A QTL on chromosome 17 identified by Genome-Wide Association Mapping controls postharvest cold tolerance of Cucurbita pepo L.
Alicia García
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorAlejandro Castro-Cegrí
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorAlba López
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorMaría Segura
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorÁlvaro Benítez
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorDolores Garrido
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorFrancisco Palma
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorCorresponding Author
Cecilia Martínez
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Correspondence
Manuel Jamilena,
Email: [email protected]
Cecilia Martínez,
Email: [email protected]
Search for more papers by this authorCorresponding Author
Manuel Jamilena
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Correspondence
Manuel Jamilena,
Email: [email protected]
Cecilia Martínez,
Email: [email protected]
Search for more papers by this authorAlicia García
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorAlejandro Castro-Cegrí
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorAlba López
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorMaría Segura
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorÁlvaro Benítez
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Search for more papers by this authorDolores Garrido
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorFrancisco Palma
Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain
Search for more papers by this authorCorresponding Author
Cecilia Martínez
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Correspondence
Manuel Jamilena,
Email: [email protected]
Cecilia Martínez,
Email: [email protected]
Search for more papers by this authorCorresponding Author
Manuel Jamilena
Department of Biology and Geology and Department of Agronomy, Research Centers CIAIMBITAL and CeiA3, University of Almería, Almería, Spain
Correspondence
Manuel Jamilena,
Email: [email protected]
Cecilia Martínez,
Email: [email protected]
Search for more papers by this authorAbstract
The worldwide cultivated Cucurbita pepo L. is one of the most diverse species in the plant kingdom. In this study, chilling tolerance over a wide range of cultivars was characterized to discover the allelic variants to improving the postharvest quality of the immature fruit during cold storage. For this purpose, fruits from 126 accessions of worldwide origin have been evaluated for weight loss and chilling injury after 3, 7 and 14 days of cold storage, classifying them into tolerant, partially tolerant, and sensitive accessions. To verify this classification, antioxidant capacity and lipid peroxidation (MDA) of contrasting accessions (tolerant vs. sensitive) were assessed. The antioxidant capacity significantly decreased during cold storage in the sensitive accessions, while it was maintained in tolerant accessions. Additionally, the sensitive accessions presented a higher accumulation of MDA during this period. Finally, a GWAS analysis using GBS data available in CuGenDBv2, combined with weight loss percentage data, led to the identification of a candidate QTL located on chromosome 17 that regulates postharvest cold tolerance in zucchini. The region contains four SNPs whose alternative alleles were significantly associated with lower weight loss percentage and chilling injury indices during cold storage. Two SNPs are located in the 3’ UTR region of the gene CpERS1, a gene involved in ethylene perception. The other two SNPs generate missense mutations in the coding region of a Pectin methyl esterase inhibitor gene (CpPMI). The role of this QTL and these variants in chilling tolerance is discussed.
Open Research
DATA AVAILABILITY STATEMENT
All relevant data can be found within the manuscript and its supporting materials. The GBS data of C. pepo used in this study is available at CuGenDBv2 database (http://cucurbitgenomics.org/v2/).
The transcriptomic data were deposited in NCBI-SRA database (https://www.ncbi.nlm.nih.gov/sra/). Project number: PRJNA1019120.
Supporting Information
| Filename | Description |
|---|---|
| ppl14602-sup-0001-Figures.pdfPDF document, 493.9 KB | Appendix S1: Supplementary Figures |
| ppl14602-sup-0002-Tables.xlsxExcel 2007 spreadsheet , 41.1 KB | Table S1. PI information of the C. pepo accessions analyzed from the USDA-GRIN germplasm bank. Table S2. Evaluation of postharvest quality parameters across the accessions panel: Average of %WL and CI Index and Standard Errors (SE). Haplotype of the 4 significant SNPs identified in the GWAS analysis for PI accessions (Ref/Alt). Pink color indicates reference genotype, white color heterozygous, green color alternative genotype. Table S3. Antioxidant capacity of FRAP experiment (expressed in μg/mgDW) and MDA content (expressed in ng/mgDW). Data correspond to average and the SE. Different letters indicate significant differences between the accessions during cold storage (ANOVA, p ≤ 0.05). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Aghdam, M.S., Moradi, M., Razavi, F. & Rabiei, V. (2019) Exogenous phenylalanine application promotes chilling tolerance in tomato fruits during cold storage by ensuring supply of NADPH for activation of ROS scavenging systems. Scientia Horticulturae, 246, 818–825.
