Sequence and genetic map of Meloidogyne hapla : A compact nematode genome for plant parasitism

Abstract

We have established Meloidogyne hapla as a tractable model plant-parasitic nematode amenable to forward and reverse genetics, and we present a complete genome sequence. At 54 Mbp, M. hapla represents not only the smallest nematode genome yet completed, but also the smallest metazoan, and defines a platform to elucidate mechanisms of parasitism by what is the largest uncontrolled group of plant pathogens worldwide. The M. hapla genome encodes significantly fewer genes than does the freeliving nematode Caenorhabditis elegans (most notably through a reduction of odorant receptors and other gene families), yet it has acquired horizontally from other kingdoms numerous genes suspected to be involved in adaptations to parasitism. In some cases, amplification and tandem duplication have occurred with genes suspected of being acquired horizontally and involved in parasitism of plants. Although M. hapla and C. elegans diverged >500 million years ago, many developmental and biochemical pathways, including those for dauer formation and RNAi, are conserved. Although overall genome organization is not conserved, there are areas of microsynteny that may suggest a primary biological function in nematodes for those genes in these areas. This sequence and map represent a wealth of biological information on both the nature of nematode parasitism of plants and its evolution.compaction ͉ dauer ͉ development ͉ horizontal gene transfer ͉ gene N ematodes are an abundant and species-rich animal phylum.They share a common body plan on which various adaptations have evolved, enabling Nematoda to occupy essentially all ecological niches, including being parasites of many other organisms (1). Parasitism of plants appears to have arisen independently in three of the major 12 nematode clades (2) and results in annual losses to world agriculture estimated to exceed $US100 billion (3, 4). The majority of damage is caused by sedentary endoparasitic forms in the order Tylenchida, which includes the root-knot nematodes (Meloidogyne spp., RKN). RKN have a cosmopolitan distribution and a host range that spans most crops, although individual RKN species exhibit a more restricted host range. Mature female RKN release hundreds of eggs onto the surface of the root that hatch in the soil as second-stage larvae (L2) and typically reinfect the same plant. RKN L2 are similar in function to dauer larvae (5), which were first described as an adaptation to parasitism to overcome adverse environmental conditions and facilitate dispersal (6), but have been best studied in the free-living nematode Caenorhabditis elegans (7). These larvae are developmentally arrested, motile, nonfeeding, nonaging, and long-lived. Like C. elegans dauers, RKN L2 are detergent-resistant (5), use the glyoxylate pathway (8), and exhibit intestinal morphology with sparse luminal microvilli and numerous lipid storage vesicles that permit long-term survival in the soil. RKN L2 penetrate the root and migrate intercellularly into the vascular cylinder. Migration is accompanied by extensive ...

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes

“…All pectate lyases characterized in plant-parasitic nematodes belong to polysaccharide lyase (PL) family 3. In root-knot nematodes, PL3s are present as multigenic families in both M. incognita and Meloidogyne hapla (7,14). Functional PL3's have also been isolated in cyst nematodes (15,16) and in Aphelenchoidea.…”

TheDitylenchus destructorgenome provides new insights into the evolution of plant parasitic nematodes

“…Compared with other plant nematodes and C. elegans, no obvious extreme gene family expansions, like G protein-coupled receptor (GPCR) in M. halpa [8] and SPRY domain (domain in SP1a and the ryanodine receptor) proteins in G. pallida [9], were found. In the list of the top 25 Pfam hits featured from D. destructor compared with the other clade 12 plant nematodes, more proteins containing trypsin (PF00089), ABC transporter (PF00005), sugar (and other) transporter (PF00083) and short chain dehydrogenase (PF00106) domains (electronic supplementary material, table S3) were found.…”

“…To gain in-depth insights into the parasitic mechanism, genome sequences of nematodes with different life cycles were considered. Genome sequences are available for three sedentary endoparasitic nematodes (M. incognita, M. hapla and G. pallida) and one migratory endoparasite (Pratylenchus coffeae) in this clade [7][8][9][10]. In this study, we sequenced another migratory endoparasitic nematode (Ditylenchus destructor) that was positioned at the base of the most economically important plant nematodes, including root-knot and cyst nematodes, on the SSU rDNA tree [6].…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…A number of cellulase genes probably acquired from different sources have been found in genomes of plantparasitic nematodes [35][36][37]. Interestingly, these cellulase genes have experienced multiple post-transfer duplication events [37] and are different from those present in necromenic nematodes (see above), thereby suggesting that they might be involved in degradation of the plant cell wall.…”