Redirection of auxin flow in<i>Arabidopsis thaliana</i>roots after infection by root-knot nematodes

Kyndt, Tina; Goverse, A.; Haegeman, Annelies; Warmerdam, Sonja; Wanjau, Cecilia Ngonyo; Jahani, Mona; Engler, Gilbert; Engler, Janice de Almeida; Gheysen, Godelieve

doi:10.1093/jxb/erw230

Cited by 65 publications

(71 citation statements)

References 33 publications

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“…A similar result has been reported by Doyle & Lambert (), in which the expression of Mj‐CM‐1 in transformed soybean hairy roots gave an abnormal root development phenotype. Moreover, auxin has also been demonstrated to be involved in the induction and formation of the plant‐parasitic nematode feeding site, possibly by manipulating the balance between auxin transport and synthesis (Goverse et al ., ; Kyndt et al ., ); however, in the present investigation, it is not clear whether the alteration of auxin accumulation caused by ectopic expression of Mi‐CM‐3 in the transgenic line of N. benthamiana may have contributed to the parasitism of M. incognita . Therefore, more work is needed in future research to investigate the exact mechanism of the interaction between the nematode CM effector and the plant.…”

Section: Discussioncontrasting

confidence: 57%

A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism

et al. 2018

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Meloidogyne incognita is the most economically important plant‐parasitic nematode. Meloidogyne incognita manipulates plant cell development and metabolism by injecting effectors from the oesophageal glands into the plant host. Chorismate mutase (CM) is one such effector that may contribute to successful parasitism by M. incognita. This investigation identified and functionally characterized a novel CM effector, Mi‐CM‐3, which is more similar to CMs from bacteria than from other phytoparasitic nematodes. Spatial and temporal expression assays showed Mi‐cm‐3 mRNA accumulates specifically in the subventral oesophageal glands and transcription is up‐regulated during the early parasitic stages of the nematode. In planta gene silencing of Mi‐cm‐3 attenuated nematode parasitism. In addition, Mi‐cm‐3 could fully restore the full virulence phenotype of the pathogenic bacterium Xanthomonas oryzae pv. oryzae by complementation when it was introduced into a mutant strain carrying a deletion in the CM gene. Transient expression of Mi‐CM‐3 caused a reduction in levels of salicylic acid (SA) and mRNA of gene PR1 in Nicotiana benthamiana in response to oomycete pathogen Phytophthora capsici infection, while confocal observations showed that Mi‐CM‐3 was localized within the cytoplasm and the nucleus, but not the plastids, of transfected N. benthamiana leaf cells. Constitutive expression of Mi‐CM‐3 in N. benthamiana plants inhibited root growth and increased susceptibility to M. incognita infection. These results provide direct experimental evidence to show that Mi‐CM‐3 may play an important role in suppressing plant immunity by regulating the SA pathway during the early parasitic stage of M. incognita so as to promote nematode parasitism.

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Section: Discussioncontrasting

confidence: 57%

A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism

et al. 2018

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“…In rice, both GA and auxin have been shown to play the same role in promoting susceptibility to hemibiotrophs such as M. oryzae and Xoo (Yang et al ., ; Domingo et al ., ; Fu et al ., ; Qin et al ., ). Studies on RKNs also show the importance of auxin in the induction of the giant cell and gall formation in Arabidopsis (Karczmarek et al ., ; Gheysen & Mitchum, ; Kyndt et al ., ). Our results also demonstrated that foliar application of the synthetic auxin analog NAA can increase the amount of nematode infection, proving that auxin can also render rice plants more susceptible to M. graminicola .…”

Section: Discussionmentioning

confidence: 98%

“…Previous studies have shown the importance of JA in basal immunity against RKNs (Cooper et al, 2005;Fujimoto et al, 2011;Nahar et al, 2011;Gleason et al, 2016;Hu et al, 2017). By contrast, auxin enhances susceptibility to RKNs by promoting induction of giant cell and gall formation (Karczmarek et al, 2004;Gheysen & Mitchum, 2011;Kyndt et al, 2016). Because the hormone analysis showed that GA treatment modulates both auxin and JA in rice roots, we decided to further examine the auxin and JA pathway and their interaction with GA after M. graminicola infection in rice.…”

