Transcriptome analysis reveals wax and phytohormone metabolism potentially involved in shooting shrivelling of apple branches overwinter
Yanlong Gao A , Zhongxing Zhang A , Shuangcheng Wang A , Naiying Ma A and Yanxiu Wang
A *
+ Author Affiliations
- Author Affiliations
A College of Horticulture, Gansu Agricultural University, Lanzhou 730070, China.
Functional Plant Biology 50(7) 540-558 https://doi.org/10.1071/FP22283
Submitted: 25 November 2022 Accepted: 27 March 2023 Published: 10 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Shoot shrivelling severely threatens growth and development of deciduous trees in the northern hemisphere, and we observed that there was a significant difference in shoot shrivelling rate between different apple varieties in practice. In this study, we investigated the anatomical and physiological characteristics of branches from different germplasm resources combined with an analysis of the transcriptome. Transcriptomes of samples treated in the initial dormancy, deep dormancy and freeze–thaw periods were generated and characterised. In three different periods, 7233 differentially expressed genes (DEGs) were identified including 3538 upregulated genes and 3695 downregulated genes. DEGs related to plant hormone signal transduction, starch and sucrose metabolism, cutin, suberin and wax biosynthesis were significantly enriched. Physiological characterisation showed that dormancy overwinter can induce the accumulation of soluble sugar and starch, shoot shrivelling rate of ‘Fuji’ was 2.31 times that of the ‘Delicious’; and the critical water content of ‘Delicious’ was significantly higher than ‘Fuji’. Phytohormone contents and proportions varied irregularly according to the overwintering phase among two varieties. Wax content, morphology and composition also exhibited difference. In conclusion, branch microstructure, phytohormone and wax metabolism all determined the overwintering performance of trees and phytohormones can regulate wax metabolism to ensure normal overwintering of trees.
Keywords: apple, critical water content, cutin and suberin, gene, plant phytohormone, shooting shrivelling, transcriptome, wax metabolism.
References
Aguilera J, Randez-Gil F, Prieto JA (2007) Cold response in Saccharomyces cerevisiae: new functions for old mechanisms. FEMS Microbiology Reviews 31, 327–341.| Cold response in Saccharomyces cerevisiae: new functions for old mechanisms.Crossref | GoogleScholarGoogle Scholar |
Bertrand A, Castonguay Y (2003) Plant adaptations to overwintering stresses and implications of climate change. Canadian Journal of Botany 81, 1145–1152.
| Plant adaptations to overwintering stresses and implications of climate change.Crossref | GoogleScholarGoogle Scholar |
Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Science 187, 89–96.
| Characterization of the ABA signal transduction pathway in Vitis vinifera.Crossref | GoogleScholarGoogle Scholar |
Boriboonkaset T, Theerawitaya C, Yamada N, Pichakum A, Supaibulwatana K, Cha-Um S, Takabe T, Kirdmanee C (2013) Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress. Protoplasma 250, 1157–1167.
| Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress.Crossref | GoogleScholarGoogle Scholar |
Castroverde CDM, Dina D (2021) Temperature regulation of plant hormone signaling during stress and development. Journal of Experimental Botany 72, 7436–7458.
| Temperature regulation of plant hormone signaling during stress and development.Crossref | GoogleScholarGoogle Scholar |
Cui S-M, Sadayoshi K, Ogawa Y, Nii N (2004) Effects of water stress on sorbitol content in leaves and roots, anatomical changes in cell nuclei, and starch accumulation in leaves of young peach trees. Journal of the Japanese Society for Horticultural Science 73, 25–30.
| Effects of water stress on sorbitol content in leaves and roots, anatomical changes in cell nuclei, and starch accumulation in leaves of young peach trees.Crossref | GoogleScholarGoogle Scholar |
Dalal M, Inupakutika M (2014) Transcriptional regulation of ABA core signaling component genes in sorghum (Sorghum bicolor L. Moench). Molecular Breeding 34, 1517–1525.
| Transcriptional regulation of ABA core signaling component genes in sorghum (Sorghum bicolor L. Moench).Crossref | GoogleScholarGoogle Scholar |
Domínguez E, Heredia-Guerrero JA, Heredia A (2011) The biophysical design of plant cuticles: an overview. New Phytologist 189, 938–949.
