Chin J Plan Ecolo ›› 2017, Vol. 41 ›› Issue (8): 815-825.doi: 10.17521/cjpe.2017.0018

• Research Articles •     Next Articles

Arbuscular mycorrhiza improves plant adaptation to phosphorus deficiency through regulating the expression of genes relevant to carbon and phosphorus metabolism

Li-Jiao XU1,2, Xue-Lian JIANG1,3, Zhi-Peng HAO1, Tao LI1, Zhao-Xiang WU1,4, Bao-Dong CHEN1,2,*()   

  1. 1State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China

    2University of Chinese Academy of Sciences, Beijing 100049, China

    3School of Life Sciences, University of Science and Technology of China, Hefei 230026, China

    4Jiangxi Engineering and Technology Research Center for Ecological Remediation of Heavy Metal Pollution, Institute of Biology and Resources, Jiangxi Academy of Sciences, Nanchang 330096, China
  • Online:2017-09-29 Published:2017-08-10
  • Contact: Bao-Dong CHEN E-mail:bdchen@rcees.ac.cn
  • About author:

    KANG Jing-yao(1991-), E-mail: kangjingyao_nj@163.com

Abstract:

Aims Arbuscular mycorrhizal (AM) symbiosis plays an important role in plant adaptation to phosphorus (P) deficiency. The mycorrhizal fungi can directly regulate P stress response of the host plants, and can also indirectly influence neighbor plants via AM exudates. This study aimed to reveal the regulation mechanisms of plant response to P deficiency by AM associations. Methods In a compartmentation cultivation experiment with Zea mays ‘B73’ and AM fungus Rhizophagus irregularis ‘DAOM197198’, we investigated mycorrhizal effects on plant P nutrition and the expression of plant and fungal genes related to P and carbon (C) metabolisms under both low P (10 mg?kg-1) and high P (100 mg?kg-1) conditions. The cultivation system consisted of three compartments, namely donor compartment, buffer compartment and receiver compartment divided by two pieces of microporous filters with pore size of 0.45 μm. Maize plant in donor compartment inoculated with AM fungus served as a source of AM exudates. The microporous filters could restrict the development of extraradical mycelium of AM fungi, but allow diffusion of AM exudates. Real-time PCR was performed to quantify the gene expression levels both in maize plants and AM fungi. Important findings The experimental results indicated that under low P conditions mycorrhizal colonization increased plant dry weight and P concentration in donor plants, and up-regulated plant genes encoding P transporters Pht1;2, Pht1;6, phosphoenolpiruvate carboxylase (PEPC), inorganic pyrophosphatase (TC289), glycerol-3-phosphate transporter (G3PT) and malate synthase (MAS1). The expression of AM fungal genes encoding P transporter (GiPT), GlcNAc transporter (NGT1), GlcNAc kinase (HXK1b), GlcNAc phosphomutase (AGM1), UDP GlcNAc pyrophosphorylase (UAP1), chitin synthase (CHS1), GlcNAc-6-phosphate deacetylase (DAC1) and glucosamine-6-phosphate isomerase (NAG1) was significantly higher under low P conditions compared with high P conditions. However, for the receiver plants, plant dry mass and P concentration were only significantly increased by higher P addition, while inoculation treatment significantly up-regulated the expression of P transporter genes Pht1;2 and Pht1;6, C metabolism related genes G3PT, PEPC, TC289 and MAS1. The study proved that AM exudates could potentially stimulate plant response to P deficiency by regulating functional genes relevant to P and C metabolisms in the mycorrhizal associations.

Key words: compartment cultivation system, arbuscular mycorrhiza, carbon and phosphorus metabolism, functional gene, phosphorus deficiency

Fig. 1

Diagram of the compartment cultivation system. Different compartments were separated by microporous filter with pore size of 0.45 μm. AM and NM represent inoculation of donor plants with AM fungus and the non-mycorrhizal control respectively. There are two phosphorus levels (10 mg?kg-1 and 100 mg?kg-1), and three replications for each treatment (n = 3)."

Fig. 2

Effects of mycorrhizal inoculation on maize dry mass under different P levels (mean ± SD). LP and HP refer to low P level (10 mg·kg-1) and high P level (100 mg·kg-1) respectively. AMD and NMD represent donor plants with and without AM fungus incubation, while AMR and NMR represent receiver plants with and without AM exudates respectively. Different letters above the columns indicate significant difference (p < 0.05) between corresponding treatments. # indicates significant difference (p < 0.05) between different P levels under the same inoculation treatment."

