Genome-wide isolation and expression analysis of vacuolar processing enzyme (VPE) gene family in four apple cultivars with different storability

References

• Albertini, A., Simeoni, F., Galbiati, M., Bauer, H., Tonelli, C., & Cominelli, E. (2014). Involvement of the vacuolar processing enzyme γVPE in response of Arabidopsis thaliana to water stress. Biologia Plantarum, 58(3), 531–538. https://doi.org/10.1007/s10535-014-0417-6
   Web of Science ®Google Scholar
• Alonso, J. M., & Cranell, A. (1995). A putative vacuolar processing protease is regulated by ethylene and also during fruit ripening in citrus fruit. Plant Physiology, 109(2), 541–547. https://doi.org/10.1104/pp.109.2.541
   PubMed Web of Science ®Google Scholar
• Ariizumi, T., Higuchi, K., Arakaki, S., Sano, T., Asamizu, E., & Ezura, H. (2011). Genetic suppression analysis in novel vacuolar processing enzymes reveals their roles in controlling sugar accumulation in tomato fruits. Journal of Experimental Botany, 62(8), 2773–2786. https://doi.org/10.1093/jxb/erq451
   PubMed Web of Science ®Google Scholar
• Brumos, J. (2021). Gene regulation in climacteric fruit ripening. Current Opinion in Plant Biology, 63, 102042. https://doi.org/10.1016/j.pbi.2021.102042
   PubMed Web of Science ®Google Scholar
• Busatto, N., Farneti, B., Tadiello, A., Velasco, R., Costa, G., & Costa, F. (2016). Candidate gene expression profiling reveals a time specific activation among different harvesting dates in ‘Golden Delicious’ and ‘fuji’ apple cultivars. Euphytica, 208(2), 401–413. https://doi.org/10.1007/s10681-015-1621-y
   Web of Science ®Google Scholar
• Chai, Y., Li, A., Chit Wai, S., Song, C., Zhao, Y., Duan, Y., Zhang, B., & Lin, Q. (2020). Cuticular wax composition changes of 10 apple cultivars during postharvest storage. Food Chemistry, 324, 126903. https://doi.org/10.1016/j.foodchem.2020.126903
   PubMed Web of Science ®Google Scholar
• Cheng, Z., Guo, X., Zhang, J., Liu, Y., Wang, B., Li, H., & Lu, H. (2019). βVPE is involved in tapetal degradation and pollen development by activating proprotease maturation in Arabidopsis thaliana. Journal of Experimental Botany, 71(6), 1943–1955. https://doi.org/10.1093/jxb/erz560
   Web of Science ®Google Scholar
• Cheng, Z., Zhang, J., Yin, B., Liu, Y., Wang, B., Li, H., & Lu, H. (2019). γVPE plays an important role in programmed cell death for xylem fiber cells by activating protease CEP1 maturation in Arabidopsis thaliana. International Journal of Biological Macromolecules, 137, 703–711. https://doi.org/10.1016/j.ijbiomac.2019.07.017
   PubMed Web of Science ®Google Scholar
• Gong, P., Li, Y., Tang, Y., Wei, R., Zhu, H., Wang, Y., & Zhang, C. (2018). Vacuolar processing enzyme (VvβVPE) from Vitis vinifera, processes seed proteins during ovule development, and accelerates seed germination in VvβVPE heterologously over-expressed Arabidopsis. Plant Science, 274, 420–431. https://doi.org/10.1016/j.plantsci.2018.06.023
   PubMed Web of Science ®Google Scholar
• Harada, T., Sunako, T., Wakasa, Y., Soejima, J., Satoh, T., & Niizeki, M. (2000). An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-ACS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theoretical and Applied Genetics, 101(5–6), 742–746. https://doi.org/10.1007/s001220051539
   Web of Science ®Google Scholar
• Hu, Y., Han, Z., Wang, T., Li, H., Li, Q., Wang, S., Tian, J., Wang, Y., Zhang, X., Xu, X., Han, Z., Lü, P., & Wu, T. (2022). Ethylene response factor MdERF4 and histone deacetylase MdHDA19 suppress apple fruit ripening through histone deacetylation of ripening-related genes. Plant Physiology, 188(4), 2166–2181. https://doi.org/10.1093/plphys/kiac016
   PubMed Web of Science ®Google Scholar
• Jobling, J. J., & McGlasson, W. B. (1995). A comparison of ethylene production, maturity and controlled atmosphere storage life of gala, Fuji and Lady Williams apples (Malus domestica, Borkh.). Postharvest Biology and Technology, 6(3–4), 209–218. https://doi.org/10.1016/0925-5214(94)00002-A
