Skip to main content

Advertisement

Log in

Foliar Application of Abscisic Acid Alleviates Cadmium Stress by Modulating Differential Physiological and Transcriptome Response in Leaves, Stems, and Roots of Mung Bean Seedlings

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Abscisic acid (ABA) has been well known to strongly improve plant tolerance to heavy metals. However, the comprehensive mechanism of alleviating cadmium (Cd) stress in different plant organ was not been fully elucidated. In this study, foliar spray of 10 μM ABA significantly (p < 0.05) improved the plant height, root length, and the number of lateral roots, and reduced Cd accumulation and effectively restored the mineral contents caused by Cd induced change in leaves, stems, and roots of mung bean seedlings. Transcriptome analysis revealed that a total of 2241 differentially expressed genes (DEGs) (|fold-change|≥ 2.0 and FDR ≤ 0.05) were identified in the ABA + Cd-treated mung bean seedlings compared to the Cd-treated group, with 898, 908, and 859 DEGs identified in leaves, stems, and roots, respectively. Foliar application of ABA predominantly affected the KEGG pathways including phenylpropanoid biosynthesis, alpha-linolenic acid metabolism, starch and sucrose metabolism, and cyanoamino acid metabolism, and regulated the genes related to lipid metabolism, cell wall processes, secondary metabolism, defense and stress responses, hormone signal transduction, photosynthesis, and cell division to mitigate Cd toxicity of the mung bean seedlings. However, ABA exerted distinct effects on the gene profiles of leaves, stems, and roots under Cd stress. Interestingly, although exogenous ABA was applied to the leaves, the genes involved in hormone signaling were found to be regulated primarily in roots on the first day and subsequently in stems and leaves at later stages, indicating that exogenous ABA participates in mitigating Cd toxicity through signal transduction. Notably, significant upregulation of transporter-related genes was observed mainly in leaves and stems, including ABC transporters, NRT1/PTR FAMILY protein encoding genes, and WAT1-related protein encoding genes, which may contribute to the transportation of the ABA, Cd, and nutriments. Furthermore, the expression of genes encoding crucial photosynthetic proteins exhibited significant upregulation or downregulation upon exogenous ABA treatment, implying that exogenous ABA also ameliorated Cd stress by modulating leaf photosynthetic activity. This study may contribute to understanding the molecular mechanism of ABA-alleviated Cd stress in mung bean and identifying a number of highly regulated genes that could potentially be used to improve plant tolerance to heavy metals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  • Aloui A, Dumas-Gaudot E, Daher Z, Van Tuinen D, Aschi-Smit S, Morandi D (2012) Influence of arbuscular mycorrhizal colonisation on cadmium induced Medicago truncatula root isoflavonoid accumulation. Plant Physiol Biochem 60:233–239

    Article  CAS  PubMed  Google Scholar 

  • Breria CM, Hsieh CH, Yen JY, Nair R, Lin CY, Huang SM, Noble TJ, Schaeitner R (2020) Population structure of the world vegetable center mungbean mini core collection and genome–wide association mapping of loci associated with variation of seed coat luster. Trop Plant Biol 13:1–12

    Article  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang L, Ramireddy E, Schmulling T (2013) Lateral root formation and growth of Arabidopsis is redundantly regulated by cytokinin metabolism and signalling genes. J Exp Bot 64:5021–5032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang J, Li X, Fu W, Wang J, Yong Y, Shi H, Ding Z, Kui H, Gou X, He K, Li J (2019) Asymmetric distribution of cytokinins determines root hydrotropism in Arabidopsis thaliana. Cell Res 29:984–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen L, Long C, Wang D, Yang J (2020a) Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators. Chemosphere 242:125112

    Article  CAS  PubMed  Google Scholar 

  • Chen TT, Liu FF, Xiao DW, Jiang XY, Li P, Zhao SM, Hou BK, Li YJ (2020b) The Arabidopsis UDP–glycosyltransferase75B1, conjugates abscisic acid and affects plant response to abiotic stresses. Plant Mol Biol 102:389–401

