Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection

Abstract

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.

Dynamics in the tomato root transcriptome on infection with the potato cyst nematode Globodera rostochiensis

“…The presence of the parasite induces drastic changes in plant gene expression (reviewed by Gheysen and Fenoll, 2002). Several molecular approaches have been exploited to pinpoint changes in plant gene expression as a result of nematode infections, including protein analysis (Rahimi et al, 1993), promoter reporter-gene fusions (Barthels et al, 1997;Favery et al, 1998Favery et al, , 2004Goddijn et al, 1993;Goverse et al, 1998;Mazarei et al, 2003Mazarei et al, , 2004Niebel et al, 1996;Puzio et al, 2000), in situ hybridization (Goellner et al, 2001;Niebel et al, 1993), reverse transcriptase-polymerase chain reaction (RT-PCR) (Karczmarek et al, 2008;Vaghchhipawala et al, 2001), differential display (Hermsmeier et al, 1998(Hermsmeier et al, , 2000Vercauteren et al, 2001), microarray analysis (Alkharouf et al, 2006;Hammes et al, 2005;Ithal et al, 2007;Jammes et al, 2005;Khan et al, 2004;Puthoff et al, 2003Puthoff et al, , 2007 and serial analysis of gene expression (SAGE) (Uehara et al, 2007). The outcome of these studies has culminated in the identification of a relatively small group of genes that are involved in a wide range of nematode-affected plant processes.…”

Manipulation of two α‐endo‐β‐1,4‐glucanase genes, AtCel6 and GmCel7, reduces susceptibility to Heterodera glycines in soybean roots

“…Many crops and Arabidopsis share similar modes of action regarding disease resistance. For example, the homologues of the avr genes of bean and pea (Dangl et al, 1992) and an SCNinduced gene of soybean (Mazarei et al, 2004) were identified in Arabidopsis and behaved in a similar fashion. Conversely, Arabidopsis resistance genes effective against crop pathogens have been identified and found to have the same functionality in crops.…”

“…Mazarei et al . (), who analysed the expression of the Arabidopsis homologue of a soybean gene that was up‐regulated during SCN infection, found that the pair of homologues behaved in a similar fashion following cyst nematode infection, and that the promoter of the Arabidopsis homologue functioned normally in soybean. They suggested that Arabidopsis shares molecular events of cyst nematode parasitism with soybean, and that the Arabidopsis– H. schachtii interaction is a suitable model for the soybean– H. glycines pathosystem.…”

“…Exploitation of the extensive genetic knowledge that is available on the model species Arabidopsis thaliana, which is readily infected by the sugar beet cyst nematode (H. schachtii) (Sijmons et al, 1991), a close relative of SCN, may facilitate such a project. Mazarei et al (2004), who analysed the expression of the Arabidopsis homologue of a soybean gene that was up-regulated during SCN infection, found that the pair of homologues behaved in a similar fashion following cyst nematode infection, and that the promoter of the Arabidopsis homologue functioned normally in soybean. They suggested that Arabidopsis shares molecular events of cyst nematode parasitism with soybean, and that the Arabidopsis-H. schachtii interaction is a suitable model for the soybean-H. glycines pathosystem.…”

Functional characterization of Arabidopsis genes changing expression during cyst nematode Heterodera schachtii infection

“…Several lines of evidence showed that phytohormones play an important role in response to cyst nematode infection and syncytium formation. GUS activity has been detected in syncytia when fused with auxin-responsive plant promoters (Karczmarek et al 2004, Mazarei et al 2004. Using auxin-insensitive tomato and Arabidopsis mutants, Goverse et al (2000) demonstrated the direct involvement of auxin in feeding site formation.…”