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Perez-Quintero, A. L.

Publications and source records attributed to Perez-Quintero, A. L..

5 recordsLinked to original sources

Two domesticated species of rice shaped the population structure of Xanthomonas oryzae pv. oryzae in Africa

African rice (Oryza glaberrima) was independently domesticated in West Africa around 3000 years ago, and has long been intertwined in the history of the region. The gradual replacement of African rice by Asian rice (Oryza sativa), which was introduced when European settlers arrived, has since dominated rice cultivation in Africa. Domesticated rice species are affected by bacterial leaf blight (BLB), which is caused by the pathogen Xanthomonas oryzae pv. oryzae (Xoo). Here we provide evidence that the bacterial leaf blight pathogen in Africa (AfXoo) belongs to a distinct phylogroup from the one circulating in Asia (AsXoo), and has a different evolutionary history. Analysis of 88 AfXoo genomes identified five groups, one of which is a highly diverse population that might have probably given rise to three independent clonal populations based on multiple genetic tests. Tip-dating analysis revealed that the emergence and expansion of AfXoo coincided with the rise and fall of African rice nearly a thousand years ago, and O. sativa served as a bottleneck in the evolution of AfXoo over time. Although the type III effectors (T3E), proteins that are secreted by the pathogen to evade host resistance or seize control of host nutrients, are highly conserved in AfXoo, we observed some variation in effector families. Different evolutionary modifications in the transcription activator-like effectors (TALEs), especially in repeat variable di-residues (RVDs), likely enabled adaptation to both host species. Previous analyses carried out on samples collected in Burkina Faso have shown that there could be more than one TALE repertoire combination in the field, and genome sequencing data revealed potential TALE evolutionary mechanisms that could happen. Our research provides a comprehensive genetic history of bacterial blight in West Africa, and its past and present impact on rice cultivation in the region. Author summaryFor thousands of years, rice cultivation has been an integral part of African agriculture. However, the cultivation of the locally domesticated African rice cultivar (Oryza glaberrima) has been gradually shifted towards Asian rice varieties (Oryza sativa), which has affected the adaptation of the native pathogen population. One of these pathogens is the causal agent of bacterial leaf blight, Xanthomonas oryzae pv. oryzae (Xoo). Here we performed a population genomics approach to understand the evolutionary history and virulence spectrum of African Xoo (AfXoo), a unique phylogroup within the Xanthomonas oryzae species. Our results suggest that AfXoo were first adapted to African rice at least a thousand years ago. The introduction of O. sativa has shaped the recent population dynamics of AfXoo. TALEs are tightly conserved in AfXoo with multiple sequence variations unique to different populations, which could be explained by different evolutionary forces acting upon both domesticated rice. Our results highlight the interplay between crop domestication and cultivation and pathogen evolution.

genomics↗

The emergence of bacterial blight pathogen followed the dispersal pattern of rice in Asia

Crop domestication has a significant effect on the evolutionary trajectory of plant pathogens by providing new ecological niches and abundant resources. The domestication of Asian rice (Oryza sativa) in Asia, approximately 9,000 years ago, might have shaped the genetic makeup of associated microbes into modern threats. In this study, we provide insight into the evolutionary history and dispersal pattern of the rice bacterial blight (BB) pathogen, Xanthomonas oryzae pv. oryzae (Xoo), one of the most destructive rice pathogens in the last century. The analysis of 433 Asian Xoo (AXoo) genomes identified twelve modern populations derived from three ancestral lineages (AXooL). Each population emerged with a unique genetic composition including the combination of pathogenicity factors. Bayesian reconstruction suggests that Xoo lineages emerged alongside O. sativa domestication hotspots and followed the dispersal pattern of rice across the continent. An ancient Xoo lineage (AXooL1) emerged in China and was likely dispersed with japonica rice. A second lineage (AXooL2) which could have turned up from China and spread across India, then evolved due to the domestication and spread of indica rice, and later on expanded eastward of Asia.. We also showed that recombination played a significant role in the emergence of AXooL3, which appeared more recently and might have spread with the rice trading routes. Our study aligns the evolution and dissemination of the phylogroup AXoo with the history of O. sativa, offering valuable insights for the formulation of precise disease management strategies. AUTHOR SUMMARYRice domestication was a crucial step in the development of Asian civilization. However, this process also affected the evolution of an associated pathogen, leading to its emergence as a global threat. Rice bacterial blight (BB), caused by the pathogen Xanthomonas oryzae pv. oryzae (Xoo), has been a scourge in many Asian countries. Using population genomics, we explored the diversity and evolutionary history of Xoo in Asia (AXoo). Here we show that two ancestral pathogen lineages emerged in rice domestication centers (China and India) and dispersed with rice across the continent. More recently, recombination played a crucial role in the appearance of a third lineage that spread through trading activity. This study provides the implications of the adaptation of AXoo in Oryza sativa, and might be valuable in forecasting BB outbreaks.

genomics↗

A pre-loaded and assembled human Ago2-miRISC orchestrates Shigella-induced vacuolar rupture through the targeting of RhoGDIα

The enteroinvasive bacterium Shigella flexneri causes bacillary dysentery. It invades intestinal epithelial cells and forms a bacterium-containing vacuole, which it rapidly ruptures to reach the cytosol. Here, we found that human Argonaute 2 (Ago2), the central component of miRNA-induced silencing complex (miRISC), positively regulates early steps of Shigella infection, including vacuolar rupture. This is consistent with the rapid recruitment of Ago2 at Shigella entry foci. The ability of Ago2 to form an assembled miRISC was found required for vacuolar maturation, while its slicer activity is dispensable for this process. Furthermore, we found that the RhoGTPase inhibitor RhoGDI is targeted by specific miRNAs, pre-loaded in Ago2, which, collectively, accelerate vacuolar rupture. Therefore, a pre-loaded and assembled Ago2-miRISC orchestrates vacuolar maturation by targeting RhoGDI. These findings may have wider implications in the understanding of how stored Ago2-loaded miRNAs control immediate steps of infection, prior to the differential expression of microbe-responsive miRNAs.