- Beji, S., Fontaine, V., Devaux, R., Thomas, M., Negro, S.S., Bahrman, N., Siol, M., Aubert, G., Burstin, J., Hilbert, J.L., Delbreil, B. & Lejeune-Hénaut, I. (2020) Genome-wide association study identifies favorable SNP alleles and candidate genes for frost tolerance in pea. BMC Genomics, 21(1), 1–21.
10.1186/s12864-020-06928-w Google Scholar
- Benítez, Á., Iglesias-Moya, J., Segura, M., Carvajal, F., Palma, F., Garrido, D., Martínez, C. & Jamilena, M. (2022) RNA-seq based analysis of transcriptomic changes associated with ABA-induced postharvest cold tolerance in zucchini fruit. Postharvest Biology and Technology, 192, 112023.
- Benzie, I.F.F. & Strain, J.J. (1996) The Ferric Reducing Ability of Plasma (FRAP) as a Measure of “Antioxidant Power”: The FRAP Assay. Analytical Biochemistry, 239(1), 70–76.
- Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. & Buckler, E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 23(19), 2633–2635.
- Carvajal, F., Martinez, C., Jamilena, M. & Garrido, D. (2011) Differential response of zucchini varieties to low storage temperature. Scientia Horticulturae. 130(1), 90–96.
- Carvajal, F., Palma, F., Jamilena, M. & Garrido, D. (2015a) Cell wall metabolism and chilling injury during postharvest cold storage in zucchini fruit. Postharvest Biology and Technology, 108, 68–77.
- Carvajal, F., Palma, F., Jamilena, M. & Garrido, D. (2015b) Preconditioning treatment induces chilling tolerance in zucchini fruit improving different physiological mechanisms against cold injury. Annals of Applied Biology, 166(2), 340–354.
- Carvajal, F., Palma, F., Jiménez-Muñoz, R., Jamilena, M., Pulido, A. & Garrido, D. (2017) Unravelling the role of abscisic acid in chilling tolerance of zucchini during postharvest cold storage. Postharvest Biology and Technology, 133, 26–35.
- Castro-Cegrí, A., Carvajal, F., Osorio, S., Jamilena, M., Garrido, D. & Palma, F. (2023a) Postharvest abscisic acid treatment modulates the primary metabolism and the biosynthesis of t-zeatin and riboflavin in zucchini fruit exposed to chilling stress. Postharvest Biology and Technology, 204, 112457.
- Castro-Cegrí, A., García-Pérez, P., Jamilena, M., Garrido, D., Palma, F. & Lucini, L. (2024) Exogenous abscisic acid mitigates chilling injury in zucchini during cold storage by eliciting a time-dependent shaping of specialized metabolites. Postharvest Biology and Technology. 212, 112864.
- Castro-Cegrí, A., Ortega-Muñoz, M., Sierra, S., Carvajal, F., Santoyo-Gonzalez, F., Garrido, D. & Palma, F. (2023b) Application of polysaccharide-based edible coatings to improve the quality of zucchini fruit during postharvest cold storage. Scientia Horticulturae, 314, 111941.
- Castro-Cegrí, A., Sierra, S., Hidalgo-Santiago, L., Esteban-Muñoz, A., Jamilena, M., Garrido, D. & Palma, F. (2023c) Postharvest treatment with Abscisic Acid alleviates chilling injury in zucchini fruit by regulating phenolic metabolism and non-enzymatic antioxidant system. Antioxidants, 12(1), 211.
- Chen, B. & Yang, H. (2013) 6-Benzylaminopurine alleviates chilling injury of postharvest cucumber fruit through modulating antioxidant system and energy status. Journal of the Science of Food and Agriculture, 93(8), 1915–1921.
