Variation and inheritance of the XanthomonasraxX‐raxSTAB gene cluster required for activation of XA21‐mediated immunity

Abstract

Summary The rice XA21‐mediated immune response is activated on recognition of the RaxX peptide produced by the bacterium Xanthomonas oryzae pv. oryzae ( Xoo ). The 60‐residue RaxX precursor is post‐translationally modified to form a sulfated tyrosine peptide that shares sequence and functional similarity with the plant sulfated tyrosine (PSY) peptide hormones. The 5‐kb raxX‐raxSTAB gene cluster of Xoo encodes RaxX, the RaxST tyrosylprotein sulfotransferase, and the RaxA and RaxB components of a predicted type I secretion system. To assess raxX‐raxSTAB gene cluster evolution and to determine its phylogenetic distribution, we first identified rax gene homologues in other genomes. We detected the complete raxX‐raxSTAB gene cluster only in Xanthomonas spp., in five distinct lineages in addition to X. oryzae . The phylogenetic distribution of the raxX‐raxSTAB gene cluster is consistent with the occurrence of multiple lateral (horizontal) gene transfer events during Xanthomonas speciation. RaxX natural variants contain a restricted set of missense substitutions, as expected if selection acts to maintain peptide hormone‐like function. Indeed, eight RaxX variants tested all failed to activate the XA21‐mediated immune response, yet retained peptide hormone activity. Together, these observations support the hypothesis that the XA21 receptor evolved specifically to recognize Xoo RaxX.

The Xanthomonas RaxH-RaxR Two-Component Regulatory System Is Orthologous to the Zinc-Responsive Pseudomonas ColS-ColR System

“…The raxX-raxSTAB gene cluster apparently has been gained and lost multiple times during Xanthomonas speciation [ 8 ]. In all cases identified [ 8 ], this cluster is located in the same genome neighborhood, between the gcvP gene encoding a subunit of glycine dehydrogenase [ 43 ] on one side, and the minCDE operon encoding proteins required for cell division [ 44 ] on the other ( Figure 1 ). The gene denoted as “mfsX” is predicted to encode a major facilitator subfamily permease [ 8 ].…”

“…In all cases identified [ 8 ], this cluster is located in the same genome neighborhood, between the gcvP gene encoding a subunit of glycine dehydrogenase [ 43 ] on one side, and the minCDE operon encoding proteins required for cell division [ 44 ] on the other ( Figure 1 ). The gene denoted as “mfsX” is predicted to encode a major facilitator subfamily permease [ 8 ]. The eptA , lpxE , and arnT genes are predicted to encode enzymes involved in lipid A remodeling, as described below ( Section 3.3 , Section 3.4 and Section 3.5 ).…”

“…RaxX is a secreted sulfopeptide similar to the plant PSY sulfopeptide growth hormone [ 6 , 7 ], and is synthesized by some but not all Xanthomonas spp. [ 8 ].…”

Recent advances in developing disease resistance in plants

“…Use of the PRR gene Xa21 continues to be expanded. Xa21 of rice produces a receptor kinase that recognizes a small sulfonated peptide (RaxX) synthesized by Xoo and some related species and confers resistance to bacterial blight of rice 10, 11 . The effectiveness of Xa21 is limited to diseases caused by Xanthomonas species that produce RaxX 10 .…”

“…Xa21 of rice produces a receptor kinase that recognizes a small sulfonated peptide (RaxX) synthesized by Xoo and some related species and confers resistance to bacterial blight of rice 10, 11 . The effectiveness of Xa21 is limited to diseases caused by Xanthomonas species that produce RaxX 10 . Fortunately, transfer of Xa21 to banana provides resistance to bacterial wilt, which is threatening banana and enset production in east Africa, because the pathogen, Xanthomonas vasicola pv.…”