Reactions of Citrullus amarus and Cucumis metuliferus to Meloidogyne chitwoodi, Meloidogyne enterolobii and Meloidogyne luci
Published 2024-04-30
Keywords
- histopathology,
- plant resistance,
- root-knot nematodes,
- rootstock
How to Cite
Copyright (c) 2024 Aida Magdalena FULLANA, Carla MALEITA, Duarte SANTOS, Isabel ABRANTES, Francisco Javier SORRIBAS, Ariadna GINÉ
This work is licensed under a Creative Commons Attribution 4.0 International License.
Abstract
Meloidogyne chitwoodi, M. enterolobii, and M. luci are present in some EU countries, with restricted distributions, and plant resistance can be used to manage these nematodes. Two pot experiments were conducted under controlled conditions for 56 d to assess the host suitability of two potential rootstocks, Cucumis metuliferus BGV11135 and Citrullus amarus BGV5167, to one isolate of each nematode. The susceptible cucumber (Cucumis sativus) ‘Dasher II’, watermelon (Citrullus lanatus) ‘Sugar Baby’ and tomato (Solanum lycopersicum) ‘Coração-de-Boi’ were included for comparisons. A histopathological study using confocal-laser microscopy was also conducted 15 d after nematode inoculations. In the pot test, the rootstocks showed lower numbers of galls, egg masses, and eggs per plant than their susceptible ones. Reproduction indices of the rootstocks varied from immune to moderately resistant, depending on the isolate-rootstock combination. In the histopathological study, M. enterolobii and M. luci induced similar numbers of giant cells (GC) per feeding site in all germplasms. However, GC volumes and numbers of nuclei in rootstocks were lower than in the susceptible germplasms. GCs induced by M. chitwoodi were only detected in susceptible cucumber. These results emphasize the potential of C. metuliferus and C. amarus as effective, eco-friendly strategies for managing root-knot nematodes, and show the complex these host-pathogen interactions.
Downloads
Metrics
References
- Aydinli G., Kurtar E.S., Mennan S., 2019. Screening of Cucurbita maxima and Cucurbita moschata genotypes for resistance against Meloidogyne arenaria, M. incognita, M. javanica, and M. luci. Journal of Nematology 51: 2019–2057. https://doi.org/10.21307/jofnem-2019-057 DOI: https://doi.org/10.21307/jofnem-2019-057
- Bent E., Loffredo A., McKenry M.V., Becker J.O., Borneman J., 2008. Detection and investigation of soil biological activity against Meloidogyne incognita. Journal of Nematology 40(2): 109–118.
- Brown C.R., Mojtahedi H., Santo G.S., Williamson V.M., 1997. Effect of the Mi gene in tomato on reproductive factors of Meloidogyne chitwoodi and M. hapla. Journal of Nematology 29(3): 416-419.
- Castagnone-Sereno P., 2012. Meloidogyne enterolobii (= M. mayaguensis): profile of an emerging, highly pathogenic, root-knot nematode species. Nematology 14(2): 133–138. https://doi.org/10.1163/156854111X601650 DOI: https://doi.org/10.1163/156854111X601650
- Elling A.A., 2013. Major emerging problems with minor Meloidogyne species. Phytopathology 103: 1092–1102. https://doi.org/10.1094/PHYTO-01-13-0019-RVW DOI: https://doi.org/10.1094/PHYTO-01-13-0019-RVW
- EPPO, 2016. PM 7/41 (3) Meloidogyne chitwoodi and Meloidogyne fallax. Bulletin OEPP/EPPO 46(2): 171–189. DOI: https://doi.org/10.1111/epp.12292
- EPPO, 2017. EPPO Alert List: Addition of Meloidogyne luci together with M. ethiopica. EPPO Reporting Service, 2017/2018. Available at: https://gd.eppo.int/reporting/article-6186. Accessed August 05, 2023
- EPPO, 2023a. EPPO Alert List 2013-10. Available at: https://www.eppo.int/ACTIVITIES/plant_quarantine/alert_list. Accessed November 03, 2023
- EPPO, 2023b. Meloidogyne chitwoodi. EPPO global database. Available at: https://gd.eppo.int/taxon/MELGCH Accessed November 03, 2023
