control by RsmA34. The importance of small non-coding RNAs has been highlighted recently in X. euvesicatoria, X. campestris pv. campestris and X. oryzae pv. oryzae112. Several functional studies with vascular as well as non-vascular xanthomonads have indicated the importance of a repertoire of cell wall-degrading enzymes for virulence, although effects vary with the pathosystem and some show minimal contribution to overall virulence. Interestingly, cell wall-degrading enzymes, specifically xylanases, are secreted by outer membrane vesicles (OMVs) in X. euvesicatoria113. OMVs have also been called a type zero secretion system114. T3SEs could also be transported through OMVs or function in coordination with them. About half of the X. campestris pv. campestris OMV proteome consisted of virulence-associated proteins115. How these OMVs and associated virulence factors contribute to pathogenesis remains to be explored. Post-translational regulation of HrpG was recently demonstrated, in which stabilization of HrpG relied on host-induced phosphorylation of the ATP-dependent Lon protease116. A novel regulator, designated TfmR (T3SS and fatty acid mechanism regulator), was responsible for the upstream regulation of the T3SS in X. citri pv. citri117. The study also showed that fatty acids can have an important role in metabolic regulation of HrpG and HrpX. A two-component system (TCS), which consists of membrane-bound histidine kinase and a cytosolic response regulator, has an important role in niche adaptation of Xanthomonas spp. In X. citri pv. citri, cyclic di-GMP binds to RavS, which in turn induces phosphotransfer to RavR. The interaction between RavS and RavR, through a series of events, results in modulation of phosphorylation levels of RavS, which in turn is involved in switching between swimming and virulence, confirming the importance of this TCS in regulating lifestyles118. In another X. citri pv. citri strain, proteolysis of the histidine kinase VgrS prevents its autophosphorylation, which in turn promotes osmotolerance119. The histidine kinase PcrK can sense plant-derived stimuli, specifically the hormone cytokinin, which enables X. citri pv. citri to adapt to oxidative stress by regulating downstream genes including TonB-dependent receptor and other virulence-related genes120. Another TCS, involving StoS and SreKRS, regulates carbohydrate metabolism, chemotaxis, synthesis of extracellular polysaccharide and Hrp expression121. This TCS was proposed to contribute to fitness given its advantage in survival of X. oryzae pv. oryzae outside the host and overall adaptation121. XooNet is an in silico platform that has integrated genomic information to improve predictions of regulatory networks involving TCSs associated with virulence in X. oryzae pv. oryzae122. Other secretion systems that have not been discussed here in detail include the type IV secretion system and the T6SS. The type IV secretion system, and its effectors, and the T6SS have been characterized for their role in mediating xanthomonad interactions with the surrounding microbial community29,62,63,123. These interspecies and community level interactions need to be further explored to evaluate their contribution towards overall pathogen fitness.

Virulence evolution

Horizontal gene transfer and mutation of avirulence genes to evade host resistance are among the major factors that influence the evolution of virulence in Xanthomonas spp.22,124,125. As shown with several methods, approximately 5–25% of the genome of Xanthomonas spp. is acquired via recombination126,127.

Comparison between pathogenic and non-pathogenic strains has been useful in elucidating stepwise evolution of pathogenicity and the associated factors. Comparisons of pathogenic and non-pathogenic strains predicted recombination-driven species diversification and host expansion in X. arboricola21. A distinct phylogenetic cluster of non-pathogenic strains lacked the hrpG and hrpX genes essential for regulation of the T3SS (ref.46). Acquisition and positive selection of several pathogenicity-associated genes at different evolutionary phases were shown for X. arboricola46,127. Genetic exchange from genera other than Xanthomonas has also been reported. For example, a recent study found a strain of X. arboricola pv. juglandis carrying a large genomic segment (~95 kb), with genes conferring copper resistance, that resembled genes in Stenotrophomonas maltophilia and Pseudomonas aeruginosa18. Horizontal gene transfer resulting in exchange of virulence factors between Xanthomonas spp. has been reported on several occasions. Although common in several Xanthomonas spp., TALEs were not reported until recently in X. perforans. Interestingly, two TALEs — AvrHah1 and a homologue of AvrBs3, PthXp1 — occurred in distinct lineages, indicating multiple independent TALE acquisitions22. TALEs have been studied extensively in X. oryzae pathovars, which carry a large repertoire of these effectors. Strains of X. oryzae that had been exposed to previously domesticated rice cultivars were shown to carry higher numbers of TALEs than strains not exposed128. Additionally, due to the repetitive region shared among the TALEs, recombination is frequent, thus creating novel TALEs128.

