The role of Fragaria vesca homolog of a (Z)-3:(E)-2-hexenal isomerase in the development of green-leafy fruit aroma

Rong Zhang , Dylan Nunnally Martínez , Elli A. Koskela , Amparo Monfort

Horticulture Research ›› 2025, Vol. 12 ›› Issue (10) : 163

PDF (1023KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (10) :163 DOI: 10.1093/hr/uhaf163
Article
research-article
The role of Fragaria vesca homolog of a (Z)-3:(E)-2-hexenal isomerase in the development of green-leafy fruit aroma
Author information +
History +
PDF (1023KB)

Abstract

The green leaf volatiles (Z)-3-hexenal and (E)-2-hexenal are key components of the characteristic strawberry aroma, an important determinant of consumer preferences. Green leaf volatiles (GLVs) are C6 compounds that impart fresh, green notes and are involved in plant wounding responses. GLV biosynthesis requires several enzymatic steps to convert polyunsaturated fatty acids to C6-aldehydes, alcohols, and esters, respectively. However, the biosynthesis of GLVs in strawberries, such as the isomerization of (Z)-3-hexenal to (E)-2-hexenal, remains poorly understood. In this study, we identified a (Z)-3:(E)-2-hexenal isomerase gene (FvHI) using phylogenetic analysis, characterized its expression in different tissues, and characterized its function using stable transformation. Volatile analysis by gas chromatography-mass spectrometry (GC-MS) of fruits from a Fragaria vesca near-isogenic line (NIL) collection revealed a distinct ratio of (Z)-3-hexenal and (E)-2-hexenal in lines containing Fragaria bucharica introgressions in the distal end of linkage group 5. Consequently, FvHI was located within this genomic region. The coding sequence of FvHI was nearly identical between the recurrent parent and a selected NIL individual containing an introgression in the distal end linkage group 5, indicating that the contrasting ratio of (Z)-3 and (E)-2 GLV isomers may be attributed to transcriptional differences. Accordingly, FvHI expression in ripe fruits was lower in the selected NIL individual than in the recurrent parent. Lastly, FvHI overexpression decreased (Z)-3-hexenal accumulation and increased (E)-2-hexenal accumulation in the recurrent parent and the selected NIL individual. These results suggest that FvHI plays a role in producing the characteristic strawberry aroma by converting (Z)-3-hexenal to (E)-2-hexenal.

Cite this article

Download citation ▾
Rong Zhang, Dylan Nunnally Martínez, Elli A. Koskela, Amparo Monfort. The role of Fragaria vesca homolog of a (Z)-3:(E)-2-hexenal isomerase in the development of green-leafy fruit aroma. Horticulture Research, 2025, 12(10): 163 DOI:10.1093/hr/uhaf163

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was funded by the ‘Agencia Estatal de Investigación’ (AEI) (Ministry of Science, Innovation, and Universities; Government of Spain) through grants RTA2013-00010-00-00, PID2020-119052RR-I00 and TED2021-130898B-C32 and through the grant CEX2019-000902-S funded by MICIU/AEI/10.13039/501100011033. This work was also supported by the CERCA Programme/Generalitat de Catalunya and by the “European Union NextGeneration EU/PRTR”. Rong Zhang was supported by a China Scholarship Council predoctoral grant. Dylan Nunally Martinez is a recipient of the predoctoral fellowship HORIZON-MSCA-2021-COFUND-01 rePLANT-GA101081581 Funded by the European Union. Dr. Koskela was supported by a grant from Ella and Georg Ehrnrooth foundation.

Author contributions

Rong Zhang: Investigation, formal analysis, original draft and review. Dylan Nunnally Martinez: formal analysis, manuscript review and editing. Elli A. Koskela: investigation, formal analysis, writing, editing and review. Amparo Monfort: resources, investigation, writing, editing and review. All authors participated in editing the manuscript and approved the final version.

Data availability

All data is available in the tables and figures within the manuscript and supplementary material.

