Insights into the molecular mechanisms underlying responses of apple trees to abiotic stresses

Xuewei Li , Ziqing Ma , Yi Song , Wenyun Shen , Qianyu Yue , Abid Khan , Muhammad Mobeen Tahir , Xiaofei Wang , Mickael Malnoy , Fengwang Ma , Vincent Bus , Shuangxi Zhou , Qingmei Guan

Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) : 144

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) :144 DOI: 10.1093/hr/uhad144
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Insights into the molecular mechanisms underlying responses of apple trees to abiotic stresses
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Abstract

Apple (Malus × domestica) is a popular temperate fruit crop worldwide. However, its growth, productivity, and quality are often adversely affected by abiotic stresses such as drought, extreme temperature, and high salinity. Due to the long juvenile phase and highly heterozygous genome, the conventional breeding approaches for stress-tolerant cultivars are time-consuming and resource-intensive. These issues may be resolved by feasible molecular breeding techniques for apples, such as gene editing and marker-assisted selection. Therefore, it is necessary to acquire a more comprehensive comprehension of the molecular mechanisms underpinning apples’ response to abiotic stress. In this review, we summarize the latest research progress in the molecular response of apples to abiotic stressors, including the gene expression regulation, protein modifications, and epigenetic modifications. We also provide updates on new approaches for improving apple abiotic stress tolerance, while discussing current challenges and future perspectives for apple molecular breeding.

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Xuewei Li, Ziqing Ma, Yi Song, Wenyun Shen, Qianyu Yue, Abid Khan, Muhammad Mobeen Tahir, Xiaofei Wang, Mickael Malnoy, Fengwang Ma, Vincent Bus, Shuangxi Zhou, Qingmei Guan. Insights into the molecular mechanisms underlying responses of apple trees to abiotic stresses. Horticulture Research, 2023, 10 (8) : 144 DOI:10.1093/hr/uhad144

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Acknowledgements

This project was supported by grants from the National Key Research and Development Project (2022YFD1602107), the National Natural Science Foundation of China (32172530), the Key S&T Special Projects of Shaanxi Province, China (2020zdzx03-01-02), and the Key S&T Special Projects of Shanxi Province, China (202201140601027-6).

Conflict of interest statement

The authors declare that they have no conflict of interest.

References

[1]

Xiong L, Zhu J . Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant. 2001; 112: 152-66

[2]

Stocker TF . Climate change. The closing door of climate targets. Science. 2013; 339: 280-2

[3]

Smith P, Gregory PJ . Climate change and sustainable food production. Proc Nutr Soc. 2013; 72: 21-8

[4]

White MA, Diffenbaugh NS, Jones GV et al. Extreme heat reduces and shifts United States premium wine production in the 21st century. Proc Natl Acad Sci U S A. 2006; 103: 11217-22

[5]

Diffenbaugh NS, Pal JS, Trapp RJ et al. Fine-scale processes regulate the response of extreme events to global climate change. Proc Natl Acad Sci U S A. 2005; 102: 15774-8

[6]

Zhang H, Yu F, Xie P et al. A Gγ protein regulates alkaline sensitivity in crops. Science. 2023; 379: eade8416

[7]

Allen CD, Macalady AK, Chenchouni H et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag. 2010; 259: 660-84

[8]

Mantova M, Menezes-Silva PE, Badel E et al. The interplay of hydraulic failure and cell vitality explains tree capacity to recover from drought. Physiol Plant. 2021; 172: 247-57

[9]

Malnoy M, Viola R, Jung MH et al. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci. 2016; 7: 1904

[10]

Pompili V, Dalla Costa L, Piazza S et al. Reduced fire blight susceptibility in apple cultivars using a high-efficiency CRISPR/Cas9-FLP/FRT-based gene editing system. Plant Biotechnol J. 2020; 18: 845-58

[11]

Niu C, Jiang L, Cao F et al. Methylation of a MITE insertion in the MdRFNR1-1 promoter is positively associated with its allelic expression in apple in response to drought stress. Plant Cell. 2022; 34: 3983-4006

[12]

