Abstract
Cadmium (Cd) toxicity has been widely studied in different plant species. However, the mechanism involved in its toxicity and the cell response to Cd has not been well established. In the present study, we investigated the possible mechanism of calcium (Ca) in protecting Arabidopsis from Cd toxicity. The results showed that 50 μM Cd significantly inhibited the seedling growth and decreased the chlorophyll content in Arabidopsis. Specifically, the primary root (PR) length was decreased but the lateral root (LR) number was increased under Cd stress. Furthermore, Cd enhanced the hydrogen peroxide (H2O2) content and lipid peroxidation as indicated by malondialdehyde (MDA) accumulation. Cd also altered the level and the distribution of auxin in PR tips (as evidenced by DR5::GUS and PIN:GFP reporter expression) and the expression of several putative auxin biosynthetic, catabolic, and transport pathway-related genes. Application of 3 mM Ca alleviated the inhibition of Cd on the root growth. Ca application not only led to reducing oxidative injuries but also restoring the normal auxin transport and distribution in Arabidopsis root under Cd stress. Taken together, these results suggest that Ca alleviates the root growth inhibition caused by Cd through maintaining auxin homeostasis in Arabidopsis seedlings.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- Aux/IAA:
-
Auxin/indole-3-acetic acid
- Ca:
-
Calcium
- CAT:
-
Catalase
- CAX2:
-
Calcium exchanger 2
- Cd:
-
Cadmium
- CPx-ATPases:
-
A class of P-type ATPases that pump heavy metals
- EDTA:
-
Ethylene diamine tetraacetic acid
- EGTA:
-
Ethylene glycol-bis(β-aminoethyl ether)-N,N,N′,N′-tetraacetic acid
- GH3:
-
Gretchen Hagen3
- GSH:
-
Glutathione
- GUS:
-
β-Glucuronidase
- H2O2 :
-
Hydrogen peroxide
- HMA4:
-
Heavy metal-associated domains 4
- IAA:
-
Indole-3-acetic acid
- IAM:
-
Indole-3-acetamide
- IAN:
-
Indole-3-acetonitrile
- IAOx:
-
Indole-3-acetaldoxime
- IBA:
-
Indole-3-butyric acid
- IPA:
-
Indole-3-pyruvic acid
- IRT1:
-
Iron-regulated transporter
- LCT1:
-
Low-affinity cation transporter
- LR:
-
Lateral root
- 1/2MS:
-
Half-strength Murashige and Skoog
- NIT:
-
Nitrilases
- PIN:
-
PIN-FORMED
- POD:
-
Peroxidase
- PR:
-
Primary root
- ROS:
-
Reactive oxygen species
- SIMR:
-
Stress-induced morphogenic response
- SOD:
-
Superoxide dismutase
- TAA:
-
Aminotransferase
- TAM:
-
Tryptamine
- TCA:
-
Trichloroacetic acid
- Trp:
-
Tryptophan
- X-Gluc:
-
5-Bromo-4-chloro-3-indolyl-β-d-glucuronic acid
- WT:
-
Wild-type
References
Ádám AL, Bestwick CS, Barna B, Mansfield JW (1995) Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. Phaseolicola. Planta 197:240–249
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175
Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44
Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10:e0114571
Aidid SB, Okamoto H (1993) Responses of elongation growth rate, turgor pressure and cell wall extensibility of stem cells of Impatiens balsamina to lead, cadmium and zinc. Biometals 6:245–249
Allan AC, Rubery PH (1991) Calcium deficiency and auxin transport in Cucurbita pepo L. seedlings. Planta 183:604–612
Amudha J, Balasubramani G (2011) Recent molecular advances to combat abiotic stress tolerance in crop plants. Biotechnol Mol Biol Rev 6:31–58
Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Environ Sci Technol 7:1–85
Banguelos G, Bangerth F, Marschner H (1987) Relationship between polar basipetal auxin transport and acropetal Ca2+ transport into tomato fruits. Plant Physiol 71:321–327
Benavides MP, Gallego SM, Tomaro M (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Berleth T, Sachs T (2001) Plant morphogenesis: long-distance coordination and local patterning. Curr Opin Plant Biol 4:57–62
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
Bramm J (1992) Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc Natl Acad Sci U S A 89:3213–3216
Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249:187–195
Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol 154:810–819
Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213:45–50
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Colorado P, Rodriguez A, Nicolas G, Rodriguez D (1994) Abscisic acid and stress regulate gene expression during germination of chick-pea seeds. Possible role of calcium. Physiol Plant 91:461–467
Cosio C, Mrtinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiol 134:716–725
dela Fuente RK, Leopold AC (1973) A role for calcium in auxin transport. Plant Physiol 51:845–847
Elobeid M, Gōbel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in poplar. J Exp Bot 63:1413–1421
Farzadfar S, Zarinkamar F, Modarres-Sanavy SA, Hojati M (2013) Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environ Sci Pollut Res 20:1413–1422
Feng JG, Shi QH, Wang XF, Wei M, Yang FJ, Xu HN (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123:521–530
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cd affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969
Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714
Gussarson M, Asp H, Adalsteinsson S, Jensén P (1996) Enhancement of Cd effects on growth and nutrient composition of birch (Betula pendula) by buthionine sulphoxinine (BSO). J Exp Bot 47:211–215
Hausmann N, Fengler S, Hennig A, Franz-Wachtel M, Hampp R, Neef M (2014) Cytosolic calcium, hydrogen peroxide and related gene expression and protein modulation in Arabidopsis thaliana cell cultures respond immediately to altered gravitation: parabolic flight data. Plant Biol 16:120–128
Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442
Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133
Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–711
Hu YF, Yang LJ, Na XF, You J, Hu W, Liang XL, Liu J, Mao LN, Wang XM, Wang HH, Bi YR (2012) Narciclasine inhibits the responses of Arabidopsis roots to auxin. Planta 236:597–612
Hu YF, Zhou GY, Na XF, Yang LJ, Nan WB, Liu X, Zhang YQ, Li JL, Bi YR (2013) Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. J Plant Physiol 170:965–975
Huang YX, Liao BH, Xiao LT, Liu SC, Wang ZK (2006) Effects of Cd2+ on seedling growth and phytohormone contents of Glycine max. J Environ Sci 27:1398–1401
Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Panneerselvam R (2007a) Calcium chloride effects on salinity-induced oxidative stress, proline metabolism and indole alkaloid accumulation in Catharanthus roseus. C R Biol 330:674–683
Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R (2007b) Water deficit stress mitigation by calcium chloride in Catharanthus roseus: effects on oxidative stress, proline metabolism and indole alkaloid accumulation. Colloids Surf B: Biointerfaces 60:110–116
Janda T, Szalai G, Tari I, Páldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling in maize (Zea mays L) plants. Planta 208:175–180
Jiang YW, Huang BR (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52:341–349
John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76
Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238
Kinraide TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118:513–520
Kinraide TB, Perler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259:201–208
Kolbert Z, Petö A, Lehotai N, Feigl G, Erdei L (2012) Long-term copper (Cu2+) exposure impacts on auxin, nitric oxide (NO) metabolism and morphology of Arabidopsis thaliana L. Plant Growth Regul 68:151–159
Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956
Kováčik J, Klejdus B, Hedbavny J, Bačkor M (2009) Salicylic acid alleviates NaCl-induced changes in the metabolism of Matricaria chamomilla plants. Ecotoxicology 18:544–554
Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen activated protein kinase cascade in plants. PANS 97:2940–2945
Küpper H, Küpper F, Spiller M (1996) Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. J Exp Bot 47:259–266
Lang ML, Zhang YX, Chai TY (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158
Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351
Lee J, Mulkey T, Evans M (1983) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73:874–876
Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682
Li BH, Li Q, Su YH, Chen H, Xiong LM, Mi GH, Kronzucker HJ, Shi WM (2011) Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis. Plant Cell Environ 34:933–946
McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou WJ (2011) Insight into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574
Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2:a001594
Padmaja K, Prasad DDK, Prasad ARK (1990) Inhibition of chlorophyll synthesis in Phaseolus vulgaris seedlings by cadmium acetate. Photosynthetica 24:399–405
Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036–10046
Pasternak T, Rudas V, Potters G, Jansen MAK (2005) Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ Exp Bot 53:299–314
Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J (2011) Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol 52:490–508
Porra RJ, Thompson WA, Kriedman PA (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105
Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169
Prochazkova D, Sairam RK, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Sci 161:765–771
Qin WM, Lan WZ, Yang X (2004) Involvement of NADPH oxidase in hydrogen peroxide accumulation by Aspergillus niger elicitor-induced Taxus chinensis cell cultures. J Plant Physiol 161:355–361
Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453
Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471–1479
Renu D, Sudhir KS (1999) Glyoxalase I from Brassica juncea is a calmodulin stimulated protein. Biochim Biophys Acta 1450:460–467
Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20:600–608
Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243
Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gómez M, Del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357
Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Sarwat M, Ahmad P, Nabi G, Hu X (2013) Ca2+ signals: the versatile decoders of environmental cues. Crit Rev Biotechnol 33:97–109
Shaked-Sachray L, Weiss D, Reuveni M, Nissim-Levi A, Oren-Shamir M (2002) Increase anthocyanin accumulation in aster flowers at elevated temperature due to magnesium treatment. Physiol Plant 114:559–565
Sharma P, Deswal R (2004) Detection and characterization of calcineurin-like activity in Brassica juncea and its activation by low temperature. Plant Physiol Biochem 42:579–584
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50
Shi GR, Cai QS, Liu CF, Wu L (2010) Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul 61:45–52
Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM (2012) Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int J Mol Sci 13:6604–6619
Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57:4059–4070
Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–36
Sofo A, Vitti A, Nuzzaci M, Tataranni G, Scopa A, Vangronsveld J et al (2013) Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context. Physiol Plant 149:487–498
Song WY, Zhang ZB, Shao HB, Guo XL, Cao HX, Zhao HB, Fu ZY, Hu XJ (2008) Relationship between calcium decoding elements and plant abiotic stress resistance. Int J Biol Sci 4:116–125
Song A, Li P, Li ZJ, Fan FL, Nikolic M, Liang YC (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333
Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT et al (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Doležal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191
Sudha G, Ravishankar GA (2003) The role of calcium channels in anthocyanin production in callus cutures of Daucus carota. Plant Growth Regul 40:163–169
Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminum induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61:347–356
Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol 22:19–25
Tamás L, Bočová B, Huttová J, Liptáková Ľ, Mistrík I, Valentovičová K et al (2012) Impact of the auxin signaling inhibitor p-chlorophenoxyisobutyric acid on short-term Cd-induced hydrogen peroxide production and growth response in barley root tip. J Plant Physiol 169:1375–1381
Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754
Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176
Tian SK, Lu LL, Zhang J, Wang K, Brown PH, He ZL, Liang J, Yang XE (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84:63–69
Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I et al (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22:2660–2679
Trofimova MS, Andreev IM, Kuznetsov VV (1999) Calcium is involved in regulation of the synthesis of HSPs in suspension-cultured sugar beet cells under hyperthermia. Physiol Plant 105:67–73
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616
Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3:525–536
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971
Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206
Veljovic-Jovanovic SD, Noctor G, Foyer CH (2002) Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Biochem 40:501–507
Vitti A, Nuzzaci M, Scopa A, Tataranni G, Remans T et al (2013) Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with cucumber mosaic virus (CMV) or exposed to cadmium. Int J Mol Sci 14:6889–6902
Wan G, Najeeb U, Jilani G, Naeem MS, Zhou W (2011) Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. Environ Sci Pollut Res 18:1478–1486
Wang CQ, Song H (2009) Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28:1341–1349
Wang CQ, Wang BS (2007) Ca2+-CaM is involved in betacyanin accumulation induced by darkness in C3 halophyte Suaeda salsa. J Integr Plant Biol 49:1378–1385
Wang CQ, Zhang YF, Liu T (2005) Activity changes of CaM and Ca2+-ATPase during low temperature-induced anthocyanin accumulation in Alternanthera bettzickiana. Physiol Plant 124:260–266
Wang M, Zou J, Duan X, Jiang W, Liu D (2007) Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresour Technol 98:82–88
Wang YN, Li KX, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645
Wang WH, Yi XQ, Han AD, Liu TW, Chen J, Wu FH, Dong XJ, He JX, Pei ZM, Zheng HL (2012) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot 63:177–190
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
Xavier V, Fabienne L, Stephanie K, Vitrac X, Larronde F, Krisa S, Decendit A, Deffieux G (2000) Sugar sensing and Ca2+ calmodulin requirement in Vitis vinifera cells producing anthocyanins. Phytochemistry 53:659–665
Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183
Xu J, Yin HX, Liu XJ, Li X (2010) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459
Yang T, Poovaiah BW (2000) Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J Biol Chem 275:3137–3143
Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058
Yuan HM, Xu HH, Liu WC, Lu YT (2013) Copper regulates primary root elongation through PIN1-mediated auxin redistribution. Plant Cell Physiol 54:766–778
Zhang FQ, Zhang HX, Wang GP, Xu LL, Shen ZG (2009) Cadmium-induced accumulation of hydrogen peroxide in the leaf apoplast of Phaseolus aureus and Vicia sativa and the roles of different antioxidant enzymes. J Hazard Mater 168:76–84
Zhao Y, Christensen SK, Fankhauser X, Cashman JR, Cohen JD, Wei-gel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309
Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857
Zhao FY, Hu F, Zhang SY, Wang K, Zhang CR, Liu T (2013) MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environ Sci Pollut Res 20:5449–5460
Zhu XF, Lei 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
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31170225; 31201145), National Program on Key Basic Research Project (2012CB026105), Foundation of Science and Technology Program of Gansu Province (1208RJZA224), the National High Technology Research and Development Program (2007AA021401), and Foundation of Science and Technology Program of Gansu Province (1107RJYA005).
Author contribution
Yurong Bi was the mastermind, designed all experiments and polished the manuscript; Ping Li wrote the manuscript, carried out the quantitative reverse transcription PCR analysis, confocal microscopy, and fluorescence intensity analysis; Chengzhou Zhao measured H2O2, TBARS content, and enzyme activity; Xiaoyu Wang measured the fresh weight and the chlorophyll content and element content; Jianfeng Wang and Feng Wang carried out the determination of the IAA oxidase activity; Yongqiang Zhang and Xiaomin Wang helped in drafting the manuscript and interpretation of the results. All authors have read and approved the final manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Bhumi Nath Tripathi
Electronic supplementary material
Below is the link to the electronic supplementary material.
Table S1
(DOC 31 kb)
Rights and permissions
About this article
Cite this article
Li, P., Zhao, C., Zhang, Y. et al. Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma 253, 185–200 (2016). https://doi.org/10.1007/s00709-015-0810-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-015-0810-9