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Journal of Integrative Agriculture  2025, Vol. 24 Issue (9): 3693-3697    DOI: 10.1016/j.jia.2025.03.006
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Natural variations in the promoter alter SGT3 gene expression and affect steroidal glycoalkaloid content in potatoes

Nanling Zhou*, Xiaomei Zhang*, Ruqian Bai*, Chao Wang, Junmei Guan, Ding Fan, Yi Shang, Yuxin Jia#, Ling Ma#

School of Life Sciences, Yunnan Normal University, Kunming 650500, China

 Highlights 
● Natural variations in the SGT3 promoter TATA box repeats directly modulate gene expression and SGAs content in tubers, providing a novel molecular marker for low-steroidal glycoalkaloids (SGAs) breeding.
The SGT3 promoter haplotype with (TA)10 exhibits significantly higher transcriptional activity, correlating with high SGAs content, while the (TA)13 haplotype is linked to low SGAs in natural germplasms.
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摘要  

马铃薯中的龙葵素(α-茄碱和α-卡茄碱)是一类具有生物活性的甾体糖苷生物碱(Steroidal glycoalkaloids, SGAs),属于植物次生代谢产物。这类化合物由疏水的甾体骨架(茄啶醇)和亲水的寡糖链组成,主要分布在马铃薯的块茎、芽眼和表皮组织中。龙葵素在植物防御系统中发挥重要作用,能够抵抗病原微生物和害虫侵袭,但当其含量超过200 mg/100 g鲜重时,会对人体产生毒性作用,引起胃肠道不适和神经系统症状。其生物合成途径起始于胆固醇,经过一系列氧化、转氨和糖基化反应,最终由糖基转移酶催化完成。光照、机械损伤和贮藏条件等因素均可诱导龙葵素含量升高,这既是马铃薯重要的品质安全指标,也是育种研究中需要重点调控的目标性状。该研究以二倍体马铃薯自交系E4-63为材料,将E4-63各组织中龙葵素含量与龙葵素合成基因的表达量进行相关性分析,发现SGT3基因表达量与龙葵素含量呈极显著正相关(r = 0.894),其编码的糖基转移酶催化了龙葵素生物合成的最后一步。深入研究发现,在SGT3基因启动子区存在TATA-box重复序列的自然变异,形成 (TA)10(TA)13两种单倍型。通过双荧光素酶报告系统等实验证实,pro::SGT3(TA)10的启动子活性显著高于pro::SGT3(TA)13单倍型的,从而导致SGT3基因表达量增加和SGAs积累升高。通过对137份马铃薯种质的基因型-薯块龙葵素含量关联分析,发现pro::SGT3(TA)10单倍型在高SGAs材料中出现频率达92%,显著高于低SGAs材料中的68%。基于这一发现,研究团队开发了可区分SGT3启动子单倍型的分子标记,为马铃薯低毒品种选育提供了重要工具。该研究首次将启动子变异与薯块SGAs含量建立直接关联,相比基因编辑等人工干预手段,利用自然存在的pro::SGT3(TA)13单倍型降低SGAs含量,既避免了中间代谢产物积累的风险,又符合食品安全要求。研究成果不仅深化了对植物次生代谢调控的理解,也为马铃薯分子设计育种提供了新思路。通过分子标记辅助选择,可以实现对薯块SGAs含量的精准调控,对培育兼具抗病性和食用安全性的马铃薯新品种具有重要意义。



Received: 31 October 2024   Online: 20 March 2025   Accepted: 26 January 2025
Fund: This work was financially supported by the Guangdong Major Project of Basic and Applied Basic Research, China (2021B0301030004), the National Natural Science Foundation of China (32360757, U2202206 and 32361143517), and the Yunnan Fundamental Research Projects, China (202201AT070037, 202501AS070012).
About author:  #Correspondence Ling Ma, E-mail: May_ynnu@ynnu.edu.cn; Yuxin Jia, E-mail: jiayuxin@ynnu.edu.cn * These authors contributed equally to this study.

