Please wait a minute...
Journal of Arid Land  2017, Vol. 9 Issue (1): 143-152    DOI: 10.1007/s40333-016-0027-6
Orginal Article     
Mycorrhizal colonization of chenopods and its influencing factors in different saline habitats, China
Yinan ZHAO, Hongqing YU, Tao ZHANG*(), Jixun GUO*()
Institute of Grassland Science, Northeast Normal University, Key Laboratory of Vegetation Ecology, Ministry of Education, Changchun 130024, China
Download: HTML     PDF(396KB)
Export: BibTeX | EndNote (RIS)      


Chenopodiaceae is one of the most important families in arid and saline environments. Several studies have observed the mycorrhizal structure in Chenopodiaceae plants (i.e., chenopods), but the mycorrhizal colonization status of chenopods in saline habitats and the influencing factors are still not well understood. The mycorrhizal colonization of twenty chenopod species in three different saline habitats (a saline alkaline meadow in the Songnen Plain of northeastern China, a saline desert in the Junggar Basin of northwestern China, and a saline alpine meadow in the Tibetan Plateau of western China) and the chenopod-associated environmental factors (including soil moisture, soil available phosphorous (P) concentration, pH, and salt content) were analyzed. Our results showed that approximately 60% of the studied chenopods were colonized by arbuscular mycorrhizal (AM) fungi with a colonization percentage ranging from 5% to 33%. Structural analysis of mycorrhizal association indicated that vesicles were quite common, while arbuscules and hyphal coils were relatively rare. In addition, a positive correlation between mycorrhizal colonization rate and soil electrical conductivity (r=0.920, P<0.01) and two negative correlations of mycorrhizal colonization rates with soil moisture (r= -0.818, P<0.01) and the soil available P concentration (r= -0.876, P<0.01) confirmed that mycorrhizal colonization rate in the roots of chenopods was environment-dependent.

Key wordsadaptation      arbuscular mycorrhizal fungi      Chenopodiaceae      salinization      restoration     
Received: 10 July 2016      Published: 31 July 2017
Corresponding Authors: Tao ZHANG,Jixun GUO     E-mail:;
Cite this article:

Yinan ZHAO, Hongqing YU, Tao ZHANG, Jixun GUO. Mycorrhizal colonization of chenopods and its influencing factors in different saline habitats, China. Journal of Arid Land, 2017, 9(1): 143-152.

URL:     OR

1 Aguilera L E, Gutierrez J R, Moreno R J.1998. Vesiculo arbuscular mycorrhizae associated with saltbushes Atriplex spp. (Chenopodiaceae) in the Chilean arid zone. Revista Chilena de Historia Natural, 71: 291-302.
2 Aleman R, Tiver F.2010. Endomycorrhizal infection levels among chenopod plant species at port wakefield, south Australia. Transactions of the Royal Society of South Australia, 134(1): 1-4.
3 Aliasgharzadeh N, Rastin S N, Towfighi H, et al.2001. Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza, 11(3): 119-122.
4 Allen E B, Allen M F.1986. Water relations of xeric grasses in the field: interactions of mycorrhizas and competition. New Phytologist, 104(4): 559-571.
5 Allen M F.1983. Formation of vesicular-arbuscular mycorrhizae in Atriplex gardneri (Chenopodiaceae): seasonal response in a cold desert. Mycologia, 75(5): 773-776.
6 Allen M F, Allen E B.1990. Carbon source of VA mycorrhizal fungi associated with Chenopodiaceae from a semiarid shrub-steppe. Ecology, 71(5): 2019-2021.
7 Asghari H R, Marschner P, Smith S E, et al.2005. Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant and Soil, 273(1-2): 245-256.
8 Balzergue C, Puech-Pagès V, Bécard G, et al.2011. The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. Journal of Experimental Botany, 62(3): 1049-1060.
9 Barrow J R, Havstad K M, McCaslin B D.1997. Fungal root endophytes in fourwing saltbush, Atriplex canescens, on arid rangelands of southwestern USA. Arid Soil Research and Rehabilitation, 11(2): 177-185.
10 Bouwmeester H J, Roux C, Lopez-Raez J A, et al.2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends in Plant Science, 12(5): 224-230.
11 Bruce A, Smith S E, Tester M.1994. The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytologist, 127(3): 507-514.