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Schwieterman ML, Colquhoun TA, Jaworski EA. et al. Strawberry flavor: diverse chemical compositions, a seasonal influence, and effects on sensory perception. PLoS One. 2014; 9:e88446

[2]

Chambers AH, Pillet J, Plotto A. et al. Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach. BMC Genomics. 2014; 15:217

[3]

Sánchez-Sevilla JF, Cruz-Rus E, Valpuesta V. et al. Deciphering gamma-decalactone biosynthesis in strawberry fruit using a combination of genetic mapping, RNA-Seq and eQTL analyses. BMC Genomics. 2014; 15:218

[4]

Aharoni A, Giri AP, Verstappen FWA. et al. Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell. 2004; 16:3110-31

[5]

Pillet J, Chambers AH, Barbey C. et al. Identification of a methyl-transferase catalyzing the final step of methyl anthranilate synthesis in cultivated strawberry. BMC Plant Biol. 2017; 17:147

[6]

Barbey CR, Hogshead MH, Harrison B. et al. Genetic analysis of methyl anthranilate, mesifurane, linalool, and other flavor compounds in cultivated strawberry (Fragaria x ananassa). Front Plant Sci. 2021; 12:615749

[7]

Edger PP, Poorten TJ, VanBuren R. et al. Origin and evolution of the octoploid strawberry genome. Nat Genet. 2019; 51:541-7

[8]

Urrutia M, Bonet J, Arús P. et al. A near-isogenic line (NIL) collec-tion in diploid strawberry and its use in the genetic analysis of morphologic, phenotypic and nutritional characters. Theor Appl Genet. 2015; 128:1261-75

[9]

Urrutia M, Rambla JL, Alexiou KG. et al. Genetic analysis of the wild strawberry (Fragaria vesca) volatile composition. Plant Physiol Biochem. 2017; 121:99-117

[10]

Schieberle P, Hofmann T. Evaluation of the character impact odorants in fresh strawberry juice by quantitative measure-ments and sensory studies on model mixtures. J Agric Food Chem. 1997; 45:227-32

[11]

Ulrich D, Hoberg E, Rapp A. et al. Analysis of strawberry flavour—discrimination of aroma types by quantification of volatile com-pounds. ZFür Leb-Forsch A. 1997; 205:218-23

[12]

Ulrich D, Komes D, Olbricht K. et al. Diversity of aroma patterns in wild and cultivated Fragaria accessions. Genet Resour Crop Evol. 2007; 54:1185-96

[13]

Kim I, Ahn D, Choi JH. et al. Changes in volatile compounds in short-term high CO2-treated ‘Seolhyang’ strawberry (Fragaria x ananassa) fruit during cold storage. Molecules. 2022; 27:6599

[14]

Jetti R, Yang E, Kurnianta A. et al. Quantification of selected aroma-active compounds in strawberries by headspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis. J Food Sci. 2007; 72: S487-96

[15]

Fan Z, Hasing T, Johnson TS. et al. Strawberry sweetness and con-sumer preference are enhanced by specific volatile compounds. Hortic Res. 2021; 8:66

[16]

Fall R, Karl T, Hansel A. et al. Volatile organic compounds emit-ted after leaf wounding: on-line analysis by proton-transfer-reaction mass spectrometry. J Geophys Res Atmospheres. 1999; 104: 15963-74

[17]

Scala A, Allmann S, Mirabella R. et al. Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci. 2013; 14:17781-811

[18]

Engelberth J. Selective inhibition of jasmonic acid accumulation byasmall α β-unsaturated carbonyl and phenidone reveals dif-ferent modes of octadecanoid signalling activation in response to insect elicitors and green leaf volatiles in Zea mays. BMC Res Notes. 2011; 4:377

[19]

Halitschke R, Ziegler J, Keinänen M. et al. Silencing of hydroper-oxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. Plant J. 2004; 40: 35-46

[20]

Hirao T, Okazawa A, Harada K. et al. Green leaf volatiles enhance methyl jasmonate response in Arabidopsis. J Biosci Bioeng. 2012; 114:540-5

[21]

Farmaki T, Sanmartín M, Jiménez P. et al. Differential distri-bution of the lipoxygenase pathway enzymes within potato chloroplasts. JExp Bot. 2007; 58:555-68

[22]

Viswanath KK, Varakumar P, Pamuru RR. et al. Plant lipoxyge-nases and their role in plant physiology. J Plant Biol. 2020; 63: 83-95

[23]

Grechkin AN, Hamberg M. The “heterolytic hydroperoxide lyase” is an isomerase producing a short-lived fatty acid hemiac-etal. Biochim Biophys Acta BBA-Mol Cell Biol Lipids. 2004; 1636: 47-58

[24]

Fauconnier M-L, Mpambara A, Delcarte J. et al. Conversion of green note aldehydes into alcohols by yeast alcohol dehydroge-nase. Biotechnol Lett. 1999; 21:629-33

