Chin J Plan Ecolo ›› 2018, Vol. 42 ›› Issue (7): 764-773.doi: 10.17521/cjpe.2018.0089

• Research Articles • Previous Articles     Next Articles

Transmembrane H + and Ca 2+ fluxes through extraradical hyphae of arbuscular mycorrhizal fungi in response to drought stress

XU Li-Jiao1,2, HAO Zhi-Peng1, XIE Wei1,2, LI Fang1,2, CHEN Bao-Dong1,2,*()   

  1. 1 State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
  • Online:2018-06-11 Published:2018-07-20
  • Contact: Bao-Dong CHEN E-mail:bdchen@rcees.ac.cn
  • Supported by:
    Supported by the Strategic Priority Research Program of the Chinese Academy of Sciences(XDB15030102);the National Natural Science Foundation of China(41371264);the National Natural Science Foundation of China(41401281)

Abstract:

Aims Arbuscular mycorrhizal fungi (AMF) can form symbiotic associations with most terrestrial plants to improve plant growth and stress resistance. It has been well demonstrated that AMF can promote plant acquisition of water and enhance plant tolerance to drought. In this study, AMF extraradical hyphae were obtained from in vitro culture of AMF Rhirophagus irregularis with hairy carrot (Daucus carota var. sativa) root to investigate the morphological and physiological changes of hyphae in response to drought stress induced by polyethylene glycol (PEG).

Methods The influence of drought stress on the hyphal morphology was observed by using the field emission-scanning electron microscope-energy dispersive X-ray spectroscopy (FE-SEM-EDS), while H + and Ca 2+ion fluxes through living hyphae were monitored by non-invasive micro-test technique (NMT).

Important findings The results showed that significant H+ efflux and Ca2+ influx through the tip and side of the extraradical hyphae were detected in response to drought stress induced by PEG for 1 h. Fluorescence probing confirmed that the intracellular pH value and Ca2+ concentration of hyphae significantly increased under PEG treatment. The morphology of hyphae changed and the pH value of the growth medium decreased after treatment with PEG for 24 h. The P, Ca, and Fe elements accumulated at the hyphosphere to enhance the nutrient absorption by hyphae. The study confirmed that AMF regulated the transmembrane H+ and Ca2+ flux to promote the material exchange between hyphae and environment under drought stress. The acidification of the hyphosphere environment potentially promoted the absorption of nutrients and also the signal exchange between AMF and the host plant to enhance plant drought tolerance.

Key words: arbuscular mycorrhizal fungi, drought stress, H+, Ca2+, non-invasive micro-test technology

Table 1

Formulation of the M medium"

离子/化合物
Ion/Compound
含量
Content (mg·L-1)
离子/化合物
Ion/Compound
含量
Content (mg·L-1)
Mg2+ 70.8 Fe2+ 0.1
SO42- 280.1 Mn2+ 1.6
K+ 61 Zn2+ 0.6
NO3- 230 BO33- 0.24
Cl- 37.2 甘氨酸 Glycine 3
H2PO4- 4.8 维生素B1 Vitamin B1 0.1
Ca2+ 49 维生素B6 Vitamin B6 0.1
I- 0.58 烟酸 Nicotinic acid 0.5
Na+ 0.43 肌醇 Inositol 50

Fig. 1

Diagram of the two-compartments in vitro culture system of arbuscular mycorrhizal fungi with hairy carrot root. Mycorrhizal compartment was filled with solid M medium gelled with 0.4% phytagel, allowing development of mycorrhizal roots; extraradical mycelium ramified into hyphal compartment filled with liquid M medium without sucrose and phytagel, and the roots that crossed the central wall were trimmed to prevent their growth in hyphal compartment (referred to St-Arnaud et al., 1996)."

Fig. 2

The pH value of culture medium in hyphal compartment after treatment by PEG (mean ± SD, n = 6). Different lowercase letters indicate significant difference between treatments (Duncan’s multiple range test, p < 0.05)."

Fig. 3

FE-SEM images and selective elemental analysis (by EDS) of arbuscular mycorrhizal fungi hyphae after treatment by PEG for 1 h (PEG 1 h) and 24 h (PEG 24 h). CK 1 h and CK 24 h are corresponding controls."