Shen X, He J, Ping Y et al. The positive feedback regulatory loop of miR160-Auxin response factor 17-HYPONASTIC LEAVES 1 mediates drought tolerance in apple trees. Plant Physiol. 2022; 188: 1686-708

[13]

Shen X, Ping Y, Bao C et al. Mdm-miR160-MdARF17-MdWRKY33 module mediates freezing tolerance in apple. Plant J. 2023; 114: 262-78

[14]

Baldoni E, Genga A, Cominelli E . Plant MYB transcription factors: their role in drought response mechanisms. Int J Mol Sci. 2015; 16: 15811-51

[15]

Sun X, Wang Y, Sui N . Transcriptional regulation of bHLH during plant response to stress. Biochem Biophys Res Commun. 2018; 503: 397-401

[16]

Li J, Han G, Sun C et al. Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Signal Behav. 2019; 14: 1613131

[17]

Babu MM, Luscombe NM, Aravind L et al. Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol. 2004; 14: 283-91

[18]

Jia D, Jiang Q, van Nocker S et al. An apple (Malus domestica) NAC transcription factor enhances drought tolerance in transgenic apple plants. Plant Physiol Biochem. 2019; 139: 504-12

[19]

An JP, Li R, Qu FJ et al. An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. J Plant Physiol. 2018; 221: 74-80

[20]

Xie YP, Bao C, Chen P et al. Abscisic acid homeostasis is mediated by feedback regulation of MdMYB88 and MdMYB124. J Exp Bot. 2021; 72: 592-607

[21]

Geng DL, Chen P, Shen X et al. MdMYB88 and MdMYB124 enhance drought tolerance by modulating root vessels and cell walls in apple. Plant Physiol. 2018; 178: 1296-309

[22]

Liu X, Zhao C, Gao Y et al. A multifaceted module of BRI1 ETHYLMETHANE SULFONATE SUPRESSOR1 (BES1)-MYB88 in growth and stress tolerance of apple. Plant Physiol. 2021; 185: 1903-23

[23]

Chen P, Zhi F, Li X et al. Zinc-finger protein MdBBX7/MdCOL9, a target of MdMIEL1 E3 ligase, confers drought tolerance in apple. Plant Physiol. 2022; 188: 540-59

[24]

Fang H, Dong Y, Yue X et al. The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell Environ. 2019; 42: 2090-104

[25]

Yang YY et al. Apple MdSAT1 encodes a bHLHm1 transcription factor involved in salinity and drought responses. Planta. 2021; 253: 46

[26]

Wang Y, Jiang H, Mao Z et al. Ethylene increases the cold tolerance of apple via the MdERF1B-MdCIbHLH1 regulatory module. Plant J. 2021; 106: 379-93

[27]

Zhao Q, Fan Z, Qiu L et al. MdbHLH130, an apple bHLH transcription factor, confers water stress resistance by regulating stomatal closure and ROS homeostasis in transgenic tobacco. Front Plant Sci. 2020; 11: 543696

[28]

Dong Q, Zheng W, Duan D et al. MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings. Plant Sci. 2020; 299: 110611

[29]

Meng D, Li Y, Bai Y et al. Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress. Plant Physiol Biochem. 2016; 103: 71-83

[30]

An JP, Zhang XW, Bi SQ et al. The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant J. 2020; 101: 573-89

[31]

Yu L, Liu W, Guo Z et al. Interaction between MdMYB63 and MdERF106 enhances salt tolerance in apple by mediating Na(+)/H(+) transport. Plant Physiol Biochem. 2020; 155: 464-71

[32]

Zhang C, An N, Jia P et al. MdNup62 interactions with MdHSFs involved in flowering and heat-stress tolerance in apple. BMC Plant Biol. 2022; 22: 317

[33]

Wang N, Liu W, Yu L et al. HEAT SHOCK FACTOR A8a modulates favonoid synthesis and drought tolerance. Plant Physiol. 2020; 184: 1273-90

[34]

An JP, Yao JF, Wang XN et al. MdHY5 positively regulates cold tolerance via CBF-dependent and CBF-independent pathways in apple. J Plant Physiol. 2017; 218: 275-81

[35]

An JP, Qu FJ, Yao JF et al. The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res. 2017; 4: 17023

