The Novel Cyst Nematode Effector Protein 19C07 Interacts with the Arabidopsis Auxin Influx Transporter LAX3 to Control Feeding Site Development

Lee, Chris; Chronis, Demosthenis; Kenning, Charlotte; Péret, Benjamin; Hewezi, Tarek; Davis, Eric; Baum, Thomas J.; Hussey, R. S.; Bennett, Malcolm J.; Mitchum, Melissa G.

doi:10.1104/pp.110.167197

Cited by 146 publications

(149 citation statements)

References 73 publications

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“…However, the mechanisms by which cyst nematodes regulate auxin accumulation, transport, and signaling are not fully understood. Recently, we found that H. schachtii 19C07 effector protein interacts with an auxin influx transporter, LAX3 (Auxin transporter-like protein 3), probably to maintain auxin balance during the early stages of syncytium formation (Lee et al, 2011). In this context, our finding that the 10A07 effector directly targets IAA16 provides additional insights into how cyst nematode effectors potentially manipulate auxin response.…”

Section: Discussionmentioning

confidence: 71%

The Cyst Nematode Effector Protein 10A07 Targets and Recruits Host Posttranslational Machinery to Mediate Its Nuclear Trafficking and to Promote Parasitism in Arabidopsis

et al. 2015

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Plant-parasitic cyst nematodes synthesize and secrete effector proteins that are essential for parasitism. One such protein is the 10A07 effector from the sugar beet cyst nematode, Heterodera schachtii, which is exclusively expressed in the nematode dorsal gland cell during all nematode parasitic stages. Overexpression of H. schachtii 10A07 in Arabidopsis thaliana produced a hypersusceptible phenotype in response to H. schachtii infection along with developmental changes reminiscent of auxin effects. The 10A07 protein physically associates with a plant kinase and the IAA16 transcription factor in the cytoplasm and nucleus, respectively. The interacting plant kinase (IPK) phosphorylates 10A07 at Ser-144 and Ser-231 and mediates its trafficking from the cytoplasm to the nucleus. Translocation to the nucleus is phosphorylation dependent since substitution of Ser-144 and Ser-231 by alanine resulted in exclusive cytoplasmic accumulation of 10A07. IPK and IAA16 are highly upregulated in the nematode-induced syncytium (feeding cells), and deliberate manipulations of their expression significantly alter plant susceptibility to H. schachtii in an additive fashion. An inactive variant of IPK functioned antagonistically to the wild-type IPK and caused a dominant-negative phenotype of reduced plant susceptibility. Thus, exploitation of host processes to the advantage of the parasites is one mechanism by which cyst nematodes promote parasitism of host plants.

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Section: Discussionmentioning

confidence: 71%

The Cyst Nematode Effector Protein 10A07 Targets and Recruits Host Posttranslational Machinery to Mediate Its Nuclear Trafficking and to Promote Parasitism in Arabidopsis

et al. 2015

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“…23 In some cases, the nematode effectors play a role in the cytoplasm in the region of the plasma membrane. Co-localization studies in vivo by bimolecular fluorescence complementation have shown that the effector Hs19C07, which is secreted by the CN H. schachtii, interacts with the transmembrane auxin influx transporter LAX3 at the plasma membrane, 24 most probably to manipulate auxin influx and allow the differentiation of the feeding cell as previously anticipated. 25 …”

Section: Cytoplasmmentioning

confidence: 86%

Effectors of root sedentary nematodes target diverse plant cell compartments to manipulate plant functions and promote infection

