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Harbingers of bloom: Identifying the molecular mechanisms controlling fruit bloom formation in cucumbers

Harbingers of bloom: Identifying the molecular mechanisms controlling fruit bloom formation in... The Plant Cell, 2025, 37, koaf187 https://doi.org/10.1093/plcell/koaf187 Advance access publication 28 July 2025 In Brief Harbingers of bloom: Identifying the molecular mechanisms controlling fruit bloom formation in cucumbers 1,2, Róisín Fattorini * Assistant Features Editor, The Plant Cell, American Society of Plant Biologists Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3BF, UK *Author for correspondence: [email protected] Glandular trichomes are epidermal outgrowths, described as The MYB transcription factor CsRAX3 was identified as a poten - “natural cell factories” because they synthesize large amounts of tial upstream regulator of CsLsi2 through a yeast 1-hybrid library screen. Additional biochemical assays confirmed that CsRAX3 specialized metabolites (Huchelmann et al. 2017). Many of these could bind to the CsLsi2 promoter and gene in vitro and activate metabolites play a role in protecting the plant from biotic and abio- transcription in planta. CsRAX3 transcript levels were high in tic stresses, including extreme temperatures, high UV light, and glandular trichomes as compared with areas of the fruit surface herbivory (Wagner 1991; Huchelmann et al. 2017). Glandular tri- lacking trichomes. Cucumber CRISPR-Cas9–mediated csrax3 chomes are therefore an important target for crop improvement. knockout lines had a reduced fruit bloom phenotype and lower With a developmental understanding comes the possibility of pre- CsLsi2 expression levels when compared with wild type plants. cise genome editing for breeding crops with desirable glandular tri- Cumulatively, this shows that CsRAX3 likely directly activates chome traits, density, and distribution (Schuurink and Tissier CsLsi2 and, in doing so, promotes bloom formation. 2020). Cucumber (Cucumis sativus L.) is an economically important Glandular trichome density was similar in cucumber fruits of vegetable that is grown worldwide (Huang et al. 2009). The cucum- wild type, cslsi2, and csrax3 plants. Given that glandular trichomes ber fruit epidermis contains multicellular glandular trichomes that secrete the silicon that forms fruit bloom, the authors selected a synthesize, store, and deposit silicon. Silicon is a major component gene involved in glandular trichome development (CsTBH; in fruit bloom: a fine off-white powder that forms on the cucumber Zhang et al. 2021) as a potential candidate acting further up- fruit surface (Zhang et al. 2025). Fruit bloom can be beneficial to stream in the regulatory pathway. A combination of biochemical crop plants by reducing pathogen invasion and improving drought assays, gene expression analyses, and investigations with cstbh resistance (e.g. Ebercon et al. 1977; Samuels et al. 1993). However, knockout lines revealed that CsTBH likely directly regulates due to consumer preference for bright and glossy fruits, fruit bloom CsRAX3 and CsLsi2 (Fig.). As such, CsTBH regulates glandular tri- has a negative effect on cucumber market value (Zhang et al. 2025). chome development and silicon deposition. In a recent study, Yaqi Zhang and colleagues (Zhang et al. 2025) Overall, Zhang et al. (2025) have provided a genetic under- identified key molecular components controlling bloom formation standing of the formation of cucumber fruit bloom. This research on the cucumber fruit epidermis. Two cucumber inbred lines were has potential application in breeding cucumbers with desirable used: one with a fruit bloom phenotype (3548-1) and one with a fruit traits, including bloom-free varieties. The genetic regulators non–fruit bloom phenotype (3649-1). Crossing and backcrossing identified here could also be used as molecular hooks in future experiments revealed that the non–fruit bloom phenotype re- studies to explore the wider regulatory network and cellular sulted from a single mendelian recessive gene, and its genomic lo- mechanisms that underlie the remarkable ability of glandular tri- cation was deduced through bulk segregation analysis sequencing chomes to act as natural cell factories. and fine mapping. This genomic region