   Web of Science ®Google Scholar
• Kinoshita, T., Yamada, K., Hiraiwa, N., Kondo, M., Nishimura, M., & Hara-Nishimura, I. (1999). Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. The Plant Journal: For Cell and Molecular Biology, 19(1), 43–53. https://doi.org/10.1046/j.1365-313X.1999.00497.x
   PubMed Web of Science ®Google Scholar
• Li, Z., Yue, H., & Xing, D. (2012). MAP kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytologist, 195(1), 85–96. https://doi.org/10.1111/j.1469-8137.2012.04131.x
   PubMed Web of Science ®Google Scholar
• Lv, J., Ge, Y., Li, C., Zhang, M., & Li, J. (2017). Identification and analysis of genes involved in the jasmonate pathway in response to ethephon and 1-methylcyclopropene during the ripening of apple fruit. Journal of the American Society for Horticultural Science, 142(3), 184–191. https://doi.org/10.21273/JASHS04054-17
   Web of Science ®Google Scholar
• Lv, J., Zhang, M., Zhang, J., Ge, Y., Li, C., Meng, K., & Li, J. (2018). Effects of methyl jasmonate on expression of genes involved in ethylene biosynthesis and signaling pathway during postharvest ripening of apple fruit. Scientia Horticulturae, 229, 157–166. https://doi.org/10.1016/j.scienta.2017.11.007
   Web of Science ®Google Scholar
• Lv, J., Zhang, Y., Sun, M., Chen, J., Ge, Y., & Li, J. (2023). 1-methylcyclopropene (1-MCP) treatment differentially mediated expression of vacuolar processing enzyme (VPE) genes and delayed programmed cell death (PCD) during ripening and senescence of apple fruit. Scientia Horticulturae, 307, 111489. https://doi.org/10.1016/j.scienta.2022.111489
   Web of Science ®Google Scholar
• Martinez, D. E., Bartoli, C. G., Grbic, V., & Guiamet, J. J. (2007). Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. Journal of Experimental Botany, 58(5), 1099–1107. https://doi.org/10.1093/jxb/erl270
   PubMed Web of Science ®Google Scholar
• Nakaune, S., Yamada, K., Kondo, M., Kato, T., Tabata, S., Nishimura, M., & Hara-Nishimura, I. (2005). A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development. The Plant Cell, 17(3), 876–887. https://doi.org/10.1105/tpc.104.026872
   PubMed Web of Science ®Google Scholar
• Prasad, S. C., Kisku, A. V., & Sarin, N. B. (2018). Understanding the gamma-vacuolar processing enzyme gene regulation by promoter-GUS fusion approach. Plant Archives, 18(1), 679–689. https://doi.org/10.51470/0972-5210
   Google Scholar
• Rantong, G., & Gunawardena, A. H. (2018). Vacuolar processing enzymes, AmVPE1 and AmVPE2, as potential executors of ethylene regulated programmed cell death in the lace plant (Aponogeton madagascariensis). Botany, 96(4), 235–247. https://doi.org/10.1139/cjb-2017-0184
   Google Scholar
• Song, J., Yang, F., Xun, M., Xu, L., Tian, X., Zhang, W., & Yang, H. (2020). Genome-Wide identification and characterization of vacuolar processing enzyme gene family and diverse expression under stress in apple (Malus × Domestica). Frontiers in Plant Science, 11, 626. https://doi.org/10.3389/fpls.2020.00626
   PubMed Web of Science ®Google Scholar
• Sunako, T., Sakuraba, W., Senda, M., Akada, S., Ishikawa, R., Niizeki, M., & Harada, T. (1999). An allele of the ripening-specific 1-aminocyclopropane-1-carboxylic acid synthase gene (ACS1) in apple fruit with a long storage life. Plant Physiology, 119(4), 1297–1303. https://doi.org/10.1104/pp.119.4.1297
   PubMed Web of Science ®Google Scholar
• Tang, C. N., Wan Abdullah, W. M. A. N., Wee, C. Y., Balia Yusof, Z. N., Yap, W. S., Cheng, W. H., Baharum, N. A., Ong-Abdullah, J., Loh, J. Y., & Lai, K. S. (2023). Promoter cis-element analyses reveal the function of αVPE in drought stress response of Arabidopsis. Biology, 12(3), 430. https://doi.org/10.3390/biology12030430
   PubMedGoogle Scholar
