Sains Malaysiana 46(2)(2017): 189–195
http://dx.doi.org/10.17576/jsm-2017-4602-02
Nitric
Oxide Increases Pb Tolerance by Lowering Pb Uptake and Translocation
as well as Phytohormonal Changes in Cowpea (Vigna unguiculata
(L.) Walp.)
(Nitrik
Oksida Meningkatkan Toleransi Pb dengan Menurunkan pengambilan Pb
dan Translokasi serta Perubahan Fitohormon dalam Kacang Panjang
(Vigna unguiculata (L.) Walp.))
OMID SADEGHIPOUR*
Department of Agronomy, Yadegar-e-Imam Khomeini (RAH)
Shahre-rey Branch, Islamic Azad University, Tehran, Iran
Received: 11 August 2015/Accepted: 16 May 2016
ABSTRACT
Lead (Pb) is one of the most abundant toxic heavy metals which
adversely affected growth and yield of crop plants. Nitric oxide (NO),
an endogenous signaling molecule, has been suggested to be involved in defense
responses to biotic and abiotic stresses in plants. The present study was done
to induce Pb tolerance in cowpea plants by exogenous NO application
using two levels of Pb, 0 and 200 mg Pb (NO3)2 kg-1 soil
and three NO levels, 0, 0.5 and 1 mM sodium nitroprusside (SNP),
as NO donor. The results showed that Pb treatment caused a
significant increase in Pb concentration in all plant parts. Roots had higher
levels of Pb than the stems, leaves and seeds. Furthermore, lead toxicity
reduced auxin (IAA), cytokinin and gibberellic acid
(GA3) content but increased abscisic acid (ABA)
level. Moreover Pb stress decreased stomatal conductance, leaf area and
consequently seed yield of cowpea. Exogenous application of NO at
0.5 mM noticeably alleviated the lead toxicity by improving the leaf area,
stomatal conductance and seed yield. NO increased Pb tolerance by
lowering Pb uptake and translocation, enhancing the promoting phytohormone (IAA,
cytokinin and GA3) level and reducing ABA content.
Keywords: Leaf area; Pb toxicity; plant hormones; seed yield;
stomatal conductance
ABSTRAK
Plumbum (Pb) merupakan salah satu logam berat
toksik paling banyak yang telah menjejaskan pertumbuhan dan hasil tanaman
tumbuhan. Nitrik
oksida (NO), molekul isyarat endogen disyaki terlibat dalam
tindakan pertahanan terhadap stres biotik dan abiotik dalam tumbuh-tumbuhan. Kajian ini dijalankan untuk mengaruh toleransi Pb dalam tumbuhan kacang panjang
dengan aplikasi NO eksogen menggunakan dua tahap Pb, 0
dan 200 mg Pb (NO3)2 kg-1 tanih
dan tiga peringkat NO, 0, 0.5 dan 1 mM sodium nitroprusid
(SNP),
sebagai penderma NO. Keputusan kajian
menunjukkan bahawa rawatan Pb telah menyebabkan peningkatan ketara dalam
kepekatan Pb pada semua bahagian tumbuhan. Akar
mempunyai tahap Pb yang lebih tinggi daripada batang, daun dan biji benih. Selain itu, ketoksikan plumbum mengurangkan kandungan auksin
(IAA),
sitokinin dan asid giberelik (GA3) tetapi meningkatkan
tahap asid absisik (ABA). Tambahan
pula tekanan Pb mengurangkan konduktans stoma, keluasan daun dan penghasilan
biji benih kacang panjang. Aplikasi eksogen NO pada
0.5 mM didapati mengurangkan keracunan plumbum dengan memperbaiki keluasan
daun, konduktans stoma dan hasil biji benih. NO meningkatkan
toleransi Pb dengan mengurangkan penyerapan Pb dan translokasi, menggalakkan
peningkatan tahap fitohormon (IAA, sitokinin dan GA3)
serta mengurangkan kandungan ABA.
Kata kunci: Hasil benih;
hormon tumbuhan; keluasan daun; ketoksikan PB; konduktans stoma
REFERENCES
An, L., Liua, Y., Zhanga, M.,
Chen, T. & Wang, X. 2005. Effects of nitric oxide on growth of maize
seedling leaves in the presence or absence of ultraviolet-B radiation. Journal
of Plant Physiology 162: 317-326.
Atici, O., Agar, G. & Battal, P. 2005.
Changes in phytohormone contents in chickpea seeds germinating under lead or
zinc stress. Biologia Plantarum 49(2): 215-222.
Ayanwuyi, E. & Akintonde, J.O. 2012. Effect
of climate change on cowpea production in kuje area council, abuja,
nigeria. International Journal of Advanced Research in Management and Social
Sciences 1(2): 273-283.
Balba, A.M., El Shibiny, G. & El Khatib, E.