| The biophysical design of plant cuticles: an overview.Crossref | GoogleScholarGoogle Scholar |
Duarte KE, de Souza WR, Santiago TR, Sampaio BL, Ribeiro AP, Cotta MG, da Cunha BADB, Marraccini PRR, Kobayashi AK, Molinari HBC (2019) Identification and characterization of core abscisic acid (ABA) signaling components and their gene expression profile in response to abiotic stresses in Setaria viridis. Scientific Reports 9, 4028
| Identification and characterization of core abscisic acid (ABA) signaling components and their gene expression profile in response to abiotic stresses in Setaria viridis.Crossref | GoogleScholarGoogle Scholar |
Franks PJ, Gibson A, Bachelard EP (1995) Xylem permeability and embolism susceptibility in seedlings of Eucalyptus camaldulensis Dehnh. From two different climatic zones. Functional Plant Biology 22, 15–21.
| Xylem permeability and embolism susceptibility in seedlings of Eucalyptus camaldulensis Dehnh. From two different climatic zones.Crossref | GoogleScholarGoogle Scholar |
Fukuda S, Satoh A, Kasahara H, Matsuyama H, Takeuchi Y (2008) Effects of ultraviolet-B irradiation on the cuticular wax of cucumber (Cucumis sativus) cotyledons. Journal of Plant Research 121, 179–189.
| Effects of ultraviolet-B irradiation on the cuticular wax of cucumber (Cucumis sativus) cotyledons.Crossref | GoogleScholarGoogle Scholar |
Gabriela-Anca Maier C, Post-Beittenmiller D (1998) Epicuticular wax on leek in vitro developmental stages and seedlings under varied growth conditions. Plant Science 134, 53–67.
| Epicuticular wax on leek in vitro developmental stages and seedlings under varied growth conditions.Crossref | GoogleScholarGoogle Scholar |
Hu W, Yan Y, Shi H, Liu J, Miao H, Tie W, Ding Z, Ding X, Wu C, Liu Y, Wang J, Xu B, Jin Z (2017) The core regulatory network of the abscisic acid pathway in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress. BMC Plant Biology 17, 145
| The core regulatory network of the abscisic acid pathway in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Huang Z, Zhao N, Qin M, Xu A (2018) Mapping of quantitative trait loci related to cold resistance in Brassica napus L. Journal of Plant Physiology 231, 147–154.
| Mapping of quantitative trait loci related to cold resistance in Brassica napus L.Crossref | GoogleScholarGoogle Scholar |
Kazemi-Shahandashti S-S, Maali-Amiri R (2018) Global insights of protein responses to cold stress in plants: signaling, defence, and degradation. Journal of Plant Physiology 226, 123–135.
| Global insights of protein responses to cold stress in plants: signaling, defence, and degradation.Crossref | GoogleScholarGoogle Scholar |
Kim KS, Park SH, Jenks MA (2007) Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. Journal of Plant Physiology 164, 1134–1143.
| Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit.Crossref | GoogleScholarGoogle Scholar |
Kong E, Liu D, Guo X, Yang W, Sun J, Li X, Zhan K, Cui D, Lin J, Zhang A (2013) Anatomical and chemical characteristics associated with lodging resistance in wheat. The Crop Journal 1, 43–49.
| Anatomical and chemical characteristics associated with lodging resistance in wheat.Crossref | GoogleScholarGoogle Scholar |
Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiology 151, 1918–1929.
| The impact of water deficiency on leaf cuticle lipids of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Kurepin LV, Emery RJN, Pharis RP, Reid DM (2007) The interaction of light quality and irradiance with gibberellins, cytokinins and auxin in regulating growth of Helianthus annuus hypocotyls. Plant, Cell & Environment 30, 147–155.
| The interaction of light quality and irradiance with gibberellins, cytokinins and auxin in regulating growth of Helianthus annuus hypocotyls.Crossref | GoogleScholarGoogle Scholar |
Lenka SK, Muthusamy SK, Chinnusamy V, Bansal KC (2018) Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana. Molecular Biotechnology 60, 350–361.
| Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Martínez-Medina A, Del Mar Alguacil M, Pascual JA, Van Wees SCM (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. Journal of Chemical Ecology 40, 804–815.
| Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants.Crossref | GoogleScholarGoogle Scholar |
Mayr S, Cochard H, Améglio T, Kikuta SB (2007) Embolism formation during freezing in the wood of Picea abies. Plant Physiology 143, 60–67.
| Embolism formation during freezing in the wood of Picea abies.Crossref | GoogleScholarGoogle Scholar |
Meng S, Cao Y, Li H, Bian Z, Wang D, Lian C, Yin W, Xia X (2019) PeSHN1 regulates water-use efficiency and drought tolerance by modulating wax biosynthesis in poplar. Tree Physiology 39, 1371–1386.
| PeSHN1 regulates water-use efficiency and drought tolerance by modulating wax biosynthesis in poplar.Crossref | GoogleScholarGoogle Scholar |
Mills D, Zhang G, Benzioni A (2001) Effect of different salts and of ABA on growth and mineral uptake in Jojoba shoots grown in vitro. Journal of Plant Physiology 158, 1031–1039.
| Effect of different salts and of ABA on growth and mineral uptake in Jojoba shoots grown in vitro.Crossref | GoogleScholarGoogle Scholar |
Monder MJ, Kozakiewicz P, Jankowska A (2019) Anatomical structure changes in stem cuttings of rambler roses induced with plant origin preparations. Scientia Horticulturae 255, 242–254.
| Anatomical structure changes in stem cuttings of rambler roses induced with plant origin preparations.Crossref | GoogleScholarGoogle Scholar |
Nantawanit N, Panijpan B, Ruenwongsa P (2011) Studying how plants defend themselves: a chemical weapon produced by chilli fruit. Journal of Biological Education 45, 244–250.
| Studying how plants defend themselves: a chemical weapon produced by chilli fruit.Crossref | GoogleScholarGoogle Scholar |
Oliveira AFM, Meirelles ST, Salatino A (2003) Epicuticular waxes from caatinga and cerrado species and their efficiency against water loss. Anais da Academia Brasileira de Ciências 75, 431–439.
| Epicuticular waxes from caatinga and cerrado species and their efficiency against water loss.Crossref | GoogleScholarGoogle Scholar |
Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Höfer R, Schreiber L, Chory J, Aharoni A (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiology 145, 1345–1360.
| The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion.Crossref | GoogleScholarGoogle Scholar |
Planchet E, Rannou O, Ricoult C, Boutet-Mercey S, Maia-Grondard A, Limami AM (2011) Nitrogen metabolism responses to water deficit act through both abscisic acid (ABA)-dependent and independent pathways in Medicago truncatula during post-germination. Journal of Experimental Botany 62, 605–615.
| Nitrogen metabolism responses to water deficit act through both abscisic acid (ABA)-dependent and independent pathways in Medicago truncatula during post-germination.Crossref | GoogleScholarGoogle Scholar |
Redillas MCFR, Park S-H, Lee JW, Kim YS, Jeong JS, Jung H, Bang SW, Hahn T-R, Kim J-K (2012) Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnology Reports 6, 89–96.
| Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress.Crossref | GoogleScholarGoogle Scholar |
Riederer M (2006) Thermodynamics of the water permeability of plant cuticles: characterization of the polar pathway. Journal of Experimental Botany 57, 2937–2942.
| Thermodynamics of the water permeability of plant cuticles: characterization of the polar pathway.Crossref | GoogleScholarGoogle Scholar |
Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52, 2023–2032.
| Protecting against water loss: analysis of the barrier properties of plant cuticles.Crossref | GoogleScholarGoogle Scholar |
Rim JE, Pinsky PM, van Osdol WW (2007) Using the method of homogenization to calculate the effective diffusivity of the stratum corneum. Journal of Membrane Science 293, 174–182.
| Using the method of homogenization to calculate the effective diffusivity of the stratum corneum.Crossref | GoogleScholarGoogle Scholar |
Roy R, Mazumder PB, Sharma GD (2009) Proline, catalase and root traits as indices of drought resistance in bold grained rice (Oryza sativa) genotypes. African Journal of Biotechnology 8, 6521–6528.
