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Root Defense in Salicylic Acid-Altering Arabidopsis Plants in Responses to Cadmium Stress

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Abstract

The regulatory role of salicylic acid (SA) has been extensively reported in plants subjected to cadmium (Cd) stress. However, the underlying mechanisms still remain to be elucidated. This study provided evidence that root biological processes played crucial roles in SA-altering Arabidopsis plant responses to Cd stress. The nahG (naphthalene hydroxylase G)-transformed plants (with a significantly reduced endogenous SA) displayed a stronger tolerance, while the mutant snc1 (suppressor of nonexpressor of PR gene, constitutive 1; with high endogenous SA) was more sensitive, compared with wild-type (WT) plants under Cd stress. Correspondingly, a stronger antioxidative defense and a weaker oxidative stress were detected in nahG roots, while a more severe oxidative damage occurred in snc1 roots. The expression of a set of redox-related genes was examined, and mostly presented a higher level in nahG roots. A higher content of total flavonoids was observed in nahG roots under Cd stress, which was positively correlated with the expression of flavonoid biosynthesis-related genes. The metal-chelating and -sequestrating genes presented higher expression levels in nahG than in other two genotypes following Cd exposure. Noticeably, the pectin methylesterase inhibitor-encoding genes displayed dramatically high basal expression levels in nahG roots, and further induced under Cd stress. Accordingly, the pectin methylesterase activity was the least in nahG under both control and Cd stress. These results suggest that nahG-conferred Cd tolerance is associated with the root antioxidation defense, flavonoid biosynthesis, metal chelation and sequestration, and cell wall modification.

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Abbreviations

nahG:

Naphthalene hydroxylase G

PC:

Phytochelatin

PCS:

Phytochelatin synthase

PMEI:

Pectin methylesterase inhibitor

SA:

Salicylic acid

snc1:

Suppressor of npr1-1 constitutive 1

References

  • Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analyses. Verlag Chemie, Weinheim

    Google Scholar 

  • Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727

    Article  CAS  PubMed  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Brunner I, Sperisen C (2013) Aluminum exclusion and aluminum tolerance in woody plants. Front Plant Sci 4:1–12

    Article  Google Scholar 

  • Chen H, Li Y, Ma X, Guo L, He Y, Ren Z, Kuang Z, Zhang X, Zhang Z (2019) Analysis of potential strategies for cadmium stress tolerance revealed by transcriptome analysis of upland cotton. Sci Rep 9:86

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic Biol Med 108:465–477

    Article  CAS  PubMed  Google Scholar 

  • Choppala G, Bolan N, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391

    Article  CAS  Google Scholar 

  • Corso M, Schvartzman MS, Guzzo F, Souard F, Malkowski E, Hanikenne M, Verbruggen N (2018) Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytol 218:283–297

    Article  CAS  PubMed  Google Scholar 

  • Di Ferdinando M, Brunetti C, Agati G, Tattini M (2014) Multiple functions of polyphenols in plants inhabiting unfavorable Mediterranean areas. Environ Exp Bot 103:107–116

    Article  CAS  Google Scholar 

  • Duan YP, Yuan S, Tu SH, Feng WQ, Xu F, Zhang ZW, Chen YE, Wang X, Shang J, Lin HH (2010) Effects of cadmium stress on alternative oxidase and photosystem II in three wheat cultivars. Z Naturforsch C 65:87–94

    Article  CAS  PubMed  Google Scholar 

  • Eichhorn H, Klinghamme M, Becht P, Tenhaken R (2006) Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. J Exp Bot 57:2193–2201

    Article  CAS  PubMed  Google Scholar 

  • Garmash EV, Velegzhaninov IO, Grabelhych OI, Borovik OA, Silina EV, Voinikov VK, Golovko TK (2017) Expression profiles of genes for mitochondrial respiratory energy-dissipating systems and antioxidant enzymes in wheat leaves during de-etiolation. J Plant Physiol 215:110–121

    Article  CAS  PubMed  Google Scholar 

  • Gondor OS, Pál M, Darkó É, Janda T, Szalai G (2016) Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.). PLoS One 11:e0160157

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Griffith OW, Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (s-n-butyl-homocysteine sulfoximine). J Biol Chem 254:7558–7560

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Liu C, Li H, Yi K, Ding N, Li N, Lin Y, Fu Q (2018) Endogenous salicylic acid is required for promoting cadmium tolerance of Arabidopsis by modulating glutathione metabolisms. Sci Total Environ 615:476–485

    Article  CAS  Google Scholar 

  • Guo B, Liu C, Liang I, Li N, Fu Q (2019) Salicylic acid signals plant defence against cadmium toxicity. Int J Mol Sci 20:e2960