1991. Effect of lead increments on the yield and lead content
of tomato plants. Water, Air & Soil Pollution 57-58(1):
93-99.
Beligni, M.V. & Lamattina, L. 2000. Nitric
oxide stimulates seed germination and de-etiolation and inhibits hypocotyls
elongation, three light inducible responses in plants. Planta 210:
215-221.
Bhardwaj, P., Chaturvedi, A.K. & Prasad, P.
2009. Effect of enhanced lead and cadmium in soil on physiological and
biochemical attributes of Phaseolus vulgaris L. Natural Science 7(8):
63-75.
Bharwana, S.A., Ali, S.,
Farooq, M.A., Iqbal, N., Hameed, A., Abbas, F. & Ahmad, M.S.A. 2014. Glycine betaine-induced lead toxicity tolerance
related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake
and oxidative stress in cotton. Turkish Journal of Botany 38: 281-292.
Cenkci, S., Cigerci, I.H.,
Yildiz, M., Özay, C., Bozdag, A. & Terzi, H. 2010. Lead contamination reduces chlorophyll
biosynthesis and genomic template stability in Brassica rapa L. Environmental and Experimental Botany 67(3): 467-473.
Chatterjee, C., Dube, B.K., Sinha, P. &
Srivastava, P. 2004. Detrimental effects of lead
phytotoxicity on growth, yield and metabolism of rice. Communications
in Soil Science and Plant Analysis 35: 255-265.
Eick, M.J., Peak, J.D.,
Brady, P.V. & Pesek, J.D. 1999. Kinetics of lead absorption/ desorption on goethite: residence
time effect. Soil Science 164: 28-39.
Elzbieta, W. & Miroslawa,
C. 2005. Lead-induced
histological and ultrastructural changes in the leaves of soybean (Glycine
max (L.) Merr.). Soil Science and Plant Nutrition 51(2):
203-212.
Esim, N. & Atici, O. 2013. Nitric oxide alleviates boron
toxicity by reducing oxidative damage and growth inhibition in maize seedlings (Zea mays L.). Australian
Journal of Crop Science 7(8): 1085-1092.
Fernandes, J.E. & Henriques, F.S. 1991. Biochemical, physiological and structural effects of excess copper
in plants. Botanical Review 57: 246-273.
Garcia-Mata, C. & Lamattina, L.
2001. Nitric oxide induces stomatal closure
and enhances the adaptive plant responses against drought stress. Plant
Physiology 126: 1196-1204.
Gouvea, C.M.C.P., Souza, J.F., Magalhaes, C.A.N. &
Martins, I.J. 1997. NO-releasing substances that induce growth elongation in
maize root segments. Plant Growth Regulation 21: 183-187.
Habib, N., Ashraf, M. & Shahbaz, M.
2013. Effect of exogenously applied nitric
oxide on some key physiological attributes of rice (Oryza sativa L.)
plants under salt stress. Pakistan Journal of Botany 45(5): 1563-1569.
Hasanuzzaman, M., Nahar, K., Alam, M.M.
& Fujita, M. 2012. Exogenous nitric
oxide alleviates high temperature induced oxidative stress in wheat (Triticum
aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase
system. Australian Journal of Crop Science 6(8): 1314-1323.
Hayat, S., Hasan, S.A., Mori, M.,
Fariduddin, Q. & Ahmad, A. 2010. Nitric Oxide in Plant Physiology. Nitric Oxide:
Chemistry, Biosynthesis, and Physiological Role. Weinheim: Wiley-VCH Verlag
GmbH & Co. KGaA.
He, J.M., Xu, H., She, X.P., Song, X.G.
& Zhao, W.M. 2005. The
role and the interrelationship of hydrogen peroxide and nitric oxide in the
UV-B-induced stomatal closure in broad bean. Functional Plant Biology 32: 237-247.
Hussain, M., Ahmad, M.S.A. &
Kausar, A. 2006. Effect of lead and
chromium on growth, photosynthetic pigments and yield components in mash
bean [Vigna mungo (L.) Hepper]. Pakistan Journal of Botany 38:
1389-1396.
Iqbal, J. & Mushtaq, S. 1987. Effect
of lead on germination, early seedling growth, soluble protein and acid
phosphatase content in Zea mays. Pakistan Journal of
Scientific and Industrial Research 30: 853-856.
Islam, E., Yang, X., Li, T., Liu, D.,
Jin, X. & Meng, F. 2007. Effect of Pb toxicity on root morphology, physiology and
ultrastructure in the two ecotypes of Elsholtzia argyi. Journal
of Hazardous Materials 147(3): 806-816.
Jhanji, S., Setia, R.C., Kaur, N.,
Kaur, P. & Setia, N. 2012. Role of
nitric oxide in cadmium-induced stress on growth, photosynthetic components and
yield of Brassica napus L. Journal of Environmental Biology 33:
1027-1032.
