Large parallel deletions are associated with massive gene losses and virulence acquisition in Meloidogyne incognita

Abstract

The root-knot nematode Meloidogyne incognita is a major constraint to crop production worldwide. The resistance gene Mi-1.2 has been widely deployed in tomato varieties to control this parasite. However, virulent nematode populations, overcoming the Mi-1.2-mediated resistance, have increasingly emerged in fields. Understanding the genetic mechanisms underlying resistance circumvention is therefore essential towards sustainable crop protection. Here, we investigated the transcriptomic and genomic changes in two virulent M. incognita populations that escaped Mi-1.2 resistance, as compared to their avirulent progenitor populations controlled by the resistance. These two geographically distant virulent populations were both obtained from experimental evolution on resistant tomatoes. First, our transcriptomic analyses revealed hundreds of strongly downregulated genes, in parallel, in both virulent populations. Most of these down-regulated genes are clustered in two main genome regions. The long-read whole-genome sequencing of the four populations revealed parallel structural variations in both virulent populations. This included two large deletions spanning ca. 1.3 Mb and 0.6 Mb. The two big deletions encompass clusters of downregulated genes, suggesting they have in fact been lost in virulent populations. Short-read genome sequencing and PCR validation confirmed the two deletions in the two virulent populations. The largest deletion includes predicted effector and orphan genes. The parallel large-scale structural variations identified here are likely to underlie the rapid adaptation of M. incognita to Mi-1.2-mediated resistance. These findings highlight genome structural plasticity as one of the potential key drivers of virulence acquisition in these asexually reproducing parasites.