Leaf trichome diversity, acylsugar concentration, and their relationships to leaf area in Solanum galapagense

Main Article Content

Ilan Henzler
https://orcid.org/0009-0001-4794-2092
Hamid Khazaei
https://orcid.org/0000-0002-5202-8764

Abstract

Glandular trichomes are physical and chemical barriers used by some tomato wild relatives to confer resistance against insect pests and diseases transmitted by them. Solanum galapagense has been identified as one of the potential sources of insect pest resistance. The present study aimed to examine the trichome diversity and acylsugar concentration of 26 accessions of S. galapagense along with one cultivated tomato (S. lycopersicum) and one cherry tomato (S. l. cerasiforme) cultivar. The results revealed large phenotypic variation among S. galapagense accessions for all studied traits. The S. galapagense accessions had significantly higher trichome types IV density on the adaxial and abaxial surfaces of the leaf and greater acylsugar concentration but a smaller leaflet area than the cultivated tomato. The selected cherry tomato line represents greater trichome type IV density and acylsugar concentration than other groups. The acylsugar concentration was positively associated with trichome type IV but negatively associated with trichome type V on both leaf surfaces. DNA markers revealed the presence of two previously identified whitefly-resistance alleles in S. galapagense accessions. This study will support breeding programmes aiming to improve insect pest resistance in tomato cultivars using crop wild relatives.

 

 

Article Details

How to Cite
Henzler, I. and Khazaei, H. (2024) “Leaf trichome diversity, acylsugar concentration, and their relationships to leaf area in Solanum galapagense”, Genetic Resources, 5(9), pp. 1–12. doi: 10.46265/genresj.NLVC6810.
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Original Articles
References

Andrade, M C et al. (2017). “Inheritance of type IV glandular trichome density and its association with whitefly resistance from Solanum galapagense accession LA1401”. Euphytica 213, pp. 52–52. DOI: https://doi.org/10.1007/s10681-016-1792-1.

Antonious, G et al. (2005). “Natural products: seasonal variation in trichome counts and contents in Lycopersicum hirsutum f. glabratum”. Journal of Environmental Science and Health 40, pp. 619–631. DOI: https://doi.org/10.1081/PFC-200061567.

Baier, J E et al. (2015). “Indirect selection of industrial tomato genotypes that are resistant to spider mites (Tetranychus urticae)”. Genetics and Molecular Research 14, pp. 244–252. DOI: http://dx.doi.org/10.4238/2015.January.16.8.

Bergau, N et al. (2015). “The development of type VI glandular trichomes in the cultivated tomato Solanum lycopersicum and a related wild species S. habrochaites”. BMC Plant Biology 15, pp. 289–289. DOI: https://doi.org/10.1186/s12870-015-0678-z.

Bleeker, P M, P J Diergaarde, et al. (2011). “Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies”. Phytochemistry 72, pp. 68–73. DOI: https://doi.org/10.1016/j.phytochem.2010.10.014.

Bleeker, P M, R Mirabella, et al. (2012). “Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative”. Proceedings of the National Academy of Sciences of the United States of America 109, pp. 20124–20129. DOI: https://doi.org/10.1073/pnas.1208756109.

Damalas, C A and I G Eleftherohorinos (2011). “Pesticide exposure, safety issues, and risk assessment indicators”. International Journal of Environmental Research and Public Health 8, pp. 1402–1419. DOI: https://doi.org/10.3390/ijerph8051402.

Dari, L, A Addo, and K A Dzisi (2016). “Pesticide use in the production of tomato (Solanum lycopersicum L.) in some areas of Northern Ghana”. African Journal of Agricultural Research 11, pp. 352–355. DOI: https://doi.org/10.5897/AJAR2015.10325.

Darwin, S C (2009). The systematics and genetics of tomatoes on the Galápagos Islands (Solanum, Solanaceae). UK. URL: https://discovery.ucl.ac.uk/id/eprint/18994/1/18994.pdf.

Darwin, S C, S Knapp, and I E Peralta (2003). “Taxonomy of tomatoes in the Galápagos Islands: Native and introduced species of Solanum section Lycopersicon (Solanaceae)”. Systematics and Biodiversity 1(1), pp. 29–53. DOI: https://doi.org/10.1017/S1477200003001026.

DaSilva, A A et al. (2019). “Glandular trichomes that mediate resistance to green peach aphid in tomato genotypes from the cross between S. galapagense and S. lycopersicum”. Acta Scientiarum Agronomy 41. DOI: https://doi.org/10.4025/actasciagron.v41i1.42704.

De Souza-Marinke, L et al. (2022). “Selection of tomato genotypes with high resistance to Tetranychus evansi mediated by glandular trichomes”. Phytoparasitica 50, pp. 629–643. DOI: https://doi.org/10.1007/s12600-022-00984-6.