Overall, local host and environmental factors likely drive the emergence and selection of any pathogen, including Xanthomonas spp. Genome-wide recombination between X. perforans and X. euvesicatoria led to intraspecific variability in effector repertoires and virulence factors, with different recombinants in different global production regions48. The X. perforans strains isolated in the early 1990s in Florida, USA, carried bacteriocins that were antagonistic to the endemic X. euvesicatoria population129. By the late 1990s and 2000s, gradual erosion of bacteriocin activity was observed in X. perforans strains as distinct phylogenetic lineages emerged as a result of recombination with other closely related Xanthomonas spp.130. Once introduced to a new population, virulence factors can be selected for or gradually erode from the gene pool. In X. perforans, avrBsT has increased in frequency and has become established in the Florida population, whereas avrXv3 was lost130,131. Similarly, distinct X. oryzae pv. oryzae lineages isolated from the Philippines and shifts in pathogenic races were correlated with change in the cultivars132. The apparent fitness of emerging X. oryzae pv. oryzae races was speculated to be associated with changes in cropping patterns, fertilizer use, environment and overall adaptation of the pathogen49. Among the 30 TALE families described in X. oryzae pv. oryzae strains isolated from the Philippines, diversification was observed only after the lineage formation and likely during host adaptation132. These findings illustrate the dynamics of Xanthomonas spp. diversity and evolution of virulence.

Plant resistance and evasion

Xanthomonas spp. stimulate PTI and ETI. Host immunity is triggered by flagellin, potentially through several PAMP receptors133,134,135,136. FLS2 encodes the flagellin receptor, which recognizes the immunogenic component of flagellin133,137. Host glycosidases, such as β-galactosidase 1, together with host proteases, release immunogenic peptides from flagellin of plant pathogenic bacteria137. However, some variants of flagellin from Xanthomonas spp. fail to trigger an FLS2-dependent response138. Furthermore, flagellin from X. oryzae pv. oryzae fails to elicit an FLS2-dependent response in A. thaliana or a response to a rice FLS2 homologue, whether in rice or transferred to A. thaliana139. Other bacteria also trigger host responses, including LPS, xanthan gum, peptidoglycan, cell wall-degrading enzymes, elongation factor Tu and quorum sensing molecules140,141,142,143,144. Many T3SEs of Xanthomonas spp. suppress PTI72,83,84,85,145,146,147,148,149 (Fig. 3). Basal immunity has also been reported to be suppressed by other extracellular compounds, including the exopolysaccharide xanthan144.

Dominant resistance genes, which comprise the distinct components of ETI, target many species of Xanthomonas. The resistance gene Xa21 has similar functions to the receptor-like kinases involved in PTI150. XA21 is broadly effective against strains of X. oryzae. The receptor recognizes an extracellular, sulfated small peptide called RaxX151. Some other Xanthomonas spp. also produce RaxX152. RaxX can mimic plant peptide hormones and may have a function in virulence151. Several resistance genes are members of the NLR family, including Bs2 (pepper), Bs4 (tomato), Xa1 and Xo1 (rice), and Zar1 (A. thaliana)107,108,110,153,154. Each of these NLRs has cognate effectors in the respective pathogens, which are subject to various evolutionary processes enabling evasion of host ETI; for example, disruption of avirulence gene expression through frameshift mutation, stop codons or transposon insertion130,155. Likewise, several avirulence genes are carried by Xanthomonas spp. on self-transmissible plasmids and may be lost over the course of a single season156. The durability of dominant resistance genes that recognize major pathogen virulence or fitness factors showed mixed results over the years. Disruption of AvrXa7 activity in X. oryzae pv. oryzae strains in response to Xa7 recognition in rice resulted in the loss of avirulence activity, although the pathogen incurred a substantial fitness penalty157. Nevertheless, Xa7 recognition can also be overcome by acquisition of alternate effectors with no Xa7-dependent ETI activity that provides a similar fitness effect89,93,97,98. By contrast, a single amino acid substitution in AvrBs2, which is required for full virulence of numerous Xanthomonas spp., enabled X. euvesicatoria to evade Bs2 recognition in commercial pepper varieties, while maintaining virulence146,149,158,159. Some T3SEs can suppress ETI in specific cases30. The NLRs XA1 and XO1 are triggered by several TALEs, and therefore loss of even one or two TALEs from X. oryzae, which contains upwards of 27 different genes, is problematic. Furthermore, iTALEs, a class of truncated genes encoding TALEs, which were previously considered pseudogenes, can inhibit the recognition by XA1 and XO1 (refs109,160) (Fig. 4).

