Hatching stimulation activity of steroidal glycoalkaloids toward the potato cyst nematode, &lt;i&gt;Globodera rostochiensis&lt;/i&gt;

Shimizu, Kosuke; Kushida, Atsuhiko; Akiyama, Ryota; Lee, Hyoung Jae; Okamura, Yuya; Masuda, Yuki; Sakata, Itaru; Tanino, Keiji; Matsukida, Seiji; Inoue, Tsutomu; Sugimoto, Yukihiro; Mizutani, Masaharu

doi:10.5511/plantbiotechnology.20.0516a

Cited by 9 publications

(12 citation statements)

References 24 publications

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“…The hatching assay, using eggs of G. pallida , showed that SolA is extremely active in sub-nM concentrations, which is much lower than the values reported for glycoalkaloid hatching stimulants such as α-tomatine, which induces only average hatching rates at µM concentrations (Shimizu et al 2020 ). Furthermore, from our results, G. pallida seems to be equally sensitive to SolA compared to G. rostochiensis and G. tabacum , which were studied by Sakata et al ( 2020 ).…”

Section: Discussionmentioning

confidence: 89%

“…Hence, the root exudate probably contains additional, unknown, hatching stimulants, causing a high hatching rate despite the low SolA concentration. As already discussed, tomatidine and α-tomatine may contribute to induce hatching, but are not very effective and alone cannot explain the hatching rates obtained (Shimizu et al 2020 ). Other host species of PCN such as potato, are known to produce a range of hatching factors as well, like α-chaconine, α-solanine and solanidine (Stobiecki et al 2003 ; Shakya and Navarre 2008 ), which induce hatching in G. rostochiensis , but only at nM concentrations (Ochola et al 2020 ).…”

Section: Discussionmentioning

confidence: 91%

“…The activity of the synthetic SolA was only 65% of the activity of the tomato root exudate, suggesting the presence of other hatching factors (Tanino et al 2011 ). Shimizu et al ( 2020 ) tested the hatching activity of the major steroidal glycoalkaloids in potato and tomato root exudates, on G. rostochiensis. Despite the significant hatching stimulant activity of all the tested compounds, including α-solanine, α-chaconine and α-tomatine, however, when compared to SolA the activities were quite weak.…”

Section: Introductionmentioning

confidence: 99%

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UPLC-MS/MS analysis and biological activity of the potato cyst nematode hatching stimulant, solanoeclepin A, in the root exudate of Solanum spp.

Guerrieri

Floková

Vlaar

et al. 2021

Planta

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Main conclusion Solanoeclepin A is a hatching stimulant for potato cyst nematode in very low (pM) concentrations. We report a highly sensitive method for the analysis of SolA in plant root exudates using UHPLC-MS/MS and show that there is considerable natural variation in SolA production in Solanum spp. corresponding with their hatching inducing activity. Abstract Potato cyst nematode (PCN) is a plant root sedentary endoparasite, specialized in the infection of solanaceous species such as potato (Solanum tuberosum) and tomato (Solanum lycopersicum). Earlier reports (Mulder et al. in Hatching agent for the potato cyst nematode, Patent application No. PCT/NL92/00126, 1996; Schenk et al. in Croat Chem Acta 72:593–606, 1999) showed that solanoeclepin A (SolA), a triterpenoid metabolite that was isolated from the root exudate of potato, induces the hatching of PCN. Its low concentration in potato root exudate has hindered progress in fully understanding its hatching inducing activity and exploitation in the control of PCN. To further investigate the role of SolA in hatching of PCN, the establishment of a highly sensitive analytical method is a prerequisite. Here we present the efficient single-step extraction and UHPLC-MS/MS based analysis for rapid determination of SolA in sub-nanomolar concentrations in tomato root exudate. This method was used to analyze SolA production in different tomato cultivars and related solanaceous species, including the trap crop Solanum sisymbriifolium. Hatching assays with PCN, Globodera pallida, with root exudates of tomato genotypes revealed a significant positive correlation between SolA concentration and hatching activity. Our results demonstrate that there is natural variation in SolA production within solanaceous species and that this has an effect on PCN hatching. The analytical method we have developed can potentially be used to support breeding for crop genotypes that induce less hatching and may therefore display reduced infection by PCN.

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Section: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

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UPLC-MS/MS analysis and biological activity of the potato cyst nematode hatching stimulant, solanoeclepin A, in the root exudate of Solanum spp.

