Slow and steady wins the race: the negative regulators of ethylene biosynthesis in horticultural plants

Dongdong Li , Shuang Zeng , Ruyi Dai , Kunsong Chen

Horticulture Research ›› 2025, Vol. 12 ›› Issue (7) : 108

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (7) :108 DOI: 10.1093/hr/uhaf108
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Slow and steady wins the race: the negative regulators of ethylene biosynthesis in horticultural plants
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Abstract

The gaseous hormone ethylene controls a variety of physiological processes in horticultural plants, including fruit ripening and elongation, flower development and senescence, and responses to stresses. The functions of ethylene in these processes are intimately linked to its precise biosynthesis, which is finely tuned by a complex network of positive and negative regulators. While significant progress has been made in understanding the roles of positive regulators in ethylene biosynthesis, the negative regulators of ethylene biosynthesis has only recently begun to receive more focus. Ethylene biosynthesis is a simple two-step reaction in land plants, committed by two dedicated enzymes, 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO). Over the past decade, a growing number of research has identified a wide range of transcriptional, posttranscriptional and epigenetic negative regulators for ACS and/or ACO in horticultural plants, greatly enhancing our understanding of the intricate network that modulates ethylene production. In this review, we provide a comprehensive overview of the negative regulators that mediate ethylene biosynthesis in horticultural plants, with respect to their functions and molecular mechanisms, and their responses to external environmental stimuli or internal growth signals.

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Dongdong Li, Shuang Zeng, Ruyi Dai, Kunsong Chen. Slow and steady wins the race: the negative regulators of ethylene biosynthesis in horticultural plants. Horticulture Research, 2025, 12(7): 108 DOI:10.1093/hr/uhaf108

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2022YFD2100102 to KC), the National Natural Science Foundation of China (32402638 to DL) and the Zhejiang Provincial Natural Science Foundation of China (LQ24C020001 to DL).

Author contributions

D.L. and K.C. conceived and designed this review article. D.L., S.Z. R.D., and K.C. wrote the manuscript. D.L. drew the figure and made the tables. All authors were involved in reviewing and editing the manuscript, and approved the final manuscript.

Data availability

Not applicable to this review.

Conflict of interest statement

The authors declare that they have no competing interests.

References

[1]

Dubois M, Van den Broeck L, Inze D. The pivotal role of ethylene in plant growth. Trends Plant Sci. 2018; 23:311-23

[2]

Liu YD, Tang MF, Liu MC. et al. The molecular regulation of ethylene in fruit ripening. Small Methods. 2020; 4:1900485

[3]

Sharma K, Gupta S, Sarma S. et al. Mutations in tomato 1-aminocyclopropane carboxylic acid synthase2 uncover its role in development beside fruit ripening. Plant J. 2021; 106:95-112

[4]

Martinez-Romero D, Bailen G, Serrano M. et al. Tools to maintain postharvest fruit and vegetable quality through the inhibition of ethylene action: a review. Crit Rev Food Sci Nutr. 2007; 47:543-60

[5]

Hurr BM, Huber DJ, Vallejos CE. et al. Ethylene-induced over-production of reactive oxygen species is responsible for the development of watersoaking in immature cucumber fruit. J Plant Physiol. 2013; 170:56-62

[6]

Hu BX, Sun DW, Pu HB. et al. Recent advances in detecting and regulating ethylene concentrations for shelf-life extension and maturity control of fruit: a review. Trends Food Sci Tech. 2019; 91: 66-82

[7]

Xin T, Zhang Z, Li S. et al. Genetic regulation of ethylene dosage for cucumber fruit elongation. Plant Cell. 2019; 31:1063-76

[8]

Chen H, Sun J, Li S. et al. An ACC oxidase gene essential for cucumber carpel development. Mol Plant. 2016; 9:1315-27

[9]

Martin A, Troadec C, Boualem A. et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature. 2009; 461:1135-8

[10]

Li JG, Yuan RC. NAA and ethylene regulate expression of genes related to ethylene biosynthesis, perception, and cell wall degra-dation during fruit abscission and ripening in ’Delicious’ apples. J Plant Growth Regul. 2008; 27:283-95

[11]

Sriskantharajah K, El Kayal W, Torkamaneh D. et al. Transcrip-tomics of improved fruit retention by hexanal in ’Honeycrisp’ reveals hormonal crosstalk and reduced cell wall degradation in the fruit abscission zone. Int J Mol Sci. 2021; 22:8830