Table 2

Concentrations of P, Ca and Fe at the tip and side of arbuscular mycorrhizal fungi hyphae after treatment by PEG for 1 h and 24 h (determined by energy-dispersive X-ray spectroscopy) (mean ± SD, n = 6)"

P Ca Fe
原子百分比
Atom percentage content (%)
质量分数
Mass percentage content (%)
原子百分比
Atom percentage content (%)
质量分数
Mass percentage content (%)
原子百分比
Atom percentage content (%)
质量分数
Mass percentage content (%)
尖端 Tip CK 1 h 29.53 ± 2.03cd 30.03 ± 0.52d 5.97 ± 0.68c 6.14 ± 0.72c 15.86 ± 0.26c 24.64 ± 2.07cd
24 h 31.34 ± 2.34c 32.85 ± 0.61d 4.49 ± 0.86c 5.39 ± 1.27c 14.60 ± 1.26c 26.53 ± 1.91c
PEG 1 h 38.80 ± 1.07b 39.62 ± 0.41c 16.15 ± 0.84a 18.00 ± 0.87a 37.15 ± 0.69a 37.44 ± 1.13b
24 h 51.49 ± 1.63a 50.46 ± 0.39a 5.32 ± 1.45c 4.91 ± 0.66c 32.48 ± 1.70ab 52.43 ± 0.49a
侧面 Side CK 1 h 23.51 ± 1.12d 39.01 ± 0.34c 7.83 ± 1.3bc 7.88 ± 1.40bc 12.03 ± 1.11d 19.51 ± 1.39d
24 h 28.00 ± 1.67cd 43.47 ± 1.07bc 9.84 ± 0.83b 10.32 ± 0.92b 12.07 ± 0.78d 19.17 ± 0.87d
PEG 1 h 37.69 ± 0.84b 37.51 ± 1.43c 10.34 ± 1.12b 12.03 ± 0.75b 28.54 ± 0.76b 33.28 ± 1.13b
24 h 56.12 ± 2.21a 45.04 ± 0.47b 14.99 ± 0.73a 16.21 ± 0.40a 35.09 ± 1.43a 41.70 ± 0.60ab

Fig. 4

The effect of PEG treatment for 1 h and 24 h on the pH value at the tip and side of arbuscular mycorrhizal fungi hypha. Fluorescence image at 488 nm excitation shows the pH variation in the hyphal cell."

Fig. 5

The effect of PEG treatment for 1 h and 24 h on the Ca2+ concentration at the tip and side of arbuscular mycorrhizal fungi hypha. Fluorescence image at 488 nm excitation shows the Ca2+ variation in the hyphal cell."

Fig. 6

The effects of PEG treatment on H+ (A) and Ca2+ (B) flux at the tip and side of arbuscular mycorrhizal hyphae (mean ± SD, n = 6). tip stands for hyphal tip, and side stands for lateral hypha. Columns marked by different letters are significantly different according to Duncan’s multiple range test (p < 0.05)."

