WHOP, a Genomic Region Associated With Woody Hosts in thePseudomonas syringaeComplex Contributes to the Virulence and Fitness ofPseudomonas savastanoipv.savastanoiin Olive Plants

Abstract

Bacteria from the Pseudomonas syringae complex belonging to phylogroups 1 and 3 (PG1 and PG3, respectively) isolated from woody hosts share a genomic region herein referred to as WHOP (from woody host and Pseudomonas spp.), which is absent in strains infecting herbaceous organs. In this work, we show that this region is also encoded in P. syringae pv. actinidifoliorum (PG1) and six additional members of PG3, namely, Pseudomonas savastanoi pv. retacarpa, three P. syringae pathovars, Pseudomonas meliae, and Pseudomonas amygdali. Partial conservation of the WHOP occurs in only a few PG2 strains. In P. savastanoi pv. savastanoi NCPPB 3335, the WHOP region is organized into four operons and three independently transcribed genes. While the antABC and catBCA operons mediate the catabolism of anthranilate and catechol, respectively, the ipoABC operon confers oxygenase activity to aromatic compounds. The deletion of antABC, catBCA, or ipoABC in NCPPB 3335 caused reduced virulence in woody olive plants without affecting knot formation in nonwoody plants; catBCA, dhoAB, and PSA3335_3206 (encoding a putative aerotaxis receptor) were also required for the full fitness of this strain exclusively in woody olive plants. Overall, this study sheds light on the evolution and adaptation of bacteria from the P. syringae complex to woody hosts and highlights the enzymatic activities encoded within the WHOP region that are essential for this process.

Comparative genomics of Pseudomonas syringae reveals convergent gene gain and loss associated with specialization onto cherry (Prunus avium)

“…A cluster of genes named WHOP (woody hosts and Pseudomonas) thought to be involved in aromatic compound (lignin) degradation (Caballo-Ponce et al, 2016) was present in Psm R1 and R2, whilst P. syringae pv avii and most Pss strains contained no WHOP homologues. Two cherry P2d strains (syr2339 and syr7924) did, however, possess the catechol catBCA cluster.…”

Comparative genomics ofPseudomonas syringaereveals convergent gene gain and loss associated with specialisation onto cherry (Prunus avium)

“…A cluster of genes named WHOP ( w oody h osts and P seudomonas ) thought to be involved in aromatic compound (lignin) degradation (Caballo-Ponce et al ., 2016) was present in Psm R1 and R2, whilst P.s pv. avii and most Pss strains contained no WHOP homologues.…”

Knots Untie: Molecular Determinants Involved in Knot Formation Induced by Pseudomonas savastanoi in Woody Hosts

“…aesculi isolated from horse chestnut (Green et al, 2010), and found to be absent in the genomes of P. syringae strains infecting herbaceous hosts. Subsequent genomic analyses determined that the presence of this cluster, currently referred to as the WHOP region (from w oody ho st and P seudomonas ) (Caballo-Ponce et al, 2017), is a feature exclusive to strains of phylogroups (PGs) 1 and 3 of the P. syringae complex isolated from woody organs of woody hosts, suggesting a specific role of this region in bacterial adaptation to woody tissues (Ramos et al, 2012; Bartoli et al, 2015; Nowell et al, 2016; Caballo-Ponce et al, 2017). In agreement with this hypothesis, the ability of several strains of the P. syringae complex, including Psv strains NCPPB 3335 and PseNe107, to grow endophytically in kiwi trees has been associated with codification of the cat operon (Bartoli et al, 2015).…”

“…Genes in this region are organized into four different operons ( catBCA , antABC , ipoABC , and dhoAB ) and three independently transcribed genes ( antR , benR and a gene encoding a putative aerotaxis receptor). Although no function has yet been attributed to the dhoAB operon, the involvement of the Psv NCPPB 3335 antABC and catBCA operons in the catabolism of anthranilic acid and catechol, respectively, has been confirmed; additionally, the ipoABC operon was associated to an oxygenase activity acting on aromatic compounds (Caballo-Ponce et al, 2017). Nonetheless, the most intriguing conclusions of this work are derived from the role of the WHOP region during bacterial interactions with olive plants.…”

“…In fact, many lignin-related aromatic compounds are funneled into catechol and protocatechuate prior to their assimilation through the β-ketoadipate pathway (Harwood and Parales, 1996). While the machinery for protocatechuate degradation is widespread among P. syringae pathovars, the degradation of catechol into Krebs cycle intermediaries is generally restricted to strains of the P. syringae complex carrying the WHOP region (Caballo-Ponce et al, 2017). Hence, activities encoded in this region might provide additional pathways for the degradation of specific lignin-related compounds, allowing for the colonization of woody tissues by P. savastanoi and other strains of the P. syringae complex.…”