Guerrieri

Floková

Vlaar

et al. 2021

Planta

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“…Authentic samples of α-solanine 9 , α-chaconine 10 , and solanidine 12 were purchased from Sigma-Aldrich, and α-tomatine 6 was purchased from Tokyo Chemical Industry Co., Ltd. ( 22S , 25S )-spirosol-5-en-3β-ol 3 were isolated in our laboratory from tomatidine 4 (Chromadex), respectively, using HPLC 35 , 36 . α-Solamarine 7 and β-solamarine 8 were purified from the diploid potato clone 97H32-6 and the chemical structures were confirmed using NMR in our laboratory 37 .…”

Section: Methodsmentioning

confidence: 99%

The biosynthetic pathway of potato solanidanes diverged from that of spirosolanes due to evolution of a dioxygenase

et al. 2021

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Potato (Solanum tuberosum), a worldwide major food crop, produces the toxic, bitter tasting solanidane glycoalkaloids α-solanine and α-chaconine. Controlling levels of glycoalkaloids is an important focus on potato breeding. Tomato (Solanum lycopersicum) contains a bitter spirosolane glycoalkaloid, α-tomatine. These glycoalkaloids are biosynthesized from cholesterol via a partly common pathway, although the mechanisms giving rise to the structural differences between solanidane and spirosolane remained elusive. Here we identify a 2-oxoglutarate dependent dioxygenase, designated as DPS (Dioxygenase for Potato Solanidane synthesis), that is a key enzyme for solanidane glycoalkaloid biosynthesis in potato. DPS catalyzes the ring-rearrangement from spirosolane to solanidane via C-16 hydroxylation. Evolutionary divergence of spirosolane-metabolizing dioxygenases contributes to the emergence of toxic solanidane glycoalkaloids in potato and the chemical diversity in Solanaceae.

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“…The variation in the glycinoeclepin structure suggests that more solanoeclepins might exist and that their hatch-inducing activity can vary. In addition to solA, some weaker HFs have been identified, such as α-chaconine, α-solanine, solasodine, and solanidine [12,13]. Apart from hatch-inducing compounds, hatch inhibitors (HIs) are also known.…”

Section: Introductionmentioning

confidence: 99%

A Combination of Metabolomics and Machine Learning Results in the Identification of a New Cyst Nematode Hatching Factor

et al. 2022

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Potato Cyst Nematodes (PCNs) are an economically important pest for potato growers. A crucial event in the life cycle of the nematode is hatching, after which the juvenile will move toward the host root and infect it. The hatching of PCNs is induced by known and unknown compounds in the root exudates of host plant species, called hatching factors (HFs, induce hatching independently), such as solanoeclepin A (solA), or hatching stimulants (HSs, enhance hatching activity of HFs). Unraveling the identity of unknown HSs and HFs and their natural variation is important for the selection of cultivars that produce low amounts of HFs and HSs, thus contributing to more sustainable agriculture. In this study, we used a new approach aimed at the identification of new HFs and HSs for PCNs in potato. Hereto, root exudates of a series of different potato cultivars were analyzed for their PCN hatch-inducing activity and their solA content. The exudates were also analyzed using untargeted metabolomics, and subsequently the data were integrated using machine learning, specifically random forest feature selection, and Pearson’s correlation testing. As expected, solA highly correlates with hatching. Furthermore, this resulted in the discovery of a number of metabolite features present in the root exudate that correlate with hatching and solA content, and one of these is a compound of m/z 526.18 that predicts hatching even better than solA with both data methods. This compound’s involvement in hatch stimulation was confirmed by the fractionation of three representative root exudates and hatching assays with the resulting fractions. Moreover, the compound shares mass fragmentation similarity with solA, and we therefore assume it has a similar structure. With this work, we show that potato likely produces a solA analogue, and we contribute to unraveling the hatch-inducing cocktail exuded by plant roots.

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Hatching stimulation activity of steroidal glycoalkaloids toward the potato cyst nematode, <i>Globodera rostochiensis</i>

Cited by 9 publications

References 24 publications

UPLC-MS/MS analysis and biological activity of the potato cyst nematode hatching stimulant, solanoeclepin A, in the root exudate of Solanum spp.

UPLC-MS/MS analysis and biological activity of the potato cyst nematode hatching stimulant, solanoeclepin A, in the root exudate of Solanum spp.

The biosynthetic pathway of potato solanidanes diverged from that of spirosolanes due to evolution of a dioxygenase

A Combination of Metabolomics and Machine Learning Results in the Identification of a New Cyst Nematode Hatching Factor

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