[1] Augé RM, Duan X ( 1991). Mycorrhizal fungi and nonhydraulic root signals of soil drying. Plant Physiology, 97, 821-824.
doi: 10.1104/pp.97.2.821
[2] Augé RM, Toler HD, Saxton AM ( 2015). Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: A meta-analysis. Mycorrhiza, 25, 13-24.
doi: 10.1007/s00572-014-0585-4 pmid: 24831020
[3] Ayling SM, Smith SE, Smith FA ( 2000). Transmembrane electric potential difference of germ tubes of arbuscular mycorrhizal fungi responds to external stimuli. New Phytologist, 147, 631-639.
doi: 10.1046/j.1469-8137.2000.00723.x
[4] Azad AK, Sawa Y, Ishikawa T, Shibata H ( 2004). Phosphorylation of plasma membrane aquaporin regulates temperature-?dependent opening of tulip petals. Plant and Cell Physiology, 45, 608-617.
doi: 10.1093/pcp/pch069 pmid: 15169943
[5] Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lozano JM ( 2012). Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Annals of Botany, 109, 1009-1017.
doi: 10.1093/aob/mcs007 pmid: 22294476
[6] Bartnicki-Garcia S, Bracker CE, Gierz G, López-Franco R, Lu H ( 2000). Mapping the growth of fungal hyphae: Orthogonal cell wall expansion during tip growth and the role of turgor. Biophysical Journal, 79, 2382-2390.
doi: 10.1016/S0006-3495(00)76483-6 pmid: 11053117
[7] Bécard G, Fortin JA ( 1988). Early events of vesicular?-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist, 108, 211-218.
doi: 10.1111/nph.1988.108.issue-2
[8] Bunney TD, Shaw PJ, Watkins PA, Taylor JP, Beven AF, Wells B, Calder GM, Dr?bak BK ( 2000). ATP-dependent regulation of nuclear Ca 2+ levels in plant cells . FEBS Letters, 476, 145-149.
doi: 10.1016/S0014-5793(00)01709-9 pmid: 10913602
[9] Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San Segundo B ( 2014). Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiology, 165, 688-704.
doi: 10.1104/pp.113.230268 pmid: 24784760
[10] Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E ( 2016). Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiology, 171, 1009-1023.
doi: 10.1104/pp.16.00307 pmid: 27208301
[11] Duncan DB ( 1955). Multiple range and multiple F tests. Biometrics, 11, 1-42.
[12] Ferrol N, Barea JM, Azcón-Aguilar C ( 2000). The plasma membrane H +-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Current Genetics, 37, 112-118.
[13] Fromm J, Lautner S ( 2007). Electrical signals and their physiological significance in plants. Plant, Cell & Environment, 30, 249-257.
doi: 10.1111/j.1365-3040.2006.01614.x pmid: 17263772
[14] Gaxiola RA, Palmgren MG, Schumacher K ( 2007). Plant proton pumps. FEBS Letters, 581, 2204-2214.
doi: 10.1016/j.febslet.2007.03.050
[15] Gévaudant F, Duby G, von Stedingk E, Zhao R, Morsomme P, Boutry M ( 2007). Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance . Plant Physiology, 144, 1763-1776.
doi: 10.1104/pp.107.103762
[16] Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA ( 1991). Enzymatic studies on the metabolism of vesicular-?arbuscular mycorrhizas. New Phytologist, 117, 61-74.
doi: 10.1111/nph.1991.117.issue-1
[17] Gong DS, Xiong YC, Ma BL, Wang TM, Ge JP, Qin XL, Li PF, Kong HY, Li ZZ, Li FM ( 2010). Early activation of plasma membrane H +-ATPase and its relation to drought adaptation in two contrasting oat ( Avena sativa L.) genotypes. Environmental and Experimental Botany, 69, 1-8.
[18] Harrison MJ ( 2005). Signaling in the arbuscular mycorrhizal symbiosis. Annual Review Microbiology, 59, 19-42.
doi: 10.1146/annurev.micro.58.030603.123749
[19] Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T ( 2010). Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytologist, 186, 285-289.
doi: 10.1111/j.1469-8137.2009.03168.x pmid: 20409186
[20] Isfort RJ, Cody DB, Asquith TN, Ridder GM, Stuard SB, Leboeuf RA ( 1993). Induction of protein phosphorylation, protein synthesis, immediate-early-gene expression and cellular proliferation by intracellular pH modulation. FEBS Journal, 213, 349-357.
