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

Abstract

Heterodera 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. Here, we use PacBio long-read technology to assemble a H. glycines genome of 738 contigs into 123Mb with annotations for 29,769 genes. The genome contains significant numbers of repeats (34%), tandem duplicates (18.7Mb), and horizontal gene transfer events (151 genes). Using previously published effector sequences, the newly generated H. glycines genome, and comparisons to other nematode genomes, we investigate the evolutionary mechanisms responsible for the emergence and diversification of effector genes.

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

“…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, 2019;reviewed by Jones et al, 2013). 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, 2006) with high resistance to all races detected in the SCN survey in Huang-Huai Valleys (Lian et al, 2016), except for race X12, to which it is highly susceptible.…”

“…Multiple libraries with different insert sizes were constructed from Figure 2b). In addition, the sequencing results (SCN_Lian) were compared with the newly released sequencing results (SCN_Masonbrink) of 2019 (Masonbrink et al, 2019) and the genomes of the plant-parasitic nematode M. hapla (Opperman et al, 2008) and the free-living nematode C. elegans (The C. elegans sequencing consortium, 1998) ( (Table S6); therefore, the genome assembly has high single-base accuracy. In addition, the GC content and average depth of the assembled genome were calculated and mapped using 10k Windows without repeated calculation.…”

“…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, 2019).…”

“…Genome sequencing of the free-living nematode Caenorhabditis elegans (The C. elegans sequencing consortium, 1998) and the parasitic nematodes Meloidogyne hapla (Opperman et al, 2008) and Globodera rostochiensis (Akkeretal.,2016)hasprovidedreferencegenomesthat can be utilized for comparison with parasitic nematodes. The genetic mapofSCNwasreportedin2005with10linkagegroups (Atibalentja etal.,2005).AlthoughadraftgenomesequenceforSCNwasrecently published with 738 contigs in the genome, these contigs were not successfully assembled into chromosomes (Masonbrink et al, 2019).…”

Comparative Genomics Reveals Novel Target Genes Towards Specific Control of Plant-Parasitic Nematodes

“…Furthermore, the M. incognita genome employed in this original study [20] was later shown to be partially incomplete, with an improved version published afterwards [23]. Meanwhile, the availability of genome sequences for additional RKN species [24,[26][27][28][29], as well as for other plant-parasitic nematode species, including cyst nematodes [15,34,35], stem and bulb nematodes [36,37], or the more distantly related pine wilt disease nematode [38], greatly expanded the diversity of genomes for plant-parasitic nematode species. Similar genome sequencing efforts were also accomplished in the other nematode clades, including in animal parasites and free-living species, offering a novel opportunity for nematode comparative genomics.…”