Molecular Markers and Cell Cycle Inhibitors Show the Importance of Cell Cycle Progression in Nematode-Induced Galls and Syncytia

Engler, Janice de Almeida; Vleesschauwer, Vera De; Burssens, Sylvia; Celenza, John L.; Inzé, Dirk; Montagu, Marc Van; Engler, Gilbert; Gheysen, Godelieve

doi:10.2307/3870815

Cited by 47 publications

(103 citation statements)

References 11 publications

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“…The use of Arabidopsis thaliana , which is readily infected by the sugar beet cyst nematode H. schachtii (Sijmons et al ., 1991), a close relative of H. glycines , allows unprecedented advances. The Arabidopsis – H. schachtii model system has been used widely for gene expression analyses (Barthels et al ., 1997; Burrows, 1992; De Almeida Engler et al ., 1999, 2004; Favery et al ., 1998; Goddijn et al ., 1993; Goverse et al ., 2000b; Hermsmeier et al ., 2000; Juergensen et al ., 2003; Karimi et al ., 2000, 2002; Mazarei et al ., 2003; Mitchum et al ., 2004; Møller et al ., 1998; Niebel et al ., 1996; Puthoff et al ., 2003; Puzio et al ., 1998, 1999, 2000; Thurau et al ., 2003; Urwin et al ., 1997a,b, 1998; Vaghchhipawala et al ., 2004; Vercauteren et al ., 2002) as well as for genetic studies of Arabidopsis mutants (Baum et al ., 2000; Goverse et al ., 2000b; Wubben et al ., 2001).…”

Section: Introductionmentioning

confidence: 99%

Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection

Mazarei¹,

Lennon²,

Puthoff³

et al. 2004

Molecular Plant Pathology

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SUMMARY We previously isolated a partial soybean cDNA clone (D17.1) whose corresponding transcript increases in susceptible roots 1 day post inoculation (dpi) with the soybean cyst nematode, Heterodera glycines. Here we isolated the corresponding full-length cDNA from a soybean cDNA library and designated this gene of unknown function Gm17.1. Time course RNA gel blot analyses revealed that Gm17.1 mRNA steady-state levels were elevated in soybean roots following H. glycines infection up to at least 6 dpi. For further in-depth study we identified a homologous Arabidopsis thaliana gene and designated this gene At17.1. Arabidopsis is successfully infected by the sugar beet cyst nematode (H. schachtii), a close relative of H. glycines. We isolated the At17.1 promoter, fused it to the beta-glucuronidase (GUS) reporter gene, and transformed this construct into Arabidopsis plants as well as soybean hairy roots. Histochemical analysis of plant materials containing the At17.1::GUS construct revealed that the At17.1 promoter is functional in Arabidopsis as well as in soybean and that during normal plant development the At17.1 promoter directs GUS expression predominantly to the vascular tissues and root tips of both plant species. When At17.1::GUS Arabidopsis plants and soybean hairy roots were inoculated with cyst nematodes, strong GUS activity was detected within the cyst nematode-induced feeding structures. Further tests of At17.1 promoter activity in Arabidopsis revealed that this promoter was induced by auxin, jasmonic acid, mannitol and dehydration. Quantitative real-time reverse transcription-polymerase chain reaction assays of At17.1 expression confirmed the observed promoter characteristics. Based on our expression data and the observation that both the soybean and the Arabidopsis homologues behaved in a similar fashion following cyst nematode infection, it is likely that these genes are closely associated with cyst nematode parasitism of plants, potentially with hormone and osmotic changes occurring in the developing nematode feeding cells. Furthermore, these data provide additional insights into the strengths of the Arabidopsis-H. schachtii pathosystem to study cyst nematode-plant interactions in lieu of less tractable pathosystems. This finding is supported by the fact that the Arabidopsis promoter tested here produced similar results in Arabidopsis and soybean.