[21] Kühtreiber WM, Jaffe LF ( 1990). Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. The Journal of Cell Biology, 110, 1565-1573.
doi: 10.1083/jcb.110.5.1565
[22] Li T, Du J, Hao ZP, Zhang X, Chen BD ( 2012). Molecular basis for enhancement of plant drought tolerance by arbuscular mycorrhizal symbiosis: A mini-review. Acta Ecologica Sinica, 32, 7169-7176.
doi: 10.5846/stxb201110141518
[ 李涛, 杜娟, 郝志鹏, 张莘, 陈保冬 ( 2012). 丛枝菌根提高宿主植物抗旱性分子机制研究进展. 生态学报, 32, 7169-7176.]
doi: 10.5846/stxb201110141518
[23] Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD ( 2013). First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist, 197, 617-630.
doi: 10.1111/nph.12011 pmid: 23157494
[24] Liu T, Li Z, Hui C, Tang M, Zhang H ( 2016). Effect of Rhizophagus irregularis on osmotic adjustment, antioxidation and aquaporin PIP genes expression of Populus × canadensis ‘Neva’ under drought stress. Acta Physiologiae Plantarum, 38, 191. DOI: 10.1007/s11738-016-2207-6.
[25] Liu RJ, Chen YL ( 2007). Mycorrhizology. Science Press, Beijing. 447-448.
[26] Ludwig AA, Romeis T, Jones JD ( 2004). CDPK-mediated signalling pathways: Specificity and cross-talk. Journal of Experimental Botany, 55, 181-188.
doi: 10.1093/jxb/erh008 pmid: 14623901
[27] Ma R, Zhang M, Li B, Du G, Wang J, Chen J ( 2005). The effects of exogenous Ca 2+ on endogenous polyamine levels and drought-resistant traits of spring wheat grown under arid conditions . Journal of Arid Environments, 63, 177-190.
doi: 10.1016/j.jaridenv.2005.01.021
[28] Mak M, Babla M, Xu SC, O’Carrigan A, Liu XH, Gong YM, Holford P, Chen ZH ( 2014). Leaf mesophyll K+, H+and Ca2+ fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean . Environmental and Experimental Botany, 98, 1-12.
doi: 10.1016/j.envexpbot.2013.10.003
[29] Porcel R, Ruiz-Lozano JM ( 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, 1743-1750.
doi: 10.1093/jxb/erh188 pmid: 15208335
[30] Querejeta J, Egerton-Warburton LM, Allen MF ( 2003). Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia, 134, 55-64.
doi: 10.1007/s00442-002-1078-2
[31] Ramos AC, Fa?anha AR, Feijó JA ( 2008a). Ion dynamics during the polarized growth of arbuscular mycorrhizal fungi: From presymbiosis to symbiosis. In: Varma A ed. Mycorrhiza. Springer, Berlin, Heidelberg.
doi: 10.1007/978-3-540-78826-3_12
[32] Ramos AC, Fa?anha AR, Feijó JA ( 2008b). Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi . New Phytologist, 178, 177-188.
doi: 10.1111/j.1469-8137.2007.02344.x
[33] Requena N, Breuninger M, Franken P, Ocón A ( 2003). Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiology, 132, 1540-1549.
doi: 10.1016/j.colsurfa.2004.09.019 pmid: 12857834
[34] Riquelme M, Bartnicki-Garcia S ( 2004). Key differences between lateral and apical branching in hyphae of Neurospora crassa. Fungal Genetics and Biology, 41, 842-851.
[35] Rudd JJ, Franklin-Tong VE ( 2001). Unravelling response-?specificity in Ca 2+ signalling pathways in plant cells . New Phytologist, 151, 7-33.
doi: 10.1046/j.1469-8137.2001.00173.x
[36] Sánchez-Romera B, Ruiz-Lozano JM, Zamarre?o áM, García-?Mina JM, Aroca R ( 2016). Arbuscular mycorrhizal symbiosis and methyl jasmonate avoid the inhibition of root hydraulic conductivity caused by drought. Mycorrhiza, 26, 111-122.
doi: 10.1007/s00572-015-0650-7 pmid: 26070449
[37] Santi S, Locci G, Monte R, Pinton R, Varanini Z ( 2003). Induction of nitrate uptake in maize roots: Expression of a putative high-affinity nitrate transporter and plasma membrane H+- ATPase isoforms . Journal of Experimental Botany, 54, 1851-1864.
doi: 10.1093/jxb/erg208 pmid: 12869520
[38] Shi Y, Zhang Y, Han W, Feng R, Hu Y, Guo J, Gong H ( 2016). Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L. Frontiers in Plant Science, 7, 196. DOI: 10.3389/fpls.?2016.?00196.
[39] Smith S, Read D ( 2008). Mycorrhizal Symbiosis. Academic Press, New York.