    Article  PubMed  CAS  Google Scholar 

  • Gutsch A, Sergeant K, Keunen E, Prinsen E, Guerriero G, Renaut J, Hausman JF, Cuypers A (2019) Does long-term cadmium exposure influence the composition of pectic polysaccharides in the cell wall of Medicago sativa stems? BMC Plant Biol 19:271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han JP, Köster P, Drerup MM, Scholz M, Li S, Edel KH, Hashimoto K, Kuchitsu K, Hippler M, Kudla J (2019) Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca2+ binding. New Phytol 221:1935–1949

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Zhao Y, Jin D, Zhang L, Bi XH, Chen HX, Xu Q, Ma CY, Li GZ (2012) Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant Soil 354:81–95

    Article  CAS  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  CAS  PubMed  Google Scholar 

  • Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185

    Article  CAS  Google Scholar 

  • Hong MJ, Kim DY, Lee TG, Jeon WB, Seo YW (2010) Functional characterization of pectin methylesterase inhibitor (PMEI) in wheat. Genes Genet Syst 85:97–106

    Article  CAS  PubMed  Google Scholar 

  • Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia H, Wang X, Dou Y, Liu D, Si W, Fang H, Zhao C, Chen S, Xi J, Li J (2016) Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci Rep 6:39702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia Z, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  Google Scholar 

  • Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keilig K, Ludwig-Müller J (2009) Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot Studies 50:311–318

    CAS  Google Scholar 

  • Khan MI, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462

    PubMed  PubMed Central  Google Scholar 

  • Khare D, Mitsuda N, Lee S, Song WY, Hwang D, Ohme-Takagi M, Martinoia E, Lee Y, Hwang JU (2017) Root avoidance of toxic metals requires the GeBP-LIKE 4 transcription factor in Arabidopsis thaliana. New Phytol 213:1257–1273

    Article  CAS  PubMed  Google Scholar 

  • Kumari A, Pandey-Rai S (2018) Enhanced arsenic tolerance and secondary metabolism by modulation of gene expression and proteome profile in Artemisia annua L. after application of exogenous salicylic acid. Plant Physiol Biochem 132:590–602

    Article  CAS  PubMed  Google Scholar 

  • Li J, Lu H, Liu J, Hong H, Yan C (2015) The influence of flavonoid amendment on the absorption of cadmium in Avicennia marina roots. Ecotoxicol Environ Saf 120:1–6

    Article  CAS  PubMed  Google Scholar 

  • Lionetti V, Fabri E, De Caroli M, Hansen AR, Willats WG, Piro G, Bellincampi D (2017) Three pectin methylesterase inhibitors protect cell wall integrity for Arabidopsis immunity to Botrytis. Plant Physiol 173:1844–1863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867

    Article  PubMed  PubMed Central  Google Scholar 

  • Lugon-Moulin N, Zhang M, Gadani F, Rossi L, Koller D, Krauss M, Wagner GJ (2004) Critical review of the science and options for reducing cadmium in tobacco (Nicotiana tabacum L.) and other plants. Adv Agron 83:111–180

    Article  CAS  Google Scholar 

  • Maleva M, Garmash E, Chukina N, Malec P, Waloszek A, Strzałka K (2018) Effect of the exogenous anthocyanin extract on key metabolic pathways and antioxidant status of Brazilian elodea (Egeria densa (Planch.) Casp.) exposed to cadmium and manganese. Ecotoxicol Environ Saf 160:197–206

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Moudouma CFM, Gloaguen V, Riou C, Forestier L, Saladin G (2012) High concentration of cadmium induces AtPCS2 gene expression in Arabidopsis thaliana (L.) Heynh ecotype Wassilewskija seedlings. Acta Physiol Plant 34:1083–1091

    Article  CAS  Google Scholar 

  • Müller K, Levesque-Tremblay G, Bartels S, Weitbrecht K, Wormit A, Usadel B, Haughn G, Kermode AR (2013) Demethylesterification of cell wall pectins in Arabidopsis thaliana plays a role in seed germination. Plant Physiol 161:305–316

    Article  PubMed  CAS  Google Scholar 

  • Napoleão TA, Soares G, Vital CE, Bastos C, Castro R, Loureiro ME, Giordano A (2017) Methyl jasmonate and salicylic acid are able to modify cell wall but only salicylic acid alters biomass digestibility in the model grass Brachypodium distachyon. Plant Sci 263:46–54

    Article  PubMed  CAS  Google Scholar 

  • Newman MA, van Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM (2001) Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris: a plant defense response activated by hrp gene-dependent and hrp geneindependent mechanisms. Mol Plant Microbe Interact 14:785–792

    Article  CAS  PubMed  Google Scholar 

  • Owens DK, Alerding AB, Crosby KC, Bandara AB, Westwood JH, Winkel BSJ (2008) Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiol 147:1046–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288

    Article  CAS  PubMed  Google Scholar 

  • Paynel F, Schaumann A, Arkoun M, Douchiche O, Morvan C (2009) Temporal regulation of cell-wall pectin methylesterase and peroxidase isoforms in cadmium-treated flax hypocotyl. Ann Bot 104:1363–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranocha P, Francoz E, Burlat V, Dunand C (2014) Expression of PRX36, PMEI6 and SBT1.7 is controlled by complex transcription factor regulatory networks for proper seed coat mucilage extrusion. Plant Signal. Behav. 9:e977734