[12]

Ma X, Yuan Y, Wu Q. et al. LcEIL2/3 are involved in fruitlet abscission via activating genes related to ethylene biosynthesis and cell wall remodeling in litchi. Plant J. 2020; 103:1338-50

[13]

Hewitt S, Kilian B, Koepke T. et al. Transcriptome analysis reveals potential mechanisms for ethylene-inducible pedicel-fruit abscission zone activation in non-climacteric sweet cherry (Prunus avium L.). Horticulturae. 2021; 7:270

[14]

Cheng L, Li R, Wang X. et al. A SlCLV3-SlWUS module regulates auxin and ethylene homeostasis in low light-induced tomato flower abscission. Plant Cell. 2022; 34:4388-408

[15]

Xie Q, Hu Z, Zhu Z. et al. Overexpression of a novel MADS-box gene SlFYFL delays senescence, fruit ripening and abscission in tomato. Sci Rep. 2014; 4:4367

[16]

Li C, Ma X, Huang X. et al. Involvement of HD-ZIP I transcription factors LcHB2 and LcHB3 in fruitlet abscission by promoting transcription of genes related to the biosynthesis of ethylene and ABA in litchi. Tree Physiol. 2019; 39:1600-13

[17]

Zhao ML, Li CQ, Ma XS. et al. KNOX protein KNAT1 regulates fruitlet abscission in litchi by repressing ethylene biosynthetic genes. JExp Bot. 2020; 71:4069-82

[18]

Ma X, Ying P, He Z. et al. The LcKNAT1-LcEIL2/3 regulatory module is involved in fruitlet abscission in litchi. Front Plant Sci. 2022; 12:802016

[19]

Zacarias L, Tudela D, Primomillo E. Role of ethylene in the opening and senescence of citrus flowers. Sci Hortic. 1991; 46: 55-60

[20]

Cheng C, Yu Q, Wang Y. et al. Ethylene-regulated asymmetric growth of the petal base promotes flower opening in rose (Rosa hybrida). Plant Cell. 2021; 33:1229-51

[21]

Yin J, Chang X, Kasuga T. et al. A basic helix-loop-helix tran-scription factor, PhFBH4, regulates flower senescence by mod-ulating ethylene biosynthesis pathway in petunia. Hortic Res. 2015; 2:15059

[22]

Ji XT, Mao YX, Yuan YP. et al. PhERF71 regulates petunia flower senescence by modulating ethylene biosynthesis. Postharvest Biol Technol. 2024; 216:113070

[23]

Xu H, Luo D, Zhang F. DcWRKY 75 promotes ethylene induced petal senescence in carnation (Dianthus caryophyllus L.). Plant J. 2021; 108:1473-92

[24]

Ji X, Wang M, Xu Z. et al. PlMYB308 regulates flower senescence by modulating ethylene biosynthesis in herbaceous peony. Front Plant Sci. 2022; 13:872442

[25]

Tan Y, Liu J, Huang F. et al. PhGRL2 protein, interacting with PhACO1, is involved in flower senescence in the petunia. Mol Plant. 2014; 7:1384-7

[26]

SunZ, WuM, WangS. et al. An insertion of transposon in DcNAP inverted its function in the ethylene pathway to delay petal senescence in carnation (Dianthus caryophyllus L.). Plant Biotechnol J. 2023; 21:2307-21

[27]

Chen H, Bullock DA, Alonso JM. et al. To fight or to grow: the balancing role of ethylene in plant abiotic stress responses. Plan Theory. 2021; 11:33

[28]

Shi J, Habben JE, Archibald RL. et al. Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize. Plant Physiol. 2015; 169:266-82

[29]

Tao JJ, Cao YR, Chen HW. et al. Tobacco translationally controlled tumor protein interacts with ethylene receptor tobacco histidine kinase1 and enhances plant growth through promotion of cell proliferation. Plant Physiol. 2015; 169:96-114

[30]

Dong Y, Tang M, Huang Z. et al. The miR164a-NAM3 module con-fers cold tolerance by inducing ethylene production in tomato. Plant J. 2022; 111:440-56

[31]

Tsuchisaka A, Yu GX, Jin HL. et al. A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms reg-ulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009; 183:979-1003

[32]

Van de Poel B, Bulens I, Markoula A. et al. Targeted sys-tems biology profiling of tomato fruit reveals coordination of the Yang cycle and a distinct regulation of ethylene biosyn-thesis during postclimacteric ripening. Plant Physiol. 2012; 160: 1498-514

