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 free-living 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.

Fig. 1.

Genetic linkage map of M. hapla. Linkage groups (LG) with three or more markers at LOD8 are shown. At this LOD, 17 of the 293 markers could not be assigned to linkage groups (yellow box). H1 and H2 are PCR markers used to monitor crosses. Markers with the same name and suffix a or b segregate as codominant markers. Stars indicate markers that deviate from 1:1 segregation at P > 0.01. Numbers to the left of the linkage groups indicate genetic distances in cM. Markers highlighted in pink are codominant and have been merged with the genomic sequence of VW9. Numbers in blue indicate contig number from the assembly.

Fig. 2.

Protein analysis for M. hapla genome. (A) The 20 most common protein domains found in M. hapla based on an HMM search of Pfam22 compared with the number of occurrences of each domain found in C. elegans. Domains that are within the 20 most common for C. elegans are indicated with a *. Number of domains detected are indicated. (B) Percent similarity of genomic sequence to known proteins categorized based on best BlastX match to NCBI's nonredundant protein database. (C) Summary of the three major GO categories based on a comparison of protein sequences to the Uniprot swissprot+trembl database.

Fig. 3.

The pectate lysae gene family in M. hapla. (A) Neighbor joining analysis of pectate lysases encoded by 22 genes throughout the M. hapla genome; these enzymes are not found in C. elegans. Secreted pectate lysase from Streptomyces coelicolor was used as an outgroup. Colors map to genomic locations shown in B.