- EPPO, 2023c. Meloidogyne enterolobii. EPPO global database. Available at: https://gd.eppo.int/taxon/MELGMY Accessed August 05, 2023
- EPPO, 2023d. Meloidogyne luci. EPPO global database. Available at: https://gd.eppo.int/taxon/MELGLC Accessed August 05, 2023
- Expósito A., Munera M., Giné A., López-Gómez M., Cáceres A., … Sorribas F.J., 2018. Cucumis metuliferus is resistant to root-knot nematode Mi1.2 gene (a)virulent isolates and a promising melon rootstock. Plant Pathology 67: 1161–1167. https://doi.org/10.1111/ppa.12815 DOI: https://doi.org/10.1111/ppa.12815
- Expósito A., García S., Giné A., Escudero N., Sorribas F.J., 2019. Cucumis metuliferus reduces Meloidogyne incognita virulence against the Mi1.2 resistance gene in a tomato-melon rotation sequence. Pest Management Science 75: 1902–1910. https://doi.org/10.1002/ps.5297 DOI: https://doi.org/10.1002/ps.5297
- Expósito A., Pujolà M., Achaerandio I., Giné A., Escudero N., … Sorribas F.J., 2020. Tomato and melon Meloidogyne resistant rootstocks improve crop yield but melon fruit quality is influenced by the cropping season. Frontiers Plant Science 11: 560024-14. https://doi.org/10.3389/fpls.2020.560024 DOI: https://doi.org/10.3389/fpls.2020.560024
- Fassuliotis G., 1970. Resistance of Cucumis spp. to the root-knot nematode, Meloidogyne incognita acrita. Journal of Nematology 2: 174–178.
- Fullana A.M., Expósito A., Escudero N., Cunquero M., Loza-Alvarez P., … Sorribas F.J., 2023. Crop rotation with Meloidogyne-resistant germplasm is useful to manage and revert the (a)virulent populations of Mi1.2 gene and reduce yield losses. Frontiers Plant Science 14: 1133095-13. https://doi.org/10.3389/fpls.2023.1133095 DOI: https://doi.org/10.3389/fpls.2023.1133095
- García-Mendívil H.A., Munera M., Giné A., Escudero N., Picó M.B., … Sorribas F.J., 2019. Response of two Citrullus amarus accessions to isolates of three species of Meloidogyne and their graft compatibility with watermelon. Crop Protection 119: 208–213. https://doi.org/10.1016/j.cropro.2019.02.005 DOI: https://doi.org/10.1016/j.cropro.2019.02.005
- Giné A., López‐Gómez M., Vela M.D., Ornat C., Talavera M., … Sorribas F.J., 2014. Thermal requirements and population dynamics of root‐knot nematodes on cucumber and yield losses under protected cultivation. Plant Pathology 63(6): 1446–1453. https://doi.org/10.1111/ppa.12217 DOI: https://doi.org/10.1111/ppa.12217
- Guner N., Wehner T.C., Pitrat M., 2008. Overview of potyvirus resistance in watermelon. In: Proceedings of the IXth EUCARPIA Meeting on Genetics and Breeding of Cucurbitaceae. (M Pitrat ed.), Institut National de la Recherche Agronomique, Avignon, France, 445–451.
- Gusmini G., Song R., Wehner T.C., 2005. New sources of resistance to gummy stem blight in watermelon. Crop Science 45(2): 582–588. https://doi.org/10.2135/cropsci2005.0582 DOI: https://doi.org/10.2135/cropsci2005.0582
- Hadisoeganda W.W., Sasser J.N., 1982. Resistance of tomato, bean, southern pea, and garden pea cultivars to root-knot nematodes based on host suitability. Plant Disease 66: 145–150. DOI: https://doi.org/10.1094/PD-66-145
- Hanna H.Y., 2000. Double-cropping muskmelons with nematode-resistant tomatoes increases yield, but mulch color has no effect. HortScience 35: 1213–1214. https://doi.org/10.21273/HORTSCI.35.7.1213 DOI: https://doi.org/10.21273/HORTSCI.35.7.1213
- Holbrook C.C., Knauf D.A., Dickson D.W., 1983. A technique for screening peanut for resistance to Meloidogyne incognita. Plant Disease 57: 957–958. DOI: https://doi.org/10.1094/PD-67-957
- Hussey R.S., Barker K.R., 1973. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Report 57: 1025–1038.