contained the CsLsi2 gene, which encodes a silicon efflux transporter. In plants with a non – Recent related articles in The Plant Cell fruit bloom phenotype, the CsLsi2 gene had a single-nucleotide polymorphism that introduced a premature stop codon, making the protein nonfunctional. CsLsi2 was highly expressed within • Wu et al. (2024) show that tomato (Solanum lycopersicum) multicel- the glandular trichomes of cucumber fruit. Cucumber lular trichome development involves cell expansion in basal cells CRISPR-Cas9–mediated cslsi2 knockout mutants had non–fruit and cell division in apical cells. This is regulated by a gradient of a bloom phenotypes, and transmission electron microscopy– HD-Zip IV regulator (Woolly) and key downstream targets. energy-dispersive spectroscopy revealed that wild type plants con- • Shen et al. (2024) show that CsTL regulates cucumber tendril tained silicon in the extracellular regions of glandular trichome formation, and they identify an interaction partner (CsTEN) cell walls, which the mutants lacked. These experiments demon- and downstream target (CsUFO). These findings could benefit strate that silicon efflux mediated by CsLsi2 is necessary for cu - crop breeding by enabling the production of cucumber vari- cumber fruit bloom formation. eties lacking tendrils. Received July 19, 2025. Accepted July 23, 2025. © The Author(s) 2025. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which per- mits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 | The Plant Cell, 2025, Vol. 37, No. 8 Figure. Fruit bloom formation in cucumber fruits requires silicon efflux mediated by CsLsi2. A) Images of the cucumber fruit epidermis from knockout mutant lines (cstbh, csrax, cslsi2) and corresponding wild type (WT) plants. B) Confocal microscopy images of cstbh, csrax3, cslsi2, and WT cucumber glandular trichomes with stained lignin and cellulose. C) A schematic summarizing our current understanding of how the CsTBH-CsRAX3-CsLsi2 module regulates fruit bloom formation in cucumber. Adapted from Zhang et al. (2025; Figures 2, 4, 5, 7). Shen J, Jiang Y, Pan J, Sun L, Li Q, He W, Sun P, Zhao B, Zhao H, Ke X, Data availability et al. The GRAS transcription factor CsTL regulates tendril forma- No new data were generated or analysed in support of this tion in cucumber. Plant Cell. 2024:36(8):2818–2833. https://doi.org/ research. 10.1093/plcell/koae123 Wagner GJ. Secreting glandular trichomes: more than just hairs. Plant References Physiol. 1991:96(3):675–679. https://doi.org/10.1104/pp.96.3.675 Wu M, Bian X, Hu S, Huang B, Shen J, Du Y, Wang Y, Xu M, Xu H, Yang Ebercon A, Blum A, Jordan WR. A rapid colorimetric method for epicu- M, et al. A gradient of the HD-Zip regulator Woolly regulates mul- ticular wax contest of sorghum leaves. Crop Sci. 1977:17(1):179–180. ticellular trichome morphogenesis in tomato. Plant Cell. https://doi.org/10.2135/cropsci1977.0011183X001700010047x Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni 2024:36(6):2375–2392. https://doi.org/10.1093/plcell/koae077 P, et al. The genome of the cucumber, Cucumis sativus L. Nat Genet. Zhang Y, Shen J, Bartholomew ES, Dong M, Chen S, Yin S, Zhai X, Feng 2009:41(12):1275–1281. https://doi.org/10.1038/ng.475 Z, Ren H, Liu X. TINY BRANCHED HAIR functions in multicellular Huchelmann A, Boutry M, Hachez C. Plant glandular trichomes: nat- trichome development through an ethylene pathway in Cucumis ural cell factories of high biotechnological interest. Plant Physiol. sativus L. Plant J. 2021:106(3):753–765. https://doi.org/10.1111/tpj. 2017:175(1):6–22. https://doi.org/10.1104/pp.17.00727 Samuels AL, Glass ADM, Ehret DL, Menzies JG. The effects of silicon sup- Zhang Y, Sun L, Shan L, Zhao X, Dong M, Yin S, Dong Y, Wang T, Li S, plementation on cucumber fruit: changes in surface characteristics. Yang L, et al. A molecule module controlling silicon efflux in glan- Ann Bot. 1993:72(5):433–440. https://doi.org/10.1006/anbo.1993.1129 dular trichomes is required for fruit bloom formation in cucum- Schuurink R, Tissier A. Glandular trichomes: micro-organs with ber. Plant Cell. 2025:37(8):koaf175. https://doi.org/10.1093/plcell/ model status? New Phytol. 2020:225(6):2251–2266. https://doi. org/10.1111/nph.16283 koaf175 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Plant Cell Oxford University Press

