Abstract
Changes in growth parameters, root and leaf anatomy, and stress hormone contents in Cd-stressed soybean (Glycine max L.) seedlings were investigated. Under treatment with 40 µM CdCl2, the whole plant, root and leaf FW and DW significantly decreased. Also, the whole plant and root length decreased, as well as the chlorophyll and carotenoid contents. This heavy metal affected root and leaf anatomy. In comparison to control, root diameter increased as a consequence of the greater size of the cortex and the vascular cylinder area, and vascular tissues were markedly affected by Cd. In leaflets, the curvature of the mesophyll in internerval areas was observed after Cd treatment. Cd also affected the mesophyll thickness which was reduced by the presence of shorter and narrower cells of the palisade parenchyma. Jasmonic acid content dropped dramatically in Cd-stressed roots, meanwhile ABA and metabolites increased at different times of Cd stress suggesting their involvement in Cd response. ABA peaked at 24 h of Cd stress whereas a strong peak of ABA-GE appeared immediately after the ABA peak. DPA started increasing at 6 h of Cd treatment and the highest peak was recorded at 24 h, as well as the ABA peak. The DPA and ABA-GE contents were higher than the ABA ones Therefore, the alterations induced by the Cd-phytotoxic effect on the growth and anatomy of the soybean seedlings as well as on the ABA and JA root content suggest a possible involvement of these hormones on the sensing and response mediation of these compounds in the organ that first senses the stress.
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Abbreviations
- ABA:
-
Abscisic acid
- ABA-GE:
-
Abscisic acid glucose ester
- Cd:
-
Cadmium
- DPA:
-
Dihydrophaseic acid
- JA:
-
Jasmonic acid
References
Abdo FA, Nassar DMA, Gomaa EF, Nassar RMA (2012) Minimizing the harmful effects of cadmium on vegetative growth, leaf anatomy, yield and physiological characteristics of soybean plant Glycine max (L.) Merrill] by foliar spray with active yeast extract or with garlic cloves extract. Re J Agr Biol Sci 8:24–35
Agronoticias América Latina y el Caribe (2013). Investigan la contaminación por cadmio y arsénico en la producción de soja en Argentina. (For more information: Latin American and Caribbean Agronews: Cadmium and arsenic contamination in Argentine soybean was investigated). http://www.fao.org/agronoticias/agro-noticias/detalle/es/c/209282/
Anjum SA, Xie X, Wang L, Sallem (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032
Atıcı Ö, Agar G, Battal P (2003) Interaction between endogenous plant hormones and α-amylase in germinating chickpea seeds under cadmium exposure. Fresenius Environ Bull 12:781–785
Banerjee S, Flores-Rozas H (2005) Cadmium inhibits mismatch repair by blocking the ATPase activity of the MSH2–MSH6 complex. Nucleic Acids Res 33:1410–1419
Barceló J, Poschenrieder C (1990) Plant water relation as affected by heavy metal stress: a rewire. J Plant Nutr 13:1–37
Baron KN, Schroeder DF, Stasolla C (2012) Transcriptional response of abscisic acid (ABA) metabolism and transport to cold and heat stress applied at the reproductive stage of development in Arabidopsis thaliana. Plant Sci 189:48–59
Benabid H, Fouzi Ghorab M (2012) Is the decrease of chlorophyll first alert of pollution? A study of the effect of cadmium on chlorophyll content of Canadian wonder beans (Phaseolus vulgaris). Int Conf Chem Civ Environ Eng 279–282
Benavides MP, Gallego SM, Tomaro M (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Clemens S (2006) Evolution and function of phytochelatin synthases. J Plant Physiol 163:319–332
Dal Corso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Beha 5:663–667
Dražić G, Mihailovic N, Stojanovic Z (2004) Cadmium toxicity: the effect on macro-and micronutrients contents in soybean seedlings. Biol Plant 48:605–607
Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442
Ernst WHO, Verkleji JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248
Fediuc E, Lips SH, Erdei L (2005) O-Acetylserine (thiol) lyase activity in Phragmities and Typha plants under cadmium and NaCl stress conditions and the involvement of ABA in the stress response. J Plant Physiol 162:865–872
Finkelstein R, Gibson SI (2002) ABA and sugar interactions regulating development: ‘cross-talk’ or ‘voices in a crowd’? Curr Opin Plant Biol 5:26–32
Fujimaki S, Suzui N, Ishioka NS, Kawachi N, Ito S, Chino M, Nakamura S (2010) Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152:1796–1806
Fusconi A, Gallo C, Camusso W (2007) Effects of cadmium on root apical meristems of Pisum sativum L. cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat Res 632:9–19
Gidda SK, Miersch O, Levitin A, Schmidt J, Wasternack C, Varin L (2003) Biochemical and molecular characterization of a hydroxyjasmonate sulfotransferase from Arabidopsis thaliana. J Biol Chem 278:17895–17900
Groppa MD, Ianuzzo MP, Tomaro ML, Benavides MP (2007) Polyamine metabolism in sunflower plants under long-term cadmium or copper stress. Amino Acids 32:265–275
Hamann T, Bennett M, Mansfield J, Somerville C (2009) Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J 57:1015–1026