• Tang, Y., Wang, R., Gong, P., Li, S., Wang, Y., Zhang, C., & Cao, H. (2016). Gene cloning, expression and enzyme activity of Vitis vinifera vacuolar processing enzymes (VvVPEs). Public Library of Science One, 11(8), e0160945. https://doi.org/10.1371/journal.pone.0160945
   Google Scholar
• Teper-Bamnolker, P., Danieli, R., Peled-Zehavi, H., Belausov, E., Abu-Abied, M., Avin-Wittenberg, T., Sadot, E., & Eshel, D. (2021). Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death. Autophagy, 17(10), 3109–3123. https://doi.org/10.1080/15548627.2020.1856492
   PubMed Web of Science ®Google Scholar
• Van Wyk, S. G., Du Plessis, M., Cullis, C. A., Kunert, K. J., & Vorster, B. J. (2014). Cysteine protease and cystatin expression and activity during soybean nodule development and senescence. BMC Plant Biology, 14(1), 294. https://doi.org/10.1186/s12870-014-0294-3
   PubMedGoogle Scholar
• Vorster, B. J., Cullis, C. A., & Kunert, K. J. (2019). Plant vacuolar processing enzymes. Frontiers in Plant Science, 10, 479–486. https://doi.org/10.3389/fpls.2019.00479
   PubMed Web of Science ®Google Scholar
• Wan Abdullah, W. M. A. N., Saidi, N. B., Yusof, M. T., Wee, C. Y., Loh, H. S., Ong-Abdullah, J., & Lai, K. S. (2022). Vacuolar processing enzymes modulating susceptibility response to Fusarium oxysporum f. sp. cubense tropical race 4 infections in banana. Frontiers in Plant Science, 12, 769855. https://doi.org/10.3389/fpls.2021.769855
   PubMed Web of Science ®Google Scholar
• Wang, N., Duhita, N., Ariizumi, T., & Ezura, H. (2016). Involvement of vacuolar processing enzyme SlVPE5 in post-transcriptional process of invertase in sucrose accumulation in tomato. Plant Physiology and Biochemistry, 108, 71–78. https://doi.org/10.1016/j.plaphy.2016.06.037
   PubMed Web of Science ®Google Scholar
• Wang, W., Cai, J., Wang, P., Tian, S., & Qin, G. (2017). Post-transcriptional regulation of fruit ripening and disease resistance in tomato by the vacuolar protease SlVPE3. Genome Biology, 18(1), 47–70. https://doi.org/10.1186/s13059-017-1178-2
   PubMedGoogle Scholar
• Xu, F., Lu, F., Xiao, Z., & Li, Z. (2020). Influence of drop shock on physiological responses and genes expression of apple fruit. Food Chemistry, 303, 125424. https://doi.org/10.1016/j.foodchem.2019.125424
   PubMed Web of Science ®Google Scholar
• Zhang, F., Xue, H., Lu, X., Zhang, B., Wang, F., Ma, Y., & Zhang, Z. (2015). Autotetraploidization enhances drought stress tolerance in two apple cultivars. Trees, 29(6), 1773–1780. https://doi.org/10.1007/s00468-015-1258-4
   Web of Science ®Google Scholar
• Zhang, H., Tao, X., & Zhang, F. (2021). Genome-wide identification and expression analysis of the vacuolar processing enzyme (VPE) family genes in pear. The Journal of Horticultural Science and Biotechnology, 96(4), 469–478. https://doi.org/10.1080/14620316.2021.1882887
   Web of Science ®Google Scholar
• Zhu, L., Wang, X., Tian, J., Zhang, X., Yu, T., Li, Y., & Li, D. (2022). Genome-wide analysis of VPE family in four Gossypium species and transcriptional expression of VPEs in the upland cotton seedlings under abiotic stresses. Functional & Integrative Genomics, 22(2), 179–192. https://doi.org/10.1007/s10142-021-00818-4
   PubMed Web of Science ®Google Scholar
• Zhu, L., Yang, C., You, Y., Liang, W., Wang, N., Ma, F., & Li, C. (2019). Validation of reference genes for qRT-PCR analysis in peel and flesh of six apple cultivars (Malus domestica) at diverse stages of fruit development. Scientia Horticulturae, 244, 165–171. https://doi.org/10.1016/j.scienta.2018.09.033
   Web of Science ®Google Scholar
• Zhu, Y., & Barritt, B. H. (2008). Md-ACS1 and md-ACO1 genotyping of apple (Malus x domestica Borkh.) breeding parents and suitability for marker-assisted selection. Tree Genetics & Genomes, 4(3), 555–562. https://doi.org/10.1007/s11295-007-0131-z
   Web of Science ®Google Scholar