[33]

Pattyn J, Vaughan-Hirsch J, van de Poel B. The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol. 2021; 229:770-82

[34]

Lyzenga WJ, Booth JK, Stone SL. The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. 1-aminocyclopropane-1-carboxylate synthase 7. Plant J. 2012; 71:23-34

[35]

Tang X, Mei Y, He K. et al. The RING-type E3 ligase RIE1 sus-tains leaf longevity by specifically targeting AtACS7 to fine-tune ethylene production in Arabidopsis. Proc Natl Acad Sci USA. 2024; 121:e2411271121

[36]

Li T, Jiang Z, Zhang L. et al. Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J. 2016; 88:735-48

[37]

Wang Y, Lu Q, Li B. et al. LED white light-activated transcription factor MdHY5 inhibits ethylene biosynthesis during apple fruit ripening. Postharvest Biol Technol. 2023; 202:112372

[38]

Zang N, Li X, Qi L. et al. H2O2-activated transcription factor MdERF4 negatively regulates ethylene biosynthetic during fruit ripening by suppressing MdACS1 transcription. Postharvest Biol Technol. 2023; 204:112461

[39]

He Y, Liu H, Li H. et al. Transcription factors DkBZR1/2 regulate cell wall degradation genes and ethylene biosynthesis genes during persimmon fruit ripening. JExp Bot. 2021; 72:6437-46

[40]

Yang YY, Shan W, Yang TW. et al. MaMYB4 is a negative regulator and a substrate of RING-type E3 ligases MaBRG2/3 in controlling banana fruit ripening. Plant J. 2022; 110:1651-69

[41]

Liu W, Zhang L, Ma L. et al. The HY5 transcription factor nega-tively regulates ethylene production by inhibiting ACS1 expres-sion under blue light conditions in pear. Hortic Plant J. 2023; 9: 920-30

[42]

Ding X, Liu X, Jiang G. et al. SlJMJ7 orchestrates tomato fruit ripening via crosstalk between H3K4me3 and DML2-mediated DNA demethylation. New Phytol. 2022; 233:1202-19

[43]

Hu YA, Han ZY, Wang T. et al. Ethylene response factor MdERF4 and histone deacetylase MdHDA19 suppress apple fruit ripening through histone deacetylation of ripening-related genes. Plant Physiol. 2022; 188:2166-81

[44]

Wang KL, Yoshida H, Lurin C. et al. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature. 2004; 428: 945-50

[45]

Yoshida H, Nagata M, Saito K. et al. Arabidopsis ETO1 specif-ically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol. 2005; 5:14

[46]

Chen Y, Guo P, Dong Z. The role of histone acetylation in transcriptional regulation and seed development. Plant Physiol. 2024; 194:1962-79

[47]

Houben M, Van de Poel B. 1-aminocyclopropane-1-carboxylic acid oxidase (ACO): the enzyme that makes the plant hormone ethylene. Front Plant Sci. 2019; 10:695

[48]

Wu C, Wei W, Cai D. et al. A novel module of MaMADS31-MaBZR2 confers negative regulation of banana fruit ripening. Hortic. Plant J. 2024; 11:633-44

[49]

Xu Y, Liu Z, Lv T. et al. Exogenous Ca2+ promotes transcription factor phosphorylation to suppress ethylene biosynthesis in apple. Plant Physiol. 2023; 191:2475-88

[50]

Han YC, Kuang JF, Chen JY. et al. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. 2016; 171:1070-84

[51]

Jia H, Chen S, Liu D. et al. Ethylene-induced hydrogen sulfide negatively regulates ethylene biosynthesis by persulfidation of ACO in tomato under osmotic stress. Front Plant Sci. 2018; 9:1517

[52]

Liu M, Wei JW, Liu W. et al. S-nitrosylation of ACO homolog 4 improves ethylene synthesis and salt tolerance in tomato. New Phytol. 2023; 239:159-73

[53]

Dong CH, Jang M, Scharein B. et al. Molecular association of the Arabidopsis ETR1 ethylene receptor and a regulator of ethylene signaling, RTE1. JBiolChem. 2010; 285:40706-13

[54]

Chung MY, Vrebalov J, Alba R. et al. A tomato (Solanum lycop-ersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 2010; 64:936-47

[55]

Karlova R, Rosin FM, Busscher-Lange J. et al. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell. 2011; 23:923-41

