Abstract
Plant-parasitic nematodes cause extensive annual yield losses to worldwide agricultural production. Most cultivated plants have no known resistance against nematodes and the few bearing a resistance gene can be overcome by certain species. Chemical methods that have been deployed to control nematodes have largely been banned from use due to their poor specificity and high toxicity. Hence, there is an urgent need for the development of cleaner and more specific control methods. Recent advances in nematode genomics, including in phytoparasitic species, provide an unprecedented opportunity to identify genes and functions specific to these pests. Using phylogenomics, we compared 61 nematode genomes, including 16 for plant-parasitic species and identified more than 24,000 protein families specific to these parasites. In the genome of Meloidogyne incognita, one of the most devastating plant parasites, we found ca. 10,000 proteins with orthologs restricted only to phytoparasitic species and no further homology in protein databases. Among these phytoparasite-specific proteins, ca. 1000 shared the same properties as known secreted effectors involved in essential parasitic functions. Of these, 68 were novel and showed strong expression during the endophytic phase of the nematode life cycle, based on both RNA-seq and RT-qPCR analyses. Besides effector candidates, transcription-related and neuro-perception functions were enriched in phytoparasite-specific proteins, revealing interesting targets for nematode control methods. This phylogenomics analysis constitutes a unique resource for the further understanding of the genetic basis of nematode adaptation to phytoparasitism and for the development of more efficient control methods.
Highlights
Plant parasitism has emerged at least four times independently in the phylum Nematoda and encompasses approximately 15% of the whole nematode biodiversity [1]
As Alien Index (AI) ≥ 14 represents a good balance between precision and recall of phylogenetically confirmed horizontal gene transfer (HGT) [48], we considered M. incognita proteins returning an AI ≥ 14 as likely to result from acquisition via HGT
By comparing the 12,683 M. incognita plant-parasitic nematodes (PPN)-specific proteins identified by OrthoFinder and the Diamond homology search, we found that only 22% (2770) returned hits against the NCBI’s nr databank
Summary
Plant parasitism has emerged at least four times independently in the phylum Nematoda and encompasses approximately 15% of the whole nematode biodiversity [1]. Phytoparasitic nematodes cause considerable damage to worldwide agriculture, only a few species, mainly in the clade Tylenchida, are responsible for the majority of the losses. Of the genus Meloidogyne are the most devastating plant-parasitic nematodes, with susceptible hosts covering more than 4000 plant species, including the major economically important crops [2,3]. RKN, the tropical polyphagous apomictic species M. incognita, M. javanica and M. arenaria, together with the facultative sexual species M. hapla from temperate regions, are considered the most damaging. Annual global crop production losses due to root infection by these sedentary endoparasites exceed. Most severe yield losses occur in tropical regions, with the RKN wide host range restricting options for disease control through crop rotation. Within RKN species, this wide host range is subdivided into ‘host races’ with distinct ranges of host compatibilities. The employment of resistant cultivars to reduce the losses can be limited due to the occurrence of ‘resistance-breaking’ virulent RKN isolates and species mixtures [7]
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