Effect of Citrullus amarus accessions on the population dynamics of Meloidogyne incognita and M. javanica and watermelon yield
Introduction
Watermelon (Citrullus lanatus (Thunb.) Matsum. and Nakai) is the world’s most cultivated cucurbit crop with an estimated production of ca. 104 million tonnes in 3.2 million ha (FAOSTAT, 2018), representing 44.4 % of the cucurbit production worldwide. Several soil-borne pathogens including root-knot nematodes (RKN), Meloidogyne Goeldi spp., can affect watermelon. Crop yield losses due to RKN range from 24 % to 50 % on watermelon cultivated in open field or plastic greenhouse (Davis, 2007; López-Gómez et al., 2014; Hallmann and Meressa, 2018). Grafting vegetables onto resistant rootstocks is an increasingly common environmentally friendly alternative to soil fumigants and chemical plant protection products for the management of the most important soil-borne pathogens (Thies et al., 2015b). In addition, grafting can provide tolerance to abiotic stressors (Kyriacou et al., 2016). Watermelon is usually grafted onto fusarium wilt resistant rootstocks (Miguel et al., 2004), which are mainly inter-specific hybrids between Cucurbita maxima Lam. x Cucurbita moschata Duchesne, and Lagenaria siceraria (Molina) Standl., that also improve fruit yield in compatible scion-rootstock combinations (Kyriacou et al., 2016). Nonetheless, both of them are susceptible to RKN (Huitrón et al., 2007; López-Gómez et al., 2016; Giné et al., 2017; Levi et al., 2017) in comparison to the poor host status of watermelon (López-Gómez et al., 2014). Grafting watermelon onto RKN susceptible rootstocks results in an exponential increase of the nematode densities at the end of the crop from low densities at planting and compromises the subsequent crops if no other control methods are used (Greco and Di Vito, 2009). To avoid increasing the incidence of RKN, intensive research to identify watermelon rootstocks resistant to both fusarium wilt and RKN has been conducted (Thies and Levi, 2003, 2007; Huitrón et al., 2007; Thies et al., 2010, 2015a, 2015c, 2016; Keinath et al., 2019). As a result, Citrullus amarus Schrad. cv. Carolina Strongback was jointly released by USDA-ARS and Clemson University (Kemble et al., 2019). More recently, García-Mendívil et al. (2019) reported two C. amarus accessions compatible with watermelon that were resistant to M. arenaria (Neal) Chitwood, M. incognita (Kofoid & White) Chitwood, M. javanica (Treub) Chitwood, and fusarium wilt, and that did not negatively impact fruit quality parameters. These characterizations should be complemented with other studies concerning the effect of both C. amarus accessions on nematode population growth, and the effect of increasing nematode densities on plant productivity, owing to the fact that growers need plants able to suppress nematode reproduction without compromising crop yields. The effect that the plant has on nematode population growth is estimated through measuring the nematode densities after the completion of one nematode generation, or at the end of the crop (Pf) in relation to that at sowing or transplanting (Pi). This relationship serve to categorize the host status of a given plant to a nematode species through some parameters such as the maximum multiplication rate (a), the maximum population density (M), and the equilibrium density (E, Pf = Pi; Pf/Pi = 1). Values of a and E are higher for susceptible plants than for resistant or poor hosts (Seinhorst, 1970). In addition to that, the level of plant resistance can also be categorized according to the reproduction index of the nematode, defined as the proportion of the nematode reproduction in a given germplasm compared to that in a susceptible standard (Hadisoeganda and Sasser, 1982). The effect of increasing nematode densities on plant productivity is estimated by the Seinhorst’s damage function model that allows us to estimate the tolerance limit (T) and the minimum relative plant productivity (m) at the highest nematode densities (Seinhorst, 1998).
Despite the benefits of using plant resistance as an alternative to chemical control, it needs to be used in a proper manner to avoid the selection of virulent RKN populations by the repeated cultivation of plants bearing the same R gene(s), which has been observed on tomato and pepper (Verdejo-Lucas et al., 2009; Thies, 2011; Ros-Ibáñez et al., 2014; Expósito et al., 2019). In this scenario, the effect of repeated cultivation of both C. amarus accessions on nematode selection for virulence should also be determined in order to anticipate any potential risks that it occurs and to design good plant resistance management practices to avoid this phenomenon.
Thus, the aims of this study were to determine i) the effect of watermelon grafted onto C. amarus accessions BGV0005164 and BGV0005167 on M. incognita and M. javanica population growth; ii) the effect of increasing nematode densities on plant productivity; and iii) the effect of repeated cultivation of watermelon grafted onto both C. amarus accessions and C. lanatus ‘Robusta’ on M. incognita reproduction, disease severity, crop yield and selection for nematode virulence.
Section snippets
Nematode inoculum
Isolates Agropolis of M. incognita and MJ05 of M. javanica were used in the experiments. Both RKN isolates were grown on the susceptible tomato (Solanum lycopersicumL.) cv. Durinta (Seminis Seeds, St. Louis, Missouri). The nematode inoculum consisted of second-stage juveniles (J2) obtained from eggs by blender maceration of infected roots in a 5 % commercial bleach solution (40 g/L NaOCl) for 10 min according to the Hussey and Barker (1973) method. The egg suspension was firstly filtered
Relationship between increasing Pi of M. incognita or M. javanica on ungrafted and grafted watermelon and relationship between Pf and plant biomass
The mean sand temperature during the experiment ranged from 20.6 °C to 30.6 °C. The maximum multiplication rate (a), the maximum population density (M), and the equilibrium density (E) of M. incognita and M. javanica were higher in ungrafted than in grafted watermelon irrespective of the C. amarus accession (Table 1, Fig. 1). The a, M and E values of M. incognita isolate Agropolis in CI64 were 37 %, 72 % and 68 % respectively lower than in SB, and they were 28 %, 76 % and 77 % lower in CI67.
Discussion
The present study provides novel information of the host status to M. incognita and M. javanica of watermelon grafted onto C. amarus accessions BGV0005164 and BGV0005167. It also sheds new light on the effect that these have on crop yield and the risk of nematode virulence selection. The results have shown that watermelon grafted onto either of the C. amarus accessions used in this study performed as poorer host to Meloidogyne species than the ungrafted, which has been identified as a poor host
Conclusion
C. amarus accessions BGV0005164 and BGV0005167 performed as poorer hosts to M. incognita and M. javanica. Watermelon grafted onto these C. amarus accessions improved fruit yield when they were cultivated in nematode infested soils without affecting its level of resistance to M. incognita after two consecutive crops. Even though both C. amarus accessions are compatible with watermelon and are resistant to RKN and fusarium wilt, the BGV0005167 is the most promising one because it did not affect
CRediT authorship contribution statement
Helio A. García-Mendívil: Investigation, Formal analysis, Visualization, Validation, Writing - original draft, Funding acquisition. Francisco Javier Sorribas: Conceptualization, Methodology, Validation, Resources, Supervision, Formal analysis, Project administration, Writing - review & editing, Funding acquisition.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
The authors thank MINECO and FEDER for funding project AGL2013-49040-C2-1-R, the Ministry of Science and Innovation from the Spanish Government and FEDER for funding project AGL2017-89785-R, and CONACYT for providing PhD funding to Helio Adan García-Mendívil. Thanks are also given to Maria Belén Picó and Carmina Gisbert from COMAV-UPV for providing seeds of C. amarus accessions BGV0005164 and BVG0005167, and to Ariadna Giné, Sergi García, Alejandro Expósito, Anna Sanz, and Miquel Masip for
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