The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes

Abstract

BackgroundHeterodera glycines, commonly referred to as the soybean cyst nematode (SCN), is an obligatory and sedentary plant parasite that causes over a billion-dollar yield loss to soybean production annually. Although there are genetic determinants that render soybean plants resistant to certain nematode genotypes, resistant soybean cultivars are increasingly ineffective because their multi-year usage has selected for virulent H. glycines populations. The parasitic success of H. glycines relies on the comprehensive re-engineering of an infection site into a syncytium, as well as the long-term suppression of host defense to ensure syncytial viability. At the forefront of these complex molecular interactions are effectors, the proteins secreted by H. glycines into host root tissues. The mechanisms of effector acquisition, diversification, and selection need to be understood before effective control strategies can be developed, but the lack of an annotated genome has been a major roadblock.ResultsHere, we use PacBio long-read technology to assemble a H. glycines genome of 738 contigs into 123 Mb with annotations for 29,769 genes. The genome contains significant numbers of repeats (34%), tandem duplicates (18.7 Mb), and horizontal gene transfer events (151 genes). A large number of putative effectors (431 genes) were identified in the genome, many of which were found in transposons.ConclusionsThis advance provides a glimpse into the host and parasite interplay by revealing a diversity of mechanisms that give rise to virulence genes in the soybean cyst nematode, including: tandem duplications containing over a fifth of the total gene count, virulence genes hitchhiking in transposons, and 107 horizontal gene transfers not reported in other plant parasitic nematodes thus far. Through extensive characterization of the H. glycines genome, we provide new insights into H. glycines biology and shed light onto the mystery underlying complex host-parasite interactions. This genome sequence is an important prerequisite to enable work towards generating new resistance or control measures against H. glycines.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5485-8) contains supplementary material, which is available to authorized users.

Chromosome‐level reference genome of X12, a highly virulent race of the soybean cyst nematode Heterodera glycines

“…The assembly was estimated to contain 86.29% of core genes according to CEGMA analysis and 53.4% of complete single‐copy genes. The assembled genome is more contiguous than is the previously published H. glycines genome (Masonbrink et al, ), with 1.2‐fold more contigs and a 1.09‐fold greater N50 contig length. The mapping rate for reads back to the assembled genome is approximately 90.72%.…”

“…The assembled genome is estimated to be 141.01 Mb, with scaffold and contig N50 sizes of 16.27 Mb and 330.54 kb, respectively (Figure b). In addition, the sequencing results ( SCN _ Lian ) were compared with the newly released sequencing results ( SCN _ Masonbrink ) of 2019 (Masonbrink et al, ) and the genomes of the plant–parasitic nematode M. hapla (Opperman et al, ) and the free‐living nematode C. elegans (The C. elegans sequencing consortium, ) (Table ). The genome size of SCN _ Lian is 141.01 Mb, which is almost identical to that of SCN_Masonbrink , at 123 Mb.…”

“…Remarkably, only 53.4% of the genes in the H. glycines assembly are single copy according to the BUSCO analysis, with 3.7% duplicated. For comparison, the BUSCO results for SCN_Masonbrink indicate that 56% of the genes in H. glycines are single copy, with 16% duplicated (Masonbrink et al, ).…”

“…The genomes of Heterodera glycines are challenging to sequence and assemble because these animals are dioecious with exceptionally high levels of population heterozygosity (Masonbrink et al, ; reviewed by Jones et al, ). To assemble this highly heterozygous population, H. glycines race X12 was first purified using ZDD2315, an elite resistant soybean germplasm in China (Lu, Gai, Zheng, & Li, ) with high resistance to all races detected in the SCN survey in Huang‐Huai Valleys (Lian et al, ), except for race X12, to which it is highly susceptible.…”

“…The genetic map of SCN was reported in 2005 with 10 linkage groups (Atibalentja et al, ). Although a draft genome sequence for SCN was recently published with 738 contigs in the genome, these contigs were not successfully assembled into chromosomes (Masonbrink et al, ). Genome sequencing of the X12 race is extremely important for our understanding of SCN virulence genes.…”