- Chizk, T.M., Clark, J.R., Johns, C., Nelson, L., Ashrafi, H., Aryal, R. & Worthington, M.L. (2023) Genome-wide association identifies key loci controlling blackberry postharvest quality. Frontiers in Plant Science, 14, 1182790.
- Frazee, A.C., Pertea, G., Jaffe, A.E., Langmead, B., Salzberg, S.L. & Leek, J.T. (2015) Ballgown bridges the gap between transcriptome assembly and expression analysis. Nature biotechnology, 33(3), 243.
- García-Abadillo, J., Barba, P., Carvalho, T., Sosa-Zuñiga, V., Lozano, R., Carvalho, H.F., Garcia-Rojas, M., Salazar, E. & Sánchez, J.I. (2024) Dissecting the complex genetic basis of pre- and postharvest traits in Vitis vinifera L. using genome-wide association studies. Horticulture Research, 11(2), https://doi.org/10.1093/hr/uhad283.
- García, A., Aguado, E., Martínez, C., Loska, D., Beltrán, S., Valenzuela, J.L., Garrido, D. & Jamilena, M. (2020) The ethylene receptors CpETR1A and CpETR2B cooperate in the control of sex determination in Cucurbita pepo. Journal of Experimental Botany, 71(1), 154–167.
- Hakim, A., Purvis, A.C. & Mullinix, B.G. (1999) Differences in chilling sensitivity of cucumber varieties depends on storage temperature and the physiological dysfunction evaluated. Postharvest Biology and Technology, 17(2), 97–104.
- Heath, R.L. & Packer, L. (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1), 189–198.
- Hernandez, C.O., Labate, J., Reitsma, K., Fabrizio, J., Bao, K., Fei, Z., Grumet, R. & Mazourek, M. (2023) Characterization of the USDA Cucurbita pepo, C. moschata, and C. maxima germplasm collections. Frontiers in Plant Science, 14, 1130814.
- Jiménez-Muñoz, R., Palma, F., Carvajal, F., Castro-Cegrí, A., Pulido, A., Jamilena, M., Romero-Puertas, M.C. & Garrido, D. (2021) Pre-storage nitric oxide treatment enhances chilling tolerance of zucchini fruit (Cucurbita pepo L.) by S-nitrosylation of proteins and modulation of the antioxidant response. Postharvest Biology and Technology, 171, 111345.
- Kong, X.M, Ge, W.Y, Wei, B.D, Zhou, Q., Zhou, X., Zhao, Y.B & Ji, S.J (2020) Melatonin ameliorates chilling injury in green bell peppers during storage by regulating membrane lipid metabolism and antioxidant capacity. Postharvest Biology and Technology, 170, 111315.
- Kong, X.M, Zhou, Q., Luo, F., Wei, B.D, Wang, Y.J, Sun, H. Jun, Zhao, Y.B & Ji, S. J (2019) Transcriptome analysis of harvested bell peppers (Capsicum annuum L.) in response to cold stress. Plant Physiology and Biochemistry, 139, 314–324.
- Li, C., Dong, S., Beckles, D.M., Liu, X., Liu, D., Miao, H., Zhang, S. & Gu, X. (2022) Identification of QTLs controlling cold tolerance in cucumber (Cucumis sativus L.) seedlings. Scientia Horticulturae, 305, 111383.
- Li, M.X., Yeung, J.M.Y., Cherny, S.S. & Sham, P.C. (2012) Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Human Genetics, 131(5), 747–756.
- Liu, Q., Xin, D., Xi, L., Gu, T., Jia, Z., Zhang, B. & Kou, L. (2022) Novel applications of exogenous melatonin on cold stress mitigation in postharvest cucumbers. Journal of Agriculture and Food Research, 10, 100459.
- Liu, Y., Yang, X., Zhu, S. & Wang, Y. (2016) Postharvest application of MeJA and NO reduced chilling injury in cucumber (Cucumis sativus) through inhibition of H2O2 accumulation. Postharvest Biology and Technology, 119, 77–83.