[36]

Zhao J, Guo R, Guo C et al. Evolutionary and expression analyses of the apple basic leucine zipper transcription factor family. Front Plant Sci. 2016; 7: 376

[37]

Yang J, Huo Z, Wang P et al. Indicator-based spatiotemporal characteristics of apple drought in North China. Nat Hazards. 2021; 108: 2123-42

[38]

Lauri P-É, Barigah TS, Lopez G et al. Genetic variability and phenotypic plasticity of apple morphological responses to soil water restriction in relation with leaf functions and stem xylem conductivity. Trees. 2016; 30: 1893-908

[39]

Aras S, Keles H . Responses of apple plants to drought stress. J Agric Stud. 2019; 7: 5

[40]

Liao X, Guo X, Wang Q et al. Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J. 2017; 89: 510-26

[41]

Xie YP, Bao C, Chen P et al. ABA homeostasis is mediated by a feedback regulation of MdMYB88 and MdMYB124. J Exp Bot. 2020; 72: 592-607

[42]

Geng D, Shen X, Xie Y et al. Regulation of phenylpropanoid biosynthesis by MdMYB88 and MdMYB124 contributes to pathogen and drought resistance in apple. Hortic Res. 2020; 7: 102

[43]

Li XW, Chen P, Xie Y et al. Apple SERRATE negatively mediates drought resistance by regulating MdMYB88 and MdMYB124 and microRNA biogenesis. Hortic Res. 2020; 7: 98

[44]

Liu X, Li R, Dai Y et al. A B-box zinc finger protein, md BBX10, enhanced salt and drought stresses tolerance in Arabidopsis. Plant Mol Biol. 2019; 99: 437-47

[45]

Jiang L, Zhang D, Liu C et al. MdGH3.6 is targeted by MdMYB94 and plays a negative role in apple water-deficit stress tolerance. Plant J. 2022; 109: 1271-89

[46]

Han D, Hou Y, Wang Y et al. Overexpression of a Malus baccata WRKY transcription factor gene (MbWRKY5) increases drought and salt tolerance in transgenic tobacco. Can J Plant Sci. 2018; 99: 173-83

[47]

Chen P, Yan M, Li L et al. The apple DNA-binding one zinc-finger protein MdDof54 promotes drought resistance. Hortic Res. 2020; 7: 195

[48]

Ji XL, Li HL, Qiao ZW et al. The BTB-TAZ protein MdBT2 negatively regulates the drought stress response by interacting with the transcription factor MdNAC143 in apple. Plant Sci. 2020; 301: 110689

[49]

Han D, Ding H, Chai L et al. Isolation and characterization of MbWRKY1, a WRKY transcription factor gene from Malus baccata (L.) Borkh involved in drought tolerance. Can J Plant Sci. 2018; 98: 1023-34

[50]

Han D, Zhang Z, Ding H et al. Molecular cloning and functional analysis of MbWRKY3 involved in improved drought tolerance in transformed tobacco. J Plant Interact. 2018; 13: 329-37

[51]

Han D, Zhang Z, Ding H et al. Isolation and characterization of MbWRKY2 gene involved in enhanced drought tolerance in transgenic tobacco. J Plant Interact. 2018; 13: 163-72

[52]

Zhang YL, Zhang CL, Wang GL et al. Apple AP2/EREBP transcription factor MdSHINE2 confers drought resistance by regulating wax biosynthesis. Planta. 2019; 249: 1627-43

[53]

Wang RK, Cao ZH, Hao YJ . Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples. Physiol Plant. 2014; 150: 76-87

[54]

Li X, Xie Y, Lu L et al. Contribution of methylation regulation of MpDREB2A promoter to drought resistance of Mauls prunifolia . Plant Soil. 2019; 441: 15-32

[55]

Li XL, Meng D, Li MJ et al. Transcription factors MhDREB2A/MhZAT10 play a role in drought and cold stress response crosstalk in apple. Plant Physiol. 2023; 192: 2203-20

[56]

Bao C, Qin G, Cao F et al. MdZAT5 regulates drought tolerance via mediating accumulation of drought-responsive miRNAs and mRNAs in apple. New Phytol. 2022; 236: 2131-50