Harbingers of bloom: Identifying the molecular mechanisms controlling fruit bloom formation in cucumbers

Fattorini, Róisín
The Plant Cell , Volume 37 (8): 1 – Jul 28, 2025
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Oxford University Press
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© The Author(s) 2025. Published by Oxford University Press on behalf of American Society of Plant Biologists.
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1040-4651
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1532-298X
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10.1093/plcell/koaf187
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Abstract

The Plant Cell, 2025, 37, koaf187 https://doi.org/10.1093/plcell/koaf187 Advance access publication 28 July 2025 In Brief Harbingers of bloom: Identifying the molecular mechanisms controlling fruit bloom formation in cucumbers 1,2, Róisín Fattorini * Assistant Features Editor, The Plant Cell, American Society of Plant Biologists Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3BF, UK *Author for correspondence: [email protected] Glandular trichomes are epidermal outgrowths, described as The MYB transcription factor CsRAX3 was identified as a poten - “natural cell factories” because they synthesize large amounts of tial upstream regulator of CsLsi2 through a yeast 1-hybrid library screen. Additional biochemical assays confirmed that CsRAX3 specialized metabolites (Huchelmann et al. 2017). Many of these could bind to the CsLsi2 promoter and gene in vitro and activate metabolites play a role in protecting the plant from biotic and abio- transcription in planta. CsRAX3 transcript levels were high in tic stresses, including extreme temperatures, high UV light, and glandular trichomes as compared with areas of the fruit surface herbivory (Wagner 1991; Huchelmann et al. 2017). Glandular tri- lacking trichomes. Cucumber CRISPR-Cas9–mediated csrax3 chomes are therefore an important target for crop improvement. knockout lines had a reduced fruit bloom phenotype and lower With a developmental understanding comes the possibility of pre- CsLsi2 expression levels when compared with wild type plants. cise genome editing for breeding crops with desirable glandular tri- Cumulatively, this shows that CsRAX3 likely directly activates chome traits, density, and distribution (Schuurink and Tissier CsLsi2 and, in doing so, promotes bloom formation. 2020). Cucumber (Cucumis sativus L.) is an economically important Glandular trichome density was similar in cucumber fruits of vegetable that is grown worldwide (Huang et al. 2009). The cucum- wild type, cslsi2, and csrax3 plants. Given that glandular trichomes ber fruit epidermis contains multicellular glandular trichomes that secrete the silicon that forms fruit bloom, the authors selected a synthesize, store, and deposit silicon. Silicon is a major component gene involved in glandular trichome development (CsTBH; in fruit bloom: a fine off-white powder that forms on the cucumber Zhang et al. 2021) as a potential candidate acting further up- fruit surface (Zhang et al. 2025). Fruit bloom can be beneficial to stream in the regulatory pathway. A combination of biochemical crop plants by reducing pathogen invasion and improving drought assays, gene expression analyses, and investigations with cstbh resistance (e.g. Ebercon et al. 1977; Samuels et al. 1993). However, knockout lines revealed that CsTBH likely directly regulates due to consumer preference for bright and glossy fruits, fruit bloom CsRAX3 and CsLsi2 (Fig.). As such, CsTBH regulates glandular tri- has a negative effect on cucumber market value (Zhang et al. 2025). chome development and silicon deposition. In a recent study, Yaqi Zhang and colleagues (Zhang et al. 2025) Overall, Zhang et al. (2025) have provided a genetic under- identified key molecular components controlling bloom formation standing of the formation of cucumber fruit bloom. This research on the cucumber fruit epidermis. Two cucumber inbred lines were has potential application in breeding cucumbers with desirable used: one with a fruit bloom phenotype (3548-1) and one with a fruit traits, including bloom-free varieties. The genetic regulators non–fruit bloom phenotype (3649-1). Crossing and backcrossing identified here could also be used as molecular hooks in future experiments revealed that the non–fruit bloom phenotype re- studies to explore the wider regulatory network and cellular sulted from a single mendelian recessive gene, and its genomic lo- mechanisms that underlie the remarkable ability