Rozi A, Jia Y (2003) A theoretical study of effects of cytosolic Ca2+ oscillations on activation of glycogen phosphorylase. Biophysical Chemistry 106, 193–202.
| A theoretical study of effects of cytosolic Ca2+ oscillations on activation of glycogen phosphorylase.Crossref | GoogleScholarGoogle Scholar |
Santos-Espinoza AM, González-Mendoza D, Ruiz-Valdiviezo VM, Luján-Hidalgo MC, Jonapa-Hernández F, Valdez-Salas B, Gutiérrez-Miceli FA (2020) Changes in the physiological and biochemical state of peanut plants (Arachis hypogaea L.) induced by exposure to green metallic nanoparticles. International Journal of Phytoremediation 23, 747–754.
| Changes in the physiological and biochemical state of peanut plants (Arachis hypogaea L.) induced by exposure to green metallic nanoparticles.Crossref | GoogleScholarGoogle Scholar |
Semenikhina Y, Kambulov S, Boyko A, Nadolinsky Y, Podlesniy D (2021) Influence of the main tillage methods on the moisture temperature mode of the soil and the yield of winter wheat. IOP Conference Series: Earth and Environmental Science 723, 032048
| Influence of the main tillage methods on the moisture temperature mode of the soil and the yield of winter wheat.Crossref | GoogleScholarGoogle Scholar |
Seo PJ, Lee SB, Suh MC, Park M-J, Go YS, Park C-M (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. The Plant Cell 23, 1138–1152.
| The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Seok K, Yun K, Ho C (2012) Changes of freezing temperature in peach shoot during winter season. Horticulture Abstracts 2, 195–264.
| Changes of freezing temperature in peach shoot during winter season.Crossref | GoogleScholarGoogle Scholar |
Singh S, Singh M (2000) Genotypic basis of response to saliniity stress in some crosses of spring wheat Triticum aestivum L. Euphytica 115, 209–214.
| Genotypic basis of response to saliniity stress in some crosses of spring wheat Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar |
Singh A, Jha SK, Bagri J, Pandey GK (2015) ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis. PLoS ONE 10, e0125168
| ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Tamminen I, Mäkelä P, Heino P, Palva ET (2001) Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. The Plant Journal 25, 1–8.
| Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Wang M (2008) The relationship between the branch tissue structure and cold resistance of Zanthoxylum bungeanum. Gansu Science Journal 4, 45–47.
| The relationship between the branch tissue structure and cold resistance of Zanthoxylum bungeanum.Crossref | GoogleScholarGoogle Scholar |
Wei J, Zheng G, Dong X, Li H, Liu S, Wang Y, Liu Z (2022) Integration of transcriptome and proteome analysis reveals the mechanism of freezing tolerance in winter rapeseed. Plant Growth Regulation 96, 103–118.
| Integration of transcriptome and proteome analysis reveals the mechanism of freezing tolerance in winter rapeseed.Crossref | GoogleScholarGoogle Scholar |
Wilner J (1959) Note on an electrolytic procedure for differentiating between frost injury of roots and shoots in woody plants. Canadian Journal of Plant Science 39, 512–513.
| Note on an electrolytic procedure for differentiating between frost injury of roots and shoots in woody plants.Crossref | GoogleScholarGoogle Scholar |
Xing L, Zhang D, Song X, Weng K, Shen Y, Li Y, Zhao C, Ma J, An N, Han M (2016) Genome-wide sequence variation identification and floral-associated trait comparisons based on the re-sequencing of the ‘Nagafu No. 2’ and ‘Qinguan’ varieties of apple (Malus domestica Borkh.). Frontiers in Plant Science 7, 908
| Genome-wide sequence variation identification and floral-associated trait comparisons based on the re-sequencing of the ‘Nagafu No. 2’ and ‘Qinguan’ varieties of apple (Malus domestica Borkh.).Crossref | GoogleScholarGoogle Scholar |
Zhao Y, Wang Z-X, Yang Y-M, Liu H-S, Shi G-L, Ai J (2020) Analysis of the cold tolerance and physiological response differences of amur grape (Vitis amurensis) germplasms during overwintering. Scientia Horticulturae 259, 108760–108760.
| Analysis of the cold tolerance and physiological response differences of amur grape (Vitis amurensis) germplasms during overwintering.Crossref | GoogleScholarGoogle Scholar |