[57]

Shan D, Wang C, Song H et al. The MdMEK2-MdMPK6-MdWRKY17 pathway stabilizes chlorophyll levels by directly regulating MdSUFB in apple under drought stress. Plant J. 2021; 108: 814-28

[58]

Zhao K, Shen X, Yuan H et al. Isolation and characterization of dehydration-responsive element-binding factor 2C (MsDREB2C) from Malus sieversii Roem. Plant Cell Physiol. 2013; 54: 1415-30

[59]

Yang W, Liu XD, Chi XJ et al. Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta. 2011; 233: 219-29

[60]

Sharma V, Goel P, Kumar S et al. An apple transcription factor, MdDREB76, confers salt and drought tolerance in transgenic tobacco by activating the expression of stress-responsive genes. Plant Cell Rep. 2019; 38: 221-41

[61]

Li X, Zhou S, Liu Z et al. Fine-tuning of SUMOylation modulates drought tolerance of apple. Plant Biotechnol J. 2022; 20: 903-19

[62]

Pramsohler M, Hacker J, Neuner G . Freezing pattern and frost killing temperature of apple (Malus domestica) wood under controlled conditions and in nature . Tree Physiol. 2012; 32: 819-28

[63]

Quamme HA . Relationship of the low temperature exotherm to apple and pear production in North America. Can J Plant Sci. 1976; 56: 493-500

[64]

El Yaacoubi A et al. Potential vulnerability of Moroccan apple orchard to climate change-induced phenological perturbations: effects on yields and fruit quality. Int J Biometeorol. 2020; 64: 377-87

[65]

Chen X, Li S, Zhang D et al. Sequencing of a wild apple (Malus baccata) genome unravels the differences between cultivated and wild apple species regarding disease resistance and cold tolerance . G3-Genes Genom Genet. 2019; 9: 2051-60

[66]

Miura K, Jin JB, Lee J et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell. 2007; 19: 1403-14

[67]

Shi Y, Ding Y, Yang S . Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 2018; 23: 623-37

[68]

Xie Y, Chen P, Yan Y et al. An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol. 2018; 218: 201-18

[69]

An JP, Li R, Qu FJ et al. R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple. Plant J. 2018; 96: 562-77

[70]

Feng XM, Zhao Q, Zhao LL et al. The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol. 2012; 12: 22

[71]

An JP, Wang XF, Espley RV et al. An apple B-box protein MdBBX37 modulates anthocyanin biosynthesis and hypocotyl elongation synergistically with MdMYBs and MdHY5. Plant Cell Physiol. 2020; 61: 130-43

[72]

Wang Y, Mao Z, Jiang H et al. A feedback loop involving MdMYB108L and MdHY5 controls apple cold tolerance. Biochem Biophys Res Commun. 2019; 512: 381-6

[73]

An JP, Wang XF, Zhang XW et al. An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation. Plant Biotechnol J. 2020; 18: 337-53

[74]

Xie XB et al. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ. 2012; 35: 1884-97

[75]

Han D, du M, Zhou Z et al. Overexpression of a Malus baccata NAC transcription factor gene MbNAC25 increases cold and salinity tolerance in Arabidopsis . Int J Mol Sci. 2020; 21

[76]

Chen K, Song M, Guo Y et al. MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress-responsive signals. Plant Biotechnol J. 2019; 17: 2341-55

[77]

Chen K, Guo Y, Song M et al. Dual role of MdSND1 in the biosynthesis of lignin and in signal transduction in response to salt and osmotic stress in apple. Hort Res. 2020; 7: 204

[78]

Yin X, Xia Y, Xie Q et al. The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance. J Exp Bot. 2020; 71: 1801-14

[79]

Zhu JK . Salt and drought stress signal transduction in plants. Annu Rev Plant Biol. 2002; 53: 247-73

[80]

An JP, Zhang XW, Xu RR et al. Apple MdERF4 negatively regulates salt tolerance by inhibiting MdERF3 transcription. Plant Sci. 2018; 276: 181-8

[81]

An JP, Yao JF, Xu RR et al. An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant. 2018; 164: 279-89

