The SL–MdDWARF53–MdbHLH1 module regulates MdAT1-mediated redox homeostasis and alkaline salt tolerance mechanism in apple

Xiaomin Zhu , Yuqing Zhu , Xiaoyu Zhou , Yong Zhang , Chanyu Wang , Shaoxuan Li , Zhijuan Sun , Qiang Zhao , Xiaodong Zheng , Caihong Wang , Yike Tian

Horticulture Research ›› 2026, Vol. 13 ›› Issue (7) : 089

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Horticulture Research ›› 2026, Vol. 13 ›› Issue (7) :089 DOI: 10.1093/hr/uhag089
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The SL–MdDWARF53–MdbHLH1 module regulates MdAT1-mediated redox homeostasis and alkaline salt tolerance mechanism in apple
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Abstract

Alkaline salt stress is a key environmental factor restricting the sustainable development of the apple industry, significantly affecting the yield and quality of apple. In recent years, strigolactone (SLs) has been proven to play a central regulatory role in plant stress responses. However, its role and mechanism under alkaline salt stress remain unknown. Based on this, we found that exogenous application of the SL analog GR245DS can significantly enhance the adaptability of apple to alkaline salt stress. To elucidate the underlying molecular mechanisms, RNA sequencing (RNA-seq) analysis identified the key transcription factor MdbHLH1, whose expression was strongly induced by alkaline salt stress. Overexpression of MdbHLH1 conferred a salt-alkali tolerant phenotype. Further investigation demonstrated that MdbHLH1 directly binds to and activates the promoter of MdAT1 (Alkali Tolerance 1), a crucial alkali-tolerance gene. The MdbHLH1- MdAT1 module enhances alkaline salt stress resistance by promoting hydrogen peroxide (H2O2) efflux and alleviating oxidative damage. More in-depth studies revealed that MdbHLH1 interacts with MdD53 (MdDWARF53), a repressor in the SL signaling pathway. SL signaling induces ubiquitination and degradation of MdD53, thereby releasing MdbHLH1 to activate MdAT1 expression and ultimately improving alkaline stress tolerance in apple. This study elucidates a key SL–MdD53–MdbHLH1- MdAT1 regulatory pathway that enhances saline-alkali tolerance in apple by mitigating oxidative stress, thereby providing mechanistic insights into apple’s adaptation to saline-alkali environments.

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Xiaomin Zhu, Yuqing Zhu, Xiaoyu Zhou, Yong Zhang, Chanyu Wang, Shaoxuan Li, Zhijuan Sun, Qiang Zhao, Xiaodong Zheng, Caihong Wang, Yike Tian. The SL–MdDWARF53–MdbHLH1 module regulates MdAT1-mediated redox homeostasis and alkaline salt tolerance mechanism in apple. Horticulture Research, 2026, 13 (7) : 089 DOI:10.1093/hr/uhag089

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References

[1]

Flowers TJ, Galal HK, Bromham L, et al. Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol. 2010; 37: 604-12

[2]

Nutan KK, Singla-Pareek SL, Pareek A . The Saltol QTL-localized transcription factor OsGATA8 plays an important role in stress tolerance and seed development in Arabidopsis and rice. J Exp Bot. 2020; 71: 684-98

[3]

Yang Y, Guo Y . Unraveling salt stress signaling in plants. Journal of Integrative Plant Biology. 2018; 60(9): 796-804.

[4]

Gomez-Roldan V, Fermas S, Brewer PB, et al. Strigolactone inhibition of shoot branching. Nature. 2008; 455: 189-94

[5]

Umehara M, Hanada A, Yoshida S, et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature. 2008; 455: 195-200

[6]

Cooper JW, Hu Y, Beyyoudh L, et al. Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. Plant Cell Environ. 2018; 41: 1298-310

[7]

Ha CV, Leyva-González MA, Osakabe Y, et al. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA. 2014; 111: 851-6

[8]

Gu P, Tao W, Zhang Y, et al. The D14-SDEL1-SPX4 cascade integrates the strigolactone and phosphate signalling networks in rice. New Phytol. 2023; 239(2): 673-86.

[9]

Ma N, Hu C, Wan L, et al. Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. Frontiers. Plant Sci. 2017; 8: 1671

[10]

Nisa ZU, Wang Y, Ali N, et al. Strigolactone signaling gene from soybean GmMAX2a enhances the drought and salt-alkaline resistance in Arabidopsis via regulating transcriptional profiles of stress-related genes. Functional & Integrative Genomics. 2023; 23: 216

[11]

Liu Y, Wang X, Liu Y, et al. Synthetic strigolactone (rac-GR24) alleviates the photosynthetic inhibition and oxidative damage in alfalfa (Medicago sativa L.) under salt stress. Grassland Research. 2023; 1: e12417

[12]

Jiang L, Liu X, Xiong G, et al. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature. 2013; 504: 401-5

[13]

