Abstract

Root-knot nematode (RKN; Meloidogyne spp.) is a major crop pathogen worldwide. Effective resistance exists for a few plant species, including that conditioned by Mi in tomato (Solanum lycopersicum). We interrogated the root transcriptome of the resistant (Mi+) and susceptible (Mi-) cultivars 'Motelle' and 'Moneymaker,' respectively, during a time-course infection by the Mi-susceptible RKN species Meloidogyne incognita and the Mi-resistant species Meloidogyne hapla. In the absence of RKN infection, only a single significantly regulated gene, encoding a glycosyltransferase, was detected. However, RKN infection influenced the expression of broad suites of genes; more than half of the probes on the array identified differential gene regulation between infected and uninfected root tissue at some stage of RKN infection. We discovered 217 genes regulated during the time of RKN infection corresponding to establishment of feeding sites, and 58 genes that exhibited differential regulation in resistant roots compared to uninfected roots, including the glycosyltransferase. Using virus-induced gene silencing to silence the expression of this gene restored susceptibility to M. incognita in 'Motelle,' indicating that this gene is necessary for resistance to RKN. Collectively, our data provide a picture of global gene expression changes in roots during compatible and incompatible associations with RKN, and point to candidates for further investigation.

Highlights

  • Root-knot nematode (RKN; Meloidogyne spp.) is a major crop pathogen worldwide

  • There is a strong correlation between water uptake and RKN inoculum (Meon et al, 1978), suggesting that much of the yield loss caused by RKN can be attributed to compromised root function, it is clear that RKN infection broadly influences whole plant physiology (Myuge, 1956; Owens and Rubinstein, 1966; Loveys and Bird, 1973; Wallace, 1974)

  • At the time we initiated this study, the most comprehensive source of tomato gene sequences was a collection of ESTs clustered into tentative consensus (TC) sequences by The Institute for Genomic Research (TIGR)

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Summary

Introduction

Root-knot nematode (RKN; Meloidogyne spp.) is a major crop pathogen worldwide. Effective resistance exists for a few plant species, including that conditioned by Mi in tomato (Solanum lycopersicum). Various approaches, including construction of subtractive cDNA libraries from individual GCs (Wilson et al, 1994), promoter-trapping strategies (Sijmons et al, 1994; Barthels et al, 1997; Favery et al, 2004), and in situ hybridizations (Lohar et al, 2004; Gal et al, 2006), have examined gene expression patterns during RKN feeding site initiation These experiments have revealed that genes regulating the cell cycle (Niebel et al, 1996; de Almeida Engler et al, 1999), cell wall synthesis (Niebel et al, 1993; Goellner et al, 2001; Vercauteren et al, 2002), and transcription regulation (Bird and Wilson, 1994) are up-regulated in GCs. Based on a mixed-model analysis (Wolfinger et al, 2001), we found that, in the absence of RKN, only one gene, encoding a glycosyltransferase, was found to be differentially regulated between the ‘Moneymaker’ and ‘Motelle’ transcriptomes Experimental downregulation of this gene via virus-induced gene silencing (VIGS) restores susceptibility to M. incognita in ‘Motelle,’ indicating that this function is necessary for Mi-mediated resistance. Glycosyltransferases have been implicated in carbohydrate biosynthesis and associated in plant stress and defense responses (Dixon, 2001; Qi et al, 2005; Vogt and Jones, 2000) and cell wall synthesis (Egelund et al, 2004; Lao et al, 2003); this is the first report, to our knowledge, of a role for a glycosyltransferase in nematode resistance

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