[82]

Liang X, Li Y, Yao A et al. Overexpression of MxbHLH18 increased iron and high salinity stress tolerance in Arabidopsis thaliana. Int J Mol Sci. 2022; 23

[83]

Ma Y, Xue H, Zhang F et al. The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol J. 2021; 19: 311-23

[84]

Han D, Zhou Z, du M et al. Overexpression of a Malus xiaojinensis WRKY transcription factor gene (MxWRKY55) increased iron and high salinity stress tolerance in Arabidopsis thaliana. In Vitro Cell Dev Bio Plant. 2020; 56: 600-9

[85]

Han D, Han J, Xu T et al. Isolation and preliminary functional characterization of MxWRKY64, a new WRKY transcription factor gene from Malus xiaojinensis Cheng et Jiang . In Vitro Cell Dev Bio Plant. 2021; 57: 202-13

[86]

Han D, Xu T, Han J et al. Overexpression of MxWRKY53 increased iron and high salinity stress tolerance in Arabidopsis thaliana. In Vitro Cell Dev Bio Plant. 2022; 58: 266-78

[87]

Han D et al. Isolation and preliminary functional analysis of MbWRKY4 gene involved in salt tolerance in transgenic tobacco. Int J Agric Biol. 2018; 20: 2045-52

[88]

Crocco CD, Botto JF . BBX proteins in green plants: insights into their evolution, structure, feature and functional diversification. Gene. 2013; 531: 44-52

[89]

Gangappa SN, Botto JF . The BBX family of plant transcription factors. Trends Plant Sci. 2014; 19: 460-70

[90]

Liu X, Li R, Dai Y et al. Genome-wide identification and expression analysis of the B-box gene family in the apple (Malus domestica Borkh.) genome . Mol Gen Genomics. 2018; 293: 303-15

[91]

An JP, Wang XF, Zhang XW et al. Apple B-box protein BBX37 regulates jasmonic acid mediated cold tolerance through the JAZ-BBX37-ICE1-CBF pathway and undergoes MIEL1-mediated ubiquitination and degradation. New Phytol. 2021; 229: 2707-29

[92]

Geng D l et al. Physiological and transcriptomic analyses of roots from Malus sieversii under drought stress . J Integr Agric. 2019; 18: 1280-94

[93]

Wang DR, Yang K, Wang X et al. Overexpression of MdZAT5, an C2H2-type zinc finger protein, regulates anthocyanin accumulation and salt stress response in apple Calli and Arabidopsis. Int J Mol Sci. 2022; 23: 1897

[94]

Yang Q, Chen Q, Zhu Y et al. Identification of MdDof genes in apple and analysis of their response to biotic or abiotic stress. Funct Plant Biol. 2018; 45: 528-41

[95]

Zhang Z, Yuan L, Liu X et al. Evolution analysis of Dof transcription factor family and their expression in response to multiple abiotic stresses in Malus domestica. Gene. 2018; 639: 137-48

[96]

Cao ZH, Zhang SZ, Wang RK et al. Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS One. 2013; 8: e69955

[97]

Zhao C, Liu X, He J et al. Apple TIME FOR COFFEE contributes to freezing tolerance by promoting unsaturation of fatty acids. Plant Sci. 2021; 302: 110695

[98]

Jing Y, Pei T, Li C et al. Overexpression of the FERONIA receptor kinase MdMRLK2 enhances apple cold tolerance. Plant J. 2023; 115: 236-52

[99]

Jiang L, Shen W, Liu C et al. Engineering drought-tolerant apple by knocking down six GH3 genes and potential application of transgenic apple as a rootstock. Hortic Res. 2022; 9: uhac122

[100]

Mao K, Dong Q, Li C et al. Genome wide identification and characterization of apple bHLH transcription factors and expression analysis in response to drought and salt stress. Front Plant Sci. 2017; 8: 480

[101]

Yang J, Gao M, Huang L et al. Identification and expression analysis of the apple (Malus × domestica) basic helix-loop-helix transcription factor family. Sci Rep. 2017; 7: 28

[102]