Zhou F, Lin Q, Zhu L, et al. D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling . Nature. 2013; 504: 406-10

[14]

Hu Q, Liu H, He Y, et al. Regulatory mechanisms of strigolactone perception in rice. Cell. 2024; 187: 7551-7567.e17

[15]

Toledo-Ortiz G, Huq E, Quail PH . The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell. 2003; 15: 1749-70

[16]

Fernández-Calvo P, Chini A, Fernández-Barbero G, et al. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell. 2011; 23: 701-15

[17]

Song Y, Li S, Sui Y, et al. SbbHLH85, a bHLH member, modulates resilience to salt stress by regulating root hair growth in sorghum. Theor Appl Genet. 2022; 135: 201-16

[18]

Abe H, Urao T, Ito T, et al. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell. 2003; 15: 63-78

[19]

Zeng R, Shi Y, Yang S, et al. A natural variant of COOL1 gene enhances cold tolerance for high-latitude adaptation in maize. Cell. 2025; 188: 1315-1329.e13

[20]

Shi H, Ishitani M, Kim C, et al. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter . Proc Natl Acad Sci USA. 2000; 97: 6896-901

[21]

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

[22]

Zhang HX, Blumwald E . Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol. 2002; 19: 765-8

[23]

Chakravorty D, Trusov Y, Zhang W, et al. An atypical heterotrimeric G-protein γ-subunit is involved in guard cell K+-channel regulation and morphological development in Arabidopsis thaliana . Plant J. 2011; 67: 840-51

[24]

Li S, Liu Y, Zheng L, et al. The plant-specific G protein γ subunit AGG3 influences organ size and shape in Arabidopsis thaliana. New Phytol. 2012; 194: 690-703

[25]

Wang L, et al. Strigolactones regulate thermotolerance by modulating the antioxidant system in tomato. Plant Sci. 2023; 326: 111518

[26]

Marzec M . Strigolactones as part of the plant defence system. Trends Plant Sci. 2016; 21: 900-3

[27]

Yang Y, Guo Y . Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol. 2018; 217: 523-39

[28]

Lian Y, Lian C, Wang L, et al. Suppressor of MAX2 like 6, 7, and 8 interact with DDB1 binding wd repeat domain hypersensitive to ABA DEFICIENT 1 to regulate the drought tolerance and target sucrose nonfermenting 1 related protein kinase 2.3 to abscisic acid response in Arabidopsis. Biomolecules. 2023; 13: 1406

[29]

Sun H, Guo X, Zhu X, et al. Strigolactone and gibberellin signaling coordinately regulate metabolic adaptations to changes in nitrogen availability in rice. Mol Plant. 2023; 16: 588-98

[30]

Ito S, Umehara M, Hanada A, et al. Effects of triazole derivatives on strigolactone levels and growth retardation in rice. PLoS One. 2011; 6: e21723

[31]

Zhang Y, Li J, Guo K, et al. Strigolactones alleviate AlCl3 stress by vacuolar compartmentalization and cell wall blocking in apple . Plant J. 2024; 119: 197-217

[32]

Li P, Zhao L, Qi F, et al. The receptor-like cytoplasmic kinase RIPK regulates broad-spectrum ROS signaling in multiple layers of plant immune system. Mol Plant. 2021; 14: 1652-67

[33]

Zheng X, Li Y, Xi X, et al. Exogenous Strigolactones alleviate KCl stress by regulating photosynthesis, ROS migration and ion transport in Malus hupehensis Rehd. Plant Physiol Biochem. 2021; 159: 113-22

[34]

Li C, Ji J, Wang G, et al. Over-expression of LcPDS, LcZDS, and LcCRTISO, genes from wolfberry for carotenoid biosynthesis, enhanced carotenoid accumulation, and salt tolerance in tobacco. Front Plant Sci. 2020; 11: 119

[35]

Li C, Liu G, Geng X, et al. Local regulation of auxin transport in root-apex transition zone mediates aluminium-induced root-growth inhibition. Plant J. 2021; 108: 55-66

[36]

Zheng X, Zhao Y, Shan D, et al. MdWRKY9 overexpression confers intensive dwarfing in the M26 rootstock of apple by directly inhibiting brassinosteroid synthetase MdDWF4 expression. New Phytol. 2018; 217: 1086-98

[37]

Dai HY, Li WR, Han GF, et al. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci Hortic. 2013; 164: 202-8

[38]

Zheng X, Li Y, Ma C, et al. A mutation in the promoter of the arabinogalactan protein 7-like gene PcAGP7-1 affects cell morphogenesis and brassinolide content in pear (Pyrus communis L.) stems. Plant J. 2022; 109: 47-63

[39]

Zhou LJ, Zhang CL, Zhang RF, et al. The SUMO E3 ligase MdSIZ1 targets MdbHLH104 to regulate plasma membrane H+-ATPase activity and iron homeostasis . Plant Physiol. 2019; 179: 88-106

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