    Article  CAS  PubMed  Google Scholar 

  • Cheng M, Kopittke PM, Wang A, Peter WGS, Tang C (2018) Cadmium reduces zinc uptake but enhances its translocation in the cadmium–accumulator, Carpobrotus rossii, without affecting speciation. Plant Soil 430:219–231

    Article  CAS  Google Scholar 

  • Cheng L, Pu L, Li A, Zhu X, Zhao P, Xu X, Lei N, Chen J (2022) Implication of exogenous abscisic acid (ABA) application on phytoremediation: plants grown in co–contaminated soil. Environ Sci Pollut Res Int 29(6):8684–8693

    Article  CAS  PubMed  Google Scholar 

  • Chiam NC, Fujimura T, Sano R, Akiyoshi N, Hiroyama R, Watanabe Y, Motose H, Demura T, Ohtani M (2019) Nonsense–mediated mRNA decay deficiency affects the auxin response and shoot regeneration in Arabidopsis. Plant Cell Physiol 60:2000–2014

    Article  CAS  PubMed  Google Scholar 

  • Dai M, Liu W, Hong H, Lu H, Liu J, Jia H, Yan C (2018) Exogenous phosphorus enhances cadmium tolerance by affecting cell wall polysaccharides in two mangrove seedlings Avicennia marina (Forsk.) Vierh and Kandelia obovata (S., L.) Yong differing in cadmium accumulation. Mar Pollut Bull 126:86–92

    Article  CAS  PubMed  Google Scholar 

  • Dawuda MM, Liao W, Hu L, Yu J, Xie J, Calderón-Urrea A, Jin X, Wu Y (2019) Root tolerance and biochemical response of Chinese lettuce (Lactuca sativa L.) genotypes to cadmium stress. PeerJ 7:e7530

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawuda MM, Liao W, Hu L, Yu J, Xie J, Calderón-Urrea A, Wu Y, Tang Z (2020) Foliar application of abscisic acid mitigates cadmium stress and increases food safety of cadmium–sensitive lettuce (Lactuca sativa L.) genotype. Peer. J. 8:e9270

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J Integr Plant Biol 63:180–209

    Article  CAS  PubMed  Google Scholar 

  • Fan W, Xu JM, Wu P, Yang ZX, Lou HQ, Chen WW, Jin JF, Zheng SJ, Yang JL (2019) Alleviation by abscisic acid of Al toxicity in rice bean is not associated with citrate efflux but depends on ABI5–mediated signal transduction pathways. J Integr Plant Biol 61:140–154

    Article  CAS  PubMed  Google Scholar 

  • Fernie AR (2019) Evolution: an early role for flavonoids in defense against oomycete infection. Curr Biol 29:R688–R690

    Article  CAS  PubMed  Google Scholar 

  • Gai Z, Wang Y, Ding Y, Qian W, Qiu C, Xie H, Sun L, Jiang Z, Ma Q, Wang L, Ding Z (2020) Exogenous abscisic acid induces the lipid and flavonoid metabolism of tea plants under drought stress. Sci Rep 10:12275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Q, Meng L, Zhang YN, Mao PC, Tian XX, Li SS, Zhang L (2017) Antioxidative systems, metal ion homeostasis and cadmium distribution in Iris lactea exposed to cadmium stress. Ecotox Environ Safe 139:50–55

    Article  CAS  Google Scholar 

  • Guschina IA, Harwood JL, Smith M, Beckett RP (2002) Abscisic acid modifies the changes in lipids brought about by water stress in the moss Atrichum androgynum. New Phytol 156:255–264

