Title: Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles
Vascular plant pathogens travel long distances through host veins, leading to life-threatening, systemic infections. In contrast, nonvascular pathogens remain restricted to infection sites, triggering localized symptom development. The contrasting features of vascular and nonvascular diseases suggest distinct etiologies, but the basis for each remains unclear. Here, we show that the hydrolase CbsA acts as a phenotypic switch between vascular and nonvascular plant pathogenesis. cbsA was enriched in genomes of vascular phytopathogenic bacteria in the family Xanthomonadaceae and absent in most nonvascular species. CbsA expression allowed nonvascular Xanthomonas to cause vascular blight, while cbsA mutagenesis resulted in reduction of vascular or enhanced nonvascular symptom development. Phylogenetic hypothesis testing further revealed that cbsA was lost in multiple nonvascular lineages and more recently gained by some vascular subgroups, suggesting that vascular pathogenesis is ancestral. Our results overall demonstrate how the gain and loss of single loci can facilitate the evolution of complex ecological traits. more »« less
Kunkel, Barbara N.; Johnson, Joshua M.B.
(, Cold Spring Harbor Perspectives in Biology)
Weijers, D.; Ljung, K.; Estelle, M.; Leyser, O.
(Ed.)
The plant hormone auxin governs many aspects of normal plant growth and development. Auxin also plays an important role in plant–microbe interactions, including interactions between plant hosts and pathogenic microorganisms that cause disease. It is now well established that indole-3-acetic acid (IAA), the most well-studied form of auxin, promotes disease in many plant–pathogen interactions. Recent studies have shown that IAA can act both as a plant hormone that modulates host signaling and physiology to increase host susceptibility and as a microbial signal that directly impacts the pathogen to promote virulence, but large gaps in our understanding remain. In this article, we review recent studies on the roles that auxin plays during plant–pathogen interactions and discuss the virulence mechanisms that many plant pathogens have evolved to manipulate host auxin signaling and promote pathogenesis.
Arias-Gaguancela, O.; Chapman, K.D.
(, Advances in botanical research)
Rebeille, F.; Marechal, E.
(Ed.)
N-acylethanolamines (NAEs) are a group of lipid signaling molecules derived from the phospholipid precursor N-acylphosphatidylethanolamine (NAPE). NAEs can be processed by a wide range of metabolic processes including hydrolysis by fatty acid amide hydrolase (FAAH), peroxidation by lipoxygenases (LOX), and conjugation by glycosyl- and malonyl-transferases. The diversity of NAE metabolites points to participation in multiple downstream pathways for regulation and function. NAEs with acyl chains of 18C are typically the most predominant types in vascular plants. Whereas in nonvascular plants and some algae, the arachidonic acid-containing NAE, anandamide (a functional “endocannabinoid” in animal systems), was recently reported. A signaling role for anandamide and other NAEs is well established in vertebrates, while NAEs and their oxylipin metabolites are recently becoming appreciated for lipid mediator roles in vascular plants. Here, the NAE metabolism and function in plants are overviewed, with particular emphasis on processes described in vascular plants where most attention has been focused.
Kim, Kwang Su; Ejima, Keisuke; Iwanami, Shoya; Fujita, Yasuhisa; Ohashi, Hirofumi; Koizumi, Yoshiki; Asai, Yusuke; Nakaoka, Shinji; Watashi, Koichi; Aihara, Kazuyuki; et al
(, PLOS Biology)
Sugden, Bill
(Ed.)
The scientific community is focused on developing antiviral therapies to mitigate the impacts of the ongoing novel coronavirus disease 2019 (COVID-19) outbreak. This will be facilitated by improved understanding of viral dynamics within infected hosts. Here, using a mathematical model in combination with published viral load data, we compare within-host viral dynamics of SARS-CoV-2 with analogous dynamics of MERS-CoV and SARS-CoV. Our quantitative analyses using a mathematical model revealed that the within-host reproduction number at symptom onset of SARS-CoV-2 was statistically significantly larger than that of MERS-CoV and similar to that of SARS-CoV. In addition, the time from symptom onset to the viral load peak for SARS-CoV-2 infection was shorter than those of MERS-CoV and SARS-CoV. These findings suggest the difficulty of controlling SARS-CoV-2 infection by antivirals. We further used the viral dynamics model to predict the efficacy of potential antiviral drugs that have different modes of action. The efficacy was measured by the reduction in the viral load area under the curve (AUC). Our results indicate that therapies that block de novo infection or virus production are likely to be effective if and only if initiated before the viral load peak (which appears 2–3 days after symptom onset), but therapies that promote cytotoxicity of infected cells are likely to have effects with less sensitivity to the timing of treatment initiation. Furthermore, combining a therapy that promotes cytotoxicity and one that blocks de novo infection or virus production synergistically reduces the AUC with early treatment. Our unique modeling approach provides insights into the pathogenesis of SARS-CoV-2 and may be useful for development of antiviral therapies.
