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The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode - PubMed

  • ️Wed Jan 01 2014

The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode

James A Cotton et al. Genome Biol. 2014.

Abstract

Background: Globodera pallida is a devastating pathogen of potato crops, making it one of the most economically important plant parasitic nematodes. It is also an important model for the biology of cyst nematodes. Cyst nematodes and root-knot nematodes are the two most important plant parasitic nematode groups and together represent a global threat to food security.

Results: We present the complete genome sequence of G. pallida, together with transcriptomic data from most of the nematode life cycle, particularly focusing on the life cycle stages involved in root invasion and establishment of the biotrophic feeding site. Despite the relatively close phylogenetic relationship with root-knot nematodes, we describe a very different gene family content between the two groups and in particular extensive differences in the repertoire of effectors, including an enormous expansion of the SPRY domain protein family in G. pallida, which includes the SPRYSEC family of effectors. This highlights the distinct biology of cyst nematodes compared to the root-knot nematodes that were, until now, the only sedentary plant parasitic nematodes for which genome information was available. We also present in-depth descriptions of the repertoires of other genes likely to be important in understanding the unique biology of cyst nematodes and of potential drug targets and other targets for their control.

Conclusions: The data and analyses we present will be central in exploiting post-genomic approaches in the development of much-needed novel strategies for the control of G. pallida and related pathogens.

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Figures

Figure 1
Figure 1

Scaffolds of Globodera pallida show little or no synteny with other nematodes. (A) Shows all 133 G. pallida scaffolds that contain at least five one-to-one orthologs with Caenorhabditis elegans with scaffolds ordered to maximise colinearity with the C. elegans genome. Lines connect orthologs, and G. pallida scaffolds are coloured with a mixture of the colours used for C. elegans scaffolds they have orthologs with, weighted by the numbers of orthologs to each. The relative positions of one-to-one orthologs between (B) the largest G. pallida scaffold (scaffold 1) and (C) the G. pallida scaffold with the largest number of one-to-one orthologs to C. elegans (scaffold 25). Colour and orientation of scaffolds and chromosomes are as in (A). Note that the G. pallida and C. elegans sequences are not drawn to scale in (B) or (C). (D, E) Show one-to-one orthologs between M. hapla and G. pallida, including those M. hapla scaffolds (blue) that have orthologs to (D)G. pallida scaffold 1 and (E)G. pallida scaffold 25 (red) and orthologs from those scaffolds to other G. pallida scaffolds (yellow).

Figure 2
Figure 2

Comparative genomics of Globodera pallida and other plant parasitic nematodes. (A) Euler diagrams of shared presence-and-absence of gene families in plant-parasitic nematodes with published genome descriptions, the free-living model Caenorhabditis elegans and the spirurid animal parasite Brugia malayi. (B) Phylogenetic analysis of genome content. Tree shown is a maximum-likelihood phylogeny based on concatenated alignment of single-copy orthologs. Values on edges represent the inferred numbers of births (+) and deaths (-) of gene families along that edge. Note that our approach cannot distinguish gene family losses from gains on the basal branches of this tree, so for example the value of 1,476 gene family gains on the basal branch will include gene families lost on the branch leading to B. malayi. Pie charts represent the gene family composition of each genome - the area of the circle is proportional to the predicted proteome size, and wedges represent the numbers of proteins predicted to be either singletons (that is, not members of any gene family), members of gene families common to all six genomes, members of gene families present only in a single genome, and members of all other gene families.

Figure 3
Figure 3

Transcriptional profiling of the G. pallida lifecycle. (A) Number of genes up- and downregulated between different stages in the G. pallida lifecycle. Labelled transitions are between egg and J2, J2 and early infection (7 and 14 dpi), early and late infection (21, 28 and 35 dpi) and J2 larvae and adult males. (B) Heatmap showing clustered expression profiles for all 2,052 differentially expressed genes. Genes are clustered to reflect similarity of expression profiles and then ordered by stage of highest expression, as labelled on the circumference of the figure.

Figure 4
Figure 4

Expression dynamics of Globodera pallida effectors. (A) Heatmap of 123 effector genes highlights the expression of dorsal-gland like protein (DGL) genes in J2 and 4D06 (448) family effector homologs in early infection. A variety of effector-like genes is also expressed across stages. One chorismate mutase (CM) is expressed in J2, while another is expressed principally in early infection. (B) SPRYSEC genes are present in a wide range of nematodes, but are massively expanded in G. pallida. The phylogenetic tree shows that some homologs, including the two most highly expressed across stages, are distributed among those from other species. The G. pallida radiation is monophyletic however. Most copies are expressed and expression does not often correlate with phylogenetic clusters. Expression tends to be high during the early stage of parasitism, however one particular phylogenetic cluster shows high expression in eggs and males.

Figure 5
Figure 5

Phylogeny and expression of glutathione synthetase genes in G. pallida. (A) Phylogeny of all G. pallida glutathione synthetase genes that can be aligned over at least 200 bp. Non-G. pallida sequences are from Meloidogyne incognita, Bursaphelenchus xylophilus, Wuchereria bancrofti and from mammals. Red sequences are predicted to have signal peptides. (B) Different clades of these genes show different expression dynamics. The single-copy outgroup sequence, apparently shared by all nematodes, is constitutively expressed across the lifecycle (black line). Members of the clade shared with some M. incognita sequences (green) show a peak of expression at 14 dpi, while the G. pallida-specific expansion (purple in panel A) shows a peak of expression at 7 dpi, a pattern more pronounced in copies predicted to have signal peptides (red) than those without (blue). Lines are mean expression across gene copies for each lifecycle stage; shading covers a 99% exponential confidence interval for the mean.

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