Tetraose Steroidal Glycoalkaloids from Potato Provide Resistance Against and Colorado Potato Beetle

Overview

Journal Elife

Specialty Biology

Date 2023 Sep 26

PMID 37751372

Authors

Pieter J Wolters

Doret Wouters

Yury M Tikunov

Shimlal Ayilalath

Linda P Kodde

Miriam F Strijker

Lotte Caarls

Richard G F Visser

Vivianne G A A Vleeshouwers

Affiliations

Soon will be listed here.

Abstract

Plants with innate disease and pest resistance can contribute to more sustainable agriculture. Natural defence compounds produced by plants have the potential to provide a general protective effect against pathogens and pests, but they are not a primary target in resistance breeding. Here, we identified a wild relative of potato, , that provides us with unique insight in the role of glycoalkaloids in plant immunity. We cloned two atypical resistance genes that provide resistance to and Colorado potato beetle through the production of tetraose steroidal glycoalkaloids (SGA). Moreover, we provide in vitro evidence to show that these compounds have potential against a range of different (potato pathogenic) fungi. This research links structural variation in SGAs to resistance against potato diseases and pests. Further research on the biosynthesis of plant defence compounds in different tissues, their toxicity, and the mechanisms for detoxification, can aid the effective use of such compounds to improve sustainability of our food production.

Citing Articles

Potato steroidal glycoalkaloids: properties, biosynthesis, regulation and genetic manipulation.

Liu Y, Liu X, Li Y, Pei Y, Jaleel A, Ren M Mol Hortic. 2024; 4(1):43.

PMID: 39668379 PMC: 11639122. DOI: 10.1186/s43897-024-00118-y.

Potato glycoside alkaloids exhibit antifungal activity by regulating the tricarboxylic acid cycle pathway of .

Zhang C, Chen W, Wang B, Wang Y, Li N, Li R Front Microbiol. 2024; 15:1390269.

PMID: 38686115 PMC: 11056507. DOI: 10.3389/fmicb.2024.1390269.

Characterisation and mapping of a Globodera pallida resistance derived from the wild potato species Solanum spegazzinii.

Gartner U, Armstrong M, Sharma S, Jones J, Blok V, Hein I Theor Appl Genet. 2024; 137(5):106.

PMID: 38622441 PMC: 11018675. DOI: 10.1007/s00122-024-04605-0.

Alternaria diseases on potato and tomato.

Schmey T, Tominello-Ramirez C, Brune C, Stam R Mol Plant Pathol. 2024; 25(3):e13435.

PMID: 38476108 PMC: 10933620. DOI: 10.1111/mpp.13435.

Tetraose steroidal glycoalkaloids from potato provide resistance against and Colorado potato beetle.

Wolters P, Wouters D, Tikunov Y, Ayilalath S, Kodde L, Strijker M Elife. 2023; 12.

PMID: 37751372 PMC: 10522338. DOI: 10.7554/eLife.87135.

References

Tikunov Y, Molthoff J, de Vos R, Beekwilder J, van Houwelingen A, van der Hooft J . Non-smoky glycosyltransferase1 prevents the release of smoky aroma from tomato fruit. Plant Cell. 2013; 25(8):3067-78. PMC: 3784599. DOI: 10.1105/tpc.113.114231. View

Sun K, Schipper D, Jacobsen E, Visser R, Govers F, Bouwmeester K . Silencing susceptibility genes in potato hinders primary infection of Phytophthora infestans at different stages. Hortic Res. 2022; . PMC: 8968627. DOI: 10.1093/hr/uhab058. View

Zhu S, Li Y, Vossen J, Visser R, Jacobsen E . Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res. 2011; 21(1):89-99. PMC: 3264857. DOI: 10.1007/s11248-011-9510-1. View

Domazakis E, Lin X, Aguilera-Galvez C, Wouters D, Bijsterbosch G, Wolters P . Effectoromics-Based Identification of Cell Surface Receptors in Potato. Methods Mol Biol. 2017; 1578:337-353. DOI: 10.1007/978-1-4939-6859-6_29. View

Shakya R, Navarre D . LC-MS analysis of solanidane glycoalkaloid diversity among tubers of four wild potato species and three cultivars (Solanum tuberosum). J Agric Food Chem. 2008; 56(16):6949-58. DOI: 10.1021/jf8006618. View

Keukens E, de Vrije T, van den Boom C, De Waard P, Plasman H, Thiel F . Molecular basis of glycoalkaloid induced membrane disruption. Biochim Biophys Acta. 1995; 1240(2):216-28. DOI: 10.1016/0005-2736(95)00186-7. View

You Y, van Kan J . Bitter and sweet make tomato hard to (b)eat. New Phytol. 2020; 230(1):90-100. PMC: 8126962. DOI: 10.1111/nph.17104. View

Caruso I, Lepore L, De Tommasi N, Dal Piaz F, Frusciante L, Aversano R . Secondary metabolite profile in induced tetraploids of wild Solanum commersonii Dun. Chem Biodivers. 2011; 8(12):2226-37. DOI: 10.1002/cbdv.201100038. View

Orgell W, Vaidya K, Dahm P . Inhibition of human plasma cholinesterase in vitro by extracts of solanaceous plants. Science. 1958; 128(3332):1136-7. DOI: 10.1126/science.128.3332.1136. View

10.

Campbell B, Duffey S . Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science. 1979; 205(4407):700-2. DOI: 10.1126/science.205.4407.700. View

11.

Ngou B, Ahn H, Ding P, Jones J . Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature. 2021; 592(7852):110-115. DOI: 10.1038/s41586-021-03315-7. View

12.

You F, Huo N, Gu Y, Luo M, Ma Y, Hane D . BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics. 2008; 9:253. PMC: 2438325. DOI: 10.1186/1471-2105-9-253. View

13.

Nagy E, Bennetzen J . Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res. 2008; 18(12):1918-23. PMC: 2593579. DOI: 10.1101/gr.078766.108. View

14.

Aversano R, Contaldi F, Ercolano M, Grosso V, Iorizzo M, Tatino F . The Solanum commersonii Genome Sequence Provides Insights into Adaptation to Stress Conditions and Genome Evolution of Wild Potato Relatives. Plant Cell. 2015; 27(4):954-68. PMC: 4558694. DOI: 10.1105/tpc.114.135954. View

15.

Despres L, David J, Gallet C . The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol. 2007; 22(6):298-307. DOI: 10.1016/j.tree.2007.02.010. View

16.

Friedman M . Potato glycoalkaloids and metabolites: roles in the plant and in the diet. J Agric Food Chem. 2006; 54(23):8655-81. DOI: 10.1021/jf061471t. View

17.

Hallmann C, Foppen R, van Turnhout C, de Kroon H, Jongejans E . Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature. 2014; 511(7509):341-3. DOI: 10.1038/nature13531. View

18.

Lucas J, Hawkins N, Fraaije B . The evolution of fungicide resistance. Adv Appl Microbiol. 2015; 90:29-92. DOI: 10.1016/bs.aambs.2014.09.001. View

19.

Bouarab K, Melton R, Peart J, Baulcombe D, Osbourn A . A saponin-detoxifying enzyme mediates suppression of plant defences. Nature. 2002; 418(6900):889-92. DOI: 10.1038/nature00950. View

20.

Martin R, Mok M, Mok D . Isolation of a cytokinin gene, ZOG1, encoding zeatin O-glucosyltransferase from Phaseolus lunatus. Proc Natl Acad Sci U S A. 1999; 96(1):284-9. PMC: 15131. DOI: 10.1073/pnas.96.1.284. View