Cite this article: 

Nanling Zhou, Xiaomei Zhang, Ruqian Bai, Chao Wang, Junmei Guan, Ding Fan, Yi Shang, Yuxin Jia, Ling Ma. 2025. Natural variations in the promoter alter SGT3 gene expression and affect steroidal glycoalkaloid content in potatoes. Journal of Integrative Agriculture, 24(9): 3693-3697.

Akiyama R, Umemoto N, Mizutani M. 2023. Recent advances in steroidal glycoalkaloid biosynthesis in the genus SolanumPlant Biotechnology40, 185–191.

Akiyama R, Watanabe B, Kato J, Nakayasu M, Lee H J, Umemoto N, Muranaka T, Saito K, Sugimoto Y, Mizutani M. 2022. Tandem gene duplication of dioxygenases drives the structural diversity of steroidal glycoalkaloids in the tomato clade. Plant Cell Physiology63, 981–990.

Averello V, Hegeman A D, Chen C B. 2024. Finding the balance: Modifying the cholesterol and steroidal glycoalkaloid synthesis pathway in tomato (Solanum lycopersicum L.) for human health, fruit flavor, and plant defense. Horticultural Plant Journal11, 42–56.

Boccia M, Kessler D, Seibt W, Grabe V, Rodriguez Lopez C E, Grzech D, Heinicke S, O’Connor S E, Sonawane P D. 2024. A scaffold protein manages the biosynthesis of steroidal defense metabolites in plants. Science386, 1366–1372.

Dolan L C, Matulka R A, Burdock G A. 2010. Naturally occurring food toxins. Toxins2, 2289–2332.

Grzech D, Smit S J, Alam R M, Boccia M, Nakamura Y, Hong B, Barbole R, Heinicke S, Kunert M, Seibt W, Grabe V, Caputi L, Lichman B R, O’connor S E, Aharoni A, Sonawane P D. 2025. Incorporation of nitrogen in antinutritional Solanum alkaloid biosynthesis. Nature Chemical Biology21, 131–142.

EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain), Schrenk D, Bignami M, Bodin L, Chipman J K, del Mazo J, Hogstrand C, Hoogenboom L R, Leblanc J C, Nebbia C S, Nielsen E, Ntzani E, Petersen A, Sand S, Schwerdtle T, Vleminckx C, Wallace H, Brimer L, Cottrill B, Dusemund B, et al. 2020. Risk assessment of glycoalkaloids in feed and food, in particular in potatoes and potato-derived products. EFSA Journal18, 6222.

Itkin M G, Heinig U, Tzfadia O, Bhide A J, Shinde B S, Cardenas P D, Bocobza S E, Unger T, Malitsky S, Finkers R, Tikunov Y, Bovy A, Chikate Y R, Singh P N, Rogachev I, Beekwilder J, Giri A, Aharoni A. 2013. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science341, 175–179.

Liang X X, Wang J Y, Cao L, Du X Y, Qiang J H, Li W L, Wang P Q, Hou J, Li X, Mao W W, Zhu H Y, Yang L M, Li Q, Hu J B. 2024. An allelic variation in the promoter of the LRR-RLK gene, qSS6.1, is associated with melon seed size. Journal of Integrative Agriculture23, 3522–3536.

McCue K F, Breksa A, Vilches A, Belknap W. 2018. Modification of potato steroidal glycoalkaloids with silencing RNA constructs. American Journal of Potato Research95, 9–14.

McCue K F, Allen P V, Shepherd L V, Blake A, Maccree M M, Rockhold D R, Novy R G, Stewart D, Davies H V, Belknap W R. 2007. Potato glycosterol rhamnosyltransferase, the terminal step in triose side-chain biosynthesis. Phytochemistry68, 327–334.

McCue K F, Allen P V, Shepherd L V T, Blake A, Whitworth J, Maccree M M, Rockhold D R, Stewart D, Davies H V, Belknap W R. 2006. The primary in vivo steroidal alkaloid glucosyltransferase from potato. Phytochemistry67, 1590–1597.