molecular biology↗

Plant Small RNA Species Direct Gene Silencing in Pathogenic Bacteria as well as Disease Protection

Extracellular plant small RNAs (sRNAs) and/or double-stranded RNA (dsRNA) precursors act as triggers of RNAi in interacting filamentous pathogens1-7. However, whether any of these extracellular RNA species direct gene silencing in plant-interacting bacteria remains unknown. Here, we show that Arabidopsis transgenic plants expressing sRNAs directed against virulence factors of a Pseudomonas syringae strain, reduce its pathogenesis. This Antibacterial Gene Silencing (AGS) phenomenon is directed by Dicer-Like (DCL)-dependent antibacterial sRNAs, but not cognate dsRNA precursors. Three populations of active extracellular sRNAs were recovered in the apoplast of these transgenic plants. The first one is mainly non-vesicular and associated with proteins, whereas the second one is likely located inside Extracellular Vesicles (EVs). Intriguingly, the third population is unbound to proteins and in a dsRNA form, unraveling a novel class of functional extracellular free sRNAs (efsRNAs). Both Arabidopsis transgene- and genome-derived efsRNAs were retrieved inside bacterial cells. Finally, we show that salicylic acid (SA) promotes AGS, and that a substantial set of endogenous efsRNAs exhibits predicted bacterial targets that are down-regulated by SA biogenesis and/or signaling during infection. This study thus unveils an unexpected AGS phenomenon, which may have wider implications in the understanding of how plants regulate transcriptome, microbial community composition and genome evolution of associated bacteria.

plant biology↗

Functional analysis of African Xanthomonas oryzae pv. oryzae TALomes reveals a new susceptibility gene in bacterial leaf light of rice

Most Xanthomonas species translocate Transcription Activator-Like (TAL) effectors into plant cells where they function like plant transcription factors via a programmable DNA-binding domain. Characterized strains of rice pathogenic X. oryzae pv. oryzae harbor 9-16 different tal effector genes, but the function of only a few of them has been decoded. Using sequencing of entire genomes, we first performed comparative analyses of the complete repertoires of TAL effectors, herein referred to as TALomes, in three Xoo strains forming an African genetic lineage different from Asian Xoo. A phylogenetic analysis of the three TALomes combined with in silico predictions of TAL effector targets showed that African Xoo TALomes are highly conserved, genetically distant from Asian ones, and closely related to TAL effectors from the bacterial leaf streak pathogen Xanthomonas oryzae pv. oryzicola (Xoc). Nine clusters of TAL effectors could be identified among the three TALomes, including three showing higher levels of variation in their repeat variable diresidues (RVDs). Detailed analyses of these groups revealed recombination events as a possible source of variation among TAL effector genes. Next, to address contribution to virulence, nine TAL effector genes from the Malian Xoo strain MAI1 and four allelic variants from the Burkinabe Xoo strain BAI3, thus representing most of the TAL effector diversity in African Xoo strains, were expressed in the TAL effector-deficient X. oryzae strain X11-5A for gain-of-function assays. Inoculation of the susceptible rice variety Azucena lead to the discovery of three TAL effectors promoting virulence, including two TAL effectors previously reported to target the susceptibility (S) gene OsSWEET14 and a novel major virulence contributor, TalB. RNA profiling experiments in rice and in silico prediction of EBEs were carried out to identify candidate targets of TalB, revealing OsTFX1, a bZIP transcription factor previously identified as a bacterial blight S gene, and OsERF#123, which encodes a subgroup IXc AP2/ERF transcription factor. Use of designer TAL effectors demonstrated that induction of either gene resulted in greater susceptibility to strain X11-5A. The induction of OsERF#123 by BAI3{Delta}1, a talB knockout derivative of BAI3, carrying these designer TAL effectors increased virulence of BAI3{Delta}1 validating OsERF#123 as a new, bacterial blight S gene.\n\nAuthor SummaryThe ability of most Xanthomonas plant pathogenic bacteria to infect their hosts relies on the action of a specific family of proteins called TAL effectors, which are transcriptional activators injected into the plant by the bacteria. TAL effectors enter the plant cell nucleus and bind to the promoters of specific plant genes. Genes that when induced can benefit pathogen multiplication or disease development are called susceptibility (S) genes. Here, we perform a comparative analysis of the TAL effector repertoires of three strains of X. oryzae pv. oryzae, which causes bacterial leaf blight of rice, a major yield constraint in this staple crop. Using sequencing of entire genomes, we compared the large repertoires of TAL effectors in three African Xoo strains which form a genetic lineage distinct from Asian strains. We assessed the individual contribution to pathogen virulence of 13 TAL effector variants represented in the three strains, and identified one that makes a major contribution. By combining host transcriptome profiling and TAL effector binding sites prediction, we identified two targets of this TAL effector that function as S genes, one previously identified, and one, new S gene. We validated the new S gene by functional characterization using designer TAL effectors. Both S genes encode transcription factors and can therefore be considered as susceptibility hubs for pathogen manipulation of the host transcriptome. Our results provide new insights into the diversified strategies underlying the roles of TAL effectors in promoting plant disease.

plant biology↗