Host resistance can also occur as recessive resistance. Pepper contains bs5 and bs6, which confer resistance to X. euvesicatoria161,162. Soybean contains the recessive resistance gene rxp, which provides broad resistance against strains of X. axonopodis pv. glycines163. TALE-mediated susceptibility is especially prone to recessive resistance due to DNA polymorphisms that prevent TALE binding to specific DNA sequences89,98,164 (Fig. 4). TALEs function through the transcriptional activation of plant susceptibility genes, which in rice and citrus they are crucial for effective host invasion92. The recessive resistance gene xa5 interferes with TALE function and evasion occurs through strong induction of OsSWEET11 or OsSWEET14, indicating that compatibility depends on expression levels rather than on activation of a specific susceptibility gene165. Recessive resistance in rice that happens due to polymorphism in the promoters of susceptibility genes can be evaded by TALEs with alternative binding sites97,98.

Non-conventional approaches

Understanding of Xanthomonas–host interactions has fuelled the development of disease-resistant hosts through genetic modifications. A notable example is the elongation factor-TU receptor (EFR) in A. thaliana, which recognizes a conserved EF-Tu domain in most bacterial genera134. Transfer of AtEFR from A. thaliana to tomato reduced the severity of bacterial spot disease caused by X. perforans in field conditions166. A second example relates to TALEs that bind specific DNA sequences (effector binding elements (EBEs)). Modifying EBEs so that TALEs can no longer bind can be an effective method for developing resistance. CRISPR–Cas9-mediated citrus canker resistance has been developed in grapefruit and sweet orange through modifications in the effector binding promoter region of CsLOB1106,167. A similar approach has been used to modify three SWEET genes targeted by TALEs from X. oryzae pv. oryzae in rice. EBEs targeted by avrXa7 and pthXo3 were modified in rice using TALE nucleases (TALENs), leading to the loss of susceptibility gene expression and resistance against X. oryzae pv. oryzae strains carrying the two genes168,169. Alternatively, EBEs can be added to the promoters of the resistance genes, which leads to the activation of resistance in the presence of TALEs. Researchers introduced 14 EBEs that match distinct X. citri TALEs into the ProBs314EBE promoter and fused it to the avirulence gene avrGf1, which induces a hypersensitive response in grapefruit and sweet orange170. Using resistance genes from closely related species to target single genes could lead to rapid development of pathogen virulence. Durability and a combination of multiple resistance genes targeting several pathogenicity factors should be considered when developing host resistance.

Conclusions

Xanthomonas spp. use a multitude of virulence factors that interfere with host cellular pathways. Recent studies on Xanthomonas–host interactions have been vital for unlocking mechanisms associated with Xanthomonas spp. pathogenicity, diversity and host specificity. The T3SS and associated Xop effectors are major factors influencing pathogenicity and virulence. Studies have further evaluated the importance of other pathogenicity factors, including T2SS, small RNAs and others. With an improved understanding of dynamics of virulence factors in pathogen populations, we will have a better understanding of Xanthomonas evolution in relation to host/tissue specificity and expansion. Research has evolved to integrate these novel findings when developing host resistance against Xanthomonas spp. Collectively, Xanthomonas spp. have been a model system to understand emerging bacterial plant pathogens and diversity.

