The Systematics, Morphological, and Molecular Characterization of Economically Important Plant–Parasitic Nematodes: A Themed Issue in Honor of Dr. Gary Bauchan

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 66679

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Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA, ARS, Northeast Area, Beltsville, MD 20705, USA
Interests: taxonomy and morphology of plant parasitic nematodes
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Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA, ARS, Northeast Area, Beltsville, MD 20705, USA
Interests: taxonomy and morphology of plant parasitic nematodes

Special Issue Information

Dear Colleagues,

Plant–parasitic nematodes (PPN) are recognized as one of the greatest threat to crops throughout the world. Nematodes are Earth’s most numerous multicellular animals and include species that feed on bacteria, fungi, plants, insects, and animals. Nematodes alone or in combination with other soil microorganisms have been found to attack almost every part of the plant, including mostly roots, stems, leaves, fruits, and seeds. Some nematodes are beneficial, but others cause major damage. Root–knot nematodes alone cause 5% of all crop losses around the world each year. Nematodes are one of the most important pests globally and can cause up to 14% loss of food crops. In total, nematodes cause over $100 billion in global crop damage annually. To date, only a few thousand PPN species have been described. Nematode identification has traditionally relied on morphological and anatomical characters using light microscopy and in some cases scanning electron microscopy (SCN). Lately, molecular diagnosis has been combined with morphology and taxonomy to accurately identify and describe nematode species. Despite the feasibility of molecular diagnosis in conducting quick and easy identification of specimens and its ubiquitous use by researchers on a daily basis, classical taxonomy continues to use reliable and nonoverlapping morphological characters, making it still an important and reliable tool for the identification of nematode species. Most importantly, taxonomical identification allows for the establishment of a clear link between function and morphological aspects of the specimen analysis, and it is a very suitable method for quantitative evaluations, whereas a molecular evaluation would take too long and can be too costly. Still, detailed analyses of morphological and molecular data have both significantly contributed to our overall understanding of the dynamic and complex nature of plant–nematode interactions. This Special Issue on The Systematics and Morphology of Plant-Parasitic Nematodes aims to publish articles (original research manuscripts and review articles) that focus on taxonomy, morphology, and molecular methods used for identification of PPN associated with economically important agriculture, horticultural, and forestry crops.

Dr. Zafar Handoo
Dr. Mihail Kantor
Guest Editors

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Keywords

  • plant-parasitic nematodes
  • identification
  • molecular
  • morphological
  • SEM
  • systematics
  • taxonomy

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Published Papers (11 papers)