Li K, Liu Z, Xing L et al. miRNAs associated with auxin signaling, stress response, and cellular activities mediate adventitious root formation in apple rootstocks. Plant Physiol Biochem. 2019; 139: 66-81

[103]

Yu X, Hou Y, Chen W et al. Malus hupehensis miR168 targets to ARGONAUTE1 and contributes to the resistance against Botryosphaeria dothidea infection by altering defense responses . Plant Cell Physiol. 2017; 58: 1541-57

[104]

Wang Y, Feng C, Zhai Z et al. The apple microR171i-SCARECROW-LIKE PROTEINS26.1 module enhances drought stress tolerance by integrating ascorbic acid metabolism. Plant Physiol. 2020; 184: 194-211

[105]

Xia R, Zhu H, An YQ et al. Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol. 2012; 13: R47

[106]

Niu C, Li H, Jiang L et al. Genome-wide identification of drought-responsive microRNAs in two sets of Malus from interspecific hybrid progenies. Hortic Res. 2019; 6: 75

[107]

Shen X, Song Y, Ping Y et al. The RNA binding protein MdHYL1 modulates cold tolerance and disease resistance in apple. Plant Physiol. 2023; 192: 2143-60

[108]

Niu CD, Shi HR, Zhang ZT et al. MdMYB88/124 modulates apple tree microRNA biogenesis through post-transcription processing and/or transcription pathway. Acta Physiol Plant. 2022; 44: 86

[109]

Zara H, Sebastian G, Ellis J et al. Post-translational modification by SUMO. Toxicology. 2010; 278: 288-93

[110]

Hashiguchi A, Komatsu S . Posttranslational modifications and plant-environment interaction. Meth Enzymol. 2017; 586: 97-113

[111]

Guerra D, Crosatti C, Khoshro HH et al. Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms. Front Plant Sci. 2015; 6: 57

[112]

Haimi P, Vinskien˙e J, Stepulaitien˙e I et al. Patterns of low temperature induced accumulation of dehydrins in Rosaceae crops-evidence for post-translational modification in apple. J Plant Physiol. 2017; 218: 175-81

[113]

Sun MH, Ma QJ, Hu DG et al. The glucose sensor MdHXK1 phosphorylates a tonoplast Na(+)/H(+) exchanger to improve salt tolerance. Plant Physiol. 2018; 176: 2977-90

[114]

Hu DG, Sun CH, Sun MH et al. MdSOS2L1 phosphorylates MdVHA-B1 to modulate malate accumulation in response to salinity in apple. Plant Cell Rep. 2016; 35: 705-18

[115]

Ma QJ, Sun MH, Kang H et al. A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser(254) for phosphorylation to enhance salt tolerance. Plant Cell Environ. 2019; 42: 918-30

[116]

Ma QJ, Sun MH, Lu J et al. An apple sucrose transporter MdSUT2.2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought. Plant Biotechnol J. 2019; 17: 625-37

[117]

Marino D, Froidure S, Canonne J et al. Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nat Commun. 2013; 4: 1476

[118]

An JP, Wang XF, Zhang XW et al. MdBBX22 regulates UV-B-induced anthocyanin biosynthesis through regulating the function of MdHY5 and is targeted by MdBT2 for 26S proteasome-mediated degradation. Plant Biotechnol J. 2019; 17: 2231-3

[119]

An JP, Wang XF, Zhang XW et al. Apple BT2 protein negatively regulates jasmonic acid-triggered leaf senescence by modulating the stability of MYC2 and JAZ2. Plant Cell Environ. 2021; 44: 216-33

[120]

Wang XF, An JP, Liu X et al. The nitrate-responsive protein MdBT2 regulates anthocyanin biosynthesis by interacting with the MdMYB1 transcription factor. Plant Physiol. 2018; 178: 890-906

[121]

Zhang D, Yang K, Kan Z et al. The regulatory module MdBT2-MdMYB88/MdMYB124-MdNRTs regulates nitrogen usage in apple. Plant Physiol. 2021; 185: 1924-42

[122]

Zhou L, Li YY, Zhang RF et al. The small ubiquitin-like modifier E3 ligase MdSIZ1 promotes anthocyanin accumulation by sumoylating MdMYB1 under low-temperature conditions in apple. Plant Cell Environ. 2017; 40: 2068-80