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Acknowledgements

The authors acknowledge A. M. Gochez and M. M. Shimwela for the images of Xanthomonas disease symptoms in citrus and banana, respectively.

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The authors contributed equally to all aspects of the article.

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Correspondence to Erica M. Goss or Jeffrey B. Jones.

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Overview of T3SEs in Xanthomonas Resource: http://xanthomonas.org/t3e.html

Supplementary information

Glossary

Vascular tissue

Tissue involved in transporting nutrients and fluids in plants. The primary components include xylem and phloem.

Mesophyll tissue

Leaf tissue between the epidermis layers that carries out photosynthesis.

Recombination

Genetic exchange between bacteria resulting in the incorporation of homologous and non-homologous sequences.

Type III secretion system

(T3SS). A secretion system composed of ~20 proteins that forms a syringe-like structure to deliver bacterial proteins to eukaryotic cells. Also referred to as the injectisome.

Effector-triggered immunity

(ETI). Innate immune response triggered by recognition of the type III translocated effector proteins by host resistance gene products.

Type II secretion system

(T2SS). A secretion system formed by secretin proteins, which form characteristic β-barrels for passage of secreted proteins.

Type VI secretion system

(T6SS). A secretion system that delivers bacterial proteins across a cellular envelope to adjacent target cells. Primarily known for interbacterial antagonism.

Hypersensitive response

A response mechanism found in plant hosts, characterized typically by a rapid cell death to prevent the spread of the pathogen.

Accessions

Groups of related plant material from the same species collected from a specific location. The accessions are collections to capture the diversity in a given plant species.

Pathogen or damage-associated molecular pattern (P/DAMP)-triggered immunity

(PTI/DTI). PTI refers to the immune response in hosts triggered by recognizing patterns associated with pathogen, for example, flagellin or lipopolysaccharide. DTI refers to the host immune response triggered as a result of recognition of cell wall-degradation products that are generated by the action of pathogen-secreted cell wall-degrading enzymes during pathogen invasion. PTI and DTI pathways have a significant overlap in their signalling components.

Receptor-like cytoplasmic kinases

Kinase-mediated signalling proteins that regulate plant cellular activities in response to biotic or abiotic stresses and endogenous extracellular signalling molecules.

Receptor-like kinase superfamily

Transmembrane proteins with versatile amino-terminal extracellular domains and carboxy-terminal intracellular kinases. They control a wide range of physiological responses in plants and belong to one of the largest gene families in the Arabidopsis thaliana genome, with more than 600 members.

MAPK

Protein kinases involved in regulating cellular responses to an extensive array of stimuli, including mitogens, heat shock and stress. Specific to serine and threonine amino acids.

Protoplast

The entire cell excluding the cell wall.

SWEET genes

Sugar will eventually be exported transporter (SWEET) genes encode membrane proteins with diverse function, typically facilitating sucrose and glucose efflux.

Recessive resistance

Resistance conferred by recessive allele of a gene in a plant host. The term is also used to refer to resistance conferred by mutation in disease-susceptibility genes.

Abscisic acid

A plant hormone with numerous functions in the plant developmental process, including dormancy and stress response.

Nucleotide binding, leucine-rich repeat (NLR) resistance genes

Resistance genes named after their characteristic nucleotide binding and leucine-rich repeat domains.

Two-component system

(TCS). Mediators of signal transduction in bacteria to detect the surrounding changes and relay the signal for modulating gene expression.

Pathogenic races

Groups of strains that belong to the same or closely related bacterial species, characterized by differential responses (compatible or incompatible reaction) on an array of hosts.

Dominant resistance

Resistance conferred by a single dominant resistance gene in plant hosts.

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Timilsina, S., Potnis, N., Newberry, E.A. et al. Xanthomonas diversity, virulence and plant–pathogen interactions. Nat Rev Microbiol 18, 415–427 (2020). https://doi.org/10.1038/s41579-020-0361-8

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