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Research

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11 pages, 1532 KiB  
Article
Morphometric and Molecular Diversity among Seven European Isolates of Pratylenchus penetrans
by Mesfin Bogale, Betre Tadesse, Rasha Haj Nuaima, Bernd Honermeier, Johannes Hallmann and Peter DiGennaro
Plants 2021, 10(4), 674; https://doi.org/10.3390/plants10040674 - 31 Mar 2021
Cited by 4 | Viewed by 2325
Abstract
Pratylenchus penetrans is an economically important root-lesion nematode species that affects agronomic and ornamental plants. Understanding its diversity is of paramount importance to develop effective control and management strategies. This study aimed to characterize the morphological and genetic diversity among seven European isolates. [...] Read more.
Pratylenchus penetrans is an economically important root-lesion nematode species that affects agronomic and ornamental plants. Understanding its diversity is of paramount importance to develop effective control and management strategies. This study aimed to characterize the morphological and genetic diversity among seven European isolates. An isolate from the USA was included in the molecular analyses for comparative purposes. Morphometrics of the European P. penetrans isolates generally were within the range of the original descriptions for this species. However, multiple morphometric characteristics, including body length, maximum body width, tail length and length of the post-vulval uterine sac showed discrepancies when compared to other populations. Nucleotide sequence-based analyses revealed a high level of intraspecific diversity among the isolates. We observed no correlation between D2-D3 rDNA- and COXI-based phylogenetic similarities and geographic origin. Our phylogenetic analyses including selected GenBank sequences also suggest that the controversy surrounding the distinction between P. penetrans and P. fallax remains. Full article
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48 pages, 22650 KiB  
Article
Integrative Taxonomy and Molecular Phylogeny of the Plant-Parasitic Nematode Genus Paratylenchus (Nematoda: Paratylenchinae): Linking Species with Molecular Barcodes
by Phougeishangbam Rolish Singh, Gerrit Karssen, Marjolein Couvreur, Sergei A. Subbotin and Wim Bert
Plants 2021, 10(2), 408; https://doi.org/10.3390/plants10020408 - 22 Feb 2021
Cited by 25 | Viewed by 6653
Abstract
Pin nematodes of the genus Paratylenchus are obligate ectoparasites of a wide variety of plants that are distributed worldwide. In this study, individual morphologically vouchered nematode specimens of fourteen Paratylenchus species, including P. aculentus, P. elachistus, P. goodeyi, P. holdemani, P. idalimus, P. [...] Read more.
Pin nematodes of the genus Paratylenchus are obligate ectoparasites of a wide variety of plants that are distributed worldwide. In this study, individual morphologically vouchered nematode specimens of fourteen Paratylenchus species, including P. aculentus, P. elachistus, P. goodeyi, P. holdemani, P. idalimus, P. microdorus, P. nanus, P. neoamblycephalus, P. straeleni and P. veruculatus, are unequivocally linked to the D2-D3 of 28S, ITS, 18S rRNA and COI gene sequences. Combined with scanning electron microscopy and a molecular analysis of an additional nine known and thirteen unknown species originating from diverse geographic regions, a total of 92 D2-D3 of 28S, 41 ITS, 57 18S rRNA and 111 COI new gene sequences are presented. Paratylenchus elachistus, P. holdemani and P. neoamblycephalus are recorded for the first time in Belgium and P. idalimus for the first time in Europe. Paratylenchus is an excellent example of an incredibly diverse yet morphologically minimalistic plant-parasitic genus, and this study provides an integrated analysis of all available data, including coalescence-based molecular species delimitation, resulting in an updated Paratylenchus phylogeny and the corrective reassignment of 18 D2-D3 of 28S, 3 ITS, 3 18S rRNA and 25 COI gene sequences that were previously unidentified or incorrectly classified. Full article
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12 pages, 3389 KiB  
Article
Sensitive, Accurate and Rapid Detection of the Northern Root-Knot Nematode, Meloidogyne hapla, Using Recombinase Polymerase Amplification Assays
by Sergei A. Subbotin and Julie Burbridge
Plants 2021, 10(2), 336; https://doi.org/10.3390/plants10020336 - 10 Feb 2021
Cited by 16 | Viewed by 3256
Abstract
Rapid and reliable diagnostics of root-knot nematodes are critical for selections of effective control against these agricultural pests. In this study, recombinase polymerase amplification (RPA) assays were developed targeting the IGS rRNA gene of the northern root-knot nematode, Meloidogyne hapla. The RPA assays [...] Read more.