[56]

Lee JM, Joung JG, McQuinn R. et al. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J. 2012; 70: 191-204

[57]

Dong TT, Hu ZL, Deng L. et al. A tomato MADS-Box transcription factor, SlMADS1, acts as a negative regulator of fruit ripening. Plant Physiol. 2013; 163:1026-36

[58]

Ma N, Feng H, Meng X. et al. Overexpression of tomato SlNAC1 transcription factor alters fruit pigmentation and softening. BMC Plant Biol. 2014; 14:351

[59]

Yin W, Hu Z, Cui B. et al. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycoper-sicum). Plant Physiol and Biochem. 2017; 118:235-44

[60]

Cao HH, Chen J, Yue M. et al. Tomato transcriptional repres-sor MYB70 directly regulates ethylene-dependent fruit ripening. Plant J. 2020; 104:1568-81

[61]

Xiao YY, Chen JY, Kuang JF. et al. Banana ethylene response factors are involved in fruit ripening through their interac-tions with ethylene biosynthesis genes. JExp Bo.t 2013; 64: 2499-510

[62]

Guo YF, Shan W, Liang SM. et al. MaBZR1/2 act as transcriptional repressors of ethylene biosynthetic genes in banana fruit. Physiol Plant. 2019; 165:555-68

[63]

Wei W, Yang YY, Wu CJ. et al. MaMADS1-MaNAC083 tran-scriptional regulatory cascade regulates ethylene biosyn-thesis during banana fruit ripening. Hortic Res. 2023;10: uhad177

[64]

Guan J, Liang X, Gao G. et al. The interaction between CmPIF8 and CmACO1 under postharvest red light treatment might affect fruit ripening and sucrose accumulation in oriental melon fruit. Postharvest Biol Technol. 2024; 209:112717

[65]

Wu X, Wang L, Xing Q. et al. CmPIF8-CmERF27-CmACS10-mediated ethylene biosynthesis modulates red light-induced powdery mildew resistance in oriental melon. Plant Cell Environ. 2024; 47:4135-50

[66]

Li HX, Wang SW, Zhai LL. et al. The miR156/SPL12 module orches-trates fruit colour change through directly regulating ethylene production pathway in blueberry. Plant Biotechnol J. 2024; 22: 386-400

[67]

Penarrubia L, Aguilar M, Margossian L. et al. An antisense gene stimulates ethylene hormone production during tomato fruit ripening. Plant Cell. 1992; 4:681-7

[68]

Kneissl ML, Deikman J. The tomato E8 gene influences ethylene biosynthesis in fruit but not in flowers. Plant Physiol. 1996; 112: 537-47

[69]

Shan W, Kuang JF, Wei W. et al. MaXB3 modulates MaNAC2, MaACS1, and MaACO1 stability to repress ethylene biosyn-thesis during banana fruit ripening. Plant Physiol. 2020; 184: 1153-71

[70]

Wei W, Yang YY, Su XG. et al. MaRTH1 suppression of ethy-lene response during banana fruit ripening and is controlled by MaXB3-MaNAC2 regulatory module. Postharvest Biol Technol. 2021; 182:111707

[71]

Guo JE, Hu Z, Zhu M. et al. The tomato histone deacetylase SlHDA1 contributes to the repression of fruit ripening and carotenoid accumulation. Sci Rep. 2017; 7:7930

[72]

Guo JE, Hu Z, Yu X. et al. A histone deacetylase gene, SlHDA3, acts as a negative regulator of fruit ripening and carotenoid accumulation. Plant Cell Rep. 2018; 37:125-35

[73]

Wang Y, Sun J, Wei Y. et al. Histone deacetylase MdHDT 3 suppresses ethylene biosynthesis by deacetylating MdACS1 and MdACO1 during apple fruit ripening. Postharvest Biol Technol. 2025; 219:113269

[74]

Van de Poel B, Vandenzavel N, Smet C. et al. Tissue specific analysis reveals a differential organization and regulation of both ethylene biosynthesis and E8 during climacteric ripening of tomato. BMC Plant Biol. 2014; 14:11

[75]

Akiyama R, Nakayasu M, Umemoto N. et al. Tomato E8 encodes a C-27 hydroxylase in metabolic detoxification of α-tomatine during fruit ripening. Plant Cell Physiol. 2021; 62:775-83

[76]

