Deciphering the role of apoplastic root barriers in the interaction between sedentary nematodes and Arabidopsis

The plant-parasitic nematode species Heterodera schachtii and Meloidogyne incognita infect economically important crop plants in the entire world. Their infection causes yield losses, but effective and environmentally friendly pest management strategies require high expenses or are impractical. Nematological research therefore studies plant-nematode interaction on cellular and molecular level to improve nematode control strategies. Plant-parasitic nematodes invade roots and establish feeding sites in the vascular tissue. Within root tissue, nematodes cross the endodermis, which is equipped with cell wall reinforcements and Casparian strips (CSs) in the apoplast. These cell wall modifications consist of the resilient biopolymers suberin and lignin, respectively. To examine whether suberin and the CS play a role during nematode infection of Arabidopsis, the expression of related biosynthesis genes in nematode-infected tissue was analysed. A number of suberin biosynthesis genes were significantly upregulated in infection sites, while CS related genes were downregulated. Reporter gene analysis showed differential expression of CS and suberin markers in feeding sites, indicating the presence of suberin in surrounding tissue. Histochemical staining verified the presence of a lipophilic substance, such as suberin, in an endodermis-like cell layer encircling nematode feeding sites. Finally, a typical suberin monomer composition has been verified in nematode-infected root segments. On quantitative level, this suberin monomers showed significant differences in abundance as compared to control roots. To test whether suberin or the CS affect nematode parasitism, mutants altered in suberin deposition or CS formation were used for infectivity studies. Surprisingly, not suberin alterations but defective CSs had a significant impact on nematode infection and development. The role of suberin and CSs during nematode infection and nutrient acquisition as well as the impact of the endodermal barrier surveillance system are discussed.Die Entschlüsselung der Rolle apoplastischer Wurzelbarrieren in der Interaktion zwischen sedentären Nematoden und Arabidopsis Die pflanzenparasitären Nematodenarten Heterodera schachtii und Meloidognye incognita befallen ökonomisch wichtige Nutzpflanzen weltweit. Der Befall verursacht Ertragsverluste, aber effektive und umweltverträgliche Maßnahmen zur Schädlingskontrolle sind kostspielig oder inpraktikabel. Aus diesem Grund untersucht die nematologische Forschung die Pflanze-Nematode Interaktion auf zellulärer und molekularer Ebene zur Verbesserung der Pflanzenschutzstrategien. Pflanzenparasitäre Nematoden dringen in Wurzeln ein und etablieren Nährgewebe im Zentralzylinder. Dafür durchdringen Nematoden innerhalb des Wurzelgewebes die Endodermis, welche durch Zellwandverstärkungen und den Casparischen Streifen (CS) modifiziert ist. Diese Verstärkungen bestehen jeweils aus den widerstandsfähigen Biopolymeren Suberin und Lignin. Um zu untersuchen ob Suberin und der CS eine Rolle bei der Infektion von Arabidopsis mit Nematoden spielen, wurde die Expression von zugehörigen Bio-synthesegenen in infizierten Wurzelsegmenten analysiert. Eine Reihe von Suberinbiosynthesegenen war signifikant hochreguliert in Infektionsstellen, wobei CS verwandte Gene runterreguliert waren. Die Reportergenanalyse zeigte unterschiedliche Expressionsmuster von Suberin und CS verwandten Markern in Infektionsstellen, implizierte , jedoch, das Vorliegen von Suberin in umliegendem Gewebe. Histochemische Färbungen betsätigten Ablagerungen einer lipophilen Substanz, wie Suberin, in einer Endodermis-ähnlichen Zellschicht, die die Infektionsstelle umgibt. Schließlich wurde eine typische Suberin-Monomerzusammensetzung qualitativ bestätigt. Auf quantitativer Ebene zeigten sich signifikante Unterschiede im Vergleich zu Suberin aus nicht befallenen Wurzeln. Um zu untersuchen, ob Suberin oder der CS eine Auswirkung auf den Befall von Nematoden haben, wurden transgene Pflanzenlinien mit veränderter Suberinbiosynthese oder defekter Bildung des CSs für Infektionsstudien genutzt. Überraschenderweise hatten defekte CS einen signifikanten Einfluss auf den Parasitismus und nicht die Suberinveränderungen. Die Rolle von Suberin und CS insbesondere für die Nährstoffakkumulation von Nematoden sowie der Einfluss des Barriere-Überwachungssystems der Endodermis werden diskutiert