Rapid and reliable diagnostics of root-knot nematodes are critical for selections of effective control against these agricultural pests. In this study, recombinase polymerase amplification (RPA) assays were developed targeting the IGS rRNA gene of the northern root-knot nematode, Meloidogyne hapla. The RPA assays using TwistAmp® Basic, TwistAmp® exo and TwistAmp® nfo kits (TwistDx, Cambridge, UK) allowed for the detection of M. hapla from crude extracts of females, eggs and juveniles without a DNA extraction step. The results of the RPA assays using real-time fluorescence detection (real-time RPA) in series of crude nematode extracts showed reliable detection after 13 min with a sensitivity of 1/100 of a second-stage juvenile and up to 1/1000 of a female in reaction tubes. The results of the RPA assays using lateral flow dipsticks (LF-RPA) showed reliable detection within 30 min with a sensitivity of 1/10 of a second-stage juvenile and 1/1000 of a female in reaction tubes. The RPA assay developed here is a successful tool for quick, accurate and sensitive diagnostics of M. hapla. The application of the LF-RPA assay has great potential for diagnosing infestation of this species in the lab, field or in areas with a minimal laboratory infrastructure. Full article
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25 pages, 5065 KiB  
Article
Species Diversity of Pin Nematodes (Paratylenchus spp.) from Potato Growing Regions of Southern Alberta, Canada
by Maria Munawar, Dmytro P. Yevtushenko, Juan E. Palomares-Rius and Pablo Castillo
Plants 2021, 10(2), 188; https://doi.org/10.3390/plants10020188 - 20 Jan 2021
Cited by 15 | Viewed by 3922
Abstract
Pin nematodes (Paratylenchus spp.) are polyphagous parasitic species with a wide host range and geographical distribution; their diversity is unknown in the potato growing region of Alberta, Canada. The present study aims to provide morphological and molecular characterization of three pin nematode [...] Read more.
Pin nematodes (Paratylenchus spp.) are polyphagous parasitic species with a wide host range and geographical distribution; their diversity is unknown in the potato growing region of Alberta, Canada. The present study aims to provide morphological and molecular characterization of three pin nematode species, namely P. neoprojectus, P. tateae, and a new species, Paratylenchus enigmaticus sp. nov. All of them were recovered from the potato growing region of southern Alberta. The nematodes were isolated using the sieving and flotation-centrifugation method, and their morphology was assessed by light microscopy. Molecular characterization was performed using partial 18S, D2–D3 expansion domains of the 28S and ITS ribosomal genes. This study is the first report of molecular characterization of P. tateae and P. neoprojectus, being new records from southern Alberta, and two Spanish populations of P. tateae comprising the first report of this species in Europe. The phylogenetic analysis of the 18S, D2–D3 expansion domains of the 28S and ITS ribosomal DNA regions underscores the importance of using molecular data for accurate species identification and clarifies the status of P. nanus type B and P. sheri. Moreover, our findings will be useful to determine the impact of pin nematodes on potato production in future field research. Full article
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13 pages, 4691 KiB  
Article
Morphological and Molecular Characterization of Pratylenchus dakotaensis n. sp. (Nematoda: Pratylenchidae), a New Root-Lesion Nematode Species on Soybean in North Dakota, USA
by Zafar A. Handoo, Guiping Yan, Mihail R. Kantor, Danqiong Huang, Intiaz A. Chowdhury, Addison Plaisance, Gary R. Bauchan and Joseph D. Mowery
Plants 2021, 10(1), 168; https://doi.org/10.3390/plants10010168 - 17 Jan 2021
Cited by 9 | Viewed by 8281
Abstract
Root-lesion nematodes (Pratylenchus spp.) of the genus Pratylenchus Filipjev, 1936, are among the most important nematode pests on soybean (Glycine max (L.) Merr.), along with soybean cyst and root-knot nematodes. In May 2015 and 2016, a total of six soil samples [...] Read more.
Root-lesion nematodes (Pratylenchus spp.) of the genus Pratylenchus Filipjev, 1936, are among the most important nematode pests on soybean (Glycine max (L.) Merr.), along with soybean cyst and root-knot nematodes. In May 2015 and 2016, a total of six soil samples were collected from a soybean field in Walcott, Richland County, ND and submitted to the Mycology and Nematology Genetic Diversity and Biology Laboratory (MNGDBL), USDA, ARS, MD for analysis. Later, in 2019, additional nematodes recovered from a greenhouse culture on soybean originally from the same field were submitted for further analysis. Males, females, and juveniles of Pratylenchus sp. were recovered from soil and root samples and were examined morphologically and molecularly. DNA from single nematodes were extracted, and the nucleotides feature of three genomic regions targeting on the D2–D3 region of 28S rDNA and ITS rDNA and mitochondrial cytochrome oxidase subunit I (COX1) gene were characterized. Phylogeny trees were constructed to ascertain the relationships with other Pratylenchus spp., and polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) was performed to provide a rapid and reliable differentiation from other common Pratylenchus spp. Molecular features indicated that it is a new, unnamed Pratylenchus sp. that is different from morphologically closely related Pratylenchus spp., including P. convallariae, P. pratensis, P. fallax, and P. flakkensis. In conclusion, both morphological and molecular observations indicate that the North Dakota isolate on soybean represents a new root-lesion nematode species which is named and described herein as Pratylenchus dakotaensis n. sp. Full article