Dias, D M et al. (2016). “Acyl sugars and whitefly (Bemisia tabaci) resistance in segregating populations of tomato genotypes”. Genetics and Molecular Research 15(2). DOI: http://dx.doi.org/10.4238/gmr.15027788.

Doyle, J J and J L Doyle (1990). “Isolation of plant DNA from fresh tissue”. Focus 12, pp. 13–15.

Escobar-Bravo, R, P G L Klinkhamer, and K A Leiss (2017). “Induction of jasmonic acid-associated defenses by thrips alters host suitability for conspecifics and correlates with increased trichome densities in tomato”. Plant and Cell Physiology 58(3), pp. 622–634. DOI: https://doi.org/10.1093/pcp/pcx014.

FAO (2022). FAOSTAT - Food and Agriculture Organization of the United Nations. URL: http://faostat.fao.org (visited on 03/23/2023).

Fenstemaker, S et al. (2022). “Solanum galapagense-derived purple tomato fruit color is conferred by novel alleles of the anthocyanin fruit and atroviolacium loci”. Plant Direct 6(4). DOI: https://doi.org/10.1002/pld3.394.

Firdaus, S, A W Van Heusden, N Hidayati, E D J Supena, et al. (2013). “Identification and QTL mapping of whitefly resistance components in Solanum galapagense”. Theoretical and Applied Genetics 126, pp. 1487–1501. DOI: https://doi.org/10.1007/s00122-013-2067-z.

Firdaus, S, A W Van Heusden, N Hidayati, E Darmo Jaya Supena, et al. (2012). “Resistance to Bemisia tabaci in tomato wild relatives”. Euphytica 187, pp. 31–45. DOI: https://doi.org/10.1007/s10681-012-0704-2.

Fridman, E et al. (2005). “Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of Methylketones”. The Plant Cell 17, pp. 1252–1267. DOI: https://doi.org/10.1105/tpc.104.029736.

Glas, J et al. (2012). “Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores”. International Journal of Molecular Sciences 13, pp. 17077–17103. DOI: https://doi.org/10.3390/ijms131217077.

Huchelmann, A, M Boutry, and C Hachez (2017). “Plant glandular trichomes: Natural cell factories of high biotechnological interest”. Plant Physiology 175, pp. 6–22. DOI: https://doi.org/10.1104/pp.17.00727.

Hunter, E A and J P Gibbs (2014). “Densities of Ecological Replacement Herbivores Required to Restore Plant Communities: A Case Study of Giant Tortoises on Pinta Island”. Galápagos. Restoration Ecology 22, pp. 248–256. DOI: https://doi.org/10.1111/rec.12055.

Kennedy, G G (2003). “Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon”. Annual Review of Entomology 48, pp. 51–72. DOI: https://doi.org/10.1146/annurev.ento.48.091801.112733.

Khazaei, H and A Madduri (2022). “The role of tomato wild relatives in breeding disease-free varieties”. Genetic resources 3(6), pp. 64–73. DOI: https://doi.org/10.46265/genresj.PSES6766.

Leckie, B M et al. (2016). “Differential and synergistic functionality of acylsugars in suppressing oviposition by insect herbivores”. PLoS ONE 11(4). DOI: https://doi.org/10.1371/journal.pone.0153345.

Levin, D A (1973). “The role of trichomes in plant defense”. The Quarterly Review of Biology 48, pp. 3–15. URL: https://www.journals.uchicago.edu/doi/epdf/10.1086/407484.

Lihavainen, J et al. (2017). “Low vapor pressure deficit reduces glandular trichome density and modifies the chemical composition of cuticular waxes in silver birch leaves”. Tree Physiology 37, pp. 1166–1181. DOI: https://doi.org/10.1093/treephys/tpx045.

Lucatti, A F et al. (2013). “Differences in insect resistance between tomato species endemic to the Galapagos Islands”. BMC Evolutionary Biology 13, pp. 175–175. DOI: https://doi.org/10.1186/1471-2148-13-175.

Luckwill, L C (1943). The genus Lycopersicon: An historical, biological and taxanomic survey of the wild and cultivated tomatoes. U.K: Aberdeen University Press.

Ma, J F (2004). “Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses”. Soil Science and Plant Nutrition 50(1), pp. 11–18. DOI: https://doi.org/10.1080/00380768.2004.10408447.

Mahfouze, S A and H A Mahfouze (2019). “A Comparison between CAPS and SCAR markers in the detection of resistance genes in some tomato genotypes against Tomato Yellow Leaf Curl Virus and whitefly”. Jordan Journal of Biological Sciences 12, pp. 123–133. URL: https://jjbs.hu.edu.jo/files/vol12/n2/Paper%20number%201.pdf.

Mymko, D and G Avila-Sakar (2019). “The influence of leaf ontogenetic stage and plant reproductive phenology on trichome density and constitutive resistance in six tomato varieties”. Arthropod-Plant Interactions 13, pp. 797–803. DOI: https://doi.org/10.1007/s11829-019-09690-3.

