Chin J Plan Ecolo ›› 2017, Vol. 41 ›› Issue (4): 480-488.doi: 10.17521/cjpe.2016.0210

• Orginal Article • Previous Articles     Next Articles

Effects of inoculation with arbuscular mycorrhizal fungi on photosynthetic physiology in females and males of Populus deltoides exposed to cadmium pollution

Liang-Hua CHEN, Juan LAI, Xiang-Wei HU, Wan-Qin YANG, Jian ZHANG*(), Xiao-Jun WANG, Ling-Jie TAN   

  1. Key Laboratory of Ecological Forestry Engineering, Collaborative Innovation Center of Ecological Safety in the Upper Reaches of Yangtze River, Institute of Ecology & Forestry, Sichuan Agricultural University, Chengdu 611130, China
  • Received:2016-06-27 Accepted:2016-12-25 Online:2017-05-19 Published:2017-04-10
  • Contact: Jian ZHANG


Aims Populus deltoides is an important plantation tree species in the middle and lower reaches of the Yangtze River and in Huai River Plain. The extensively cultivated varieties are consisted of both females and males of P. deltoides. The objective of this paper was to characterize the difference in cadmium (Cd) tolerance between the sexes and the effects of symbiosis with Rhizophagus intraradices on their Cd tolerance.
Methods The experiment was carried out under semi-controlled conditions in a natural light greenhouse, protected from rain. Rhizophagus intraradices was inoculated on roots of both females and males when transplanting to a sand culture substrate. After one month, half of cuttings were exposed to Cd pollution (10 mg·kg-1). All cuttings were irrigated with sterile water to avoid infection by other microorganism. About three months later, the gas exchange rate, net photosynthesis rate (Pn)-intercellular CO2 concentration (Ci) curve, chlorophyll fluorescence, osmotic adjustment and phytohormone content of both females and males of P. deltoides were measured.
Important findings Our main results are as follows: (1) when compared to the controls, decreases in Pn, stomatal conductance, Ci, transpiration rate, maximum photochemical efficiency of photosystem II (PSII), effective quantum yield of PSII, photo-chemical quenching coefficient, maximum rate of carboxylation of Rubisco, photosynthetically active radiation-saturated rate of electron transport and rate of triose phosphate utilization to a different degree in both sexes of P. deltoides under Cd pollution were found, and females exhibited a greater decrease in such parameters than males. Rhizophagus intraradices inoculation mitigated the toxic effect of Cd on such parameters to a different degree in females, not in males. (2) Under Cd pollution, there was an increase in proline content in both sexes when compared to the controls. A further increase in proline content occurred in females, not in males, when inoculated with R. intraradices. (3) When compared to the controls, there was a decrease in indoleacetic acid, but an increase in abscisic acid in leaves of both sexes when exposed to Cd pollution. The amplitude changed in both phytohormones in females was greater than that in males. Rhizophagus intraradices inoculation was helpful for recovery of phytohormone balance in females, which was not observed in males. Therefore, our results indicated that (1) there were a greater negative effect exerted by Cd pollution on gas exchange rate, carbon fixation capacity and phytohormone balance and a more impairment of photosynthetic apparatus in females when compared to males, showing a less tolerance to stress conditions in females; (2) Rhizophagus intraradices inoculation could enhance the osmotic adjustment capacity in females, thus mitigate the negative effect of Cd stress on ability of carbon fixation and phytohormone balance in females. However, such positive effects derived from R. intraradices symbiosis were not observed in males.

Key words: vesicular-arbuscular mycorrhiza, Populus deltoides, cadmium pollution, dioecy, photosynthesis

Table 1

Effects of arbuscular mycorrhizae fungi (AMF) inoculation on gas exchange rate in females and males of Populus deltoides exposed to Cd pollution (mean ± SE)"

Pn (µmol·m-2·s-1)
Gs (mol·m-2·s-1)
Ci (µmol·mol-1)
Tr (mmol·m-2·s-1)
对照 - 雄株 Male 11.91 ± 0.26b 0.37 ± 0.04bcd 318.40 ± 10.05a 4.37 ± 0.27ab
Control - 雌株 Female 13.68 ± 0.79ab 0.51 ± 0.02ab 310.85 ± 7.71ab 5.50 ± 0.27a
+ 雄株 Male 12.34 ± 0.34b 0.41 ± 0.03abc 313.96 ± 7.72ab 5.11 ± 0.20a
+ 雌株 Female 14.43 ± 0.42a 0.52 ± 0.05a 313.68 ± 10.97ab 5.37 ± 0.44a
Cd污染 - 雄株 Male 9.70 ± 0.46c 0.25 ± 0.02de 270.87 ± 6.51bc 3.48 ± 0.26bc
Cd pollution - 雌株 Female 6.58 ± 0.27d 0.13 ± 0.02e 243.14 ± 9.73c 2.10 ± 0.33d
+ 雄株 Male 8.86 ± 0.35c 0.27 ± 0.02d 273.86 ± 9.00bc 2.95 ± 0.26cd
+ 雌株 Female 9.59 ± 0.28c 0.30 ± 0.01cd 288.10 ± 4.52ab 3.26 ± 0.11bcd
Fs ns ns ns ns
Fcd *** *** *** ***
FAMF * ** ns ns
Fs×cd *** *** ns **
Fs×AMF ** ns * ns
Fcd×AMF ns ns ns ns
Fs×cd×AMF ** * ns **

Fig. 1

Effects of arbuscular mycorrhizae fungi (AMF) inoculation on Pn-Ci curves of females and males of Populus deltoides under control (A) and Cd-stressed (B) conditions."