Abstract Like other eukaryotes, fungi use MAP kinase (MAPK) pathways to mediate cellular changes responding to external stimuli. In the past two decades, three well-conserved MAP kinase pathways have been characterized in various plant pathogenic fungi for regulating responses and adaptations to a variety of biotic and abiotic stresses encountered during plant infection or survival in nature. The invasive growth (IG) pathway is homologous to the yeast pheromone response and filamentation pathways. In plant pathogens, the IG pathway often is essential for pathogenesis by regulating infection-related morphogenesis, such as appressorium formation, penetration, and invasive growth. The cell wall integrity (CWI) pathway also is important for plant infection although the infection processes it regulates vary among fungal pathogens. Besides its universal function in cell wall integrity, it often plays a minor role in responses to oxidative and cell wall stresses. Both the IG and CWI pathways are involved in regulating known virulence factors as well as effector genes during plant infection and mediating defenses against mycoviruses, bacteria, and other fungi. In contrast, the high osmolarity growth (HOG) pathway is dispensable for virulence in some fungi although it is essential for plant infection in others. It regulates osmoregulation in hyphae and is dispensable for appressorium turgor generation. The HOG pathway also plays a major role for responding to oxidative, heat, and other environmental stresses and is overstimulated by phenylpyrrole fungicides. Moreover, these three MAPK pathways crosstalk and coordinately regulate responses to various biotic and abiotic stresses. The IG and CWI pathways, particularly the latter, also are involved in responding to abiotic stresses to various degrees in different fungal pathogens, and the HOG pathway also plays a role in interactions with other microbes or fungi. Furthermore, some infection processes or stress responses are co-regulated by MAPK pathways with cAMP or Ca 2+ /CaM signaling. Overall, functions of individual MAP kinase pathways in pathogenesis and stress responses have been well characterized in a number of fungal pathogens, showing the conserved genetic elements with diverged functions, likely by rewiring transcriptional regulatory networks. In the near future, applications of genomics and proteomics approaches will likely lead to better understanding of crosstalk among the MAPKs and with other signaling pathways as well as roles of MAPKs in defense against other microbes (biotic interactions).
Djami-Tchatchou, Arnaud T.; Harrison, Gregory A.; Harper, Chris P.; Wang, Renhou; Prigge, Michael J.; Estelle, Mark; Kunkel, Barbara N.
(, Molecular Plant-Microbe Interactions®)
null
(Ed.)
Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen strain Pseudomonas syringae DC3000 (PtoDC3000) produces the plant hormone auxin (indole-3-acetic acid [IAA]) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth and that this phenotype was suppressed by introducing the sid2-2 mutation, which impairs SA synthesis. Thus, host auxin signaling is required for normal susceptibility to PtoDC3000 and is involved in suppressing SA-mediated defenses. Unexpectedly, tir1 afb1 afb4 afb5 quadruple-mutant plants lacking four of the six known auxin coreceptors that exhibit decreased auxin perception, supported increased levels of bacterial growth. This mutant exhibited elevated IAA levels and reduced SA-mediated defenses, providing additional evidence that auxin promotes disease by suppressing host defense. We also investigated the hypothesis that IAA promotes PtoDC3000 virulence through a direct effect on the pathogen and found that IAA modulates expression of virulence genes, both in culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.
Gluck-Thaler, Emile, Cerutti, Aude, Perez-Quintero, Alvaro L., Butchacas, Jules, Roman-Reyna, Verónica, Madhavan, Vishnu Narayanan, Shantharaj, Deepak, Merfa, Marcus V., Pesce, Céline, Jauneau, Alain, Vancheva, Taca, Lang, Jillian M., Allen, Caitilyn, Verdier, Valerie, Gagnevin, Lionel, Szurek, Boris, Beckham, Gregg T., De La Fuente, Leonardo, Patel, Hitendra Kumar, Sonti, Ramesh V., Bragard, Claude, Leach, Jan E., Noël, Laurent D., Slot, Jason C., Koebnik, Ralf, and Jacobs, Jonathan M. Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles. Retrieved from https://par.nsf.gov/biblio/10291087. Science Advances 6.46 Web. doi:10.1126/sciadv.abc4516.