Oksanen, E (2018). “Trichomes form an important first line of defence against adverse environment-New evidence for ozone stress mitigation”. Plant, Cell & Environment 41, pp. 1497–1499. DOI: https://doi.org/10.1111/pce.13187.

Pailles, Y, M Awlia, et al. (2020). “Diverse traits contribute to salinity tolerance of wild tomato seedlings from the Galapagos Islands”. Plant Physiology 182, pp. 534–546. DOI: https://doi.org/10.1104/pp.19.00700.

Pailles, Y, S Ho, et al. (2017). “Genetic diversity and population structure of two tomato species from the Galapagos Islands”. Frontiers in Plant Science 8, pp. 138–138. DOI: https://doi.org/10.3389/fpls.2017.00138.

Paudel, S et al. (2019). “Induced plant defenses against herbivory in cultivated and wild tomato”. Journal of Chemical Ecology 45, pp. 693–707. DOI: https://doi.org/10.1007/s10886-019-01090-4.

Peck, S B (2008). “Galápagos Islands Insects: Colonization, Structure, and Evolution”. In: Encyclopedia of Entomology. Ed. by J L Capinera. Dordrecht: Springer. DOI: https://doi.org/10.1007/978-1-4020-6359-6_1019.

Pelletier, Y (1990). “The effect of water stress and leaflet size on the density of trichomes and the resistance to Colorado potato beetle larvae (Leptinotarsa decemlineata [say]) in Solanum berthaultii hawkes”. The Canadian Entomologist 122(6), pp. 1141–1147. DOI: https://doi.org/10.4039/Ent1221141-11.

R Core Team (2021). R: a language and environment for statistical computing. R Foundation for Statistical Computing. URL: https://www.R-project.org.

Rakha, M, N Bouba, et al. (2017). “Evaluation of wild tomato accessions (Solanum spp.) for resistance to two-spotted spider mite (Tetranychus urticae Koch) based on trichome type and acylsugar content”. Genetic Resources and Crop Evolution 64, pp. 1011–1022. DOI: https://doi.org/10.1007/s10722-016-0421-0.

Rakha, M, P Hanson, and S Ramasamy (2017). “Identification of resistance to Bemisia tabaci Genn. in closely related wild relatives of cultivated tomato based on trichome type analysis and choice and no-choice assays”. Genetic Resources and Crop Evolution 64, pp. 247–260. DOI: https://doi.org/10.1007/s10722-015-0347-y.

Rick, C M (1961). Biosystematic studies on Galápagos tomatoes.

Savory, E A (2004). Modification of the PGO Assay for Use in Acylsugar Quantification. Ithaca, NY, USA, pp. 36–36.

Schilmiller, A L, A L Charbonneau, and R L Last (2012). “Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes”. Proceedings of the National Academy of Sciences of the United States of America 109, pp. 16377–16382. DOI: https://doi.org/10.1073/pnas.1207906109.

Vendemiatti, E et al. (2022). “The genetic complexity of type-IV trichome development reveals the steps towards an insect-resistant tomato”. Plants 11(10), pp. 1309–1309. DOI: https://doi.org/10.3390/plants11101309.

Vosman, B, A Kashaninia, et al. (2019). “QTL mapping of insect resistance components of Solanum galapagense”. Theoretical and Applied Genetics 132, pp. 531–541. DOI: https://doi.org/10.1007/s00122-018-3239-7.

Vosman, B, W P C Van’t Westende, et al. (2018). “Broad spectrum insect resistance and metabolites in close relatives of the cultivated tomato”. Euphytica 214, pp. 46–46. DOI: https://doi.org/10.1007/s10681-018-2124-4.

W Ebert, A and R Schafleitner (2015). “Utilization of wild relatives in the breeding of tomato and other major vegetables”. Crop Wild Relatives and Climate Change, pp. 141–172. DOI: https://doi.org/10.1002/9781118854396.ch9.

Wang, X et al. (2021). “Analysis and review of trichomes in plants”. BMC Plant Biology 21, pp. 70–70. DOI: https://doi.org/10.1186/s12870-021-02840-x.

Zamir, D (2001). “Improving plant breeding with exotic genetic libraries”. Nature Reviews Genetics 2, pp. 983–989. DOI: https://doi.org/10.1038/35103590.

Zhang, X, R R Thacker, and J C Snyder (2008). “Occurrence of 2,3-dihydrofarnesoic acid, a spidermite repellent, in trichome secretions of Lycopersicon esculentum × L. hirsutum hybrids”. Euphytica 162, pp. 1–9. DOI: https://doi.org/10.1007/s10681-007-9489-0.

Zhang, Y et al. (2020). “The roles of different types of trichomes in tomato resistance to cold, drought, whiteflies, and Botrytis”. Agronomy 10, pp. 411–411. DOI: https://doi.org/10.3390/agronomy10030411.