Sains Malaysiana 46(10)(2017): 1687–1691


Nitric Oxide Accelerates Mycorrhizal Effects on Plant Growth and Root Development of Trifoliate Orange

(Nitrik Oksida Mempercepatkan Kesan Mikoriza ke atas Pertumbuhan Pokok dan Perkembangan Akar Oren Trifoliat)





1College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025



2Institute of Root Biology, Yangtze University, Jingzhou, Hubei 434025, China


3Department of Plant Sciences, Quaid-I-Azam University, Islamabad, Pakistan


4Department of Biology and Ecology, Nankai University, Tianjin, China


5Department of Chemistry, Faculty of Science, University of Hradec Kralove, Hradec Kralove,

Czech Republic


Received: 24 January 2017Accepted: 31 March 2017



Arbuscular mycorrhizal fungi (AMF) actively colonize plant roots and thus enhance plant growth through different mechanisms. In the present study, trifoliate orange (Poncirus trifoliata) seedlings inoculated with Diversispora versiformis were subjected to 0 and 0.2 mmol/L sodium nitroprusside (SNP, a nitric oxide donor) treatments. After eight weeks, exogenous SNP considerably increased root mycorrhizal colonization by 25%, showing a positive stimulating effect of NO on mycorrhizal formation. Mycorrhizal inoculation significantly increased plant growth performance (height, stem diameter, leaf number and shoot and root dry weight) and root traits (length, projected area, surface area, volume and number of 2nd and 3rd order lateral roots) than non-mycorrhizal treatment and NO (exogenous SNP treatment) heavily strengthened the mycorrhizal effects. Moreover, NO and mycorrhization induced more fine root (0-0.5 cm) formation. There was an opposite changed trend in root sucrose and leaf and root glucose contents by SNP in AMF versus non-AMF seedlings. All these results implied that NO plays important roles in mycorrhizal formation and development and also accelerates mycorrhizal effects on plant growth and root development of trifoliate orange.


Keywords: Arbuscular mycorrhizal fungi; carbohydrate; citrus; nitric oxide; sodium nitroprusside



Kulat mikoriza arbuskula (AMF) mengkoloni akar tumbuhan secara aktif dan seterusnya menggalakkan pertumbuhan pokok melalui mekanisme berbeza. Dalam kajian ini, benih oren trifoliat (Poncirus trifoliata) yang diinokulasi dengan Diversispora versiformis telah diberikan rawatan 0 dan 0.2 mmol/L sodium nitropussida (SNP, penderma nitrik oksida). Selepas lapan minggu, SNP eksogenus didapati meningkatkan pengkolonian akar mikoriza sebanyak 25% dan ini menunjukkan kesan rangsangan positif NO terhadap pembentukan mikoriza. Penginokulasian mikoriza meningkatkan prestasi pertumbuhan pokok secara signifikan (tinggi, diameter batang, jumlah daun dan berat akar kering) dan ciri akar (panjang, luas unjuran, luas permukaan, isi padu, bilangan akar lateral peringkat ke-2 dan ke-3) berbanding rawatan tanpa mikoriza serta NO (rawatan SNP eksogenus) mengukuhkan lagi kesan mikoriza. Di samping itu, rawatan NO dan mikoriza mengaruh lebih banyak pembentukan akar halus (0-0.5 cm). Terdapat trend perubahan bertentangan pada kandungan sukrosa akar, daun serta glukosa akar oleh SNP dalam benih AMF berbanding tanpa AMF. Keseluruhan keputusan kajian ini menunjukkan bahawa NO memainkan peranan penting dalam pembentukan dan perkembangan mikoriza, malah mempercepatkan kesan mikoriza ke atas pertumbuhan pokok dan perkembangan akar oren trifoliat.


Kata kunci: Cendawan mikoriza asbukula; karbohidrat; nitrik oksida; sitrus; sodium nitroprusside


Arenas-Huertero, F., Arroyo, A., Zhou, L., Sheen, J. & Leon, P. 2000. Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes and Development 14: 2085-2096.

Augin, O., Mansilla, J.P., Vilarioo, A. & Sainz, M.J. 2004. Effects of mycorrhizal inoculation on root morphology and nursery production of three grapevine rootstocks. American Journal of Enology and Viticulture 55: 108-111.