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24 pages, 3195 KiB  
Article
Global Distribution of the Reniform Nematode Genus Rotylenchulus with the Synonymy of Rotylenchulus macrosoma with Rotylenchulus borealis
by Juan E. Palomares-Rius, Ilenia Clavero-Camacho, Antonio Archidona-Yuste, Carolina Cantalapiedra-Navarrete, Guillermo León-Ropero, Sigal Braun Miyara, Gerrit Karssen and Pablo Castillo
Plants 2021, 10(1), 7; https://doi.org/10.3390/plants10010007 - 23 Dec 2020
Cited by 12 | Viewed by 4079
Abstract
Reniform nematodes of the genus Rotylenchulus are semi-endoparasites of numerous herbaceous and woody plant roots that occur largely in regions with temperate, subtropical, and tropical climates. In this study, we compared 12 populations of Rotylenchulusborealis and 16 populations of Rotylenchulusmacrosoma, [...] Read more.
Reniform nematodes of the genus Rotylenchulus are semi-endoparasites of numerous herbaceous and woody plant roots that occur largely in regions with temperate, subtropical, and tropical climates. In this study, we compared 12 populations of Rotylenchulusborealis and 16 populations of Rotylenchulusmacrosoma, including paratypes deposited in nematode collections, confirming that morphological characters between both nematode species do not support their separation. In addition, analysis of molecular markers using nuclear ribosomal DNA (28S, ITS1) and mitochondrial DNA (coxI) genes, as well as phylogenetic approaches, confirmed the synonymy of R. macrosoma with R. borealis. This study also demonstrated that R. borealis (= macrosoma) from Israel has two distinct rRNA gene types in the genome, specifically the two types of D2-D3 (A and B). We provide a global geographical distribution of the genus Rotylenchulus. The two major pathogenic species (Rotylenchulusreniformis and Rotylenchulusparvus) showed their close relationship with warmer areas with high annual mean temperature, maximum temperature of the warmest month, and minimum temperature of the coldest month. The present study confirms the extraordinary morphological and molecular diversity of R. borealis in Europe, Africa, and the Middle East and comprises a paradigmatic example of remarkable flexibility of ecological requirements within reniform nematodes. Full article
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27 pages, 4555 KiB  
Article
Morphostatic Speciation within the Dagger Nematode Xiphinema hispanum-Complex Species (Nematoda: Longidoridae)
by Antonio Archidona-Yuste, Ruihang Cai, Carolina Cantalapiedra-Navarrete, José A. Carreira, Ana Rey, Benjamín Viñegla, Gracia Liébanas, Juan E. Palomares-Rius and Pablo Castillo
Plants 2020, 9(12), 1649; https://doi.org/10.3390/plants9121649 - 26 Nov 2020
Cited by 15 | Viewed by 3495
Abstract
Dagger nematodes of the genus Xiphinema include a remarkable group of invertebrates of the phylum Nematoda comprising ectoparasitic animals of many wild and cultivated plants. Damage is caused by direct feeding on root cells and by vectoring nepoviruses that cause diseases on several [...] Read more.
Dagger nematodes of the genus Xiphinema include a remarkable group of invertebrates of the phylum Nematoda comprising ectoparasitic animals of many wild and cultivated plants. Damage is caused by direct feeding on root cells and by vectoring nepoviruses that cause diseases on several crops. Precise identification of Xiphinema species is critical for launching appropriate control measures. We deciphered the cryptic diversity of the Xiphinema hispanum-species complex applying integrative taxonomical approaches that allowed us to verify a paradigmatic example of the morphostatic speciation and the description of a new species, Xiphinema malaka sp. nov. Detailed morphological, morphometrical, multivariate and genetic studies were carried out, and mitochondrial and nuclear haploweb analyses were used for species delimitation of this group. The new species belongs to morphospecies Group 5 from the Xiphinema nonamericanum-group species. D2-D3, ITS1, partial 18S, and partial coxI regions were used for inferring the phylogenetic relationships of X. malaka sp. nov. with other species within the genus Xiphinema. Molecular analyses showed a clear species differentiation not paralleled in morphology and morphometry, reflecting a clear morphostatic speciation. These results support the hypothesis that the biodiversity of dagger nematodes in southern Europe is greater than previously assumed. Full article
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Review