- Jones J.T., Haegeman A.J., Danchin E.G., Gaur H.S., Helder J.K., … Perry R.N., 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14: 946–961. https://doi.org/10.1111/mpp.12057 DOI: https://doi.org/10.1111/mpp.12057
- Keinath A.P., Wechter W.P., Rutter W.B., Agudelo P.A., 2019. Cucurbit rootstocks resistant to Fusarium oxysporum f. sp. niveum remain resistant when coinfected by Meloidogyne incognita in the field. Plant Disease 103: 1383–1390. https://doi.org/10.1094/PDIS-10-18-1869-RE DOI: https://doi.org/10.1094/PDIS-10-18-1869-RE
- Koutsovoulos G.D., Poullet M., Elashry A., Kozlowski D.K., Sallet E., … Danchin E.G., 2020. Genome assembly and annotation of Meloidogyne enterolobii, an emerging parthenogenetic root-knot nematode. Scientific Data 7(1): 324. https://doi.org/10.1038/s41597-020-00666-0 DOI: https://doi.org/10.1038/s41597-020-00666-0
- Li X., Sun Y., Yang Y., Yang X., Xue W., … Chen S., 2021. Transcriptomic and histological analysis of the response of susceptible and resistant cucumber to Meloidogyne incognita infection revealing complex resistance via multiple signalling pathways. Frontiers Plant Science 12: 675429-675441. https://doi.org/10.3389/fpls.2021.675429 DOI: https://doi.org/10.3389/fpls.2021.675429
- Ling J., Mao Z., Zhai M., Zeng F., Yang Y., Xie B., 2017. Transcriptome profiling of Cucumis metuliferus infected by Meloidogyne incognita provides new insights into putative defense regulatory network in Cucurbitaceae. Scientific Reports 7: 3544–3559. https://doi.org/10.1038/s41598-017-03563-6 DOI: https://doi.org/10.1038/s41598-017-03563-6
- López-Gómez M., Giné A., Vela M.D., Ornat C., Sorribas F.J., … Verdejo-Lucas S., 2014. Damage functions and thermal requirements of Meloidogyne javanica and Meloidogyne incognita on watermelon. Annals of Applied Biology 165(3): 466–473. https://doi.org/10.1111/aab.12154 DOI: https://doi.org/10.1111/aab.12154
- Maleita C., Cardoso J.M., Rusinque L., Esteves I., Abrantes I., 2021. Species-specific molecular detection of the root knot nematode Meloidogyne luci. Biology 10: 775–788. https://doi.org/10.3390/biology10080775 DOI: https://doi.org/10.3390/biology10080775
- Maleita C., Correia A., Abrantes I., Esteves I., 2022. Susceptibility of crop plants to the root-knot nematode Meloidogyne luci, a threat to agricultural productivity. Phytopathologia Mediterranea 61: 169–179. doi: 10.36253/phyto-13369 DOI: https://doi.org/10.36253/phyto-13369
- Ornat C., Verdejo-Lucas S., Sorribas F.J., 1997. Effect of the previous crop on population densities of Meloidogyne javanica and yield of cucumber. Nematropica 27: 85–90.
- Pais C.S., Abrantes I., Fernandes M.F.M., Santos M.S.N.A., 1986. Técnica de electroforese aplicada ao estudo das enzimas dos nemátodes-das-galhas-radiculares, Meloidogyne spp. Ciência Biológica Ecology and Systematics 6: 19–34.