[40] St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA ( 1996). Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycological Research, 100, 328-332.
[41] Sun YP, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay R ( 1999). Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza, 9, 137-144.
doi: 10.1007/s005720050298
[42] Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frey NF, Gianinazzi-?Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, Clemente HS, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F ( 2013). Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 110, 20117-20122.
doi: 10.1073/pnas.1313452110 pmid: 24277808
[43] van Hees PA, Rosling A, Essén S, Godbold DL, Jones DL, Finlay RD ( 2006). Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis withPinus sylvestris. New Phytologist, 169, 367-378.
[44] Wu S, Zhang X, Sun Y, Wu Z, Li T, Hu Y, Su D, Lü J, Li G, Zhang Z, Zheng L, Zhang J, Chen B ( 2015). Transformation and immobilization of chromium by arbuscular mycorrhizal fungi as revealed by SEM-EDS, TEM-EDS, and XAFS. Environmental Science & Technology, 49, 14036-14047.
[45] Xiong YC, Li FM, Zhang T, Xia C ( 2007). Evolution mechanism of non-hydraulic root-to-shoot signal during the anti-drought genetic breeding of spring wheat. Environmental and Experimental Botany, 59, 193-205.
doi: 10.1016/j.envexpbot.2005.12.003
[46] Xu L, Li T, Wu Z, Feng H, Yu M, Zhang X, Chen B ( 2018). Arbuscular mycorrhiza enhances drought tolerance of tomato plants by regulating the 14-3-3 genes in the ABA signaling pathway. Applied Soil Ecology, 125, 213-221.
doi: 10.1016/j.apsoil.2018.01.012
[47] Yan F, Zhu Y, Müller C, Z?rb C, Schubert S ( 2002). Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots of white lupin under phosphate deficiency . Plant Physiology, 129, 50-63.
doi: 10.1104/pp.010869
[48] Yang PZ ( 2012). Mechanism Involved in Drought/Salt Tolerance Improvement in Alfalfa Due to Symbiotic Interaction with Rhizobium. PhD dissertation, Northwest A&F University,Yangling, Shaanxi. 4-6.
[ 杨培志 ( 2012). 紫花苜蓿根瘤菌共生对干旱及盐胁迫的响应机制研究. 博士学位论文, 西北农林科技大学, 陕西杨凌. 4-6.]
[49] Yoshida S ( 1991). Chilling-induced inactivation and its recovery of tonoplast H+-ATPase in mung bean cell suspension cultures . Plant Physiology, 95, 456-460.
doi: 10.1104/pp.95.2.456
[50] Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J ( 2015a). Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Applied Soil Ecology, 88, 41-49.
doi: 10.1016/j.apsoil.2014.11.016
[51] Zhao X, Xu M, Wei R, Liu Y ( 2015b). Expression OsCAS (calcium-sensing receptor) in an Arabidopsis mutant increases drought tolerance. PLOS ONE, 10, e0131272. DOI: 10.1371/journal.pone.0131272.
doi: 10.1371/journal.pone.0131272 pmid: 26098425
[52] Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH ( 2015). Arabidopsis calcium-dependent protein kinase 8 and catalase 3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. The Plant Cell, 27, 1445-1460.
[53] Zhou S, Han YY, Chen Y, Kong X, Wang W ( 2015). The involvement of expansins in response to water stress during leaf development in wheat. Journal of Plant Physiology, 183, 64-74.
doi: 10.1016/j.jplph.2015.05.012 pmid: 26092364
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[6] JIA Hu-Sen LI De-QuanHAN Ya-Qin. Cytochrome b-559 in Chloroplasts[J]. Chin Bull Bot, 2001, 18(02): 158 -162 .
[7] Wei Sun;Chonghui Li;Liangsheng Wang;Silan Dai*. Analysis of Anthocyanins and Flavones in Different-colored Flowers of Chrysanthemum[J]. Chin Bull Bot, 2010, 45(03): 327 -336 .
[8] . Phosphate_Stress Protein and Iron_Stress Protein in Plants[J]. Chin Bull Bot, 2001, 18(05): 571 -576 .
[9] ZHANG Da-Yong, JIANG Xin-Hua. An Ecological Perspective on Crop Prduction[J]. Chin J Plan Ecolo, 2000, 24(3): 383 -384 .
[10] Gui Ji-xun, Zhu Ting-cheng. Study of Energy Flow Between Litter and Decomposers in Aneurolepidium chinese Grassland[J]. Chin J Plan Ecolo, 1992, 16(2): 143 -148 .