Please wait a minute...
Journal of Integrative Agriculture  2026, Vol. 25 Issue (4): 1475-1487    DOI: 10.1016/j.jia.2025.12.055
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
The TEI (Tomato Elongated Internode) gene encodes a GA20ox protein conferring internode elongation in tomato

Xinyi Jia1, Hexuan Wang1, Chunying Feng1, Xinyi Zhang1, Guohao Yang1, Ping Zhang1, Qingjun Fu1, Te Wang1, Jingfu Li1, He Zhang1, Jingbin Jiang1, Ke Wen2, Xiangyang Xu1#, Huanhuan Yang1# 

1 College of Horticulture and Landscape Architecture, Northeast Agricultural University, Harbin 150030, China

2 Sanya Research Institute, Hainan Academy of Agricultural Sciences, Sanya 572000, China

 Highlights 

TEI was identified as the gibberellin 20-oxidase (GA20ox) gene, regulating the internodes of tomatoes.

TEI gene regulates cell elongation by influencing the content of endogenous gibberellins, and affects the elongation of tomato internodes.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  理想的植株结构是番茄(Solanum lycopersicum)实现高产的关键因素,而节间长度与节间数量直接影响植株高度,因此研究节间形态的调控机制对番茄遗传改良至关重要。本研究发现一种自然发生的田间突变体番茄节间伸长突变体(tei),其主要特征为节间更长、叶色更深。通过生理激素检测与显微观察发现,与野生型(WT)植株相比,tei 突变体表现出内源赤霉素 GA3 水平升高、光合能力增强以及茎节间细胞伸长的特点。对 tei  WT RNA-seq 分析结果显示,赤霉素代谢途径显著富集。采用 BSA-seq 技术对 teiWT F2 分离群体进行定位分析,结合分子标记精细定位技术成功定位到候选基因 TEI(番茄节间伸长基因);该基因编码赤霉素 20 氧化酶(GA20ox)蛋白,其基因编号为 Solyc09g042210。进一步研究发现,TEI 基因启动子区域存在大量单核苷酸多态性(SNPs)与插入缺失突变(InDel),且 tei 突变体茎中 TEI 基因的表达水平显著高于 WT;此外,敲除 TEI 基因可很大程度上消除其对节间伸长的调控作用。综上,本研究提出 TEI 基因是调控 tei 突变体节间伸长表型的主要效应基因。该发现为研究人员提供了新的研究思路,即通过调控赤霉素稳态改良作物品种,最终有望助力培育更优质的番茄品种。




Abstract  The ideal plant architecture is a critical factor in achieving high yields in tomato (Solanum lycopersicum) cultivation.  The length and number of internodes directly influence plant height.  Therefore, investigating the regulatory mechanisms of internode morphology is essential for the genetic enhancement of tomatoes.  We identified a naturally occurring field mutant, tomato elongated internode (tei), characterized by longer internodes and darker leaf color.  Physiological hormone and microscopic studies revealed that, compared to wild-type (WT) plants, the tei mutant exhibited increased endogenous GA3 levels, enhanced photosynthetic capacity, and elongation of stem internode cells.  RNA-seq analysis results of tei and WT indicated enrichment in the gibberellin pathway.  We employed BSA-seq for mapping analysis on tei, WT, and F2 populations, leading to the fine mapping of the candidate gene designated as TEI (Tomato Elongated Internode).  This gene encoded a gibberellin 20 oxidase (GA20ox) protein and was identified as Solyc09g042210.  Additionally, we discovered numerous SNPs and InDel mutations in the TEI promoter region, with expression levels of TEI in tei stems significantly higher than those in WT.  Furthermore, knocking out the TEI gene eliminated its role in elongating internodes.  We proposed that TEI serves as the primary effector gene regulating the internode elongation phenotype associated with tei.  This discovery offered researchers a novel target for enhancing crop plant varieties by modulating gibberellin homeostasis, ultimately contributing to the breeding of superior tomato varieties.


Keywords:  internode elongation       gibberellins       BSA-seq       fine mapping       tomato  
Received: 02 December 2024   Accepted: 17 November 2025 Online: 29 December 2025  
Fund: 

This study was support by the grants from the Natural Science Foundation of Heilongjiang Province, China (YQ2024C010); the Key Research and Development Plan of Heilongjiang Province, China (SC2022ZX02C0202); CARS (CARS-23-A11) and the Hainan Province “Nanhai Xinxing” Science and Technology Innovation Talent Platform Project, China (NHXXRCXM202333).