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13 pages, 1715 KiB  
Review
Optimizing Sampling and Extraction Methods for Plant-Parasitic and Entomopathogenic Nematodes
by Mahfouz M. M. Abd-Elgawad
Plants 2021, 10(4), 629; https://doi.org/10.3390/plants10040629 - 26 Mar 2021
Cited by 30 | Viewed by 4651
Abstract
Plant-parasitic and entomopathogenic nematodes (PPNs and EPNs) are key groups in crop production systems. This study aims at optimizing nematode sampling and extraction methods to benefit integrated pest management (IPM) through (a) management of PPNs and (b) use of EPNs. The impacts of [...] Read more.
Plant-parasitic and entomopathogenic nematodes (PPNs and EPNs) are key groups in crop production systems. This study aims at optimizing nematode sampling and extraction methods to benefit integrated pest management (IPM) through (a) management of PPNs and (b) use of EPNs. The impacts of these methods on PPNs and EPNs to achieve cost-effective and efficient IPM programs are presented. The common misuses of sampling and extraction methods are discussed. Professionals engaged in IPM should consider sampling the reliability level in the light of the intended goal, location, crop value, susceptibility, nematode species, and available funds. Logical sampling methodology should be expanded to integrate various factors that can recover extra EPN isolates with differential pathogenicity. It should seek for the best EPN-host matching. Merits of repeated baiting for EPN extraction from soil and sieving for PPN recovery from suspensions are presented. Their extraction values may be modelled to quantify the efficiency of nematode separation. The use of proper indices of dispersion to enhance the biocontrol potential of EPNs or save costs in nematicidal applications is ideally compatible with IPM programs. Selecting an extraction method may sometimes require further tests to find the best extraction method of the existing fauna and/or flora. Cons and pros of modern sampling and extraction techniques are highlighted. Full article
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21 pages, 2979 KiB  
Review
Taxonomy, Morphological and Molecular Identification of the Potato Cyst Nematodes, Globodera pallida and G. rostochiensis
by John Wainer and Quang Dinh
Plants 2021, 10(1), 184; https://doi.org/10.3390/plants10010184 - 19 Jan 2021
Cited by 7 | Viewed by 10036
Abstract
The scope of this paper is limited to the taxonomy, detection, and reliable morphological and molecular identification of the potato cyst nematodes (PCN) Globodera pallida and G. rostochiensis. It describes the nomenclature, hosts, life cycle, pathotypes, and symptoms of the two species. [...] Read more.
The scope of this paper is limited to the taxonomy, detection, and reliable morphological and molecular identification of the potato cyst nematodes (PCN) Globodera pallida and G. rostochiensis. It describes the nomenclature, hosts, life cycle, pathotypes, and symptoms of the two species. It also provides detailed instructions for soil sampling and extraction of cysts from soil. The primary focus of the paper is the presentation of accurate and effective methods to identify the two principal PCN species. Full article
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31 pages, 8002 KiB  
Review
Taxonomy and Identification of Principal Foliar Nematode Species (Aphelenchoides and Litylenchus)
by Zafar Handoo, Mihail Kantor and Lynn Carta
Plants 2020, 9(11), 1490; https://doi.org/10.3390/plants9111490 - 4 Nov 2020
Cited by 11 | Viewed by 9778
Abstract
Nematodes are Earth’s most numerous multicellular animals and include species that feed on bacteria, fungi, plants, insects, and animals. Foliar nematodes are mostly pathogens of ornamental crops in greenhouses, nurseries, forest trees, and field crops. Nematode identification has traditionally relied on morphological and [...] Read more.
Nematodes are Earth’s most numerous multicellular animals and include species that feed on bacteria, fungi, plants, insects, and animals. Foliar nematodes are mostly pathogens of ornamental crops in greenhouses, nurseries, forest trees, and field crops. Nematode identification has traditionally relied on morphological and anatomical characters using light microscopy and, in some cases, scanning electron microscopy (SEM). This review focuses on morphometrical and brief molecular details and key characteristics of some of the most widely distributed and economically important foliar nematodes that can aid in their identification. Aphelenchoides genus includes some of the most widely distributed nematodes that can cause crop damages and losses to agricultural, horticultural, and forestry crops. Morphological details of the most common species of Aphelenchoides (A. besseyi, A. bicaudatus, A. fragariae, A. ritzemabosi) are given with brief molecular details, including distribution, identification, conclusion, and future directions, as well as an updated list of the nominal species with its synonyms. Litylenchus is a relatively new genus described in 2011 and includes two species and one subspecies. Species included in the Litylenchus are important emerging foliar pathogens parasitizing trees and bushes, especially beech trees in the United States of America. Brief morphological details of all Litylenchus species are provided. Full article
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15 pages, 268 KiB  
Review
Nematode Identification Techniques and Recent Advances
by Mesfin Bogale, Anil Baniya and Peter DiGennaro
Plants 2020, 9(10), 1260; https://doi.org/10.3390/plants9101260 - 24 Sep 2020
Cited by 55 | Viewed by 8141
Abstract
Nematodes are among the most diverse but least studied organisms. The classic morphology-based identification has proved insufficient to the study of nematode identification and diversity, mainly for lack of sufficient morphological variations among closely related taxa. Different molecular methods have been used to [...] Read more.
Nematodes are among the most diverse but least studied organisms. The classic morphology-based identification has proved insufficient to the study of nematode identification and diversity, mainly for lack of sufficient morphological variations among closely related taxa. Different molecular methods have been used to supplement morphology-based methods and/or circumvent these problems with various degrees of success. These methods range from fingerprint to sequence analyses of DNA- and/or protein-based information. Image analyses techniques have also contributed towards this success. In this review, we highlight what each of these methods entail and provide examples where more recent advances of these techniques have been employed in nematode identification. Wherever possible, emphasis has been given to nematodes of agricultural significance. We show that these alternative methods have aided nematode identification and raised our understanding of nematode diversity and phylogeny. We discuss the pros and cons of these methods and conclude that no one method by itself provides all the answers; the choice of method depends on the question at hand, the nature of the samples, and the availability of resources. Full article
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