Abstract
Aluminum-induced exudation of organic acids from roots has been proposed as a mechanism for Al tolerance in plants. To better understand the regulatory process leading to efflux of organic acids, the possible involvement of salicylic acid (SA) in regulating Al-induced citrate release in Cassia tora L. was identified. The response of citrate efflux to exogenous SA was concentration-dependent. Application of SA at 5 μM in solution containing 20 μM Al increased citrate efflux to levels 1.76-fold higher than in controls (20 μM Al alone). However, inhibition of citrate release was observed when SA concentrations increased to more than 20 μM. Increased citrate efflux due to the SA treatment was associated with decreased inhibition of root growth and Al content in root tips, suggesting that exogenous SA could confer Al tolerance by increasing citrate efflux. We also examined citrate synthase activities (EC 4.1.3.7) and citrate concentrations in root tips exposed to Al and/or SA. However, both citrate synthase activities and citrate accumulation remained unaffected. These results indicate that SA-promotion of Al-induced citrate efflux is not correlated with increase in citrate production. Total endogenous SA concentrations were measured in root tips and the SA concentrations were significantly enhanced by Al at levels of 10–50 μM.
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Abbreviations
- CS:
-
citrate synthase
- SA:
-
salicylic acid
References
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
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Dat JF, Christine H, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455-1461
Delhaize ED, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) Ⅱ. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702
Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180
Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279
Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260
Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and aluminum-resistant cultivar. Plant Physiol 126:397–410
Li XF, Ma JF, Matsumoto H (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol 123:1537–1543
Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38:1019–1025
Malamy J, Klessig DF (1992) Salicylic acid and plant disease resistance. Plant J 2:643–654
Martínez-Estévez M, Loyola-Vargas VM, Teresa Hernández-Sotomayor SM (2001) Aluminum increases phosphorylation of particular proteins in cellular suspension cultures of coffer (Coffea arabica). J Plant Physiol 158:1375–1379
Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biol Plant 42:409–415
Miyasaka SC, Buta JG, Howeel RK, Foy CD (1991) Mechanisms of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol 96:737–743
Osawa H, Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol 126:411–420
Piñeros MA, Kochian LV (2001) A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol 125:292–305
Raskin I, Turner IM, Melander WR (1989) Regulation of heat production in the inflorescences of an arum lily by endogenous salicylic acid. Proc Natl Acad Sci USA 86:2214–2218
Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110
Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD (1997) Aluminum activates an anion channel in the apical cells of wheat roots. Proc Natl Acad Sci USA 94:6547–6552
Sharma YK, León J, Raskin I, Davis KR (1996) Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci USA 93:5099–5104
Wang SC, Xu LL, Li GJ, Chen PY, Xia K, Zhou X (2002) An ELISA for the determination of salicylic acid in plants using a monoclonal antibody. Plant Sci 162:529–535
Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid and pathogenesis-related proteins and virus resistance in tobacco. Planta 193:373–376
Yang H,Wong JWC, Yang ZM, Zhou LX (2001) The ability of Agrogyron elongatum to accumulate the single metal of cadmium, copper, nickel and lead and root exudation of organic acids. J Environ Sci 13:368–375
Yang ZM, Ma JF (2003) Aluminum regulation of citrate metabolism and possible activation of anion transporter for Al-induced citrate efflux in the roots of Cassia tora L. Physiol Plant (in press)
Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumoto H (2001) Characterization of aluminum-induced citrate secretion in aluminum-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71
Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9:809–824
Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat: Ⅰ. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117:745–751
Acknowledgements
The authors gratefully acknowledge the expert technical assistance of Dr. Hong Yang (Department of Applied Chemistry, College of Science, Nanjing Agricultural University.). This work was supported by the project sponsored by the Scientific Research Foundation for Returned Overseas Chinese Scholars, State Education Ministry.
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Yang, ZM., Wang, J., Wang, SH. et al. Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L.. Planta 217, 168–174 (2003). https://doi.org/10.1007/s00425-003-0980-0
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DOI: https://doi.org/10.1007/s00425-003-0980-0
Keywords
- Aluminum
- Cassia
- Citrate efflux
- Root elongation
- Salicylic acid