12 Camenzind T, Hempel S, Homeier J, et al.2014. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biology, 20(12): 3646-3659.
13 Chandrasekaran M, Boughattas S, Hu S J, et al.2014. A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza, 24(8): 611-625.
14 Coughlan A P, Dalpé Y, Lapointe L, et al.2000. Soil pH-induced changes in root colonization, diversity, and reproduction of symbiotic arbuscular mycorrhizal fungi from healthy and declining maple forests. Canadian Journal of Forest Research, 30(10): 1543-1554.
15 Daleo P, Fanjul E, Casariego A M, et al.2007. Ecosystem engineers activate mycorrhizal mutualism in salt marshes. Ecology Letters, 10(10): 902-908.
16 Evelin H, Kapoor R, Giri B.2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany, 104(7): 1263-1280.
17 Glenn E P, O'Leary J W, Watson M C, et al.1991. Salicornia bigelovii Torr.: an oilseed halophyte for seawater irrigation. Science, 251(4997): 1065-1067.
18 Gollotte A, van Tuinen D, Atkinson D.2004. Diversity of arbuscular mycorrhizal fungi colonizing roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza, 14(2): 111-117.
19 Hepper C M.1984. Regulation of spore germination of the vesicular-arbuscular mycorrhizal fungus Acaulospora laevis by soil pH. Transactions of the British Mycological Society, 83(1): 154-156.
20 Hildebrandt U, Janetta K, Ouziad F, et al.2001. Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza, 10(4): 175-183.
21 Hirrel M C, Mehravaran H, Gerdemann J W.1978. Vesicular-arbuscular mycorrhizae in the Chenopodiaceae and Cruciferae: do they occur?. Canadian Journal of Botany, 56(22): 2813-2817.
22 Hodge A, Fitter A H.2010. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America, 107(31): 13754-13759.
23 Ingleby K, Fahmer A, Wilson J, et al.2001. Interactions between mycorrhizal colonisation, nodulation and growth of Calliandra calothyrsus seedlings supplied with different concentrations of phosphorus solution. Symbiosis, 30(1): 15-28.
24 Jakobsen I, Abbott L K, Robson A D.1992. External hyphae of vesicular—arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytologist, 120(4): 509-516.
25 Kiers E T, Duhamel M, Beesetty Y, et al.2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333(6044): 880-882.
26 Kittiworawat S, Youpensuk S, Rerkasem B.2010. Diversity of arbuscular mycorrhizal fungi in Mimosa invisa and effect of the soil pH on the symbiosis. Chiang Mai Journal of Science, 37(3): 517-527.
27 Miransari M.2011. Arbuscular mycorrhizal fungi and nitrogen uptake. Archives of Microbiology, 193(2): 77-81.
28 Mohan J E, Cowden C C, Baas P, et al.2014. Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review. Fungal Ecology, 10: 3-19.
29 Nazeri N K, Lambers H, Tibbett M, et al.2014. Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries. Plant, Cell and Environment, 37(4): 911-921.
30 Nogueira M A, Cardoso E J N.2007. Phosphorus availability changes the internal and external endomycorrhizal colonization and affects symbiotic effectivenes. Scientia Agricola, 64(3): 295-300.
31 Oehl F, Redecker D, Sieverding E.2005. Glomus badium, a new sporocarpic mycorrhizal fungal species from European grasslands with higher soil pH. Journal of Applied Botany and Food Quality, 79(1): 38-43.
32 Olsson P A, Tyler G.2004. Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate. Journal of Ecology, 92(5): 808-815.
33 Pennisi E.2004. The secret life of fungi. Science, 304(5677): 1620-1622.
34 Plenchette C, Duponnois R.2005. Growth response of the saltbush Atriplex nummularia L. to inoculation with the arbuscular mycorrhizal fungus Glomus intraradices. Journal of Arid Environments, 61(4): 535-540.
35 Porcel R, Ruiz-Lozano J M.2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany, 55(403): 1743-1750.
36 Püschel D, Rydlová J, Vosátka M.2007. Mycorrhiza influences plant community structure in succession on spoil banks. Basic and Applied Ecology, 8(6): 510-520.