    Article  CAS  PubMed  Google Scholar 

  • Hao W, Collier SM, Moffett P, Chai J (2013) Structural basis for the interaction between the potato virus X resistance protein (Rx) and its cofactor Ran GTPase–activating protein 2 (RanGAP2). J Biol Chem 288:35868–35876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoque MN, Tahjib-Ul-Arif M, Hannan A, Sultana N, Akhter S, Hasanuzzaman M, Akter F, Hossain MS, Sayed MA, Hasan MT, Skalicky M, Li X, Brestič M (2021) Melatonin modulates plant tolerance to heavy metal stress: morphological responses to molecular mechanisms. Int J Mol Sci 22(21):11445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keatinge JDH, Easdown WJ, Yang RY, Chadha ML, Shanmugasundaram S (2011) Overcoming chronic malnutrition in a future warming world: the key importance of mungbean and vegetable soybean. Euphytica 180:129–141

    Article  Google Scholar 

  • Kısa D, Öztürk L, Doker S, Gökçe İ (2017) Expression analysis of metallothioneins and mineral contents in tomato (Lycopersicon esculentum) under heavy metal stress. J Sci Food Agric 97(6):1916–1923

    Article  PubMed  Google Scholar 

  • Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: a review. Appl Geochem 108:1–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2015) Comprehensive analysis of regulatory elements of the promoters of rice sulfate transporter gene family and functional characterization of OsSul1;1 promoter under different metal stress. Plant Signal Behav 10:e990843

    Article  PubMed  PubMed Central  Google Scholar 

  • Küpper H, Kochian LV (2010) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol 185(1):114–129

    Article  PubMed  Google Scholar 

  • Lee C, Teng Q, Zhong R, Yuan Y, Haghighat M, Ye ZH (2012) Three Arabidopsis DUF579 domain–containing GXM proteins are methyltransferases catalyzing 4–o–methylation of glucuronic acid on xylan. Plant Cell Physiol 53:1934–1949

    Article  CAS  PubMed  Google Scholar 

  • Leng Y, Li Y, Wen Y, Zhao H, Wang Q, Li SW (2020) Transcriptome analysis provides molecular evidences for growth and adaptation of plant roots in cadimium–contaminated environments. Ecotoxicol Environ Saf 204:111098

    Article  CAS  PubMed  Google Scholar 

  • Leng Y, Li Y, Ma YH, He LF, Li SW (2021) Abscisic acid modulates differential physiological and biochemical responses of roots, stems, and leaves in mung bean seedlings to cadmium stress. Environ Sci Pollut Res Int 28:6030–6043

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA–Seq data with or without a reference genome. BMC Bioinf 12:323

    Article  CAS  Google Scholar 

  • Li SW, Leng Y, Feng L, Zeng XY (2014) Involvement of abscisic acid in regulating antioxidative defense systems and IAA–oxidase activity and improving adventitious rooting in mung bean [Vigna radiata (L.) Wilczek] seedlings under cadmium stress. Environ Sci Pollut Res Int 21:525–537

    Article  CAS  PubMed  Google Scholar 

  • Li SW, Shi RF, Leng Y, Zhou Y (2016) Transcriptomic analysis reveals the gene expression profile that specifically responds to IBA during adventitious rooting in mung bean seedlings. BMC Genomics 17:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Li SW, Leng Y, Shi RF (2019) Transcriptome characterization of gene profiling during early stage of nitric oxide–induced adventitious rooting in mung bean seedlings. J Plant Growth Regul 39:430–455

    Article  Google Scholar 

  • Liang Y, Harris JM (2005) Response of root branching to abscisic acid is correlated with nodule formation both in legumes and non legumes. Am J Bot 92:1675–1683

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Chen MX, Liu R, Zhang L, Hou X, Liu S, Ding X, Jiang Y, Xu J, Zhang J, Zhao X, Liu YG (2019) Abscisic acid regulates auxin distribution to mediate maize lateral root development under salt stress. Front Plant Sci 10:716

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Q, Chen S, Li Y, Zheng F, He B, Gu M (2020) Exogenous abscisic acid (ABA) promotes cadmium (Cd) accumulation in Sedum alfredii Hance by regulating the expression of Cd stress response genes. Environ Sci Pollut Res Int 27:8719–8731