- Ma, M., Zhu, Z., Cheng, S., Zhou, Q., Zhou, X., Kong, X., Hu, M., Yin, X., Wei, B. & Ji, S. (2020) Methyl jasmonate alleviates chilling injury by regulating membrane lipid composition in green bell pepper. Scientia Horticulturae, 266, 109308.
- Martínez-Téllez, M.A., Ramos-Clamont, M.G., Gardea, A.A. & Vargas-Arispuro, I. (2002) Effect of infiltrated polyamines on polygalacturonase activity and chilling injury responses in zucchini squash (Cucurbita pepo L.). Biochemical and Biophysical Research Communications, 295(1), 98–101.
- Megías, Z., Manzano, S., Martínez, C., García, A., Aguado, E., Garrido, D., del Mar Rebolloso, M., Valenzuela, J.L. & Jamilena, M. (2017) Postharvest cold tolerance in summer squash and its association with reduced cold-induced ethylene production. Euphytica, 213, 9. https://doi.org/10.1007/s10681-016-1805-0.
10.1007/s10681-016-1805-0 Google Scholar
- Megías, Z., Martínez, C., Manzano, S., Barrera, A., Rosales, R., Valenzuela, J.L., Garrido, D. & Jamilena, M. (2014) Cold-induced ethylene in relation to chilling injury and chilling sensitivity in the non-climacteric fruit of zucchini (Cucurbita pepo L.). LWT - Food Science and Technology, 57(1), 194–199.
- Megías, Z., Martínez, C., Manzano, S., García, A., del Mar Rebolloso-Fuentes, M., Valenzuela, J.L., Garrido, D. & Jamilena, M. (2016) Ethylene biosynthesis and signaling elements involved in chilling injury and other postharvest quality traits in the non-climacteric fruit of zucchini (Cucurbita pepo). Postharvest Biology and Technology, 113, 48–57.
- Megías, Z., Martínez, C., Manzano, S., García, A., Rebolloso-Fuentes, M. del M., Garrido, D., Valenzuela, J.L. & Jamilena, M. (2015) Individual shrink wrapping of zucchini fruit improves postharvest chilling tolerance associated with a reduction in ethylene production and oxidative stress metabolites. Plos One, 10(7), e0133058.
- Nandi, L., Suresh, P., Pradeepkumara, N., Munshi, A.D., Sharma, P.K., Boopalakrishnan, G., Kumari, K., Iquebal, M.A., Jaiswal, S., Ghosh, A., Tomar, B.S., Gopala Krishnan, S., Bhattacharya, R.C., Kumar, D., Behera, T.K. & Dey, S.S. (2024) Elucidating the genetics of postharvest shelf-life of cucumber fruits and identification of associated QTLs and candidate genes. Scientia Horticulturae, 327, 112800.
- Palma, F., Carvajal, F., Jamilena, M. & Garrido, D. (2014a) Contribution of polyamines and other related metabolites to the maintenance of zucchini fruit quality during cold storage. Plant Physiology and Biochemistry, 82, 161–171.
- Palma, F., Carvajal, F., Jiménez-Muñoz, R., Pulido, A., Jamilena, M. & Garrido, D. (2019) Exogenous γ-aminobutyric acid treatment improves the cold tolerance of zucchini fruit during postharvest storage. Plant Physiology and Biochemistry, 136, 188–195.
- Palma, F., Carvajal, F., Lluch, C., Jamilena, M. & Garrido, D. (2014b) Changes in carbohydrate content in zucchini fruit (Cucurbita pepo L.) under low temperature stress. Plant Science, 217–218, 78–86.
- Palma, F., Carvajal, F., Ramos, J.M., Jamilena, M. & Garrido, D. (2015) Effect of putrescine application on maintenance of zucchini fruit quality during cold storage: Contribution of GABA shunt and other related nitrogen metabolites. Postharvest Biology and Technology, 99, 131–140.
- Pareek, S., Benkeblia, N., Janick, J., Cao, S. & Yahia, E.M. (2014) Postharvest physiology and technology of loquat (Eriobotrya japonica Lindl.) fruit. Journal of the Science of Food and Agriculture, 94(8), 1495–1504.