Hassan MJ, Shao G, Zhang G (2005) Influence of cadmium toxicity on antioxidant enzymes activity in rice cultivars with different grain Cd accumulation. J Plant Nutr 28:1259–1270
Hernández-Blanco C, Feng DX, Hu J, Sánchez-Vallet A, Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X, Sánchez-Rodríguez C, Anderson LK, Somerville S, Marco Y, Molina A (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19:890–903
Hsu YT, Kao CH (2008) Distinct roles of abscisic acid in rice seedlings during cadmium stress at high temperature. Bot Stud 49:335–342
Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3007
Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43
Jin YH, Clark AB, Slebos RJ, Al-Refai H, Taylor JA, Kunkel TA, Resnick MA, Gordenin DA (2003) Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat Genet 34:326–329
Johansen DA (1940) Plant Microtechnique VI–VII. Mc-Graw-Hill Book, New York 523
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoides and chlrophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2011) Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plant 55:187–190
Lunácková L, Masarovicová E, Král’ová K, Stresko V (2003) Response of fast growing woody plants from family Salicaceae to cadmium treatment. Bull Environ Contam Toxicol 70:576–585
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Maksimović Z, Petrović S, Pavlović M, Kovacević N, Kukić J (2007) Antioxidant activity of Filipendula hexapetala flowers. Fitoterapia 78:265–267
Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187
Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346
Ministerio de agricultura, ganadería y pesca, Presidencia de la Nación. (For more information: Ministry of Agriculture, Livestock and Fisheries. Presidency of the Nation). http://www.minagri.gob.ar/site/index.php
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
Pérez-Chaca MV, Rodríguez-Serrano M, Molina AS, Pedranzani HE, Zirulnik F, Sandalio LM, Romero-Puertas MC (2014) Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant Cell Environ. doi: 10.1111/pce.12280. [Epub ahead of print]
Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590
Popova L, Maslenkova L, Yordanova R, Krantev A, Szalai G, Janda T (2008) Salicylic acid protects photosynthesis against cadmium toxicity in pea plants. Gen Appl Plant Physiol 34:133–148
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156
Pribyl P, Cepak V, Zachleder V (2005) Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals esposure: I. The effect of cadmium. Protoplasma 226:231–240
Ranieri A, Castagna A, Scebba F, Careri M, Zagnoni I, Predieri G, Massimo Pagliari M, Sanità di Toppi L (2005) Oxidative stress and phytochelatin characterisation in bread wheat exposed to cadmium excess. Plant Physiol Biochem 43:45–54
Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278
Ren H, Gao Z, Chen L, Wei K, Liu J, Fan Y, Davies WJ, Jia W, Zhang J (2007) Dynamic analysis of ABA accumulation in relation to the rate of ABA catabolism in maize tissues under water deficit. J Exp Bot 58:211–219
Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544
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
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Sheirdil RA, Bashir K, Hayat R, Akhtar MS (2012) Effect of cadmium on soybean (Glycine max L.) growth and nitrogen fixation. Afr J Biotechnol 11:1886–1891
Smiri M (2011) Effect of cadmium on germination, growth, redox and oxidative properties in Pisum sativum seeds. J Environ Chem Ecotoxicol 3:52–59
Somashekaraia BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris) involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89
Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedling. Plant Biotechnol 22:19–25
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot. doi:10.1093/jxb/ert485
Ubeda-Tomás S, Beemster GTS, Bennett MJ (2012) Hormonal regulation of root growth: integrating local activities into global behaviour. Trends Plant Sci 17:326–331
Voutsinas G, Zarani FE, Kappas A (1997) The effect of environmental aneuploidy-inducing agents on the microtubule architecture of mitotic meristematic root cells in Hordeum vulgare. Cell Biol Int 21:411–418
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058
Wei H, Meilan R, Brunner AM, Skinner JS, Ma C, Gandhi HT, Strauss SH (2007) Field trial detects incomplete barstar attenuation of vegetative cytotoxicity in Populus trees containing a poplar LEAFY promoter: barnase sterility transgene. Mol Breeding 19:69–85
Wu F, Chen F, Wei K, Zhang GP (2004) Effect of cadmium on free aminoacid, glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57:447–454
Ye N, Jia L, Zhang J (2012) ABA signal in rice under stress conditions. Rice 5:1–9
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Pérez Chaca, M.V., Vigliocco, A., Reinoso, H. et al. Effects of cadmium stress on growth, anatomy and hormone contents in Glycine max (L.) Merr.. Acta Physiol Plant 36, 2815–2826 (2014). https://doi.org/10.1007/s11738-014-1656-z
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DOI: https://doi.org/10.1007/s11738-014-1656-z