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Section: Introductionmentioning

confidence: 99%

Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection

Mazarei¹,

Lennon²,

Puthoff³

et al. 2004

Molecular Plant Pathology

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“…To analyze the importance of cell cycle activation for the development of feeding cells, cell cycle-inhibiting drugs have been used (de Almeida-Engler et al 1999) . Upon hydroxyurea treatment (which prevents DNA synthesis), early giantcell and syncytium development was blocked in Arabidopsis .…”

Section: Polyploidy In Nfs Is Correlated With Activation Of Cell-cyclmentioning

confidence: 99%

“…However, the application of hydroxyurea at later stages resulted in normal development of the feeding sites. Upon early application (1 and 3 dai) of oryzalin (which arrests cells in mitosis), root-knot nematode development in Arabidopsis was completely inhibited (de Almeida-Engler et al 1999 ;Wiggers et al 2002) . The formation of giant-cells was initiated but their development severely hampered.…”

Section: Polyploidy In Nfs Is Correlated With Activation Of Cell-cyclmentioning

confidence: 99%

“…These data indicate that mitotic activity is also required for proper syncytium development. It was observed that oryzalin inhibits the mitotic activity in cells prior to syncytium incorporation and, as a consequence, syncytium expansion is restricted (de Almeida-Engler et al 1999) . Recently, it was demonstrated that silencing AtCDKA;1 , an essential cell cycle gene, using a NFS-promoter results in significant reduction of nematode development on A. thaliana .…”

Section: Polyploidy In Nfs Is Correlated With Activation Of Cell-cyclmentioning

confidence: 99%

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Molecular Insights in the Susceptible Plant Response to Nematode Infection

Gheysen

Mitchum

2008

Plant Cell Monographs

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Sedentary endoparasitic nematodes have evolved sophisticated strategies to form permanent feeding sites within host plant roots to ensure their survival. The process of feeding site formation entails an elaborate transformation of normal root cells into enlarged, multinucleate, and metabolically active cell types to supply the nutritional needs of the nematode. The signal-exchange that occurs between nematodes and their hosts to trigger the chain of molecular events associated with feeding cell formation has not been resolved. Presumably, the signals for the induction of feeding cells come from the nematode; thus, secretions originating in the esophageal gland cells and directly injected through the stylet into host tissues during parasitism have been implicated as key molecules. It is evident from the distinct morphological features of feeding sites that the nematode signals likely interfere with fundamental aspects of plant cell biology and differentiation. Molecular studies have shown that these changes are accompanied by extensive alterations in plant gene expression. Researchers have taken advantage of a wide array of methodologies to catalogue the genes as either up-or down-regulated in nematode feeding sites, and technological advances are now enabling feeding cell-specific analyses. As comprehensive profiles of genes expressed in feeding sites are generated, it has become increasingly important to determine which genes play essential roles in their formation. In the future, the true challenge will be to integrate our knowledge of nematode signals with host cell responses to elucidate a complete picture of feeding site formation.

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“…Expression of A‐ and B‐type cyclins has previously been studied in root‐knot nematode‐induced GCs and cyst nematode‐induced syncytia in Arabidopsis (de Almeida Engler et al ., 1999; Goverse et al ., 2000). Using a GUS reporter gene, strong promoter activity of both the CycA2; 1 and the CycB1; 1 genes was observed in young GCs and neighbouring cells within the gall tissue (de Almeida Engler et al ., 1999). This is evidence for activation of cell cycle progression through S to G2 and G2 to M phases.…”

Section: Introductionmentioning

confidence: 99%

Using laser capture microdissection to study gene expression in early stages of giant cells induced by root‐knot nematodes

Ramsay

Wang

Jones

2004

Molecular Plant Pathology

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SUMMARY Root‐knot nematodes (Meloidogyne spp.) are economically important plant parasites that induce specific feeding cells called giant cells in host roots. Study of molecular events involved in induction and differentiation of giant cells has been limited because it is difficult to obtain pure cytoplasm specifically from the highly specialized cells. In this work, laser capture microdissection (LCM) was used to collect cytoplasmic contents from paraffin‐embedded sections of 4 day post‐inoculation giant cells in tomato roots. Total RNA was isolated from the sections, and used in RT‐PCR to investigate expression of cell cycle genes in giant cells. Two D‐type cyclin genes, LeCycD3;2 and LeCycD3;3, were expressed at higher levels in giant cells compared with other cell‐cycle‐related cyclin genes, suggesting that the induction of the G1 phase of the cell cycle may be triggered in response to stimulation by the infecting nematode. LCM provides a powerful new tool to study the molecular basis of host–pathogen interactions at the cellular or subcellular level.

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Molecular Markers and Cell Cycle Inhibitors Show the Importance of Cell Cycle Progression in Nematode-Induced Galls and Syncytia

Cited by 47 publications

References 11 publications

Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection

Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection

Molecular Insights in the Susceptible Plant Response to Nematode Infection

Using laser capture microdissection to study gene expression in early stages of giant cells induced by root‐knot nematodes

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