Jaouannet

Rosso

2013

Plant Signaling & Behavior

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Sedentary plant-parasitic nematodes maintain a biotrophic relationship with their hosts over a period of several weeks and induce the differentiation of root cells into specialized feeding cells. nematode effectors, which are synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet, play a central role in these processes. Previous work on nematode effectors has shown that the apoplasm is targeted during invasion of the host while the cytoplasm is targeted during the induction and the maintenance of the feeding site. A large number of candidate effectors potentially secreted by the nematode into the plant tissues to promote infection have now been identified. This work has shown that the targeting and the role of effectors are more complex than previously thought. This review will not cover the prolific recent findings in nematode effector function but will instead focus on recent selected examples that illustrate the variety of plant cell compartments that effectors are addressed to in order reach their plant targets. Effectors of root sedentary nematodes target diverse plant cell compartments to manipulate plant functions and promote infectionMaëlle Jaouannet 1 Although different species infect a variety of plant organs most species are restricted to roots. The most intensively studied are the sedentary root endoparasites; the root-knot nematodes (RKN) and cyst nematodes (CN), which are the most damaging species worldwide. An intriguing aspect of RKN and CN infection is the ability of these obligate parasites to hijack plant cell fate and induce the redifferentiation of root cells, generally in the elongation zone, into specialized feeding cells, called giant-cells in the case of RKN and syncytia in the case of CN. These cells are enlarged, multinucleate and metabolically hyperactive cells that provide the nutrients required ensuringcompletion of the parasite life cycle. 2Although there are superficial similarities between the feeding structures induced by RKN and CN, they have entirely different ontogenies and are thought to have evolved independently. A remarkable feature of parasitism by RKN and CN is the ability of these parasites to maintain a long-lasting biotrophic interaction with the host (up to 6 weeks) that allows withdrawal of nutrients from the cytoplasm of living plant cells until the progeny are produced. Plant-endoparasitic nematode interactions therefore provide a fascinating model for the study of fundamental aspects of plant cell differentiation and plant defense suppression by the pathogen.Our understanding of the molecular mechanisms that underlie plant-nematode interactions is expanding and we are beginning to decipher the means by which the pathogen manipulates host plant cells. Effector proteins, secreted into host tissues by the nematode, are one of the key components of the molecular dialog leading to successful infection. Effectors can be defined as the molecules secreted by the pathogen that alter host-cell physiology to promote infectio...

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“…The loosening of cell walls immediately above an emerging lateral root is another process that would not occur in the root tip but would be prominent in other parts of the root system. Enzymatic cell wall separation has been reported for the loosening of cells above an emerging lateral root (Roberts et al, 2002), and more recently Lee et al (2011) demonstrated using a GUS reporter gene that a polygalacturonase gene that is up-regulated at the site of nematode (Heterodera schachtii) infection of Arabidopsis roots is also expressed in noninfected roots in a layer of cortical cells immediately above an emerging lateral root. Thus, this Arabidopsis polygalacturonase may be linked to the loosening of cortical cells where the lateral root emerges.…”

Section: Discussionmentioning

confidence: 99%

Gene Expression Profiling and Shared Promoter Motif for Cell Wall-Modifying Proteins Expressed in Soybean Cyst Nematode-Infected Roots

2011

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We hypothesized that soybean cyst nematode (SCN; Heterodera glycines) co-opts part or all of one or more innate developmental process in soybean (Glycine max) to establish its feeding structure, syncytium, in soybean roots. The syncytium is formed within the vascular bundle by partial degradation of cell walls and membranes between adjacent parenchyma cells. A mature syncytium incorporates as many as 200 cells into one large multinucleated cell. Gene expression patterns for several cell wall-modifying proteins were compared in multiple tissues undergoing major shifts in cell wall integrity. These included SCN-colonized roots, root tips where vascular differentiation occurs, flooded roots (aerenchyma), adventitious rooting in hypocotyls, and leaf abscission zones. A search in the 5# upstream promoters of these genes identified a motif (SCNbox1: WGCATGTG) common to several genes that were up-regulated in several different tissues. The polygalacturonase 11 promoters (GmPG11a/b) include the SCNbox1 motif. The expression pattern for GmPG11a was examined further in transgenic soybean containing a PG11a promoter fused to a b-glucuronidase (GUS) reporter gene. GUS expression was highest in cells undergoing radial expansion in the stele and/or cell wall dissolution. GUS staining was not observed in cortical cells where a lateral root tip or a growing nematode emerged through the root cortex.

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The Novel Cyst Nematode Effector Protein 19C07 Interacts with the Arabidopsis Auxin Influx Transporter LAX3 to Control Feeding Site Development

Cited by 146 publications

References 73 publications

The Cyst Nematode Effector Protein 10A07 Targets and Recruits Host Posttranslational Machinery to Mediate Its Nuclear Trafficking and to Promote Parasitism in Arabidopsis

The Cyst Nematode Effector Protein 10A07 Targets and Recruits Host Posttranslational Machinery to Mediate Its Nuclear Trafficking and to Promote Parasitism in Arabidopsis

Effectors of root sedentary nematodes target diverse plant cell compartments to manipulate plant functions and promote infection

Gene Expression Profiling and Shared Promoter Motif for Cell Wall-Modifying Proteins Expressed in Soybean Cyst Nematode-Infected Roots

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