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ren LL, Liu YJ, Liu HJ, Qian TT, Qi LW, Wang XR, Zeng QY (2014) Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of populus class III peroxidase family. Plant Cell 26:2404–2419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero-Puertas MC, Terrón-Camero LC, Peláez-Vico MÁ, Olmedilla A, Sandalio LM (2019) Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress. Environ Exp Bot 161:107–119

    Article  CAS  Google Scholar 

  • Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34

    Article  CAS  PubMed  Google Scholar 

  • Schilmiller AL, Stout J, Weng JK, Humphreys J, Ruegger MO, Chapple C (2009) Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J 60:771–782

    Article  CAS  PubMed  Google Scholar 

  • Semane B, Cuypers A, Smeets K, van Belleghem F, Horemans N, Schat H, Vangronsveld J (2007) Cadmium responses in Arabidopsis thaliana: Glutathione metabolism and antioxidative defence system. Physiol Plant 129:519–528

    Article  CAS  Google Scholar 

  • Sénéchal F, Mareck A, Marcelo P, Lerouge P, Pelloux J (2015) Arabidopsis PME17 activity can be controlled by pectin methylesterase inhibitor 4. Plant Signal Behav 10:e983351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shahid M, Dumat C, Khalid S, Niazi NK, Antunes PMC (2017) Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Rev Environ Contam Toxicol 241:73–137

    CAS  PubMed  Google Scholar 

  • Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, Schreiber L, Aharoni A (2011) SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 7:e1001388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y (2013) Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. J Agric Food Chem 61:3781–3788

    Article  CAS  PubMed  Google Scholar 

  • Tan M, Cheng D, Yang Y, Zhang G, Qin M, Chen J, Chen Y, Jiang M (2017) Co-expression network analysis of the transcriptomes of rice roots exposed to various cadmium stresses reveals universal cadmium-responsive genes. BMC Plant Biol 17:194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tao SY, Sun LH, Ma CY, Li LL, Li GZ, Hao L (2013) Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium. Plant Soil 372:309–318

    Article  CAS  Google Scholar 

  • Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138

    Article  CAS  PubMed  Google Scholar 

  • Tohge T, Yonekura-Sakakibara K, Niida R, Watanabe-Takahashi A, Saito K (2007) Phytochemical genomics in Arabidopsis thaliana: a case study for functional identification of flavonoid biosynthesis genes. Pure Appl Chem 79:811–823

    Article  CAS  Google Scholar 

  • Wang YY, Wang Y, Li GZ, Hao L (2019) Salicylic acid-altering Arabidopsis plant response to cadmium exposure: underlying mechanisms affecting antioxidation and photosynthesis-related processes. Ecotoxicol Environ Saf 169:645–653

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  CAS  PubMed  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wormit A, Usadel B (2018) The multifaceted role of pectin methylesterase inhibitors (PMEIs). Int J Mol Sci 19:2878

    Article  PubMed Central  CAS  Google Scholar 

  • Xia Y, Liu J, Wang Y, Zhang XX, Shen ZG, Hu Z (2018) Ectopic expression of Vicia sativa Caffeoyl-CoA O-methyltransferase(VsCCoAOMT) increases the uptake and tolerance of cadmium in Arabidopsis. Environ Exp Bot 145:47–53

    Article  CAS  Google Scholar 

  • Zawoznik MS, Groppa MD, Tomaro ML, Benavides MP (2007) Endogenous salicylic acid potentiates cadmium-induced oxidative stress in Arabidopsis thaliana. Plant Sci 173:190–197

    Article  CAS  Google Scholar 

  • Zhang X, Dong J, Liu H, Wang J, Qi Y, Liang Z (2016) Transcriptome sequencing in response to salicylic acid in Salvia miltiorrhiza. PLoS One 11:e0147849

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou YT, Liu C, Li GZ, Hao L (2019) Ethylene insensitive mutation increases Arabidopsis tolerance to Cd in NPR1-dependent manner. Plant Soil 441:49–69

    Article  CAS  Google Scholar 

  • Zhu XF, Le GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012) Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta 236:989–997

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant Nos. 31572213 to HL, 31570502 to LGZ).

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Authors and Affiliations

  1. College of Life Science, Shenyang Normal University, Shenyang, 110034, China

    Qiyu Zhao, Chunxiu Gu, Yuehang Sun, Guangzhe Li & Lin Hao

  2. College of Environment and Resource, Dalian Nationalities University, Dalian, 116605, China

    Lin-Lin Li

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  1. Qiyu Zhao
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Zhao, Q., Gu, C., Sun, Y. et al. Root Defense in Salicylic Acid-Altering Arabidopsis Plants in Responses to Cadmium Stress. J Plant Growth Regul 40, 1764–1776 (2021). https://doi.org/10.1007/s00344-020-10233-x

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