About author:  Xinyi Jia, E-mail: jia593718265@163.com; #Correspondence Xiangyang Xu, E-mail: xuxyneau@gmail.com; Huanhuan Yang, E-mail: huanyaya0126@sina.com

Cite this article: 

Xinyi Jia, Hexuan Wang, Chunying Feng, Xinyi Zhang, Guohao Yang, Ping Zhang, Qingjun Fu, Te Wang, Jingfu Li, He Zhang, Jingbin Jiang, Ke Wen, Xiangyang Xu, Huanhuan Yang. 2026. The TEI (Tomato Elongated Internode) gene encodes a GA20ox protein conferring internode elongation in tomato. Journal of Integrative Agriculture, 25(4): 1475-1487.

Anarjan M B, Begum S, Bae I, Lee S. 2023. Mutation in the GA3ox gene governs short-internode characteristic in a Korean cucumber inbred line. HorticultureEnvironmentand Biotechnology64, 485–495.

Arnaud N, Lawrenson T, Østergaard L, Sablowski R. 2011. The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Current Biology21, 1215–1219.

Berry P, Sterling M, Spink J, Baker C, Sylvester-Bradley R, Mooney S, Tams A, Ennos A. 2004. Understanding and reducing lodging in cereals. Advances in Agronomy84, 215–269.

Bishop G J, Harrison K, Jones J. 1996. The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. The Plant Cell8, 959–969.

Brian P, Grove J F, Mulholland T. 1967. Relationships between structure and growth-promoting activity of the gibberellins and some allied compounds, in four test systems. Phytochemistry6, 1475–1499.

Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal6, 1621–1624.

Chen Y, Hou M, Liu L, Wu S, Shen Y, Ishiyama K, Kobayashi M, McCarty D R, Tan B C. 2014. The maize DWARF1 encodes a gibberellin 3-oxidase and is dual localized to the nucleus and cytosol. Plant Physiology166, 2028–2039.

Chevreau E, Leblay C. 1993. The effect of mother plant pretreatment and explant choice on regeneration from in vitro pear leaves. Acta Horticulturae336, 263–268.

Cho S H, Kang K, Lee S H, Lee I J, Paek N C. 2016. OsWOX3A is involved in negative feedback regulation of the gibberellic acid biosynthetic pathway in rice (Oryza sativa). Journal of Experimental Botany67, 1677–1687.

Daviere J M, Achard P. 2016. A pivotal role of DELLAs in regulating multiple hormone signals. Molecular Plant9, 10–20.

Elkind Y, Gurnick A, Kedar N. 1991. Genetics of semideterminate growth habit in tomato. HortScience26, 1074–1075.

Fang C, Zhong H, Lin Y, Chen B, Han M, Ren H, Lu H, Luber J M, Xia M, Li W. 2018. Assessment of the cPAS-based BGISEQ–500 platform for metagenomic sequencing. Gigascience7, gix133.

Fang Q, Zhang X, Chen S, Shao L, Sun H, Yan Z. 2019. Selecting traits to reduce seasonal yield variation of summer maize in the North China Plain. Agronomy Journal111, 343–353.

Feltus F, Hart G, Schertz K, Casa A, Kresovich S, Abraham S, Klein P, Brown P, Paterson A. 2006. Alignment of genetic maps and QTLs between inter- and intra-specific sorghum populations. Theoretical and Applied Genetics112, 1295–1305.

Fukazawa J, Mori M, Watanabe S, Miyamoto C, Ito T, Takahashi Y. 2017. DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA20 oxidase 2. Plant Physiology175, 1395–1406.

Gao Z, Feng H Y, Liang X G, Zhang L, Lin S, Zhao X, Shen S, Zhou L L, Zhou S L. 2018. Limits to maize productivity in the North China Plain: A comparison analysis for spring and summer maize. Field Crops Research228, 39–47.

Goodin M M, Zaitlin D, Naidu R A, Lommel S A. 2008. Nicotiana benthamiana: Its history and future as a model for plant–pathogen interactions. Molecular Plant–Microbe Interactions21, 1015–1026.

