Both Induction and Morphogenesis of Cyst Nematode Feeding Cells Are Mediated by Auxin

Goverse, A.; Overmars, H.A.; Engelbertink, J.; Schots, A.; Bakker, J.; Helder, J.

doi:10.1094/mpmi.2000.13.10.1121

Cited by 175 publications

(235 citation statements)

References 52 publications

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“…In line with our experimental data, ET biosynthesis and signaling were generally down-regulated in giant cells on Arabidopsis (Barcala et al, 2010). Strikingly, ET has been suggested to be critical for syncytia formation during cyst nematode infections on Arabidopsis (Goverse et al, 2000;Wubben et al, 2001). However, for RKN, Lohar and Bird (2003) found no changes in susceptibility in ET-resistant Lotus japonicus, and the fact that ET was not detected in galls at 1 to 2 d post infection (Glazer et al, 1983) in combination with the transcriptional patterns observed in this study and by Barcala et al (2010) argue against a crucial role for ET-activated pathways during early giant cell differentiation; rather, they suggest that the RKN is actively suppressing the ET pathway and other defense signaling pathways in the root.…”

Section: Discussionsupporting

confidence: 89%

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

et al. 2011

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Complex defense signaling pathways, controlled by different hormones, are involved in the reaction of plants to a wide range of biotic and abiotic stress factors. We studied the ability of salicylic acid, jasmonate (JA), and ethylene (ET) to induce systemic defense in rice (Oryza sativa) against the root knot nematode Meloidogyne graminicola. Exogenous ET (ethephon) and JA (methyl jasmonate) supply on the shoots induced a strong systemic defense response in the roots, exemplified by a major up-regulation of pathogenesis-related genes OsPR1a and OsPR1b, while the salicylic acid analog BTH (benzo-1,2,3-thiadiazole-7-carbothioic acid S-methyl ester) was a less potent systemic defense inducer from shoot to root. Experiments with JA biosynthesis mutants and ET-insensitive transgenics showed that ET-induced defense requires an intact JA pathway, while JA-induced defense was still functional when ET signaling was impaired. Pharmacological inhibition of JA and ET biosynthesis confirmed that JA biosynthesis is needed for ET-induced systemic defense, and quantitative real-time reverse transcription-polymerase chain reaction data revealed that ET application onto the shoots strongly activates JA biosynthesis and signaling genes in the roots. All data provided in this study point to the JA pathway to play a pivotal role in rice defense against root knot nematodes. The expression of defense-related genes was monitored in root galls caused by M. graminicola. Different analyzed defense genes were attenuated in root galls caused by the nematode at early time points after infection. However, when the exogenous defense inducers ethephon and methyl jasmonate were supplied to the plant, the nematode was less effective in counteracting root defense pathways, hence making the plant more resistant to nematode infection.

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Section: Discussionsupporting

confidence: 89%

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

et al. 2011

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“…Similar to nodule initiation, an enhanced auxin response has been visualized at the infection sites of both cyst and root-knot nematodes, whereas auxin signaling mutants have shown significantly lower nematode infection (Hutangura et al, 1999;Goverse et al, 2000;Karczmarek et al, 2004;Grunewald et al, 2008). This suggests that auxin might trigger the initiation of both giant cells and syncytia and that auxin-dependent programs are needed for NFS establishment.…”

Section: Nematode Infection Requires Changes In the Host's Auxin Respmentioning

confidence: 94%

“…Indeed, when lateral auxin transport was inhibited chemically or genetically, radial expansion of the syncytial cell was inhibited, and small malformed cysts were produced (Goverse et al, 2000;Grunewald et al, 2009). Intriguingly, nematodes can influence the polar localization of the PIN proteins, resulting in transport of auxin to the adjacent tissues, as indicated by the redirection of basal localized PIN3 to the lateral plasma membranes (Figure 2) (Grunewald et al, 2009).…”