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Plant-parasitic nematodes are destructive pests causing losses of billions of dollars annually. An effective plant defence against pathogens relies on the recognition of pathogen-associated molecular patterns (PAMPs) by surface-localised receptors leading to the activation of PAMP-triggered immunity (PTI). Extensive studies have been conducted to characterise the role of PTI in various models of plant-pathogen interactions. However, far less is known about the role of PTI in roots in general and in plant-nematode interactions in particular. Here we show that nematode-derived proteinaceous elicitor/s is/are capable of inducing PTI in Arabidopsis in a manner dependent on the common immune co-receptor BAK1. Consistent with the role played by BAK1, we identified a leucine-rich repeat receptor-like kinase, termed NILR1 that is specifically regulated upon infection by nematodes. We show that NILR1 is essential for PTI responses initiated by nematodes and nilr1 loss-of-function mutants are hypersusceptible to a broad category of nematodes. To our knowledge, NILR1 is the first example of an immune receptor that is involved in induction of basal immunity (PTI) in plants or in animals in response to nematodes. Manipulation of NILR1 will provide new options for nematode control in crop plants in future

A suberized exodermis is required for tomato drought tolerance

Plant roots integrate environmental signals with development using exquisite spatiotemporal control. This is apparent in the deposition of suberin, an apoplastic diffusion barrier, which regulates flow of water, solutes and gases, and is environmentally plastic. Suberin is considered a hallmark of endodermal differentiation but is absent in the tomato endodermis. Instead, suberin is present in the exodermis, a cell type that is absent in the model organism Arabidopsis thaliana. Here we demonstrate that the suberin regulatory network has the same parts driving suberin production in the tomato exodermis and the Arabidopsis endodermis. Despite this co-option of network components, the network has undergone rewiring to drive distinct spatial expression and with distinct contributions of specific genes. Functional genetic analyses of the tomato MYB92 transcription factor and ASFT enzyme demonstrate the importance of exodermal suberin for a plant water-deficit response and that the exodermal barrier serves an equivalent function to that of the endodermis and can act in its place

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Plant-parasitic nematodes are destructive pests causing losses of billions of dollars annually. An effective plant defence against pathogens relies on the recognition of pathogen-associated molecular patterns (PAMPs) by surface-localised receptors leading to the activation of PAMP-triggered immunity (PTI). Extensive studies have been conducted to characterise the role of PTI in various models of plant-pathogen interactions. However, far less is known about the role of PTI in roots in general and in plant-nematode interactions in particular. Here we show that nematode-derived proteinaceous elicitor/s is/are capable of inducing PTI in Arabidopsis in a manner dependent on the common immune co-receptor BAK1. Consistent with the role played by BAK1, we identified a leucine-rich repeat receptor-like kinase, termed NILR1 that is specifically regulated upon infection by nematodes. We show that NILR1 is essential for PTI responses initiated by nematodes and nilr1 loss-of-function mutants are hypersusceptible to a broad category of nematodes. To our knowledge, NILR1 is the first example of an immune receptor that is involved in induction of basal immunity (PTI) in plants or in animals in response to nematodes. Manipulation of NILR1 will provide new options for nematode control in crop plants in future

Transcriptomic Analysis of Resistant and Susceptible Responses in a New Model Root-Knot Nematode Infection System Using Solanum torvum and Meloidogyne arenaria

Root-knot nematodes (RKNs) are among the most devastating pests in agriculture. Solanum torvum Sw. (Turkey berry) has been used as a rootstock for eggplant (aubergine) cultivation because of its resistance to RKNs, including Meloidogyne incognita and M. arenaria. We previously found that a pathotype of M. arenaria, A2-J, is able to infect and propagate in S. torvum. In vitro infection assays showed that S. torvum induced the accumulation of brown pigments during avirulent pathotype A2-O infection, but not during virulent A2-J infection. This experimental system is advantageous because resistant and susceptible responses can be distinguished within a few days, and because a single plant genome can yield information about both resistant and susceptible responses. Comparative RNA-sequencing analysis of S. torvum inoculated with A2-J and A2-O at early stages of infection was used to parse the specific resistance and susceptible responses. Infection with A2-J did not induce statistically significant changes in gene expression within one day post-inoculation (DPI), but afterward, A2-J specifically induced the expression of chalcone synthase, spermidine synthase, and genes related to cell wall modification and transmembrane transport. Infection with A2-O rapidly induced the expression of genes encoding class III peroxidases, sesquiterpene synthases, and fatty acid desaturases at 1 DPI, followed by genes involved in defense, hormone signaling, and the biosynthesis of lignin at 3 DPI. Both isolates induced the expression of suberin biosynthetic genes, which may be triggered by wounding during nematode infection. Histochemical analysis revealed that A2-O, but not A2-J, induced lignin accumulation at the root tip, suggesting that physical reinforcement of cell walls with lignin is an important defense response against nematodes. The S. torvum-RKN system can provide a molecular basis for understanding plant-nematode interactions