Table 2

Effects of arbuscular mycorrhizae fungi (AMF) inoculation on parameters derived from the fitted Pn-Ci curves in females and males of Populus deltoides exposed to Cd pollution (mean ± SE)"

Vcmax (µmol·m-2·s-1)
Jmax (µmol·m-2·s-1)
TPU (µmol·m-2·s-1)
Г (µmol·mol-1)
对照 - 雄株 Male 34.17 ± 1.14bc 88.20 ± 1.80bc 6.26 ± 0.14abcd 6.20 ± 0.36b
Control - 雌株 Female 37.80 ± 0.17b 93.60 ± 3.38b 7.91 ± 0.64abc 6.10 ± 0.21b
+ 雄株 Male 42.57 ± 1.34b 117.33 ± 6.77a 8.88 ± 0.95a 5.57 ± 0.08b
+ 雌株 Female 52.30 ± 3.13a 137.33 ± 5.78a 8.24 ± 0.63ab 5.34 ± 0.12b
Cd 污染 - 雄株 Male 25.87 ± 2.39cd 71.20 ± 2.72cd 4.17 ± 0.27d 6.87 ± 0.28b
Cd pollution - 雌株 Female 22.67 ± 1.36d 59.50 ± 3.50d 5.19 ± 0.41bcd 9.91 ± 0.46a
+ 雄株 Male 24.17 ± 2.81d 68.97 ± 4.34cd 4.68 ± 0.45cd 6.08 ± 0.20b
+ 雌株 Female 25.30 ± 1.03cd 73.23 ± 4.52bcd 6.54 ± 1.22abcd 7.02 ± 0.38b
Fs ns ns ns ns
Fcd *** *** *** ***
FAMF *** *** * ns
Fs×cd ** * * ns
Fs×AMF ns * ns **
Fcd×AMF *** *** ns **
Fs×cd×AMF ns ns ns **

Table 3

Effects of arbuscular mycorrhizae fungi (AMF) inoculation on chlorophyll a fluorescence parameters in females and males of Populus deltoides exposed to Cd pollution (mean ± SE)"

处理 Treatment 丛枝菌根 AM 性别 Sex Fv/Fm ΦPSII qP qN
对照 - 雄株 Male 0.80 ± 0.01ab 0.72 ± 0.01a 0.94 ± 0.01a 0.19 ± 0.01cd
Control - 雌株 Female 0.81 ± 0.01ab 0.73 ± 0.00a 0.96 ± 0.00a 0.19 ± 0.01cd
+ 雄株 Male 0.81 ± 0.00ab 0.73 ± 0.00a 0.94 ± 0.01a 0.24 ± 0.01bc
+ 雌株 Female 0.81 ± 0.00ab 0.73 ± 0.00a 0.93 ± 0.01a 0.17 ± 0.01d
Cd 污染 - 雄株 Male 0.78 ± 0.00bc 0.70 ± 0.01a 0.93 ± 0.01a 0.21 ± 0.01cd
Cd pollution - 雌株 Female 0.69 ± 0.01e 0.60 ± 0.02b 0.83 ± 0.01b 0.33 ± 0.01a
+ 雄株 Male 0.76 ± 0.00cd 0.70 ± 0.01a 0.92 ± 0.01a 0.26 ± 0.01b
+ 雌株 Female 0.76 ± 0.01d 0.70 ± 0.02a 0.93 ± 0.02a 0.26 ± 0.01b
Fs *** ** ** ns
Fcd *** *** *** ***
FAMF *** ** ns ns
Fs×cd *** *** ** ***
Fs×AMF *** * ** ***
Fcd×AMF ns * *** ns
Fs×cd×AMF *** ** *** ns

Fig. 2

Effects of arbuscular mycorrhizae fungi (AMF) inoculation on osmotic solutes and phytohormones in females and males of Populus deltoides exposed to Cd pollution (mean ± SE). Different letters indicate significant differences between treatments (p < 0.05) according to Tukey test."

Table 4

Statistical significance of the single and interactive effects of sex, Cd and arbuscular mycorrhizae fungi (AMF) on osmotic solutes and phytohormones based on univariate analyses of variance."

参数 Parameter 因子 Factor
Fs Fcd FAMF Fs×cd Fs×AMF Fcd×AMF Fs×cd×AMF
脯氨酸 Proline ** *** *** ** * ** ***
可溶性蛋白 Soluble protein ns ** *** * ns * ns
生长素 Auxin *** *** *** *** *** ** ***
脱落酸 Abscisic acid *** *** *** *** *** * ***
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