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Li Y, Li X, Xu D, Lin X, Liu M, Li G, Qin X (2019) FAR–red elongated hypocotyls3 negatively regulates shade avoidance responses in Arabidopsis. Plant Cell Environ 42:3280–3292

    Article  CAS  PubMed  Google Scholar 

  • Mata-Pérez C, Spoel SH (2019) Thioredoxin–mediated redox signalling in plant immunity. Plant Sci 279:27–33

    Article  PubMed  Google Scholar 

  • Meng H, Hua S, Shamsi IH, Jilani G, Li Y, Jiang L (2009) Cadmium–induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul 58:47–59

    Article  CAS  Google Scholar 

  • Ogata FT, Branco V, Vale FF, Coppo L (2021) Glutaredoxin: discovery, redox defense and much more. Redox Biol 43:101975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan W, You Y, Shentu JL, Weng YN, Wang ST, Xu QR, Liu HJ, Du ST (2020) Abscisic acid (ABA)–importing transporter 1 (AIT1) contributes to the inhibition of Cd accumulation via exogenous ABA application in Arabidopsis. J Hazard Mater 391:122189

    Article  CAS  PubMed  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  CAS  PubMed  Google Scholar 

  • Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman JF (2015) Target or barrier? The cell wall of early– and later–diverging plants vs cadmium toxicity: differences in the response mechanisms. Front Plant Sci 6:133

    Article  PubMed  PubMed Central  Google Scholar 

  • Przedpełska-Wąsowicz E, Polatajko A, Wierzbicka M (2012) The influence of cadmium stress on the content of mineral nutrients and metal–binding proteins in Arabidopsis halleri. Water Air Soil Pollut 223(8):5445–5458

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahman A, Mostofa MG, Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2015) Calcium mitigates arsenic toxicity in rice seedlings by reducing arsenic uptake and modulating the antioxidant defense and glyoxalase systems and stress markers. BioMed Res Int 2015:340812

    Article  PubMed  PubMed Central  Google Scholar 

  • Rowe JH, Topping JF, Liu J, Lindsey K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos LR, Batista BL, Lobato AKS (2018) Brassinosteroids mitigate cadmium toxicity in cowpea plants. Photosynthetica 56(2):591–605

    Article  CAS  Google Scholar 

  • Song WY, Yamaki T, Yamaji N, Ko D, Jung KH, Fujii-Kashino M, An G, Martinoia E, Lee Y, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci U S A 111:15699–15704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sudhakaran SMN, Bukkan DS (2021) A review on nutritional composition, antinutritional components and health benefits of green gram (Vigna radiata (L.) Wilczek). J Food Biochem 45:e13743

    Google Scholar 

  • Sun X, Gilroy EM, Chini A, Nurmberg PL, Hein I, Lacomme C, Birch PR, Hussain A, Yun BW, Loake GJ (2011) ADS1 encodes a MATE-transporter that negatively regulates plant disease resistance. New Phytol 192:471–482

    Article  CAS  PubMed  Google Scholar 

  • Tang RJ, Luan S (2017) Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr Opin Plant Biol 39:97–105

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Wang L, Xie Y, Yu X, Li H, Lin L et al (2020) Effects of exogenous abscisic acid on the growth and cadmium accumulation of lettuce under cadmium–stress conditions. Int J Environ Anal Chem 100:720–731

    Article  CAS  Google Scholar 

  • Volpicella M, Leoni C, Fanizza I, Distaso M, Leoni G, Farioli L, Naumann T, Pastorello E, Ceci LR (2017) Characterization of maize Chitinase-A, a tough allergenic molecule. Allergy 72:1423–1429

    Article  CAS  PubMed  Google Scholar 

  • Waadt R, Seller CA, Hsu PK, Takahashi Y, Munemasa S, Schroeder JI (2022) Plant hormone regulation of abiotic stress responses. Nature Reviews Mol Biol Cell 23(10):680–694

