RESEARCH ARTICLES

Differences in the Adaptive Development of Suberin in the Tobacco Root Endothelial Layer under Different Potassium Levels

  • Yunxiang Xu ,
  • Liwen Zhang ,
  • Peng Wang ,
  • Yingchen Gu ,
  • Madan Lal Kolhi ,
  • Biao Zhang ,
  • Yingying Zhu ,
  • Haiwei Liu
Expand
  • 1 Key Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs/Institute of Tobacco Research of CAAS, Qingdao 266101, China
    2 Graduate School of Chinese Academy of Agricultural Sciences, Beijing 100081, China

Received date: 2024-12-09

  Accepted date: 2024-03-18

  Online published: 2025-03-18

Abstract

INTRODUCTION: Apoplastic barriers differentiated from the root endoderm play important roles in plant stress resistance and nutrient uptake, and the development of suberin lamellae has become a popular research topic in recent years.
RATIONALE: Hydroponic experiments with potassium concentrations ranging from 0.1 to 4.0 mmol∙L-1 were conducted, using the cultivated tobacco variety Zhongyan 100 as the experimental material, to explore the effects of different potassium supplies on the endodermal suberization and its physiological and molecular mechanisms.
RESULTS: Low potassium (0.1 mmol∙L-1) stress significantly enhanced the endodermal suberization: the absolute length of the fully suberized region ranged from 0-2 cm in the control to 4-6 cm, and the relative proportion increased from 0-15.0% to 33.2%-44.3%. These findings indicate that suberization is one of the key morphological adaptation mechanisms in tobacco under low potassium stress. Phenotypic analysis revealed that under low potassium stress, root elongation increased while plant biomass decreased, and the potassium ion content and accumulation in both the aboveground and root parts decreased. Additionally, the flow rate and potassium ion concentration in the xylem sap decreased, indicating reduced transport efficiency. Endogenous hormone analysis revealed that low potassium stress increased the abscisic acid (ABA) content in roots while suppressing ethylene and methyl jasmonate levels, forming a specific hormonal regulatory network. The transcriptome data further supported the molecular basis of suberization development, showing significant upregulation of genes related to suberin synthesis and transport (e.g., CYP86, GPAT, and ABCG) and their upstream positive regulatory factors (MYB36, MYB41, MYB92, and MYB93).
CONCLUSION: This study is the first to reveal that low potassium stress regulates the suberization developmental program of tobacco roots through ABA-mediated hormonal signaling reprogramming, providing a novel perspective for understanding the adaptation mechanisms of plants to potassium stress.

Fluorescence imaging of transverse sections of the endodermis development in tobacco roots under three potassium concentrations (bars=130 μm)

Cite this article

Yunxiang Xu , Liwen Zhang , Peng Wang , Yingchen Gu , Madan Lal Kolhi , Biao Zhang , Yingying Zhu , Haiwei Liu . Differences in the Adaptive Development of Suberin in the Tobacco Root Endothelial Layer under Different Potassium Levels[J]. Chinese Bulletin of Botany, 2025 , 60(6) : 914 -930 . DOI: 10.11983/CBB24191

