Evolution of parasitism genes in the plant parasitic nematodes

Abstract

The plant-parasitic nematodes are considered as one of the most destructive pests, from which the migratory and sedentary endoparasitic plant parasitic nematodes infect more than 4000 plant species and cause over $100 billion crop losses annually worldwide. These nematodes use multiple strategies to infect their host and to establish a successful parasitism inside the host such as cell-wall degradation enzymes, inhibition of host defense proteins, and molecular mimicry. In the present study, the main parasitism-associated gene families were identified and compared between the migratory and sedentary endoparasitic nematodes. The results showed that the migratory and sedentary endoparasitic nematodes share a core conserved parasitism mechanism established throughout the evolution of parasitism. However, genes involved in pectin degradation and hydrolase activity are rapidly evolving in the migratory endoparasitic nematodes. Additionally, cell-wall degrading enzymes such as GH45 cellulases and pectate lyase and peptidase and peptidase inhibitors were expanded in the migratory endoparasitic nematodes. The molecular mimicry mechanism was another key finding that differs between the endoparasitic and sedentary parasitic nematodes. The PL22 gene family, which is believed to play a significant role in the molecular mechanisms of nematode parasitism, has been found to be present exclusively in migratory endoparasitic nematodes. Phylogenetic analysis has suggested that it was de novo born in these nematodes. This discovery sheds new light on the molecular evolution of these parasites and has significant implications for our understanding of their biology and pathogenicity. This study contributes to our understanding of core parasitism mechanisms conserved throughout the nematodes and provides unique clues on the evolution of parasitism and the direction shaped by the host.

Figure 1

The Phylogenetic Tree of the Plant-Parasitic Nematodes. The phylogenetic tree was generated on 2084 orthogroups, each with at least 23.1% of species containing single-copy genes. The tree was rooted at the midpoint. The nematode species were divided into two distinct clusters. The migratory endoparasitic nematodes perform a separate clade from the sendentary endoparasitic nematodes.

Figure 2

The Distribution of Genera- and Species-Specific Ortholog Families in The Plant-Parasitic Nematodes.2985 ortholog families were shared between nematode species. The highest number of species-specific ortholog families (13,864) were detected in M. floridensis, while the lowest number of species-specific ortholog families (457) were detected in M. javanica.

Figure 3

The Top 25 Annotation Results of Rapidly Evolving Gene Families Involved in Parasitism in The Migratory Endoparasitic Nematodes Compared to the Sedentary Endoparasitic Nematodes. (A) Bursaphelenchus xylophilus. (B) Ditylenchus destructor. (C) Ditylenchus dipsaci.

Figure 4

The Correlation Analysis of The Main Peptidase Families in The Plant-Parasitic Nematodes. BXY: Bursaphelenchus xylophilus, DDES: Ditylenchus destructor, DDIP: Ditylenchus dipsaci, GPAL: Globodera pallida, GROS: Globodera rostochiensis, HGLY: Heterodera glycines, MARE: Meloidogyne arenaria, MENT: Meloidogyne enterolobii, MFLO: Meloidogyne floridensis, MGRA: Meloidogyne graminicola, MHAP: Meloidogyne hapla, MINC: Meloidogyne incognita, MJAVA: Meloidogyne javanica. The nematodes were separated into two clusters based on peptidase numbers in genomes. The migratory endoparasitic nematode B. xylophilus performed a distinct clade from other species Other migratory endoparasites (Ditylenchus spp.) were placed as a sister clade to sedentary endoparasites.

Figure 5

The Correlation Analysis of The Main Peptidase Inhibitor Families in The Plant-Parasitic Nematodes. BXY: Bursaphelenchus xylophilus, DDES: Ditylenchus destructor, DDIP: Ditylenchus dipsaci, GPAL: Globodera pallida, GROS: Globodera rostochiensis, HGLY: Heterodera glycines, MARE: Meloidogyne arenaria, MENT: Meloidogyne enterolobii, MFLO: Meloidogyne floridensis, MGRA: Meloidogyne graminicola, MHAP: Meloidogyne hapla, MINC: Meloidogyne incognita, MJAVA: Meloidogyne javanica. The Pearson Correlation test based on the number of peptidase inhibitors in the plant-parasitic nematodes separated B. xylophilus from other species and placed this species as a separate clade.

Figure 6

The Distribution of Plant Cell Wall Degrading Enzymes in The Plant-Parasitic Nematodes. BXY: Bursaphelenchus xylophilus, DDES: Ditylenchus destructor, DDIP: Ditylenchus dipsaci, GPAL: Globodera pallida, GROS: Globodera rostochiensis, HGLY: Heterodera glycines, MARE: Meloidogyne arenaria, MENT: Meloidogyne enterolobii, MFLO: Meloidogyne floridensis, MGRA: Meloidogyne graminicola, MHAP: Meloidogyne hapla, MINC: Meloidogyne incognita, MJAVA: Meloidogyne javanica. The PL3, Pectate Lyase, is one of the most significant contributors to clustering enzymes in the nematode species and is abundant in the root-knot nematodes (Meloidogyne species) compared to other nematode species. This family performed a separate clade from other cell-wall degrading enzymes in the nematode genomes.

Figure 7

The Phylogenetic Tree of the PL22 (Oligogalacturonate lyase/oligogalacturonide lyase). The tree was generated using IQ-TREE v2.0 with -m MFP (model finder parameter) with -B 1000 (1000 bootstrap) options. The tree was separated into two clades. The black branch represent Bacteria clade, and the red branch represents nematodes. The green and blue branches show two differenct clades of the PL22 genes detected in the migratory endoparasitic nematodes (Bursaphelenchus xylophilus, Ditylenchus destructor and Ditylenchus dipsaci). Numbers on nodes represent bootstrap values. The nematode PL22 genes showed a clear pattern that this gene family could be a eukaryote origin.