    Article  CAS  Google Scholar 

  • Wang J, Chen J, Pan K (2013) Effect of exogenous abscisic acid on the level of antioxidants in Atractylodes macrocephala Koidz under lead stress. Environ Sci Pollut Res Int 20:1441–1449

    Article  CAS  PubMed  Google Scholar 

  • Wu PM, Leng Y, Li SW (2022) Transcriptome profiling provides new insights into ABA–mediated genes and pathways in leaves, stems, and roots of mung bean seedlings. Plant Growth Regul 98:569–587

    Article  CAS  Google Scholar 

  • Xie Q, Essemine J, Pang X, Chen H, Cai W (2020) Exogenous application of abscisic acid to shoots promotes primary root cell division and elongation. Plant Sci 292:110385

    Article  CAS  PubMed  Google Scholar 

  • Xing L, Zhao Y, Gao J, Xiang C, Zhu JK (2016) The ABA receptor PYL9 together with PYL8 plays an important role in regulating lateral root growth. Sci Rep 6:27177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Yu C, Xia X, Li M, Li H, Wang Y, Wang S, Wang C, Ma Y, Zhou G (2018) Comparative transcriptome analysis of duckweed (Landoltia punctata) in response to cadmium provides insights into molecular mechanisms underlying hyperaccumulation. Chemosphere 190:154–165

    Article  CAS  PubMed  Google Scholar 

  • Ying W, Liao L, Wei H, Gao Y, Liu X, Sun L (2023) Structural basis for abscisic acid efflux mediated by ABCG25 in Arabidopsis thaliana. Nature Plants 9(10):1697–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoyama R, Nishitani K (2001) A comprehensive expression analysis of all members of a gene family encoding cell–wall enzymes allowed us to predict cis-regulatory regions involved in cell–wall construction in specific organs of Arabidopsis. Plant Cell Physiol 42:1025–1033

    Article  CAS  PubMed  Google Scholar 

  • Yuan L, Zhu S, Shu S, Sun J, Guo S (2015) Regulation of 2,4-epibrassinolide on mineral nutrient uptake and ion distribution in Ca(NO3)2 stressed cucumber plants. J Plant Physiol 188:29–36

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Wang Z, Song J, Yue S, Yang H (2019) Cd2+ uptake inhibited by MhNCED3 from Malus hupehensis alleviates Cd–induced cell death. Environ Exp Bot 166:103802

    Article  CAS  Google Scholar 

  • Zhou M, Ghnaya T, Dailly H, Cui G, Vanpee B, Han R, Lutts S (2019) The cytokinin trans–zeatine riboside increased resistance to heavy metals in the halophyte plant species Kosteletzkya pentacarpos in the absence but not in the presence of NaCl. Chemosphere 233:954–965

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Ai H, Cao L, Sui R, Ye H, Du D, Sun J, Yao J, Chen K, Chen L (2018) Transcriptome analysis providing novel insights for Cd–resistant tall fescue responses to Cd stress. Ecotoxicol Environ Saf 160:349–356

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31760110) and Youth Science and Technology Foundation of Gansu Province (23JRRA1806).

Funding

This research was funded by the National Natural Science Foundation of China (31760110) and Youth Science and Technology Foundation of Gansu Province (23JRRA1806).

Author information

Authors and Affiliations

Authors

Contributions

Leng Yan and Wu Ping-Min: Methodology, Investigation, Preparation, Writing. Li Shi-Weng: Conceptualization, Methodology, Investigation, Funding acquisition, Supervision, Project administration. Zhang Xiao-Jun: Supervision, Writing, Revision. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Shi-Weng Li.

Ethics declarations

Conflict of interest

The authors declare that they have no known conflict of interests.

Additional information

Handling Editor: Charitha Jayasinghege.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2105 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leng, Y., Wu, PM., Li, SW. et al. Foliar Application of Abscisic Acid Alleviates Cadmium Stress by Modulating Differential Physiological and Transcriptome Response in Leaves, Stems, and Roots of Mung Bean Seedlings. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11443-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00344-024-11443-3

Keywords

Navigation