Guenin S, Mauriat M, Pelloux J, Van Wuytswinkel O, Bellini C, Gutierrez L. 2009. Normalization of qRT-PCR data: The necessity of adopting a systematic, experimental conditions-specific, validation of references. Journal of Experimental Botany60, 487–493.

Hart G, Schertz K, Peng Y, Syed N. 2001. Genetic mapping of Sorghum bicolor (L.) Moench QTLs that control variation in tillering and other morphological characters. Theoretical and Applied Genetics103, 1232–1242.

Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J. 2005. Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant and Cell Physiology46, 79–86.

Ji S, Gururani M, Lee J, Ahn B O, Chun S C. 2014. Isolation and characterisation of a dwarf rice mutant exhibiting defective gibberellins biosynthesis. Plant Biology16, 428–439.

Jupe S, Causton D, Scott I. 1988. Cellular basis of the effects of gibberellin and the pro gene on stem growth in tomato. Planta174, 106–111.

Khush G S. 1999. Green revolution: Preparing for the 21st century. Genome42, 646–655.

Khush G S. 2001. Green revolution: The way forward. Nature Reviews Genetics2, 815–822.

Kieffer M, Master V, Waites R, Davies B. 2011. TCP14 and TCP15 affect internode length and leaf shape in ArabidopsisThe Plant Journal68, 147–158.

Kwon C T, Heo J, Lemmon Z H, Capua Y, Hutton S F, Van Eck J, Park S J, Lippman Z B. 2020. Rapid customization of Solanaceae fruit crops for urban agriculture. Nature Biotechnology38, 182–188.

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research30, 325–327.

Li J, Li C, Smith S M. 2017. Hormone Metabolism and Signaling in Plants. Academic Press, United States.

Li J, Sima W, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y. 2012. Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. Journal of Experimental Botany63, 6407–6420.

Liu L, Zhao L, Liu Y, Zhu Y, Chen S, Yang L, Li X, Chen W, Xu Z, Xu P. 2024. Transcription factor OsWRKY72 controls rice leaf angle by regulating LAZY1-mediated shoot gravitropism. Plant Physiology195, 1586–1600.

Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K. 2004. Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. The Plant Journal37, 720–729.

Martí E, Gisbert C, Bishop G J, Dixon M S, García-Martínez J L. 2006. Genetic and physiological characterization of tomato cv. Micro-Tom. Journal of Experimental Botany57, 2037–2047.

Montoya T, Nomura T, Yokota T, Farrar K, Harrison K, Jones J G, Kaneta T, Kamiya Y, Szekeres M, Bishop G J. 2005. Patterns of Dwarf expression and brassinosteroid accumulation in tomato reveal the importance of brassinosteroid synthesis during fruit development. The Plant Journal42, 262–269.

Mulder N J, Apweiler R, Attwood T K, Bairoch A, Bateman A, Binns D, Bork P, Buillard V, Cerutti L, Copley R. 2007. New developments in the InterPro database. Nucleic Acids Research35, D224–D228.

Niu M, Wang H, Yin W, Meng W, Xiao Y, Liu D, Zhang X, Dong N, Liu J, Yang Y. 2022. Rice DWARF AND LOW-TILLERING and the homeodomain protein OSH15 interact to regulate internode elongation via orchestrating brassinosteroid signaling and metabolism. The Plant Cell34, 3754–3772.

Olszewski N, Sun T P, Gubler F. 2002. Gibberellin signaling: Biosynthesis, catabolism, and response pathways. The Plant Cell14, S61–S80.

Paciorek T, Chiapelli B J, Wang J Y, Paciorek M, Yang H, Sant A, Val D L, Boddu J, Liu K, Gu C. 2022. Targeted suppression of gibberellin biosynthetic genes ZmGA20ox3 and ZmGA20ox5 produces a short stature maize ideotype. Plant Biotechnology Journal20, 1140–1153.

Park S J, Jiang K, Tal L, Yichie Y, Gar O, Zamir D, Eshed Y, Lippman Z B. 2014. Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nature Genetics46, 1337–1342.

Parmagnani A S, D’Alessandro S, Maffei M E. 2022. Iron-sulfur complex assembly: Potential players of magnetic induction in plants. Plant Science325, 111483.