- Phan N.T., Waele D., Lorieux M., Xiong L., Bellafiore S., 2018. A hypersensitivity-like response to Meloidogyne graminicola in rice (Oryza sativa). Phytopathology 108(4): 521–528. https://doi.org/10.1094/PHYTO-07-17-0235-R DOI: https://doi.org/10.1094/PHYTO-07-17-0235-R
- Pinheiro J.B., Silva G.O.D., Oliveira V.R., Amaro G.B., Morais A.A.D., 2019. Prospection of genetic resistance resources to root-knot nematodes in cucurbit genotypes. Horticultura Brasiliera 37: 343–347. https://doi.org/10.1590/S0102-053620190314 DOI: https://doi.org/10.1590/s0102-053620190314
- Roberts P.A., 2002. Concepts and consequences of resistance. In: Plant Resistance to Parasitic Nematodes (J.L. Starr, R. Cook, J. Bridge, ed.), Wallingford, UK: CAB International, 25–41. DOI: https://doi.org/10.1079/9780851994666.0023
- Sorribas F.J., Ornat C., Verdejo-Lucas S., Galeano M., Valero J., 2005. Effectiveness and profitability of the Mi-resistant tomatoes to control root-knot nematodes. European Journal of Plant Pathology 111: 29–38. https://doi.org/10.1007/s10658-004-1982-x DOI: https://doi.org/10.1007/s10658-004-1982-x
- Sorribas F.J., Djian-Caporalino C., Mateille T., 2020. Nematodes. In: Integrated pest and disease management in greenhouse crops (M.L. Gullino, R. Albajes, P.C. Nicot, ed.), Springer Cham, Switzerland, 147–174. DOI: https://doi.org/10.1007/978-3-030-22304-5_5
- Tetteh A.Y., Wehner T.C., Davis A.R., 2010. Identifying resistance to powdery mildew race 2W in the USDA‐ARS watermelon germplasm collection. Crop Science 50(3): 933-939. https://doi.org/10.2135/cropsci2009.03.0135 DOI: https://doi.org/10.2135/cropsci2009.03.0135
- Thies J.A., Levi A., 2007. Characterization of watermelon (Citrullus lanatus var. citroides) germplasm for resistance to root-knot nematodes. HortScience 42(7): 1530–1533. https://doi.org/10.21273/HORTSCI.42.7.1530 DOI: https://doi.org/10.21273/HORTSCI.42.7.1530
- Thies J.A., Ariss J.J., Hassell R.L., Buckner S., Levi A., 2015. Accessions of Citrullus lanatus var. citroides are valuable rootstocks for grafted watermelon in fields infested with root-knot nematodes. HortScience 50: 4–8. https://doi.org/10.21273/HORTSCI.50.1.4 DOI: https://doi.org/10.21273/HORTSCI.50.1.4
- Waldo B.D., Branham S.E., Levi A., Wechter W.P., Rutter W.B., 2023. Distinct Genomic Loci Underlie Quantitative Resistance to Meloidogyne enterolobii Galling and Reproduction in Citrullus amarus. Plant Disease 107(7): 2126–2132. https://doi.org/10.1094/PDIS-09-22-2228-RE DOI: https://doi.org/10.1094/PDIS-09-22-2228-RE
- Walters S.A., Wehner T.C., Daykin M.E., Barker K.R., 2006. Penetration rates of root-knot nematodes into Cucumis sativus and C. metuliferus roots and subsequent histological changes. Nematropica 36: 231–242.
- Xie X., Ling J., Mao Z., Li Y., Zhao J., … Xie B., 2022. Negative regulation of root-knot nematode parasitic behavior by root-derived volatiles of wild relatives of Cucumis metuliferus CM3. Horticulture Research 9: uhac051. https://doi.org/10.1093/hr/uhac051 DOI: https://doi.org/10.1093/hr/uhac051
- Ye D.Y., Qi Y.H., Cao S.F., Wei B.Q., Zhang H.S., 2017. Histopathology combined with transcriptome analyses reveals the mechanism of resistance to Meloidogyne incognita in Cucumis metuliferus. Journal of Plant Physiology 212: 115–124. https://doi.org/10.1016/j.jplph.2017.02.002 DOI: https://doi.org/10.1016/j.jplph.2017.02.002