Section: Meloidogyne Graminicola Infection Induces Ga 12 Accumulationmentioning

confidence: 99%

“…Previous studies have shown the vital role of JA in basal resistance against the RKN M. graminicola in rice (Nahar et al ., ), M. javanica and M. incognita in tomato (Cooper et al ., ; Fujimoto et al ., ) and M. hapla in Arabidopsis and soybean (Gleason et al ., ; Hu et al ., ). By contrast, auxin is important for the induction of giant cells and gall formation by RKN (Karczmarek et al ., ; Gheysen & Mitchum, ; Kyndt et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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Gibberellin antagonizes jasmonate‐induced defense against Meloidogyne graminicola in rice

et al. 2018

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Gibberellin (GA) regulates various plant growth and developmental processes, but its role in pathogen attack, and especially nematode-plant interactions, still remains to be elucidated. An in-depth characterization of the role of GA in nematode infection was conducted using mutant lines of rice, chemical inhibitors, and phytohormone measurements. Our results showed that GA influences rice-Meloidogyne graminicola interactions in a concentration-dependent manner. Foliar spray of plants with a low concentration of gibberellic acid enhanced nematode infection. Biosynthetic and signaling mutants confirmed the importance of gibberellin for rice susceptibility to M. graminicola infection. Our study also demonstrates that GA signaling suppresses jasmonate (JA)-mediated defense against M. graminicola, and likewise the JA-induced defense against M. graminicola requires SLENDER RICE1 (SLR1)-mediated repression of the GA pathway. In contrast to observations from other plant-pathogen interactions, GA plays a dominant role over JA in determining susceptibility to M. graminicola in rice. This GA-induced nematode susceptibility was largely independent of auxin biosynthesis, but relied on auxin transport. In conclusion, we showed that GA-JA antagonistic crosstalk is at the forefront of the interaction between rice and M. graminicola, and SLR1 plays a central role in the JA-mediated defense response in rice against this nematode.

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“…PIN3 and PIN4; Feraru & Friml, 2008;Sun et al, 2010;Vragovi c et al, 2015). Recently, it was shown that development of M. incognita is hampered on Arabidopsis knockout mutants of PIN3 and PIN4 (Kyndt et al, 2016). PIN3 and PIN4 are thought to be involved in redirecting the flow of auxin during giant cell formation.…”

Section: Discussionmentioning

confidence: 99%

Genome‐wide association mapping of the architecture of susceptibility to the root‐knot nematode Meloidogyne incognita in Arabidopsis thaliana

et al. 2018

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Summary Susceptibility to the root‐knot nematode Meloidogyne incognita in plants is thought to be a complex trait based on multiple genes involved in cell differentiation, growth and defence. Previous genetic analyses of susceptibility to M. incognita have mainly focused on segregating dominant resistance genes in crops. It is not known if plants harbour significant genetic variation in susceptibility to M. incognita independent of dominant resistance.To study the genetic architecture of susceptibility to M. incognita, we analysed nematode reproduction on a highly diverse set of 340 natural inbred lines of Arabidopsis thaliana with genome‐wide association mapping. We observed a surprisingly large variation in nematode reproduction among these lines.Genome‐wide association mapping revealed four quantitative trait loci (QTLs) located on chromosomes 1 and 5 of A. thaliana significantly associated with reproductive success of M. incognita, none of which harbours typical resistance gene homologues. Mutant analysis of three genes located in two QTLs showed that the transcription factor BRASSINAZOLE RESISTANT1 and an F‐box family protein may function as (co‐)regulators of susceptibility to M. incognita in Arabidopsis.Our data suggest that breeding for loss‐of‐susceptibility, based on allelic variants critically involved in nematode feeding, could be used to make crops more resilient to root‐knot nematodes.

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Redirection of auxin flow inArabidopsis thalianaroots after infection by root-knot nematodes

Abstract: HighlightPlant auxin efflux and influx proteins redirect the plant hormone auxin towards the feeding site upon root-knot nematode infection in Arabidopsis thaliana roots.

Cited by 65 publications

References 33 publications

A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism

A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism

Gibberellin antagonizes jasmonate‐induced defense against Meloidogyne graminicola in rice

Genome‐wide association mapping of the architecture of susceptibility to the root‐knot nematode Meloidogyne incognita in Arabidopsis thaliana

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