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 isolates, 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. From two geographically distinct M. incognita avirulent isolates, previous experimental evolution assays have allowed producing two virulent M. incognita isolates that escaped Mi-1.2 resistance in tomato. Here, we investigated the transcriptomic and genomic changes in the two virulent M. incognita isolates, as compared to their avirulent progenitor isolates controlled by the resistance. First, our transcriptomic analyses revealed hundreds of strongly downregulated genes, in common, in both virulent isolates. Most of these downregulated genes are clustered in two main genome regions. Long-read whole-genome sequencing of the four isolates revealed parallel structural variations in both virulent isolates. 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 both virulent isolates. Short-read genome sequencing and PCR validation confirmed the two deletions in the two virulent isolates. 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.