Gluck-Thaler, Emile, Cerutti, Aude, Perez-Quintero, Alvaro L., Butchacas, Jules, Roman-Reyna, Verónica, Madhavan, Vishnu Narayanan, Shantharaj, Deepak, Merfa, Marcus V., Pesce, Céline, Jauneau, Alain, Vancheva, Taca, Lang, Jillian M., Allen, Caitilyn, Verdier, Valerie, Gagnevin, Lionel, Szurek, Boris, Beckham, Gregg T., De La Fuente, Leonardo, Patel, Hitendra Kumar, Sonti, Ramesh V., Bragard, Claude, Leach, Jan E., Noël, Laurent D., Slot, Jason C., Koebnik, Ralf, & Jacobs, Jonathan M. Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles. Science Advances, 6 (46). Retrieved from https://par.nsf.gov/biblio/10291087. https://doi.org/10.1126/sciadv.abc4516
Gluck-Thaler, Emile, Cerutti, Aude, Perez-Quintero, Alvaro L., Butchacas, Jules, Roman-Reyna, Verónica, Madhavan, Vishnu Narayanan, Shantharaj, Deepak, Merfa, Marcus V., Pesce, Céline, Jauneau, Alain, Vancheva, Taca, Lang, Jillian M., Allen, Caitilyn, Verdier, Valerie, Gagnevin, Lionel, Szurek, Boris, Beckham, Gregg T., De La Fuente, Leonardo, Patel, Hitendra Kumar, Sonti, Ramesh V., Bragard, Claude, Leach, Jan E., Noël, Laurent D., Slot, Jason C., Koebnik, Ralf, and Jacobs, Jonathan M.
"Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles". Science Advances 6 (46). Country unknown/Code not available. https://doi.org/10.1126/sciadv.abc4516.https://par.nsf.gov/biblio/10291087.
@article{osti_10291087,
place = {Country unknown/Code not available},
title = {Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles},
url = {https://par.nsf.gov/biblio/10291087},
DOI = {10.1126/sciadv.abc4516},
abstractNote = {Vascular plant pathogens travel long distances through host veins, leading to life-threatening, systemic infections. In contrast, nonvascular pathogens remain restricted to infection sites, triggering localized symptom development. The contrasting features of vascular and nonvascular diseases suggest distinct etiologies, but the basis for each remains unclear. Here, we show that the hydrolase CbsA acts as a phenotypic switch between vascular and nonvascular plant pathogenesis. cbsA was enriched in genomes of vascular phytopathogenic bacteria in the family Xanthomonadaceae and absent in most nonvascular species. CbsA expression allowed nonvascular Xanthomonas to cause vascular blight, while cbsA mutagenesis resulted in reduction of vascular or enhanced nonvascular symptom development. Phylogenetic hypothesis testing further revealed that cbsA was lost in multiple nonvascular lineages and more recently gained by some vascular subgroups, suggesting that vascular pathogenesis is ancestral. Our results overall demonstrate how the gain and loss of single loci can facilitate the evolution of complex ecological traits.},
journal = {Science Advances},
volume = {6},
number = {46},
author = {Gluck-Thaler, Emile and Cerutti, Aude and Perez-Quintero, Alvaro L. and Butchacas, Jules and Roman-Reyna, Verónica and Madhavan, Vishnu Narayanan and Shantharaj, Deepak and Merfa, Marcus V. and Pesce, Céline and Jauneau, Alain and Vancheva, Taca and Lang, Jillian M. and Allen, Caitilyn and Verdier, Valerie and Gagnevin, Lionel and Szurek, Boris and Beckham, Gregg T. and De La Fuente, Leonardo and Patel, Hitendra Kumar and Sonti, Ramesh V. and Bragard, Claude and Leach, Jan E. and Noël, Laurent D. and Slot, Jason C. and Koebnik, Ralf and Jacobs, Jonathan M.},
editor = {null}
}
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