Jiang, W. & Liu, D. 2010. Pb-induced cellular defense system in the root meristematic
cells of Allium sativum L. BMC Plant Biology 10: 40.
Kausar, F., Shahbaz, M. & Ashraf,
M. 2013. Protective role of
foliar-applied nitric oxide in Triticum aestivum under saline stress. Turkish Journal of Botany 37: 1155-1165.
Kopittke, P.M., Asher, C.J., Kopittke, R.A. & Menzies,
N.W. 2007. Toxic effects of Pb2+ on
growth of cowpea (Vigna unguiculata). Environmental Pollution 150(2):
280-287.
Kumari, A., Sheokand, S. & Swaraj,
K. 2010. Nitric oxide induced alleviation of
toxic effects of short term and long term Cd stress on growth, oxidative
metabolism and Cd accumulation in chickpea. Brazilian Journal of Plant
Physiology 22(4): 271-284.
Lane, S.D. & Martin, E.S. 1977. A
histochemical investigation of lead uptake in Raphanus sativus. New
Phytologist 79(2): 281-286.
Liao, Y., Chien, S.C., Wang, M., Shen,
Y., Hung, P. & Das, B. 2006. Effect
of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere. Chemosphere 65(2):
343-351.
Liu, X., Wang, L., Liu, L., Guo, Y.
& Ren, H. 2011. Alleviating effect
of exogenous nitric oxide in cucumber seedling against chilling stress. African
Journal of Biotechnology 10(21): 4380-4386.
Marschner, H. 1995. Mineral Nutrition
of Higher Plants. 2nd ed. New York:
Academic Press.
Nagajyoti, P.C., Lee, K.D. &
Sreekanth, T.V.M. 2010. Heavy metals,
occurrence and toxicity for plants: A review. Environmental Chemistry
Letters 8: 199-216.
Neill, S.J., Desikan, R. & Hancock, J. 2003. Nitric oxide as a mediator of ABA signaling in stomatal guard
cells. Bulgarian Journal of Plant Physiology (Special Issue):
124-132.
Pagnussat, G., Simontachi, M.,
Puntarulo, S. & Lamattina, L. 2002. Nitric oxide is required for root organogenesis. Plant Physiology 129:
954-956.
Pourrut, B., Shahid, M., Dumat, C.,
Winterton, P. & Pinelli, E. 2011. Lead
uptake, toxicity, and detoxification in plants. Reviews of Environmental
Contamination and Toxicology 213: 113-136.
Seregin, I.V., Shpigun, L.K. & Ivanov, V.B. 2004. Distribution and toxic effects of cadmium and lead on maize roots. Russian Journal of Plant Physiology 51(4): 525-533.
Sharma, P. & Dubey, R.S. 2005. Lead toxicity in plants. Brazilian
Journal of Plant Physiology 17(1): 35-52.
Shehab, G.G., Ahmed, O.K. & EL-Beltagi, H.S. 2010.
Effects of various chemical agents for alleviation of drought stress in rice
plants (Oryza sativa L.). Notulae Botanicae Horti Agrobotanici
Cluj-Napoca 38(1): 139-148.
Shindy, W.W. & Smith, O.E. 1975. Identification of plant hormones from
cotton ovules. Plant Physiology 55: 550-554.
Singh, P.H., Kaur, S., Daizy, R., Batish, V.P., Sharma, N.
& Kohli, R.K. 2009. Nitric oxide alleviates arsenic toxicity by reducing
oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:
289-297.
Tan, J., Zhao, H., Hong, J., Han, Y.,
Li, H. & Zhao, W. 2008. Effects
of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline
accumulation in wheat seedlings subjected to osmotic stress. World Journal
of Agricultural Sciences 4(3): 307-313.
Tanton, T.W. & Crowdy, S.H. 1971. The
distribution of lead chelate in the transpiration stream of higher plants. Pesticide Science 2(5): 211-213.
Verbruggen, N., Hermans, C. &
Schat, H. 2009. Molecular mechanisms
of metal hyperaccumulation in plants. New Phytologist 181:
759-776.
Veselov, D., Kudoyarova, G., Symonyan,
M. & Veselov, S.T. 2003. Effect of cadmium on ion uptake, transpiration and cytokinin
content in wheat seedlings. Bulgarian Journal of Plant Physiology (Special
Issue): 353-359.
Wang, Y.S. & Yang, Z.M. 2005. Nitric oxide reduces
aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant and Cell Physiology 46: 1915-1923.
Yakhin,
O.I., Yakhin, I.A., Lubyanov, A.A. & Vakhitov, V.A. 2009. Effect of cadmium
on the content of phytohormones and free amino acids, its cytogenetic effect,
and accumulation in cultivated plants. Doklady Biological Sciences 426:
274- 277.
*Corresponding
author; email: osadeghipour@yahoo.com
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