Schrager-Lavelle A, Gath N N, Devisetty U K, Carrera E, LópezDíaz I, Blazquez M A, Maloof J N. 2019. The role of a class III gibberellin 2oxidase in tomato internode elongation. The Plant Journal97, 603–615.

Sun X, Shu J, Ali Mohamed A M, Deng X, Zhi X, Bai J, Cui Y, Lu X, Du Y, Wang X. 2019. Identification and characterization of EI (Elongated Internode) gene in tomato (Solanum lycopersicum). International Journal of Molecular Sciences20, 2204.

Sun Y, Zhou K, Wang X, Li X, Zhang X, Han N, Zhang J, Chen S. 2024. Identification and characterization of CsERECTA, a major gene controlling stem elongation through regulating GA biosynthesis in cucumber. Theoretical and Applied Genetics137, 151.

Tamura K, Stecher G, Kumar S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution38, 3022–3027.

Tian Y, Yang L, Lu H, Zhang B, Li Y, Liu C, Ge T, Liu Y, Han J, Li Y, Qiu L. 2022. QTL analysis for plant height and fine mapping of two environmentally stable QTLs with major effects in soybean. Journal of Integrative Agriculture, 21, 933–946.

Wang S, Wang Y. 2022. Harnessing hormone gibberellin knowledge for plant height regulation. Plant Cell Reports41, 1945–1953.

Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics40, 761–767.

Yamaguchi M, Fujimoto H, Hirano K, Araki-Nakamura S, Ohmae-Shinohara K, Fujii A, Tsunashima M, Song X J, Ito Y, Nagae R. 2016. Sorghum Dw1, an agronomically important gene for lodging resistance, encodes a novel protein involved in cell proliferation. Scientific Reports6, 28366.

Yan P, Zhu Y, Wang Y, Ma F, Lan D, Niu F, Dong S, Zhang X, Hu J, Liu S. 2022. A new RING finger protein, PLANT ARCHITECTURE and GRAIN NUMBER 1, affects plant architecture and grain yield in rice. International Journal of Molecular Sciences23, 824.

Yang H, Zhou K, Wu Q, Jia X, Wang H, Yang W, Lin L, Hu X, Pan B, Li P. 2024. The tomato WRKY-B transcription factor modulates lateral branching by targeting BLINDPIN4, and IAA15Horticulture Research11, uhae193.

Yang X, Li R, Jablonski A, Stovall A, Kim J, Yi K, Ma Y, Beverly D, Phillips R, Novick K. 2023. Leaf angle as a leaf and canopy trait: Rejuvenating its role in ecology with new technology. Ecology Letters26, 1005–1020.

Yu Y, Qi Y, Xu J, Dai X, Chen J, Dong C H, Xiang F. 2021. Arabidopsis WRKY71 regulates ethylenemediated leaf senescence by directly activating EIN2ORE1 and ACS2 genes. The Plant Journal107, 1819–1836.

Zhang Y, Zhang B, Yan D, Dong W, Yang W, Li Q, Zeng L, Wang J, Wang L, Hicks L M. 2011. Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. The Plant Journal67, 342–353.

Zheng L, Gao C, Zhao C, Zhang L, Han M, An N, Ren X. 2019. Effects of brassinosteroid associated with auxin and gibberellin on apple tree growth and gene expression patterns. Horticultural Plant Journal5, 93–108.