Bago, B., Pfeffer, P.E. & Shachar-Hill, Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124: 949-958.

Berta, G., Fusconi, A., Trotta, A. & Scannerini, S. 1990. Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytologist 114: 207-215.

Calcagno, C., Novero, M., Genre, A., Bonfante, P. & Lnafranco, L. 2012. The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots. Mycorrhiza 22: 259-269.

Correa-Aragunde, N., Graziano, M., Chevalier, C. & Lamattina, L. 2006. Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. Journal of Experimental Botany 57: 581-588.

Correa-Aragunde, N., Graziano, M. & Lamattina, L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218: 900-905.

Cueto, M., Hernández-Perera, O. & Martín, R. 1996. Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Letters 398(2-3): 159-164.

Fernández-Marcos, M., Sanz, L., Lewis, D.R., Muday, G.K. & Lorenzo, O. 2011. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proceedings of the National Academy of Sciences USA 108: 18506-18511.

Gadkar, V., David-Schwartz, R., Kunik, T. & Kapulnik, Y. 2001. Arbuscular mycorrhizal fungi colonization. Factors involved in host recognition. Plant Physiology 127: 1493-1499.

Hu, M.Y., Li, H., Zhang, Y.J. & Liu, Q. 2009. Photosynthesis and related physiological characteristics affected by exogenous glucose in wheat seedlings under water stress. Acta Agronomica Sinica 35: 724-732 (in Chinese with English abstract).

Leshem, Y.Y. & Wills, R.B.H. 1998. Harnessing senescence delaying gases nitric oxide and nitrous oxide: A novel approach to postharvest control of fresh horticultural produce. Biologia Plantarum 41: 110-117.

Meixner, C., Vegvari, G., Ludwig-Müller, J., Gagnon, H., Steinkellner, S., Staeahelin, C., Gresshoff, P. & Vierheilig, H. 2007. Two defined alleles of the LRR receptor kinase GmNARK in supernodu-lating soybean govern differing autoregulation of mycorrhization. Physiologia Plantarum 130: 261-270.

Pagnussat, G.C., Simontacch, I.M., Puntarulo, S. & Lamattina, L. 2002. Nitric oxide is required for root organogenesis. Plant Physiology 129: 954-956.

Puppo, A., Pauly, N., Boscari, A., Mandon, K. & Brouquisse, R. 2013. Hydrogen peroxide and nitric oxide: Key regulators of the legume-rhizobium and mycorrhizal symbioses. Antioxidants and Redox Signaling 18: 2202-2219.

Sorgona, A., Abenavoli, M.R., Gringeri, P.G., Lupini, A. & Cacco, G. 2007. Root architecture plasticity of citrus rootstocks in response to nitrate availability. Journal of Plant Nutrition 30: 1921-1932.

Wu, Q.S. 2010. Arbuscular Mycorrhizal Research and Application of Horticultural Plants. Beijing: Science Press (in Chinese).

Wu, Q.S., Cao, M.Q., Zou, Y.N., Wu, C. & He, X.H. 2016. Mycorrhizal colonization represents functional equilibrium on root morphology and carbon distribution of trifoliate orange grown in a split-root system. Scientia Horticulture 199: 95-102.

Wu, Q.S., Srivastava, A.K. & Li, Y. 2015. Effect of mycorrhizal symbiosis on growth behavior and carbohdyrate metabolism of trifoliate orange under different substrate P levels. Journal of Plant Growth Regulation 34: 495-508.

Wu, Q.S., Zou, Y.N., He, X.H. & Luo, P. 2011. Arbuscular mycorrhizal fungi can alter some root characters and physiological status in trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Plant Growth Regulation 65: 273-278.

Wu, Q.S., Peng, Y.H., Zou, Y.N. & Liu, C.Y. 2010. Exogenous polyamines affect mycorrhizal development of Glomus mosseae-colonized citrus (Citrus tangerine) seedlings. ScienceAsia 36: 254-258.

Xiong, J., Lu, H., Lu, K., Duan, Y.X., An, L.Y. & Zhu, C. 2009. Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is in dispensable for crown root primordia initiation in rice seedlings. Planta 230: 599- 610.

Yao, Q., Wang, L.R., Zhu, H.H. & Chen, J.Z. 2009. Effect of arbusuclar mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Scientia Horticulturae 121: 458-461.



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