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Phylogeography of the highly invasive sugar beet nematode, Heterodera schachtii (Schmidt, 1871), based on microsatellites.

ABSTRACT: Plant-parasitic nematodes (PPNs) threaten crop production worldwide. Yet few studies have examined their intraspecific genetic diversity or patterns of invasion, critical data for managing the spread of these cryptic pests. The sugar beet nematode Heterodera schachtii, a global invader that parasitizes over 200 plant species, represents a model for addressing important questions about the invasion genetics of PPNs. Here, a phylogeographic study using 15 microsatellite markers was conducted on 231 H. schachtii individuals sampled from four continents, and invasion history was reconstructed through an approximate Bayesian computation approach, with emphasis on the origin of newly discovered populations in Korea. Multiple analyses confirmed the existence of cryptic lineages within this species, with the Korean populations comprising one group (group 1) and the populations from Europe, Australia, North America, and western Asia comprising another (group 2). No multilocus genotypes were shared between the two groups, and large genetic distance was inferred between them. Population subdivision was also revealed among the populations of group 2 in both population comparison and STRUCTURE analyses, mostly due to different divergent times between invasive and source populations. The Korean populations showed substantial genetic homogeneity and likely originated from a single invasion event. However, none of the other studied populations were implicated as the source. Further studies with additional populations are needed to better describe the distribution of the potential source population for the East Asian lineage.

SUBMITTER: Kim J

PROVIDER: S-EPMC6346664 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Project description:Productivity of sugar beet and brassica vegetable crops is constrained by the nematode Heterodera schachtii worldwide. In sugar beet cropping areas of Central Europe and North America, H. schachtii is managed by crop rotation, and cultivation of resistant brassica cover crops. The recently released nematode-tolerant sugar beet cultivars suffer less damage than susceptible cultivars at high initial population densities of H. schachtii. Many tolerant cultivars allow for less nematode reproduction than susceptible cultivars. Monoculture of susceptible hosts can facilitate the evolution of suppressive soil. Objectives of this study were to determine if susceptible hosts are required for this process, and if monoculture with sugar beet genotypes of different host status (susceptible, resistant, tolerant) impact this capacity. Additionally, we tested if amending soil with the cyst nematode pathogens Pasteuria nishizawae or Hyalorbilia sp. strain DoUCR50 favored the establishment of soil suppressiveness. In 4-year microplot studies with H. schachtii Schach0 or Schach1, one susceptible, one Schach0-resistant, and one tolerant sugar beet genotype were monocultured. In 2010, plots were amended with P. nishizawae or DoUCR50, the last being introduced into non-treated soil for Schach0, and into previously biocide-treated soil for Schach1. In 2011, respective Schach0 plots received a second amendment with DoUCR50. Nematode population densities and growth and yield parameters were determined annually. Effects of P. nishizawae and DoUCR50 on populations of H. schachtii were limited and not consistent. Starting in the second year of the monoculture, eggs of both H. schachtii pathotypes became diseased. Up to 90% of the total eggs were encumbered by the third cropping cycle, under the susceptible, resistant, and tolerant cultivar. In all years, the tolerant genotype produced the highest and most stable white sugar yields while yields of the other cultivars slowly improved during the monoculture. Results of this study suggested the presence of egg-infecting factors in this sugar beet monoculture that dramatically increased the proportions of diseased eggs. The tolerant cultivar allowed establishment of soil suppressiveness without the initial yield decline observed when susceptible sugar beet genotypes are grown in monoculture.

Project description:Beet cyst nematode (Heterodera schachtii Schm.) is one of the most damaging pests in sugar beet growing areas around the world. The Hs1pro-1 and cZR3 genes confer resistance to the beet cyst nematode, and both were cloned from sugar beet translocation line (A906001). The translocation line carried the locus from B. procumbens chromosome 1 including Hs1pro-1 gene and resistance gene analogs (RGA), which confer resistance to Heterodera schachtii. In this research, BvHs1pro-1 and BvcZR3 genes were transferred into oilseed rape to obtain different transgenic lines by A. tumefaciens mediated transformation method. The cZR3Hs1pro-1 gene was pyramided into the same plants by crossing homozygous cZR3 and Hs1pro-1 plants to identify the function and interaction of cZR3 and Hs1pro-1 genes. In vitro and in vivo cyst nematode resistance tests showed that cZR3 and Hs1pro-1 plants could be infested by beet cyst nematode (BCN) juveniles, however a large fraction of penetrated nematode juveniles was not able to develop normally and stagnated in roots of transgenic plants, consequently resulting in a significant reduction in the number of developed nematode females. A higher efficiency in inhibition of nematode females was observed in plants expressing pyramiding genes than in those only expressing a single gene. Molecular analysis demonstrated that BvHs1pro-1 and BvcZR3 gene expressions in oilseed rape constitutively activated transcription of plant-defense related genes such as NPR1 (non-expresser of PR1), SGT1b (enhanced disease resistance 1) and RAR1 (suppressor of the G2 allele of skp1). Transcript of NPR1 gene in transgenic cZR3 and Hs1pro-1 plants were slightly up-regulated, while its expression was considerably enhanced in cZR3Hs1pro-1 gene pyramiding plants. The expression of EDS1 gene did not change significantly among transgenic cZR3, Hs1pro-1 and cZR3Hs1pro-1 gene pyramiding plants and wild type. The expression of SGT1b gene was slightly up-regulated in transgenic cZR3 and Hs1pro-1 plants compared with the wild type, however, its expression was not changed in cZR3Hs1pro-1 gene pyramiding plant and had no interaction effect. RAR1 gene expression was significantly up-regulated in transgenic cZR3 and cZR3Hs1pro-1 genes pyramiding plants, but almost no expression was found in Hs1pro-1 transgenic plants. These results show that nematode resistance genes from sugar beet were functional in oilseed rape and conferred BCN resistance by activation of a CC-NBS-LRR R gene mediated resistance response. The gene pyramiding had enhanced resistance, thus offering a novel approach for the BCN control by preventing the propagation of BCN in oilseed rape. The transgenic oilseed rape could be used as a trap crop to offer an alternative method for beet cyst nematode control.

Dataset Information

Phylogeography of the highly invasive sugar beet nematode, Heterodera schachtii (Schmidt, 1871), based on microsatellites.

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