Nematode resistance in plants: the battle underground

In Europe, root-knot nematodes are increasingly important. Out of more than 90 Meloidogyne species currently described, 23 have been found on the continent. In the cooler climates, Meloidogyne hapla , M. naasi , M. chitwoodi and M. fallax are prevalent. Meloidogyne arenaria , M. javanica and M. incognita are the most common species in warmer conditions of southern Europe, but also in glasshouses in northern Europe. Morphological identification of root-knot nematodes is difficult and time consuming; therefore, many research groups have been developing molecular techniques for identification of Meloidogyne species. Meloidogyne chitwoodi and M. fallax are quarantine organisms and subject to regulations, and the highly aggressive M. enterolobii has been added to the EPPO alert list. Differences between temperate and tropical Meloidogyne species and their prevalence in Europe imply the need for different management strategies in south and north Europe. Possible crop rotations for the control of root-knot nematodes are limited due to the wide host range of several important species. The banning of methyl bromide and restrictions on other fumigant pesticides in the EU have increased the application of biofumigation significantly in south Europe. The egg-parasitising fungus Paecilomyces lilacinus is commercialised in Germany and applied as dispersible granules for application in water. Intensive research is conducted on the egg-parasitising fungus Pochonia chlamydosporia , and the obligate parasitic bacterium Pasteuria penetrans. European research has paid much attention to resistance breeding and selection. The Mi gene of tomato is widely used but resistance-breaking populations of M. incognita and M. javanica have been reported in different countries.

Root-knot nematodes ( Meloidogyne spp.) in Europe

Nematodes are considered among the most difficult animals to identify. DNA-based diagnostic methods have already gained acceptance in applications ranging from quarantine determinations to assessments of biodiversity. Researchers are currently in an information-gathering mode, with intensive efforts applied to accumulating nucleotide sequence of 18S and 28S ribosomal genes, internally transcribed spacer regions, and mitochondrial genes. Important linkages with collateral data such as digitized images, video clips and specimen voucher web pages are being established on GenBank and NemATOL, the nematode-specific Tree of Life database. The growing DNA taxonomy of nematodes has lead to their use in testing specific short sequences of DNA as a "barcode" for the identification of all nematode species.

/pdf/nematode-molecular-diagnostics-from-bands-to-barcodes-36qdzzdtpl.pdf

NEMATODE MOLECULAR DIAGNOSTICS: From Bands to Barcodes

Plant-parasitic nematodes are the most destructive group of plant pathogens worldwide and are extremely challenging to control. The recent completion of two root-knot nematode genomes opens the way for a comparative genomics approach to elucidate the success of these parasites. Sequencing revealed that Meloidogyne hapla, a diploid that reproduces by facultative, meiotic parthenogenesis, encodes approximately 14,200 genes in a compact, 54 Mpb genome. Indeed, this is the smallest metazoan genome completed to date. By contrast, the 86 Mbp Meloidogyne incognita genome encodes approximately 19,200 genes. This species reproduces by obligate mitotic parthenogenesis and exhibits a complex pattern of aneuploidy. The genome includes triplicated regions and contains allelic pairs with exceptionally high degrees of sequence divergence, presumably reflecting adaptations to the strictly asexual reproductive mode. Both root-knot nematode genomes have compacted gene families compared with the free-living nematode Caenorhabditis elegans, and both encode large suites of enzymes that uniquely target the host plant. Acquisition of these genes, apparently via horizontal gene transfer, and their subsequent expansion and diversification point to the evolutionary history of these parasites. It also suggests new routes to their control.

The genomes of root-knot nematodes.

The Mi-1 gene in tomato confers effective resistance against several species of root-knot nematode, including Meloidogyne javanica. A strain of M. javanica that can reproduce on tomato with Mi-1 was obtained from a culture of an avirulent strain after greenhouse selection. DNA blots and amplified fragment length polymorphism (AFLP) analysis indicated that the two nematode strains are closely related. Expression patterns visualized as cDNA AFLPs were nearly identical except for a cDNA fragment, Cg-1, that was present in the avirulent strain but not in the virulent strain. DNA blots showed that Cg-1 corresponds to a member of a small gene family with one or more copies missing in the virulent strain compared with the avirulent strain. Except for the presence of a histone stem loop near the 3' end of the transcript, Cg-1 shows no similarity to other sequences in GenBank. The longest open reading frame is 32 amino acids and initiates at the fourth AUG in the predicted transcript. When nematode juveniles of the Mi-1-avirulent strain were soaked in dsRNA corresponding to part of the predicted Cg-1 transcript, they produced progeny that were virulent on tomato carrying the Mi-1 gene, strongly suggesting that Cg-1 is required in the nematode for Mi-1-mediated resistance.

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-21-5-0576

Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence.

Evolutionary relationships based on nucleotide variation within the D3 26S rDNA region were examined among acollection of seven Meloidogyne hapla isolates and seven isolates of M. arenaria, M. incognita, and M. javanica. Using D3A and D3B primers, a 350-bp region was PCR amplified from genomic DNA and double-stranded nucleotide sequence obtained. Phylogenetic analyses using three independent clustering methods all provided support for a division between the automictic M. hapla and the apomictic M. arenaria, M. incognita, and M. javanica. A nucleotide sequence character distinguishing M. hapla from the three apomictic species was a 3-bp insertion within the interior of the D3 region. The three apomictic species shared a common D3 haplotype, suggesting a recent branching. Single M. hapla individuals contained two different haplotypes, differentiated by a Sau3AI restriction site polymorphism. Isolates of M. javanica appeared to have only one haplotype, while M. incognita and M. arenaria maintained more than one haplotype in an isolate.

