Crosses prior to parthenogenesis explain the current genetic diversity of tropical plant-parasitic Meloidogyne species (Nematoda: Tylenchida)
Introduction
The tropical and subtropical plant nematodes Meloidogyne are extensively studied polyphagous major agricultural pests. Different types of variability, i.e. morphological, physiological, host races … are recognized between and even within species and discussions have risen about species delineation (Lamberti, 1979, Sasser, 1979, Taylor and Netscher, 1979, Netscher, 1983, Sturhan, 1983). This is especially true within the tropical group of species, which reproduce through mitotic obligatory parthenogenesis (Triantaphyllou, 1963, Triantaphyllou, 1966, Triantaphyllou, 1981, Triantaphyllou, 1985, Rammah and Hirschmann, 1988). More recently, the focus on differentiation, especially through the use of scanning electron microscopy or molecular techniques, led to a more accurate typing and to the description of novel species in addition to the five widespread and economically important species traditionally recognized, i.e. M. incognita, M. javanica, M. arenaria, M. hapla (Eisenback, 1985) and M. mayaguensis (Rammah and Hirschmann, 1988).
Total DNA analysis of representatives of these five species evidenced a strong structure associating, in genetically isolated clusters, different lines also displaying what could be considered intraspecific diversity (Fargette et al., 1996, Fargette et al., 2005, Semblat et al., 1998). Hugall et al. (1997) reported a low diversity in mitochondrial DNA, but Stanton et al. (1997) and Blok et al. (2002) also demonstrated examples of size plasticity in the mitochondrial DNA region of M. incognita and M. arenaria. Confronting these initial observations thus leads to the suggestion that mitochondrial diversity might be larger than initially suspected.
Among the M. incognita, M. javanica, M. arenaria group, some questionable associations have been observed between mitochondrial data and nuclear supported information such as ITS variation (Hugall et al., 1999) and, more generally, morphology or host ranges characteristics (Hugall et al., 1994). This raises the question of how the diversity is organized within this group and which processes led to such a diversity pattern. Involvement of pre- vs post-parthenogenesis events has been discussed (Triantaphyllou, 1985, Hugall et al., 1994, Hugall et al., 1999, Castagnone-Sereno, 2006). Van der Beek and Pijnacker (2008), who used a mitotic isolate as a control in his work, showed that the mutational rate is very low in mitotic lines. If the mutational process cannot thus explain the observed diversity, there is as yet no clear indication on the process actually involved.
The status of agronomic pest is a direct consequence of selected traits. Implementing proper pest management approaches requires a good understanding of mechanisms, population structure, evolutionary patterns and species identification. Associating a threat to a given genotype or genetic pool is therefore a key issue. Gaining knowledge on diversity patterns and species variation and delineation is thus essential to improve management and control of such pests.
In line with this question we report here a genomic analysis and a comparative analysis of mitochondrial DNA co2-16S sequences and AFLP markers of total DNA from a selected set of Meloidogyne lines of various geographic origins. We demonstrate here that the patterns (including some “relative discordances”) observed in population structure of parthenogenetic lines of Meloidogyne show the signature of crosses prior to the establishment of parthenogenesis. We also demonstrate that several distinct maternal lineages exist, now associated with different genetic backgrounds.
Section snippets
Rationale
Congruency between mitochondrial and nuclear diversity patterns was checked. To do so, 100% stringency was first applied for the biodiversity patterns description and incongruent pattern pinpointed: the pattern comparison was based on the only structures certified by 100% bootstrap nodal values. In the second step, the diversity patterns were considered even if provided with a lower stringency (i.e. lower bootstrap values). Practically, a pre-requisite to the work was the isolation of different
Mitochondrial diversity and maternal lineages characterization
The GenBank accession numbers of the deposited sequences are provided in Table 1. Parameters of the substitution model selected by Modeltest are presented in Table 2. Topologies obtained with the three methods were the same. The tree topologies, as inferred from ML analysis, are shown in Fig. 1 (A and B for the two sequence sets of 26 and 22 lines, respectively).
The reference lines (Table 1) made as expected three major groups corresponding to M. hapla and M. mayaguensis mitotypes (Cluster 1
Discussion
Apart from clear discrimination from M. hapla and M. mayaguensis, neither mitochondrial nor AFLP markers generated any strongly structured pattern within Cluster III, although parthenogenesis is known for enhancing diversity through accumulation of mutations. This was somewhat unexpected since a clear diversity pattern was observed in previous studies (Fargette et al., 1996, Fargette et al., 2005), but on more restricted samples. Furthermore, the data here did not strictly fit with the current
Acknowledgements
The authors acknowledge the technical skills of Gwenaëlle Genson (CBGP) and partial funding by EU TS3-CT92-0098, FAIR-CT95-0896 and French organization ADEME 0575C0042.
References (52)
- et al.
Phylogenetics and speciation
Trends Ecol. Evol.
(2001) - et al.
AFLP analysis of the genetic diversity of Meloidogyne chitwoodi and Meloidogyne fallax, major agricultural pests
C.R. Acad. Sci. Biol.
(2005) Gene trees and species trees are not the same
Trends Ecol. Evol.
(2001)Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita
Nat. Biotechnol.
(2008)- et al.
Phylogeny of a rapidly evolving clade: the cichlid fishes of the Lake Malawi, East Africa
Proc. Natl. Acad. Sci. USA
(1999) - et al.
Genetic variation in tropical Meloidogyne spp. as shown by RAPD
Fundam. Appl. Nematol.
(1997) - et al.
Mitochondrial DNA differences distinguishing Meloidogyne mayaguensis from the major species of tropical root-knot nematodes
Nematology
(2002) Genetic variability and adaptative evolution in parthenogenetic root-knot nematodes
Heredity
(2006)- et al.
Nuclear and mitochondrial DNA polymorphisms in three mitotic parthenogenetic Meloidogyne spp.
Eur. J. Plant Pathol.
(2002) Diagnostic characters useful in the identification of the four most common species of root-knot nematodes (Meloidogyne spp.)
Identification of major Meloidogyne species employing enzyme phenotypes as differentiating characters
Enzymatic relationships and evolution in the genus Meloidogyne (Nematoda: Tylenchida)
J. Nematol.
Use of the esterase phenotype in the taxonomy of the genus Meloidogyne. 2. Esterase phenotypes observed in West African populations and their characterization
Rev. Nematol.
Use of the esterase phenotype in the taxonomy of the genus Meloidogyne. 3. A study of some “B” race lines and their taxonomic position
Rev. Nematol.
Characterization of resistance breaking Meloidogyne incognita-like populations using lectins, monoclonal antibodies and spores of Pasteuria
Fundam. Appl. Nematol.
An RFLP study of relationships between species, populations and resistance breaking lines of tropical Meloidogyne spp.
Fundam. Appl. Nematol.
PHYLIP (Phylogeny Inference Package) version 3.5c
The use of amplified fragment length polymorphism in determining species trees at fine taxonomic levels: analysis of a medically important snake, Trimeresurus albolabris
Mol. Ecol.
Plant Speciation
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT
Nucleic Acids. Symp.
The genus Meloidogyne and morphological characters differentiating the species
Low, but strongly structured mitochondrial DNA diversity in root-knot nematodes (Meloidogyne)
Genetics
Evolution of the AT rich mitochondrial DNA of Meloidogyne hapla
Mol. Biol. Evol.
Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne
Mol. Biol. Evol.
Economic importance of Meloidogyne spp. in subtropical and mediterranean climates
Species concept and species reality: salvaging a Linnaen rank
J. Evol. Biol.
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