[1] Ruining Zhang, Yunlin Cao, Tong Zhang, Yingyue Ma, Jiajia Li, Kunsong Chen, Xian Li. CRISPR/Cas9-mediated mutagenesis of transcriptional repressor SlMYB32 improves flavonols and flavanones accumulation in tomato fruit[J]. >Journal of Integrative Agriculture, 2026, 25(4): 1463-1474.
[2] Jingye Cheng, Rui Pan, Wenying Zhang, Tianhua He, Chengdao Li. An ancient super allele of the Vrs1 gene driving the recent success in modern barley improvement through optimising spike architecture[J]. >Journal of Integrative Agriculture, 2026, 25(2): 602-609.
[3] Guifen Zhang, Hao Wang, Yibo Zhang, Xiaoqing Xian, Cong Huang, Wanxue Liu, Fanghao Wan. Performance and functional responses of the thelytokous and arrhenotokous strains of Neochrysocharis formosa to Tuta absoluta, a globally severe tomato pest [J]. >Journal of Integrative Agriculture, 2026, 25(1): 180-191.
[4] Yanyun Tu, Lina Cheng, Xianfeng Liu, Marta Hammerstad, Chunlin Shi, Sida Meng, Mingfang Qi, Tianlai Li, Tao Xu. SlIDL6–SlHSL1/2/3 ligand-receptor pairs regulate tomato pedicel abscission[J]. >Journal of Integrative Agriculture, 2026, 25(1): 118-126.
[5] Yapeng Zhang, Wentao Cai, Qi Zhang, Qian Li, Yahui Wang, Ruiqi Peng, Haiqi Yin, Xin Hu, Zezhao Wang, Bo Zhu, Xue Gao, Yan Chen, Huijiang Gao, Lingyang Xu, Junya Li, Lupei Zha. Integrated analyses of genomic and transcriptomic data reveal candidate variants associated with carcass traits in Huaxi cattle[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3169-3184.
[6] Jian Ma, Guoliang Yuan, Xinyang Xu, Haijun Zhang, Yanhong Qiu, Congcong Li, Huijun Zhang. Identification and molecular marker development for peel color gene in melon (Cucumis melo L.)[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2589-2600.
[7] Jianqi Zeng, Dehui Zhao, Li Yang, Yufeng Yang, Dan Liu, Yubing Tian, Fengju Wang, Shuanghe Cao, Xianchun Xia, Zhonghu He, Yong Zhang. Fine mapping and candidate gene analysis of a major QTL for grain length on chromosome 5BS in bread wheat[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2465-2474.
[8] Shudong Chen, Yupan Zou, Xin Tong, Cao Xu. A tomato NBS-LRR gene Mi-9 confers heat-stable resistance to root-knot nematodes[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2869-2875.
[9] Jiaying Ma, Jian Liu, Yue Wen, Zhanli Ma, Jinzhu Zhang, Feihu Yin, Tehseen Javed, Jihong Zhang, Zhenhua Wang. Enhancing the yield and water use efficiency of processing tomatoes (Lycopersicon esculentum Miller) through optimal irrigation and salinity management under mulched drip irrigation[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2410-2424.
[10] Xuemei Hou, Meimei Shi, Zhuohui Zhang, Yandong Yao, Yihua Li, Changxia Li, Wenjin Yu, Chunlei Wang, Weibiao Liao. DNA demethylation is involved in nitric oxide-induced flowering in tomato[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1769-1785.
[11] Ru Bao, Tianli Guo, Zehua Yang, Chengyu Feng, Junyao Wu, Xiaomin Fu, Liu Hu, Changhai Liu, Fengwang Ma. Overexpression of the apple m6A demethylase gene MdALKBH1A regulates resistance to heat stress and fixed-carbon starvation[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1489-1502.
[12] Peiyu Zhang, Guoning Zhu, Chunjiao Zhang, Hongliang Zhu. Functional analysis of tomato MAP65 gene family, highlighting SlMAP65-1’s role in fruit morphogenesis[J]. >Journal of Integrative Agriculture, 2025, 24(2): 564-574.
[13] Long Cui, Fangyan Zheng, Chenhui Zhang, Sunan Gao, Jie Ye, Yuyang Zhang, Taotao Wang, Zonglie Hong, Zhibiao Ye, Junhong Zhang. The CONSTANS-LIKE SlCOL1 in tomato regulates the fruit chlorophyll content by stabilizing the GOLDEN2-LIKE protein[J]. >Journal of Integrative Agriculture, 2025, 24(2): 536-545.
[14] Yong Yang, Rong Fan, Xuejun Zhang, Meihua Li, Yongbing Zhang, Hongping Yi, Manrui Ma, Yun Yang, Bin Liu, Xingwang Liu, Huazhong Ren. Mutation in CmGhc1 confers the white hypocotyl phenotype in melon (Cucumis melo L.)[J]. >Journal of Integrative Agriculture, 2025, 24(11): 4242-4254.
[15] Lulu Yu, Muhammad Ahsan Asghar, Antonios Petridis, Fei Xu. Unlocking Dendrobium officinale’s drought resistance: Insights from transcriptomic analysis and enhanced drought tolerance in tomato[J]. >Journal of Integrative Agriculture, 2025, 24(11): 4282-4293.
No Suggested Reading articles found!