Abstract
Extensive root galling observed on plantain (Musa spp., AAB) in Nigeria was analysed using Nad5 mitochondrial DNA sequences and the causal agent identified as Meloidogyne arenaria. Following the inoculation of population cultured, Koch’s postulates was fulfilled and the same symptoms observed. This provides the first molecular confirmation of M. arenaria causing such damage to plantain and highlighting its potential as a threat to the crop. Root knot nematodes are known to affect banana and plantain production but diagnosis of the species involved is only just being accurately determined with the recent improvements in molecular techniques.
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Plantain (Musa spp. AAB) holds significant importance as a staple food crop in Central and West Africa, contributing to over 70% of the global production (FAO 2022). Plantains, unlike bananas, have a less dense root system and tend to have a shorter field longevity; plantain fields typically last for 2–3 years, whereas banana fields can endure for 7–10 years or more (Swennen et al. 1986; Swennen and Ortiz 1997). Undoubtedly, the presence of nematodes would exacerbate this problem.
In Nigeria, plantains are predominantly cultivated for local consumption on small-scale farms and backyard gardens, with surplus production sold within the local market. Yield decline has been observed in recent years, which can be attributed to various pests and diseases, including plant-parasitic nematodes (Coyne et al. 2013; Sikora et al. 2018; Coyne 2021). Root-knot nematodes (RKN; Meloidogyne spp.) infect plantain roots, causing deformation and disruption in the root system. This leads to necrosis in infected tissues, root degeneration, compromised plant anchorage, toppling, and eventual yield loss (Moens et al. 2006).
During our study, we gathered galled roots from three plantain cv. Agbagba plants (n = 3), a common false horn landrace, between April and September of 2019 in Rivers (n = 1; 4°43’12.3 “N 7°15’04.1"E) and Oyo States (n = 2; 7°18’51.1"N 3°53’40.5"E; 7°27’52.1"N 3°54’00.6"E) in Nigeria. Though the sampled plants did not display specific above-ground symptoms, small swellings were consistently observed on secondary and tertiary roots. These swellings were associated with RKN females embedded in the root tissue near the surface. Infected primary roots exhibited swelling, with diameters of ≥ 5–10 mm, in comparison to 3.5-5 mm diameters of non-infected roots. Despite RKN females frequently occurring close to the surface of newly emerged roots, adult females with egg masses, males, and all juvenile stages primarily clustered together in the root cortex. Here, they produced necrotic brown-black lesions or spots. Permanent slides of the M. arenaria specimens have been deposited; one perennial pattern (slide number UGMD 104,366) is housed at the Ghent University Museum, Zoology Collections, and another (UGnem347) is available in the UGent Nematode Collection of the Nematology Research Unit, Department of Biology, Ghent University, Ghent, Belgium.
From each plant, we dissected 10 brown-black lesions/spots manually under a stereo microscope, and observed a mean of 15 ± 2 (mean ± standard deviation) males, 6 ± 1 adult females, 2122 ± 798 eggs, 648 ± 169 s-stage juveniles (J2), and 10 ± 1 third and fourth-stage juveniles. We also extracted nematodes per 10 g fresh root (n = 10) using the methodology described by Van den Bergh et al. (2002), recording a mean of 2273 ± 444 eggs and 850 ± 109 J2s per 10 g fresh root.
We individually extracted genomic DNA from two handpicked females per population (Oyo state) and one female from Rivers State. Following the procedures described by Bert et al. (2008) and Janssen et al. (2016), we processed these samples using worm lysis buffer, proteinase K, and amplified Nad5 mtDNA fragments. We also established a pure culture from single egg masses collected from the Oyo State population, maintaining it on RKN-susceptible tomato plants (Solanum lycopersicum cv. Tropimech) under greenhouse conditions. All obtained sequences (MZ420665, MZ420666, MZ420667, MZ420668, MZ420669) demonstrated a 100% match with the M. arenaria A2 N1 haplotype reference sequences KU372356 and KU372349 (Fig. 1).
We inoculated ten plantlets of plantain cv. Agbagba with 8000 J2 + eggs (initial population density, Pi) from the single egg mass M. arenaria cultures in 8 L pots. We also included non-inoculated plantlets as negative controls. The nematode reproduction factor (final population density (Pf)/Pi) was assessed 90 days post-inoculation. All inoculated plantlets exhibited similar root swelling (galling) symptoms in comparison to the controls (Fig. 2), with a Pf/Pi ratio of 26.4.
Further to a cursory listing of M. arenaria associated with roots of banana and plantain (Musa spp.) in west and mid-western Nigeria in an internal report (Caveness 1967), this is the first listing of M. arenaria associated with plantain in Eastern Nigeria, and the first molecularly confirmed report, as well as the first report demonstrating the pathogenicity of M. arenaria on plantain. Meloidogyne spp. in Africa are often not identified at the species level (Onkendi et al. 2014), and durable molecular techniques are only recently being employed. Identification of M. arenaria using morphometrics is also prone to error due to wide variability and overlap with other species. Thus, to the best of our knowledge, this is the first report of M. arenaria naturally infecting and damaging plantain (Musa spp. AAB) and substantiated using molecular techniques.
Accurate knowledge of the nematode species affecting crop production is important in develo** mechanisms for their management, especially towards breeding for resistance. Further studies are required to assess crop losses due to M. arenaria infection on plantain and to develop effective control and management strategies in the region.
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Acknowledgements
This work has been funded by the United States Agency for International Development (USAID) and Special Research Funds Ghent University (BOF18/ DOS/066).
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Olajide, E., Kolombia, Y.A., Amah, D. et al. A report of Meloidogyne arenaria Parasitizing Plantain (Musa spp., AAB) in Nigeria. Australasian Plant Dis. Notes 18, 19 (2023). https://doi.org/10.1007/s13314-023-00505-2
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DOI: https://doi.org/10.1007/s13314-023-00505-2