丛枝菌根真菌根外菌丝跨膜H +和Ca 2+流对干旱胁迫的响应

doi:10.17521/cjpe.2018.0089

摘要/Abstract

摘要：

丛枝菌根真菌(AMF)能够和大多数陆地植物形成共生体系, 对于植物生长发育和适应各种逆境胁迫具有重要作用。很多研究表明干旱胁迫下AMF能够促进宿主植物对水分的吸收从而增强植物抗旱能力, 但目前针对AMF根外菌丝响应水分胁迫的生理变化以及AMF与宿主植物逆境信号交流的研究并不多。该研究利用AMF Rhizophagus irregularis和胡萝卜(Daucus carota var. sativa)毛状根双重无菌培养体系获得纯净根外菌丝, 向培养基添加聚乙二醇(PEG)模拟干旱胁迫, 运用场发射扫描电子显微镜(FE-SEM-EDS)观察干旱胁迫对AMF根外菌丝形态的影响, 同时采用非损伤微测技术(NMT)观测根外菌丝跨膜H ⁺和Ca ²⁺离子流变化。结果发现, PEG处理1 h后菌丝尖端和侧面发生H ⁺外流和强烈的Ca ²⁺内流, 荧光探针分析也显示菌丝胞内pH值显著上升、Ca ²⁺浓度增加; PEG处理24 h后菌丝形态发生明显变化, 培养基pH值降低, P、Ca、Fe等元素在菌丝际积累。这些试验结果表明, 干旱胁迫下AMF根外菌丝跨膜H ⁺和Ca ²⁺流发生变化, 促进了菌丝与环境之间的物质交换。菌丝酸化生长环境有利于养分吸收, 并促进AMF与宿主植物之间的信号交流以增强植物的耐旱性。

关键词: 丛枝菌根真菌, 干旱胁迫, 氢离子, 钙离子, 非损伤微测技术

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

徐丽娇, 郝志鹏, 谢伟, 李芳, 陈保冬. 丛枝菌根真菌根外菌丝跨膜H ⁺和Ca ²⁺流对干旱胁迫的响应. 植物生态学报, 2018, 42(7): 764-773. DOI: 10.17521/cjpe.2018.0089

XU Li-Jiao, HAO Zhi-Peng, XIE Wei, LI Fang, CHEN Bao-Dong. Transmembrane H ⁺ and Ca ²⁺ fluxes through extraradical hyphae of arbuscular mycorrhizal fungi in response to drought stress. Chinese Journal of Plant Ecology, 2018, 42(7): 764-773. DOI: 10.17521/cjpe.2018.0089

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图/表 8

表1 M培养基成分

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
SO₄^2-	280.1	Mn²⁺	1.6
K⁺	61	Zn²⁺	0.6
NO₃^-	230	BO₃^3-	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

图1 丛枝菌根真菌-胡萝卜毛状根分室培养系统示意图。左边是菌根室(mycorrhizal compartment), 右边是菌丝室(hyphal compartment)。菌根室中加入用质量浓度0.4%的植物凝胶固化后的M培养基, 并接入菌根化的转移Ri T-DNA胡萝卜毛状根; 菌丝室加入液体M培养基, 以供根外菌丝生长(参考St-Arnaud et al., 1996)。

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).

图2 PEG处理下菌丝室培养基的pH值(平均值±标准偏差, n = 6)。不同小写字母表示处理间差异显著 (Duncan’s多重比较, p < 0.05)。

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).

图3 PEG处理1 h (PEG 1 h)和24 h (PEG 24 h)后丛枝菌根真菌根外菌丝FE-SEM图像和能谱分析图。CK 1 h和CK 24 h为空白对照。

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.

表2 PEG处理1 h和24 h后丛枝菌根真菌菌丝尖端和侧面P、Ca和Fe的浓度值(能谱分析结果)(平均值±标准偏差, n = 6)

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

图4 PEG处理1 h和24 h对丛枝菌根真菌菌丝尖端和侧面细胞内pH值的影响。荧光图像显示激发波长为488 nm条件下菌丝内pH值变化。

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.

图5 PEG处理1 h和24 h对丛枝菌根真菌菌丝尖端和侧面细胞内Ca2+浓度的影响。荧光图像显示激发波长为488 nm条件下菌丝内Ca2+浓度变化。

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.

图6 PEG处理1 h和24 h对菌丝尖端和侧面H+ (A), 和Ca2+ (B)离子流的影响(平均值±标准偏差, n = 6)。tip表示菌丝尖端, side表示菌丝侧面。柱形上方标示不同字母代表相应处理之间有显著性差异(Duncan’s多重比较, p < 0.05)。

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).

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丛枝菌根真菌根外菌丝跨膜H ⁺和Ca ²⁺流对干旱胁迫的响应

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

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