Integrative taxonomy of root-knot nematodes reveals multiple independent origins of mitotic parthenogenesis

Abstract

During sampling of several Coffea arabica plantations in Tanzania severe root galling, caused by a root-knot nematode was observed. From pure cultures, morphology and morphometrics of juveniles and females matched perfectly with Meloidogyne africana, whereas morphology of the males matched identically with those of Meloidogyne decalineata. Based on their Cox1 sequence, however, the recovered juveniles, females and males were confirmed to belong to the same species, creating a taxonomic conundrum. Adding further to this puzzle, re-examination of M. oteifae type material showed insufficient morphological evidence to maintain its status as a separate species. Consequently, M. decalineata and M. oteifae are synonymized with M. africana, which is herewith redescribed based on results of light and scanning electron microscopy, ribosomal and mitochondrial DNA sequences, isozyme electrophoresis, along with bionomic and cytogenetic features. Multi-gene phylogenetic analysis placed M. africana outside of the three major clades, together with M. coffeicola, M. ichinohei and M. camelliae. This phylogenetic position was confirmed by several morphological features, including cellular structure of the spermatheca, egg mass position, perineal pattern and head shape. Moreover, M. africana was found to be a polyphagous species, demonstrating that “early-branching” Meloidogyne spp. are not as oligophagous as had previously been assumed. Cytogenetic information indicates M. africana (2n = 21) and M. ardenensis (2n = 51–54) to be a triploid mitotic parthenogenetic species, revealing at least four independent origins of mitotic parthenogenesis within the genus Meloidogyne. Furthermore, M. mali (n = 12) was found to reproduce by amphimixis, indicating that amphimictic species with a limited number of chromosomes are widespread in the genus, potentially reflecting the ancestral state of the genus. The wide variation in chromosome numbers and associated changes in reproduction modes indicate that cytogenetic evolution played a crucial role in the speciation of root-knot nematodes and plant-parasitic nematodes in general.

Meloidogyne aberrans sp. nov. (Nematoda: Meloidogynidae), a new root-knot nematode parasitizing kiwifruit in China

“…acronea Coetzee, 1956 [ 50 ]; M . africana Whitehead, 1959 [ 51 , 52 ]; M . graminis (Sledge and Golden, 1964) Whitehead, 1968 [ 53 , 54 ]; M .…”

PM 7/136 (1) Meloidogyne mali

“…The stylet is dorsally curved, 10-25 lm long, with rounded to ovoid stylet knobs, set off to sloping posteriorly. The males are vermiform, root-knot nematode (Janssen et al, 2017). The head is weakly offset, the head cap low and slightly narrower than the post-labial region.…”

Comparative genomics of apomictic root-knot nematodes: hybridization, ploidy, and dynamic genome change

“…We note that hybrid origins for intra-genomic divergent alleles are very well documented in both animals and plants [36][37][38][39][40] , whereas extreme ASD by asexual accumulation of mutations is controversial, with few if any clear examples. The bringing together of diverged chromosomes may be a mechanism contributing to the disruption of meiotic segregation and thus the origins of asexual modes of reproduction, and Janssen et al [7] indicate an association between cytological triploidy and apomixis in Meloidogyne .…”

“…M. enterolobii thus likely represents an independent origin of apomixis. Transitions to apomixis have happened on at least four separate occasions elsewhere in the genus Meloidogyne [7] . However, the relationship of cause and effect between the emergence of divergent genomes and the loss of meiosis remains to be deciphered.…”

“…Based on cytological examination of gamete development, most MIG nematodes have been determined to be mitotic parthenogens (apomicts), which do not undergo meiosis and reproduce asexually [4][5][6][7] . Although asexual organisms are often characterised as being less able to adapt to variable environments and interspecific competition than those with meiosis, the MIG apomicts are very successful, globally-distributed, highly-polyphagous crop pests [2] .…”