References

[1] Andersen TG, Barberon M, Geldner N (2015). Suberization—the second life of an endodermal cell. Curr Opin Plant Biol 28, 9-15.
[2] Barberon M (2017). The endodermis as a checkpoint for nutrients. New Phytol 213, 1604-1610.
[3] Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016). Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447-459.
[4] Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, Muthukumar B, Mickelbart MV, Schreiber L, Franke RB, Salt DE (2009). Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5, e1000492.
[5] Chen AL, Liu T, Deng Y, Xiao R, Zhang T, Wang Y, Yang YH, Lakshmanan P, Shi XJ, Zhang FS, Chen XP (2023). Nitrate-dependent suberization regulates cadmium uptake and accumulation in maize. Sci Total Environ 878, 162-848.
[6] Doblas VG, Geldner N, Barberon M (2017). The endodermis, a tightly controlled barrier for nutrients. Curr Opin Plant Biol 39, 136-143.
[7] Guo Z, Li ZS, Dai XY, Wang YF (2019). Effects of auxin on tobacco root growth and potassium uptake under low potassium stress. Plant Nutr Fert Sci 25, 1173-1184. (in Chinese)
  郭泽, 李子绅, 代晓燕, 王英锋 (2019). 低钾胁迫下外源生长素对烟草根系生长及钾吸收的影响. 植物营养与肥料学报 25, 1173-1184.
[8] Leide J, Hildebrandt U, Hartung W, Riederer M, Vogg G (2012). Abscisic acid mediates the formation of a suberized stem scar tissue in tomato fruits. New Phytol 194, 402-415.
[9] Liu HW, Zhang Y, Wang HY, Zhang B, He Y, Wang HH, Zhu YY, Holm PE, Shi Y (2023). Comparing cadmium uptake kinetics, xylem translocation, chemical forms, and subcellular distribution of two tobacco (Nicotiana tabacum L.) cultivars. Ecotoxicol Environ Saf 254, 114738.
[10] Liu YK, Lu M, Persson DP, Luo JP, Liang YC, Li TQ (2022). The involvement of nitric oxide and ethylene on the formation of endodermal barriers in response to Cd in hyperaccumulator Sedum alfredii. Environ Pollut 307, 11-9530.
[11] Liu YK, Tao Q, Li JX, Guo XY, Luo JP, Jupa R, Liang YC, Li TQ (2021). Ethylene-mediated apoplastic barriers development involved in cadmium accumulation in root of hyperaccumulator Sedum alfredii. J Hazard Mater 403, 123729.
[12] Lulai EC, Suttle JC, Pederson SM (2008). Regulatory involvement of abscisic acid in potato tuber wound-healing. J Exp Bot 59, 1175-1186.
[13] Luo HB, Huang CM, Cao HQ, Jiang SL, Wu XJ, Ye LP, Wei YW (2022). Effects of different potassium levels on root development and endogenous hormone content for passion fruit tissue cultured seedling. China Fruits (4), 53-58. (in Chinese)
  罗海斌, 黄诚梅, 曹辉庆, 蒋胜理, 吴兴剑, 叶丽萍, 魏源文 (2022). 不同浓度钾元素对西番莲组培苗根系生长和内源激素含量的影响. 中国果树 (4), 53-58.
[14] Lux A, Morita S, Abe J, Ito K (2005). An improved method for clearing and staining free-hand sections and whole- mount samples. Ann Bot 96, 989-996.
[15] Melino VJ, Plett DC, Bendre P, Thomsen HC, Zeisler- Diehl VV, Schreiber L, Kronzucker HJ (2021). Nitrogen depletion enhances endodermal suberization without restricting transporter-mediated root NO3- influx. J Plant Physiol 257, 153334.
[16] Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012). Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci USA 109, 10101-10106.
[17] Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer JE, Yamazaki M, Li GW, Maurel C, Takano J, Kamiya T, Salt DE, Roppolo D, Geldner N (2014). A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. eLife 3, e03115.
[18] Tao Q, Jupa R, Liu YK, Luo JP, Li JX, Ková? J, Li B, Li QQ, Wu KR, Liang YC, Lux A, Wang CQ, Li TQ (2019). Abscisic acid-mediated modifications of radial apoplastic transport pathway play a key role in cadmium uptake in hyperaccumulator Sedum alfredii. Plant Cell Environ 42, 1425-1440.