37 Raznikiewicz H, Carlgren K, Maartensson A.1994. Impact of phosphorus fertilization and liming on the presence of arbuscular mycorrhizal spores in a Swedish long-term field experiment. Swedish Journal of Agricultural Research, 24: 157-164.
38 Reddy M V, Verma N K.1981. Aphid-mycorrhizal association, and its relationship with the rhizosphere-soil pH. Comparative Physiology and Ecology, 6(3): 157-158.
39 Rodriguez A, Sanders I R.2015. The role of community and population ecology in applying mycorrhizal fungi for improved food security. The ISME Journal, 9(5): 1053-1061.
40 Ruíz-Sánchez M, Armada E, Mu?oz Y, et al.2011. Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. Journal of Plant Physiology, 168(10): 1031-1037.
41 Sambrook J, Fritsch E F, Maniatis T.1989. Molecular Cloning: A Laboratory Manual (2nd ed.). New York: Cold Spring Harbor Laboratory Press, 202-203.
42 Selosse M A, Rousset F.2011. The plant-fungal marketplace. Science, 333(6044): 828-829.
43 Sengupta A, Chaudhuri S.1990. Vesicular arbuscular mycorrhiza (VAM) in pioneer salt marsh plants of the Ganges river delta in west Bengal (India). Plant and Soil, 122(1): 111-113.
44 Shi Z Y, Feng G, Christie P, et al.2006. Arbuscular mycorrhizal status of spring ephemerals in the desert ecosystem of Junggar Basin, China. Mycorrhiza, 16(4): 269-275.
45 Shi Z Y, Mickan B, Feng G, et al.2015. Arbuscular mycorrhizal fungi improved plant growth and nutrient acquisition of desert ephemeral Plantago minuta under variable soil water conditions. Journal of Arid Land, 7(3): 414-420.
46 Sigüenza C, Espejel I, Allen E B.1996. Seasonality of mycorrhizae in coastal sand dunes of Baja California. Mycorrhiza, 6(2): 151-157.
47 Smith F A, Grace E J, Smith S E.2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist, 182(2): 347-358.
48 Smith S E, Read D J.2008. Mycorrhizal Symbiosis (3rd ed.). Amsterdam, Boston: Academic Press, 26-27.
49 Smith S E, Jakobsen I, Gr?nlund M, et al.2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology, 156(3): 1050-1057.
50 Trouvelot A, Kough J L, Gianinazzi-Pearson V.1986. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S. Physiological and Genetical Aspects of Mycorrhizae: Proceedings of the 1st European Symposium on Mycorrhizae. Paris: INRA Press, 217-221.
51 van der Heijden M G A, Streitwolf-Engel R, Riedl R, et al.2006. The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytologist, 172(4): 739-752.
52 Van Tuinen D, Jacquot E, Zhao B, et al.1998. Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Molecular Ecology, 7(7): 879-887.
53 Varga S, Kyt?viita M M.2010. Interrelationships between mycorrhizal symbiosis, soil pH and plant sex modify the performance of Antennaria dioica. Acta Oecologica, 36(3): 291-298.
54 Wagg C, Bender S F, Widmer F, et al.2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America, 111(14): 5266-5270.
55 Whiteside M D, Digman M A, Gratton E, et al.2012. Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biology and Biochemistry, 55: 7-13.
56 Wilde P, Manal A, Stodden M, et al.2009. Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environmental Microbiology, 11(6): 1548-1561.
57 Williams S E, Wollum A G, Aldon E F.1974. Growth of Atriplex canescens (Pursh) Nutt. improved by formation of vesicular-arbuscular mycorrhizae. Soil Science Society of America Journal, 38(6): 962-965.
58 Yoneyama K, Yoneyama K, Takeuchi Y, et al.2007. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta, 225(4): 1031-1038.
59 Zhang T, Shi N, Bai D S, et al.2012. Arbuscular mycorrhizal fungi promote the growth of Ceratocarpus arenarius (Chenopodiaceae) with no enhancement of phosphorus nutrition. PLoS ONE, 7(9): e41151.
[1] CHEN Shumin, JIN Zhao, ZHANG Jing, YANG Siqi. Soil quality assessment in different dammed-valley farmlands in the hilly-gully mountain areas of the northern Loess Plateau, China[J]. Journal of Arid Land, 2021, 13(8): 777-789.