[25]

D’Auria JC, Pichersky E, Schaub A. et al.Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J Cell Mol Biol. 2007; 49:194-207

[26]

Kunishima M, Yamauchi Y, Mizutani M. et al. Identification of (Z)-3:(E)-2-hexenal isomerases essential to the production of the leaf aldehyde in plants. JBiolChem. 2016; 291:14023-33

[27]

Spyropoulou EA, Dekker HL, Steemers L. et al. Identification and characterization of (3Z):(2E)-hexenal isomerases from cucum-ber. Front Plant Sci. 2017; 8:1342

[28]

Chen C, Yu F, Wen X. et al. Characterization of a new (Z)-3:(E)-2-hexenal isomerase from tea (Camellia sinensis) involved in the conversion of (Z)-3-hexenal to (E)-2-hexenal. Food Chem. 2022; 383:132463

[29]

Fan Z, Tieman DM, Knapp SJ. et al. A multi-omics framework reveals strawberry flavor genes and their regulatory elements. New Phytol. 2022; 236:1089-107

[30]

Rey-Serra P, Mnejja M, Monfort A. Shape, firmness and fruit quality QTLs shared in two non-related strawberry populations. Plant Sci. 2021; 311:111010

[31]

Li Z, Xie Q, Yan J. et al. Genome-wide identification and char-acterization of the abiotic-stress-responsive lipoxygenase gene family in diploid woodland strawberry (Fragaria vesca). J Integr Agric. 2022; 21:1982-96

[32]

Shiojiri K, Kishimoto K, Ozawa R. et al. Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA. 2006; 103:16672-6

[33]

Croft KPC, Juttner F, Slusarenko AJ. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with pseudomonas syringae pv phaseolicola. Plant Physiol. 1993; 101:13-24

[34]

Kishimoto K, Matsui K, Ozawa R. et al. Components of C6-aldehyde-induced resistance in Arabidopsis thaliana against a necrotrophic fungal pathogen, Botrytis cinerea. Plant Sci. 2006; 170: 715-23

[35]

Kikuta Y, Ueda H, Nakayama K. et al. Specific regulation of pyrethrin biosynthesis in chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol. 2011; 52:588-96

[36]

Myung K, Hamilton-Kemp TR, Archbold DD. Biosynthesis of trans-2-hexenal in response to wounding in strawberry fruit. J Agric Food Chem. 2006; 54:1442-8

[37]

Abanda-Nkpwatt D, Krimm U, Coiner HA. et al. Plant volatiles can minimize the growth suppression of epiphytic bacteria by the phytopathogenic fungus Botrytis cinerea in co-culture exper-iments. Environ Exp Bot. 2006; 56:108-19

[38]

Xu Y, Tong Z, Zhang X. et al. Plant volatile organic compound (E)-2-hexenal facilitates Botrytis cinerea infection of fruits by inducing sulfate assimilation. New Phytol. 2021; 231:432-46

[39]

Jung S, Lee T, Cheng C-H. et al.15 years of GDR: new data and functionality in the genome database for Rosaceae. Nucleic Acids Res. 2019;47:D1137-45

[40]

Katoh K, Kuma K, Toh H. et al. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005; 33:511-8

[41]

Tamura K, Stecher G, Peterson D. et al. MEGA6: molecular evo-lutionary genetics analysis version 6.0. MolBiolEvol. 2013; 30: 2725-9

[42]

Stothard P. The sequence manipulation suite: JavaScript pro-grams for analyzing and formatting protein and DNA sequences. BioTechniques. 2000; 28:1102-4

[43]

Koskela EA, Sønsteby A, Flachowsky H. et al. TERMINAL FLOWER1 is a breeding target for a novel everbearing trait and tailored flowering responses in cultivated strawberry (Fragaria x ananassa Duch.). Plant Biotechnol J. 2016; 14:1852-61

[44]

Pfaffl MW. A new mathematical model for relative quantifica-tion in real-time RT-PCR. Nucleic Acids Res. 2001; 29:e45

[45]

Karimi M, Inzé D, Depicker A. GATEWAY™ vectors for agrobacterium-mediated plant transformation. Trends Plant Sci. 2002; 7:193-5

[46]

Oosumi T, Gruszewski HA, Blischak LA. et al. High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta. 2006; 223:1219-30

PDF (1023KB)

227

Accesses

0

Citation

Detail

Sections
Recommended

/