Li FF, Fu MJ, Zhou SE. et al. A tomato HD-zip I transcription factor, VAHOX1, acts as a negative regulator of fruit ripening. Hortic Res. 2023;10:uhac236

[77]

Yang YY, Wu CJ, Shan W. et al. Mitogen-activated protein kinase 14-mediated phosphorylation of MaMYB4 negatively regulates banana fruit ripening. Hortic Res. 2023;10:uhac243

[78]

Joo S, Liu Y, Lueth A. et al. MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 2008; 54:129-40

[79]

Hu Y, Han Z, Sun Y. et al. ERF 4 affects fruit firmness through TPL4 by reducing ethylene production. Plant J. 2020; 103:937-50

[80]

Liu Y, Xiao W, Liao L. et al. A PpEIL2/3-PpNAC1-PpWRKY14 mod-ule regulates fruit ripening by modulating ethylene production in peach. J Integr Plant Biol. 2024; 66:2470-89

[81]

Wei W, Yang YY, Chen JY. et al. MaNAC029 modulates ethylene biosynthesis and fruit quality and undergoes MaXB3-mediated proteasomal degradation during banana ripening. J Adv Res. 2023; 53:33-47

[82]

Su D, Liu KD, Yu ZS. et al. Genome-wide characterization of the tomato GASA family identifies SlGASA1 as a repressor of fruit ripening. Hortic Res. 2023;10:uhac222

[83]

Li T, Liu Z, Lv T. et al. Phosphorylation of MdCYTOKININ RESPONSE FACTOR4 suppresses ethylene biosynthesis during apple fruit ripening. Plant Physiol. 2023; 191:694-714

[84]

Guo Z, Liu H, Zheng S. et al. The transcription factor PbbHLH164 is destabilized by PbRAD23C/D.1 and mediates ethylene biosyn-thesis during pear fruit ripening. J Adv Res. 2024; 66:119-31

[85]

PT, Yu S, Zhu N. et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nat Plants. 2018; 4:784-91

[86]

Wang RF, Tavano ECD, Lammers M. et al. Re-evaluation of transcription factor function in tomato fruit development and ripening with CRISPR/Cas9-mutagenesis. Sci Rep. 2019; 9:1696

[87]

Sunkar R, Li YF, Jagadeeswaran G. Functions of microRNAs in plant stress responses. Trends Plant Sci. 2012; 17:196-203

[88]

Tian JX, Zhang F, Zhang GY. et al.A long noncoding RNA functions in pumpkin fruit development through S-adenosyl-L-methionine synthetase. Plant Physiol. 2024; 195:940-57

[89]

Zuo JH, Grierson D, Courtney LT. et al. Relationships between genome methylation, levels of non-coding RNAs, mRNAs and metabolites in ripening tomato fruit. Plant J. 2020; 103: 980-94

[90]

Zhao YQ, Hu KD, Yao GF. et al.A D-cysteine desulfhydrase, SlDCD2, participates in tomato fruit ripening by modulat-ing ROS homoeostasis and ethylene biosynthesis. Hortic Res. 2023;10:uhad014

[91]

Gambhir P, Raghuvanshi U, Parida AP. et al. Elevated methylgly-oxal levels inhibit tomato fruit ripening by preventing ethylene biosynthesis. Plant Physiol. 2023; 192:2161-84

[92]

van Loon LC, Geraats BPJ, Linthorst HJM. Ethylene as a mod-ulator of disease resistance in plants. Trends Plant Sci. 2006; 11: 184-91

[93]

Fatma M, Asgher M, Iqbal N. et al. Ethylene signaling under stressful environments: analyzing collaborative knowledge. Plan Theory. 2022; 11:2211

[94]

Mao D, Yu F, Li J. et al. FERONIA receptor kinase inter-acts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant Cell Environ. 2015; 38:2566-74

[95]

Ludwikow A, Ciesla A, Kasprowicz-Maluski A. et al. Arabidopsis protein phosphatase 2C ABI1 interacts with type I ACC syn-thases and is involved in the regulation of ozone-induced ethy-lene biosynthesis. Mol Plant. 2014; 7:960-76

[96]

Dong Z, Yu Y, Li S. et al. Abscisic acid antagonizes ethylene pro-duction through the ABI4-mediated transcriptional repression of ACS4 and ACS8 in Arabidopsis. Mol Plant. 2016; 9:126-35

[97]

Luo XJ, Chen ZZ, Gao JP. et al. Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant J. 2014; 79: 44-55

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