[123]

Castro PH, Tavares RM, Bejarano ER et al. SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Sci. 2012; 69: 3269-83

[124]

Zhang YL, Tian Y, Man YY et al. Apple SUMO E3 ligase MdSIZ1 regulates cuticular wax biosynthesis by SUMOylating transcription factor MdMYB30. Plant Physiol. 2023; 191: 1771-88

[125]

Zhang RF, Guo Y, Li YY et al. Functional identification of MdSIZ1 as a SUMO E3 ligase in apple. J Plant Physiol. 2016; 198: 69-80

[126]

Zhang CL, Wang GL, Zhang YL et al. Apple SUMO E3 ligase MdSIZ1 facilitates SUMOylation of MdARF8 to regulate lateral root formation. New Phytol. 2021; 229: 2206-22

[127]

Li C, Wei Z, Liang D et al. Enhanced salt resistance in apple plants overexpressing a Malus vacuolar Na+/H+ antiporter gene is associated with differences in stomatal behavior and photosynthesis. Plant Physiol Biochem. 2013; 70: 164-73

[128]

Li W, Yan J, Wang S et al. Genome-wide analysis of SET-domain group histone methyltransferases in apple reveals their role in development and stress responses. BMC Genomics. 2021; 22: 283

[129]

Xu J, Zhou S, Gong X et al. Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J. 2018; 16: 672-87

[130]

Li Z, Wang L, He J et al. Chromosome-scale reference genome provides insights into the genetic origin and grafting-mediated stress tolerance of Malus prunifolia. Plant Biotechnol J. 2022; 20: 1015-7

[131]

Yu L, Sun Y, Zhang X et al. ROS1 promotes low temperature-induced anthocyanin accumulation in apple by demethylating the promoter of anthocyanin-associated genes. Hortic Res. 2022; 9: uhac007

[132]

Kumar G, Rattan UK, Singh AK . Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple (Malus x domestica Borkh.). PLoS One. 2016; 11: e0149934

[133]

Fustin JM, Doi M, Yamaguchi Y et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell. 2013; 155: 793-806

[134]

Hou N, Li C, He J et al. MdMTA-mediated m(6)a modification enhances drought tolerance by promoting mRNA stability and translation efficiency of genes involved in lignin deposition and oxidative stress. New Phytol. 2022; 234: 1294-314

[135]

Guo T, Liu C, Meng F et al. The m(6)a reader MhYTP2 regulates MdMLO19 mRNA stability and antioxidant genes translation efficiency conferring powdery mildew resistance in apple. Plant Biotechnol J. 2022; 20: 511-25

[136]

Limera C, Sabbadini S, Sweet JB et al. New biotechnological tools for the genetic improvement of major Woody fruit species. Front Plant Sci. 2017; 8: 1418

[137]

Velasco R, Zharkikh A, Affourtit J et al. The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet. 2010; 42: 833-9

[138]

Qin S, Xu G, He J et al. A chromosome-scale genome assembly of Malus domestica, a multi-stress resistant apple variety. Genomics. 2023; 115: 110627

[139]

Dalla Costa L, Piazza S, Pompili V et al. Strategies to produce T-DNA free CRISPRed fruit trees via agrobacterium tumefaciens stable gene transfer. Sci Rep. 2020; 10: 20155

[140]

Nishitani C, Hirai N, Komori S et al. Efficient genome editing in apple using a CRISPR/Cas9 system. Sci Rep. 2016; 6: 31481

[141]

Charrier A, Vergne E, Dousset N et al. Efficient targeted mutagenesis in apple and first time edition of pear using the CRISPR-Cas9 system. Front Plant Sci. 2019; 10: 40

[142]

Zhang Y, Zhou P, Bozorov TA et al. Application of CRISPR/Cas9 technology in wild apple (Malus sieverii) for paired sites gene editing . Plant Methods. 2021; 17: 79

[143]

Liu J, Shen F, Xiao Y et al. Genomics-assisted prediction of salt and alkali tolerances and functional marker development in apple rootstocks. BMC Genomics. 2020; 21: 550

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