[19] Tao Q, Li M, Xu Q, Ková? J, Yuan S, Li B, Li QQ, Huang R, Gao XS, Wang CQ (2022). Radial transport difference mediated by root endodermal barriers contributes to differential cadmium accumulation between japonica and indica subspecies of rice (Oryza sativa L.). J Hazard Mater 425, 128008.
[20] Vestenaa MW, Husted S, Minutello F, Persson DP (2024). Endodermal suberin restricts root leakage of cesium: a suitable tracer for potassium. Physiol Plant 176, e14393.
[21] Wang JB, Zhang QL, Tung J, Zhang X, Liu D, Deng YT, Tian ZD, Chen HL, Wang TT, Yin WX, Li B, Lai ZB, Dinesh-Kumar SP, Baker B, Li F (2024). High-quality assembled and annotated genomes of Nicotiana tabacum and Nicotiana benthamiana reveal chromosome evolution and changes in defense arsenals. Mol Plant 17, 423-437.
[22] Wang LM, Liu YQ, Ruan YJ (2015). The research progress of potassium to plant. Chin Hortic Abstr 31(5), 71, 148. (in Chinese)
  王立梅, 刘奕清, 阮玉娟 (2015). 植物钾素研究进展. 中国园艺文摘 31(5), 71, 148.
[23] Wang P, Wang CM, Gao L, Cui YN, Yang HL, de Silva NDG, Ma Q, Bao AK, Flowers TJ, Rowland O, Wang SM (2020). Aliphatic suberin confers salt tolerance to Arabidopsis by limiting Na+ influx, K+ efflux and water backflow. Plant Soil 448, 603-620.
[24] Wei XP, Liu LY, Jin XY, Xue J, Geng P, Xu ZH, Zhang LH, Wang XY, Zong W, Zhang L, Mao LC (2024a). Exogenous methyl jasmonate promotes wound healing of Chinese yam tubers (Dioscorea opposita) through the deposition of suberin polyaliphatics at the wound sites. Postharvest Biol Technol 207, 112586.
[25] Wei XP, Liu LY, Liu G, Geng P, Wei XB, Yao X, Chen JY, Gong WJ, Ge ZZ, Liu MP, Mao LC (2024b). Methyl jasmonate promotes suberin biosynthesis by stimulating transcriptional activation of AchMYC2 on AchFHT in wound healing of kiwifruit. Postharvest Biol Technol 210, 112741.
[26] Wei XP, Liu LY, Xu ZH, Xue J, Geng P, Ge ZZ, Wang XY, Zhang L, Zong W, Mao LC (2023). Methyl jasmonate facilitates wound healing of Chinese yam tubers via positively regulating the biosynthesis and polymerization of suberin polyphenolics. Sci Hortic 312, 111840.
[27] Xu HM, Liu P, Wang CH, Wu SS, Dong CQ, Lin QY, Sun WR, Huang BB, Xu MZ, Tauqeer A, Wu S (2019). Transcriptional networks regulating suberin and lignin in endodermis link development and ABA response. Plant Physiol 190, 1165-1181.
[28] Yan HF, Shi Y, Li NH, Zhang YC (2013). Progress in tobacco potassium nutrition. J Agric Sci Technol 15, 123-129. (in Chinese)
  闫慧峰, 石屹, 李乃会, 张永春 (2013). 烟草钾素营养研究进展. 中国农业科技导报 15, 123-129.
[29] Yang TZ, Shu HY, Zhao XZ (2002). Recent advances in tobacco potassium nutrition in China. Tob Sci Technol (7), 39-43. (in Chinese)
  杨铁钊, 舒海燕, 赵献章 (2002). 我国烟草钾素营养研究现状与进展. 烟草科技 (7), 39-43.
[30] Zhang B, Wu J, Zhang Y, Dong XW, Han S, Gao X, Du CW, Li HY, Chong XF, Zhu YY, Liu HW (2023). Research progress on physiological functions of suberin lamellae in water and solutes transport. Chin Bull Bot 58, 1008-1018. (in Chinese)
  张标, 吴健, 张杨, 董小卫, 韩硕, 高昕, 杜从伍, 李慧英, 种学法, 朱莹莹, 刘海伟 (2023). 木栓层在水和溶质运输中的生理功能研究进展. 植物学报 58, 1008-1018.
[31] Zhang B, Xu YX, Zhang LW, Yu SY, Zhu YY, Liu CJ, Wang P, Shi Y, Li LZ, Liu HW (2024). Root endodermal suberization induced by nitrate stress regulate apoplastic pathway rather than nitrate uptake in tobacco (Nicotiana tabacum L.). Plant Physiol Biochem 216, 109166.
[32] Zhang B, Xu YX, Zhang LW, Zhu YY, Liu HW (2024). Mechanism of low NO3- stress inhibiting apoplastic transport in tobacco roots. Chin Tob Sci 45(2), 25-34. (in Chinese)
  张标, 许耘祥, 张莉汶, 朱莹莹, 刘海伟 (2024). 低NO3-胁迫抑制烟草根系质外体运输的机制研究. 中国烟草科学 45(2), 25-34.
[33] Zhou Y, An YP, Ma R, Wang P (2024). Transcriptional regulation of suberin and its response to the environment. Acta Bot Boreali-Occident Sin 44, 1993-2006. (in Chinese)
  周月, 安永平, 马蓉, 王沛(2024). 木栓质的转录调控及其对环境的响应. 西北植物学报 44, 1993-2006.
Outlines

/