/pdf/nucleotide-substitution-patterning-within-the-meloidogyne-1rpt0xdu5z.pdf

Nucleotide Substitution Patterning within the Meloidogyne rDNA D3 Region and Its Evolutionary Implications.

A diverse collection of seven Meloidogyne hapla isolates, all identified as cytological race A, were studied for their host-parasite interactions with several common bean (Phaseolus vulgaris L.) genotypes. The M. hapla isolates showed significant (P < 0.01) differential interactions of ability to reproduce on resistant common bean cultivars. Based on the nematode egg mass production on susceptible cv. Yolano and resistant cv. NemaSnap beans, the isolates formed three groups. Four isolates produced many egg masses on both susceptible and resistant cultivars and were defined as virulent to resistance in cv. NemaSnap. Two isolates produced many egg mass numbers on susceptible cv. Yolano, but very few on resistant cv. NemaSnap, and were defined as avirulent to the resistance in NemaSnap. One isolate, WI, produced fewer egg masses on susceptible cv. Yolano than on resistant cv. Nemasnap and was defined as virulent to resistance in cv. NemaSnap. The three types of host-parasite interaction indicated a transagonal reaction for a gene-for-gene relationship between M. hapla and resistant common bean (cv. NemaSnap). Analysis of an F2 population from crosses between cultivars NemaSnap and Yolano revealed a single dominant gene pattern of segregation for a major form of resistance in cv. NemaSnap. According to an allelism test, the resistance to M. hapla in cv. NemaSnap was not derived from the line PI165426, which is the pedigree source of M. incognita resistance in cv. NemaSnap. However, PI165426 was found to have M. hapla resistance but may not be homozygous for these factors.

Virulence in Meloidogyne hapla differentiated by resistance in common bean ( Phaseolus vulgaris )

Nematode crossing experiments were conducted to test the hypothesis that virulence in Meloidogyne hapla to a dominant major resistance gene in the bean Phaseolus vulgaris cv. NemaSnap is simply inherited by a single gene, with avirulence dominant to virulence (recessive). In a new procedure established for crossing M. hapla race A isolates, females of avirulent isolate K6 and males of virulent isolates AN and LM were used as parental lines. Virulence frequencies and segregation patterns in the F3 to F5 generations indicated cross-mating with virulent males, not selection and selfing, as the source of virulence in segregating progenies. In F3 progenies, three of 29 lines expressed virulence at levels of 10.6-36.6%. The percentage of virulence from the pooled F3 data from these three lines indicated monogenic inheritance of virulence. F4 families were established from single egg masses of the three virulent F3 lines. Cohorts of F5 juveniles derived from single egg masses of F3 and F4 families were tested for virulence. Due to the facultative parthenogenesis in M. hapla race A, tests were conducted of various genetic models for inheritance of (a)virulence based on different assumptions about the mode of reproduction, gamete duplication and recombination. A segregation pattern of three avirulent (AA, Aa): one virulent (aa) for the genotypes in the F4 was determined from the F5 virulence tests. The percentages of virulence at the F5 stage and their patterns of segregation strongly supported the hypothesis that avirulence in M. hapla is controlled by a single gene, with virulence recessive to avirulence. The M. hapla (a)virulence matches the dominant resistance in P.vulgaris cv. NemaSnap, thus conforming to a gene-for-gene relationship. Our findings indicated that the (a)virulence factor can be transferred within and between M. hapla populations that have the ability to reproduce sexually, thereby maintaining genetic variation for virulence. The inheritance of virulence also suggests that other important biological traits can be transferred through this process.

Genetic analysis of (a)virulence in Meloidogyne hapla to resistance in bean (Phaseolus vulgaris)

Aphelenchoides besseyi is a plant-parasitic nematode (PPN) in the Aphelenchoididae family capable of infecting more than 200 plant species. A. besseyi is also a species complex with strains exhibiting varying pathogenicity to plants. We present the genome and annotations of six Aphelenchoides species, four of which belonged to the A. besseyi species complex. Most Aphelenchoides genomes have a size of 44.7-47.4 Mb and are amongst the smallest in clade IV, with the exception of A. fujianensis, which has a size of 143.8 Mb and is the largest. Phylogenomic analysis successfully delimited the species complex into A. oryzae and A. pseudobesseyi and revealed a reduction of transposon elements in the last common ancestor of Aphelenchoides. Synteny analyses between reference genomes indicated that three chromosomes in A. besseyi were derived from fission and fusion events. A systematic identification of horizontal gene transfer (HGT) genes across 27 representative nematodes allowed us to identify two major episodes of acquisition corresponding to the last common ancestor of clade IV or major PPNs, respectively. These genes were mostly lost and differentially retained between clades or strains. Most HGT events were acquired from bacteria, followed by fungi, and also from plants; plant HGT was especially prevalent in Bursaphelenchus mucronatus. Our results comprehensively improve the understanding of horizontal gene transfer in nematodes.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/1755-0998.13752

The Aphelenchoides genomes reveal substantial horizontal gene transfers in the last common ancestor of free-living and major plant parasitic nematodes

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Nucleotide Substitution Patterning within the Meloidogyne rDNA D3 Region and Its Evolutionary Implications.

Virulence in Meloidogyne hapla differentiated by resistance in common bean ( Phaseolus vulgaris )

Genetic analysis of (a)virulence in Meloidogyne hapla to resistance in bean (Phaseolus vulgaris)

The Aphelenchoides genomes reveal substantial horizontal gene transfers in the last common ancestor of free-living and major plant parasitic nematodes