McCue K F, Shepherd L V T, Allen P V, Maccree M M, Rockhold D R, Corsini D L, Davies H V, Belknap W R. 2005. Metabolic compensation of steroidal glycoalkaloid biosynthesis in transgenic potato tubers: Using reverse genetics to confirm the in vivo enzyme function of a steroidal alkaloid galactosyltransferase. Plant Science168, 267–273.

Mishal R, Luna-Arias J P. 2022. Role of the TATA-box binding protein (TBP) and associated family members in transcription regulation. Gene833, 146581.

Nema P K, Ramayya N, Duncan E, Niranjan K. 2008. Potato glycoalkaloids: Formation and strategies for mitigation. Journal of the Science of Food and Agriculture88, 1869–1881.

Ostreikova T O, Kalinkina O V, Bogomolov N G, Chernykh I V. 2022. Glycoalkaloids of plants in the family Solanaceae (Nightshade) as potential drugs. Pharmaceutical Chemistry Journal56, 948–957.

Paudel J R, Gardner K M, Bizimungu B, de Koeyer D, Song J, Tai H H. 2019. Genetic mapping of steroidal glycoalkaloids using selective genotyping in potato. American Journal of Potato Research96, 505–516.

Savinkova L K, Sharypova E B, Kolchanov N A. 2023. On the role of TATA boxes and TATA-binding protein in Arabidopsis thalianaPlants (Basel), 12, 1000.

Al Sinani S S S, Eltayeb E A. 2017. The steroidal glycoalkaloids solamargine and solasonine in Solanum plants. South African Journal of Botany112, 253–269.

Sonawane P D, Pollier J, Panda S, Szymanski J, Massalha H, Yona M, Unger T, Malitsky S, Arendt P, Pauwels L, Almekias-Siegl E, Rogachev I, Meir S, Cárdenas P D, Masri A, Petrikov M, Schaller H, Schaffer A A, Kamble A, Giri A P et al. 2016. Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism. Nature Plants3, 1–13.

Tang D, Jia Y, Zhang J, Li H, Cheng L, Wang P, Bao Z, Liu Z, Feng S, Zhu X, Li D, Zhu G, Wang H, Zhou Y, Zhou Y, Bryan G J, Buell C R, Zhang C, Huang S. 2022. Genome evolution and diversity of wild and cultivated potatoes. Nature606, 535–541.

Tao L L, Ting Y J, Chen H R, Wen H L, Xie H, Luo L Y, Huang K L, Zhu J Y, Liu S R, Wei C L. 2023. Core collection construction of tea plant germplasm in Anhui Province based on genetic diversity analysis using simple sequence repeat markers. Journal of Integrative Agriculture22, 2719–2728.

Tora L, Timmers H T M. 2010. The TATA box regulates TATA-binding protein (TBP) dynamics in vivoTrends in Biochemical Sciences35, 309–314.

Umemoto N, Nakayasu M, Ohyama K, Yotsu-Yamashita M, Mizutani M, Seki H, Saito K, Muranaka T. 2016. Two cytochrome P450 monooxygenases catalyze early hydroxylation steps in the potato steroid glycoalkaloid biosynthetic pathway. Plant Physiology171, 2458–2467.

Wang F Q, Bian L, Qiu P P, Guo S, Guo J H, Guo C S, Jiang J F, Liu C H, Wang Y, Liu G T, Wang Y J, Xu Y. 2023. Development and application of KASP marker for high throughput detection of the seedless trait in grapevine. Journal of Integrative Agriculture22, 3269–3283.

Yasumoto S, Lee H J, Akiyama R, Sawai S, Mizutani M, Umemoto N, Saito K, Muranaka T. 2024. Disruption of CYP88B1 by transcription activator-like effector nuclease in potato and potential use to produce useful saponins. Plant Biotechnology41, 289–293.

Yean D, Gralla J. 1997. Transcription reinitiation rate: A special role for the TATA box. Molecular and Cellular Biology17, 3809–3816.

Zhang C, Yang Z, Tang D, Zhu Y, Wang P, Li D, Zhu G, Xiong X, Shang Y, Li C, Huang S. 2021. Genome design of hybrid potato. Cell184, 3873–3883.

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