[2] HUANG Laiming, ZHAO Wen, SHAO Ming'an. Response of plant physiological parameters to soil water availability during prolonged drought is affected by soil texture[J]. Journal of Arid Land, 2021, 13(7): 688-698.
[3] LIN En, LIU Hongguang, LI Xinxin, LI Ling, Sumera ANWAR. Promoting the production of salinized cotton field by optimizing water and nitrogen use efficiency under drip irrigation[J]. Journal of Arid Land, 2021, 13(7): 699-716.
[4] ZHOU Siyuan, DUAN Yufeng, ZHANG Yuxiu, GUO Jinjin. Vegetation dynamics of coal mining city in an arid desert region of Northwest China from 2000 to 2019[J]. Journal of Arid Land, 2021, 13(5): 534-547.
[5] Masoud BAZGIR, Reza OMIDIPOUR, Mehdi HEYDARI, Nasim ZAINALI, Masoud HAMIDI, Daniel C DEY. Prioritizing woody species for the rehabilitation of arid lands in western Iran based on soil properties and carbon sequestration[J]. Journal of Arid Land, 2020, 12(4): 640-652.
[6] Zahra JAFARI, SayedHamid MATINKHAH, Mohammad R MOSADDEGHI, Mostafa TARKESH. Evaluation of the efficiency of irrigation methods on the growth and survival of tree seedlings in an arid climate[J]. Journal of Arid Land, 2020, 12(3): 495-507.
[7] LIU Weichao, FU Shuyue, YAN Shengji, REN Chengjie, WU Shaojun, DENG Jian, LI Boyong, HAN Xinhui, YANG Gaihe. Responses of plant community to the linkages in plant-soil C:N:P stoichiometry during secondary succession of abandoned farmlands, China[J]. Journal of Arid Land, 2020, 12(2): 215-226.
[8] Rashid KULMATOV, Jasur MIRZAEV, Jilili ABUDUWAILI, Bakhtiyor KARIMOV. Challenges for the sustainable use of water and land resources under a changing climate and increasing salinization in the Jizzakh irrigation zone of Uzbekistan[J]. Journal of Arid Land, 2020, 12(1): 90-103.
[9] Rentao LIU, STEINBERGER Yosef, Jingwei HOU, Juan ZHAO, Jianan LIU, Haitao CHANG, Jing ZHANG, Yaxi LUO. Conversion of cropland into agroforestry land versus naturally-restored grassland alters soil macro-faunal diversity and trophic structure in the semi-arid agro-pasture zone of northern China[J]. Journal of Arid Land, 2019, 11(2): 306-317.
[10] Lang QIU, Yinli BI, Bin JIANG, Zhigang WANG, Yanxu ZHANG, ZHAKYPBEK Yryszhan. Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China[J]. Journal of Arid Land, 2019, 11(1): 135-147.
[11] Guohua HE, Yong ZHAO, Jianhua WANG, Qingming WANG, Yongnan ZHU. Impact of large-scale vegetation restoration project on summer land surface temperature on the Loess Plateau, China[J]. Journal of Arid Land, 2018, 10(6): 892-904.
[12] SHAFIEZADEH Mohammad, MORADI Hossein, FAKHERAN Sima. Evaluating and modeling the spatiotemporal pattern of regional-scale salinized land expansion in highly sensitive shoreline landscape of southeastern Iran[J]. Journal of Arid Land, 2018, 10(6): 946-958.
[13] Qingyin ZHANG, Xiaoxu JIA, Chunlei ZHAO, Ming'an SHAO. Revegetation with artificial plants improves topsoil hydrological properties but intensifies deep-soil drying in northern Loess Plateau, China[J]. Journal of Arid Land, 2018, 10(3): 335-346.
[14] Xiaona Yu, Yongmei Huang, Engui Li, Xiaoyan Li, Weihua Guo. Effects of vegetation types on soil water dynamics during vegetation restoration in the Mu Us Sandy Land, northwestern China[J]. Journal of Arid Land, 2017, 9(2): 188-199.
[15] Ning AI, Tianxing WEI, Qingke ZHU, Fangfang QIANG, Huan MA, Wei QIN. Impacts of land disturbance and restoration on runoff production and sediment yield inthe Chinese Loess Plateau[J]. Journal of Arid Land, 2017, 9(1): 76-86.