- Pons, C., Martí, C., Forment, J., Crisosto, C.H., Dandekar, A.M. & Granell, A. (2014) A bulk segregant gene expression analysis of a peach population reveals components of the underlying mechanism of the fruit cold response. Plos One, 9(3), e90706.
- Shah, L.R., Ahmed, N., Hussain, K., Mansoor, S., Khan, T., Khan, I., Narayan, S., Afroza, B., Murtaza, I., Shikari, A.B., Bhat, B. & Masoodi, K.Z. (2024) Mapping phenotypic performance and novel SNPs for cold tolerance in tomato (Solanum lycopersicum) genotypes through GWAS and population genetics. BMC Genomic Data, 25(1), 1–23.
- Song, C., Wang, K., Xiao, X., Liu, Q., Yang, M., Li, X., Feng, Y., Li, S., Shi, L., Chen, W. & Yang, Z. (2022) Membrane lipid metabolism influences chilling injury during cold storage of peach fruit. Food Research International, 157, 111249.
- Sthapit Kandel, J., Peng, H., Hayes, R.J., Mou, B. & Simko, I. (2020) Genome-wide association mapping reveals loci for shelf life and developmental rate of lettuce. Theoretical and Applied Genetics, 133(6), 1947–1966.
- Thapa, R., Tabien, R.E., Thomson, M.J. & Septiningsih, E.M. (2020) Genome-Wide Association Mapping to identify genetic loci for cold tolerance and cold recovery during germination in rice. Frontiers in Genetics, 11, 499346.
10.3389/fgene.2020.00022 Google Scholar
- Tossi, V.E., Regalado, J.J., Martínez, J., Galván, A., Martinez Tosar, L.J., Pitta-Alvarez, S.I., Rebolloso, M.M. & Jamilena, M. (2024) UV-B alleviates postharvest chilling injury of zucchini fruit associated with a reduction in oxidative stress. Postharvest Biology and Technology, 212, 112850.
- Valenzuela, J.L., Manzano, S., Palma, F., Carvajal, F., Garrido, D. & Jamilena, M. (2017) Oxidative stress asociated with chilling injury in immature fruit: postharvest technological and biotechnological solutions. International Journal of Molecular Sciences, 18(7), 1467.
- Vicente, A.R., Saladié, M., Rose, J.K.C. & Labavitch, J.M. (2007) The linkage between cell wall metabolism and fruit softening: looking to the future. Journal of the Science of Food and Agriculture, 87(8), 1435–1448.
- Xue, C., Guan, S.C., Chen, J.Q., Wen, C.J., Cai, J.F. & Chen, X. (2020) Genome wide identification and functional characterization of strawberry pectin methylesterases related to fruit softening. BMC Plant Biology, 20(1), 1–17.
- Yi, Q., Malvar, R.A., Álvarez-Iglesias, L., Ordás, B. & Revilla, P. (2020) Dissecting the genetics of cold tolerance in a multiparental maize population. Theoretical and Applied Genetics, 133(2), 503–516.
- Yu, J., Wu, S., Sun, H., Wang, X., Tang, X., Guo, S., Zhang, Z., Huang, S., Xu, Y., Weng, Y., Mazourek, M., McGregor, C., Renner, S.S., Branham, S., Kousik, C., Patrick Wechter, W., Levi, A., Grumet, R., Zheng, Y. & Fei, Z. (2023) CuGenDBv2: an updated database for cucurbit genomics. Nucleic Acids Research, 51(D1), D1457–D1464.
- Zhang, W., Jiang, H., Cao, J. & Jiang, W. (2021) Advances in biochemical mechanisms and control technologies to treat chilling injury in postharvest fruits and vegetables. Trends in Food Science & Technology, 113, 355–365.
- Zhao, Y., Li, J., Zhao, R., Xu, K., Xiao, Y., Zhang, S., Tian, J. & Yang, X. (2020) Genome-wide association study reveals the genetic basis of cold tolerance in wheat. Molecular Breeding, 40(4), 1–13.
10.1007/s11032-020-01115-x Google Scholar
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