Section: Nematode Infection Requires Changes In the Host's Auxin Respmentioning

confidence: 99%

Manipulation of Auxin Transport in Plant Roots during Rhizobium Symbiosis and Nematode Parasitism

et al. 2009

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The plant rhizosphere harbors many different microorganisms, ranging from plant growth-promoting bacteria to devastating plant parasites. Some of these microbes are able to induce de novo organ formation in infected roots. Certain soil bacteria, collectively called rhizobia, form a symbiotic interaction with legumes, leading to the formation of nitrogen-fixing root nodules. Sedentary endoparasitic nematodes, on the other hand, induce highly specialized feeding sites in infected plant roots from which they withdraw nutrients. In order to establish these new root structures, it is thought that these organisms use and manipulate the endogenous molecular and physiological pathways of their hosts. Over the years, evidence has accumulated reliably demonstrating the involvement of the plant hormone auxin. Moreover, the auxin responses during microbe-induced de novo organ formation seem to be dynamic, suggesting that plant-associated microbes can actively modify their host's auxin transport. In this review, we focus on recent findings in auxin transport mechanisms during plant development and on how plant symbionts and parasites have evolved to manipulate these mechanisms for their own purposes.

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“…It was shown by Goverse et al (2000) and Karczmarek et al (2004) that auxin plays a crucial role in the development of nematode feeding sites. They suggested that nematodes are able locally to increase auxin concentration, thus in turn enhancing ethylene production.…”

Section: Plant Hormones Affect Expression Of Atcel2 and Kor3mentioning

confidence: 99%

“…glucanases) but also plant hormones or hormone-related compounds (De Meutter et al, 2005). On the other hand, nematodes are able to alter the hormone homeostasis within feeding sites, as shown by Goverse et al (2000) and later by Karczmarek et al (2004). Both strategies may influence expression of essential genes and thereby support the change from healthy root tissue to a feeding site.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis endo‐1,4‐β‐glucanases are involved in the formation of root syncytia induced by Heterodera schachtii

et al. 2007

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SummaryCyst nematodes induce root syncytia with specific features such as hypertrophy, increased metabolic activity and fusion with adjacent cells. Cell walls of the syncytia undergo massive changes such as thickening, local dissolution and formation of ingrowths. Cell wall degrading and modifying proteins are apparently involved in syncytium formation but detailed knowledge of this is still limited. Therefore, we studied the regulation and function of the entire Arabidopsis endo-1,4-b-glucanase gene family in syncytia induced by Heterodera schachtii. Endo-1,4-b-glucanases hydrolyze the 1,4-b-glucosidic linkages between glucose residues. Using semi-quantitative and quantitative approaches we identified seven genes that are upregulated in syncytia. Two of these genes, coding for secreted AtCel2 and membrane-bound KOR3, are shoot-specific but show high expression in syncytia at different developmental stages. In silico analysis of the promoter regions of both genes compared with other genes with modified regulation in nematode feeding sites did not reveal specific cis-acting elements that could be related to specific transcription in syncytia. However, motifs responsive to sugar and different plant hormones were identified. Accordingly, treatments with sucrose, gibberellic acid and NAA induced upregulation of AtCel2, whereas ABA triggered downregulation of both AtCel2 and KOR3 in roots. As AtCel2 is related to degradation of the cell wall matrix, we analysed the hemicellulose content in syncytia. The measured values resembled the expression pattern of AtCel2. A distinctly reduced number of females developed in cel2 and kor3 T-DNA mutants, and we therefore conclude that endo-1,4-b-glucanases play an important role in the formation and function of syncytia.

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Both Induction and Morphogenesis of Cyst Nematode Feeding Cells Are Mediated by Auxin

Cited by 175 publications

References 52 publications

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

Manipulation of Auxin Transport in Plant Roots during Rhizobium Symbiosis and Nematode Parasitism

Arabidopsis endo‐1,4‐β‐glucanases are involved in the formation of root syncytia induced by Heterodera schachtii

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