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mtCOI successfully diagnoses the four main plant-parasitic Aphelenchoides species (Nematoda: Aphelenchoididae) and supports a multiple origin of plant-parasitism in this paraphyletic genus

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Abstract

Composed mostly of fungivorous species, the genus Aphelenchoides also comprises 14 plant-parasitic species. The most common and devastating, A. besseyi, A. fragariae, A. ritzemabosi and A. subtenuis have been reported on more than 900 plant species. The combination of low inter-specific and high intra-specific morphological variability makes morphology-based identification extremely difficult within this genus, and has led to molecular tools being employed to ensure accurate diagnoses. rDNA markers are widely used for the identification of nematodes while the Cytochrome Oxidase I gene (COI) remains relatively unexplored despite its role as the standard barcode for almost all animal groups. To explore its suitability as a diagnostic tool, we studied a fragment of the mtCOI region of the four main plant-parasitic Aphelenchoides within a phylogenetic framework. We generated 69 mtCOI and 123 rDNA sequences of diverse Aphelenchoides taxa; 67 belong to the main plant-parasitic species including the first mtCOI sequence of A. fragariae and the first mtCOI and 28S sequences of A. subtenuis. mtCOI had a similar success rate for PCR amplification. Phylogenetic trees based on the three studied markers are largely in agreement with one another, validating their use for Aphelenchoides diagnosis; additionally, we were able to locate several misidentified sequences of plant-parasitic Aphelenchoides in existing databases. The concatenated analysis from the three markers resulted in a more robust insight into the phylogeny and evolution of Aphelenchoides, revealing that plant-parasitism has evolved independently at least three times within this genus, presumably from fungal-feeding ancestors.

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Acknowledgements

The first author acknowledges the PEACE Project (Erasmus Mundus), University of Costa Rica (UCR), Ministerio de Ciencia, Tecnología y Telecomunicaciones (MICITT), and the Consejo Nacional para Investigaciones Científicas y Tecnológicas (CONICIT) for financial support. This work was also supported by a special research fund UGent 01 N02312. We thank Wilfrida Decraemer for her valuable comments on the manuscript; we also thank Dieter Slos, Xue Qing, Marvin Sánchez and Gilda Monge for their collaboration during sampling, as well as Hongmei Li (Nanjing Agric. Un., China), Lorena Flores (UCR, Costa Rica) and Nicole Viaene and Nancy De Sutter (ILVO, Belgium) for providing additional samples. We acknowledge Evelyn van Hesse (NPPO, NL) for her kindness and help when providing the pure cultures. We also thank Daniel Apolônio Silva de Oliveira for his help for model calculations.

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  1. Nematology Research Unit, Department of Biology, Ghent University, Campus Ledeganck, B-9000, Ghent, Belgium

    Alcides Sánchez-Monge, Toon Janssen, Yiwu Fang, Marjolein Couvreur, Gerrit Karssen & Wim Bert

  2. Escuela de Estudios Generales, Universidad de Costa Rica, San José, 2060, Costa Rica

    Alcides Sánchez-Monge

  3. Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Yiwu Fang

  4. National Plant Protection Organization, Wageningen Nematode Collection, Geertjesweg 15, 6700HC, Wageningen, The Netherlands

    Gerrit Karssen

  5. National Plant Protection Organization, Netherlands Food and Consumer Product Safety Authority, Geertjesweg 15, 6700HC, Wageningen, The Netherlands

    Gerrit Karssen

  6. Center for Medical Genetics, Reproduction and Genetics, Reproduction Genetics and Regenerative Medicine, Vrije Universiteit Brussel, UZ Brussel, Laarbeeklaan 101, 1090, Brussels, Belgium

    Toon Janssen

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  1. Alcides Sánchez-Monge
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Correspondence to Alcides Sánchez-Monge.

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Sánchez-Monge, A., Janssen, T., Fang, Y. et al. mtCOI successfully diagnoses the four main plant-parasitic Aphelenchoides species (Nematoda: Aphelenchoididae) and supports a multiple origin of plant-parasitism in this paraphyletic genus. Eur J Plant Pathol 148, 853–866 (2017). https://doi.org/10.1007/s10658-016-1141-1

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