of glandular tri- cation was deduced through bulk segregation analysis sequencing chomes to act as natural cell factories. and fine mapping. This genomic region contained the CsLsi2 gene, which encodes a silicon efflux transporter. In plants with a non – Recent related articles in The Plant Cell fruit bloom phenotype, the CsLsi2 gene had a single-nucleotide polymorphism that introduced a premature stop codon, making the protein nonfunctional. CsLsi2 was highly expressed within • Wu et al. (2024) show that tomato (Solanum lycopersicum) multicel- the glandular trichomes of cucumber fruit. Cucumber lular trichome development involves cell expansion in basal cells CRISPR-Cas9–mediated cslsi2 knockout mutants had non–fruit and cell division in apical cells. This is regulated by a gradient of a bloom phenotypes, and transmission electron microscopy– HD-Zip IV regulator (Woolly) and key downstream targets. energy-dispersive spectroscopy revealed that wild type plants con- • Shen et al. (2024) show that CsTL regulates cucumber tendril tained silicon in the extracellular regions of glandular trichome formation, and they identify an interaction partner (CsTEN) cell walls, which the mutants lacked. These experiments demon- and downstream target (CsUFO). These findings could benefit strate that silicon efflux mediated by CsLsi2 is necessary for cu - crop breeding by enabling the production of cucumber vari- cumber fruit bloom formation. eties lacking tendrils. Received July 19, 2025. Accepted July 23, 2025. © The Author(s) 2025. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which per- mits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 | The Plant Cell, 2025, Vol. 37, No. 8 Figure. Fruit bloom formation in cucumber fruits requires silicon efflux mediated by CsLsi2. A) Images of the cucumber fruit epidermis from knockout mutant lines (cstbh, csrax, cslsi2) and corresponding wild type (WT) plants. B) Confocal microscopy images of cstbh, csrax3, cslsi2, and WT cucumber glandular trichomes with stained lignin and cellulose. C) A schematic summarizing our current understanding of how the CsTBH-CsRAX3-CsLsi2 module regulates fruit bloom formation in cucumber. Adapted from Zhang et al. (2025; Figures 2, 4, 5, 7). Shen J, Jiang Y, Pan J, Sun L, Li Q, He W, Sun P, Zhao B, Zhao H, Ke X, Data availability et al. The GRAS transcription factor CsTL regulates tendril forma- No new data were generated or analysed in support of this tion in cucumber. Plant Cell. 2024:36(8):2818–2833. https://doi.org/ research. 10.1093/plcell/koae123 Wagner GJ. Secreting glandular trichomes: more than just hairs. Plant References Physiol. 1991:96(3):675–679. https://doi.org/10.1104/pp.96.3.675 Wu M, Bian X, Hu S, Huang B, Shen J, Du Y, Wang Y, Xu M, Xu H, Yang Ebercon A, Blum A, Jordan WR. A rapid colorimetric method for epicu- M, et al. A gradient of the HD-Zip regulator Woolly regulates mul- ticular wax contest of sorghum leaves. Crop Sci. 1977:17(1):179–180. ticellular trichome morphogenesis in tomato. Plant Cell. https://doi.org/10.2135/cropsci1977.0011183X001700010047x Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni 2024:36(6):2375–2392. https://doi.org/10.1093/plcell/koae077 P, et al. The genome of the cucumber, Cucumis sativus L. Nat Genet. Zhang Y, Shen J, Bartholomew ES, Dong M, Chen S, Yin S, Zhai X, Feng 2009:41(12):1275–1281. https://doi.org/10.1038/ng.475 Z, Ren H, Liu X. TINY BRANCHED HAIR functions in multicellular Huchelmann A, Boutry M, Hachez C. Plant glandular trichomes: nat- trichome development through an ethylene pathway in Cucumis ural cell factories of high biotechnological interest. Plant Physiol. sativus L. Plant J. 2021:106(3):753–765. https://doi.org/10.1111/tpj. 2017:175(1):6–22. https://doi.org/10.1104/pp.17.00727 Samuels AL, Glass ADM, Ehret DL, Menzies JG. The effects of silicon sup- Zhang Y, Sun L, Shan L, Zhao X, Dong M, Yin S, Dong Y, Wang T, Li S, plementation on cucumber fruit: changes in surface characteristics. Yang L, et al. A molecule module controlling silicon efflux in glan- Ann Bot. 1993:72(5):433–440. https://doi.org/10.1006/anbo.1993.1129 dular trichomes is required for fruit bloom formation in cucum- Schuurink R, Tissier A. Glandular trichomes: micro-organs with ber. Plant Cell. 2025:37(8):koaf175. https://doi.org/10.1093/plcell/ model status? New Phytol. 2020:225(6):2251–2266. https://doi. org/10.1111/nph.16283 koaf175

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The Plant Cell – Oxford University Press

Published: Jul 28, 2025

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