Fig. 3

Effects of inoculation with AM fungus on maize P concentrations under different P levels (mean ± SD). LP and HP refer to low P level (10 mg·kg-1) and high P level (100 mg·kg-1) respectively. AMD and NMD represent donor plants with and without AM fungus incubation, while AMR and NMR represent receiver plants with and without AM exudates respectively. The different letters indicates significant difference (p < 0.05) between corresponding treatments. # indicates significant difference (p < 0.05) between different P levels under the same inoculation treatment; * indicates significant difference (p < 0.05) between inoculation treatments under the same P level."

Fig. 4

Expression of AM fungal genes relevant to C and P metabolisms under different P levels (mean ± SD). LP refers to low P treatments, HP refers to high P treatments, * indicates significant difference (p < 0.05) between different P levels. GiPT, AM fungal P transporter gene; NGT1, GlcNAc transporter gene, HXK1b, GlcNAc kinase gene; AGM1, GlcNAc phosphomutase gene; UAP1, UDP GlcNAc pyrophosphorylase gene; CHS1, chitin synthase gene; DAC1, GlcNAc-6-phosphate deacetylase gene; NAG1, glucosamine- 6-phosphate isomerase gene."

Fig. 5

Expression of genes relevant to C and P metabolism in maize roots from donor compartment under different P levels (mean ± SD). LP and HP refer to low P level (10 mg?kg-1) and high P level (100 mg?kg-1) respectively. AMD and NMD represent donor plants with and without AM fungus. Different letters above the columns indicate significant difference (p < 0.05) between corresponding treatments. # indicates significant difference (p < 0.05) between different P levels. Pht1;2, Pht1;6, P transporter genes; PEPC, phosphoenolpiruvate carboxylase gene; TC289, inorganic pyrophosphatase gene; G3PT, glycerol- 3-phosphate transporter gene; MAS1, malate synthase gene."

Fig. 6

Expression of genes relevant to C and P metabolism in maize roots from receiver compartment under different P levels (mean ± SD). LP and HP refer to low P level (10 mg?kg-1) and high P level (100 mg?kg-1) respectively. AMR and NMR represent receiver plants with and without AM exudates respectively. # indicates significant difference (p < 0.05) between different P levels, while $ indicates significant difference (p < 0.05) between inoculation treatments under the same P level. Pht1;2, Pht1;6, P transporter genes; PEPC, phosphoenolpiruvate carboxylase gene; TC289, inorganic pyrophosphatase gene; G3PT, glycerol-3-phosphate transporter gene; MAS1, malate synthase gene."

Appendix I

The PCR primer sequences for functional genes in maize plants"

基因 Gene 正向引物 Forward primer 反向引物 Reverse primer 文献 Reference
Action GTCCGTGCGTTTCCTTTTGT AAACCGGCCTTGACCATTCC Soderlund et al., 2009
Pht1;2 CCAACTTGCTTGGCTTTATCCT AGCCTCCCCGGACATCTC Schnable et al., 2009
Pht1;6 CTACAGCCAGAACCTGACCC ACATGACGCCCATCAGTAGC Schnable et al., 2009
G3PT TTCACCGCCTGCGTCCTT TCGCTGGGCTCCTCTTGAG Carlos et al., 2008
PEPC CACGCTGATCCTGACCATGA TCGCAAACCGAGTATGTATCTT Carlos et al., 2008
TC289 CCCTTGGCATGATCTGGAGAT CCTTGCTGCCCCTTGGTAT Carlos et al., 2008
MAS1 TGGACGCGTACAACCTCATC CTGACTCCACTGCCGACAAA Carlos et al., 2008

Appendix II

The PCR primer sequences for AM fungal genes"

基因 Gene 正向引物 Forward primer 反向引物 Reverse primer 文献 Reference
EF1β CCCATGCAGCTCGATGGTA TGCCAGGAAGTGAAGAAAATGA Yoshihiro et al., 2015
NGT1 TGGCGCAGCACTTTTGTG CGTTCGGTAGGGTAAGATAACATGA Yoshihiro et al., 2015
HXK1a CGATTGCCAACTGGTATGGA GCGCAAATTAGTCCCACCTAAG Yoshihiro et al., 2015
HXK1b GGAATCCCAACTGGCAAAGA ACATTCGTAAATTTGTACCTCCAAGA Yoshihiro et al., 2015
AGM1 AAAACAATTCGATCTGCTGAAGGT ATGCTCGTAATTTTTCGATTGCT Yoshihiro et al., 2015
UAP1 TGAACGCGTCAACCGAATC CGGTACCGGGAGCAATTTC Yoshihiro et al., 2015
CHS1 CGGCACAATTTAGGGATATAGTGA GGTTCCCCATGAATCAAACTAGTAA Yoshihiro et al., 2015
DAC1 TTTGGAAGAGTTGGTTAATTTTGGT AATACGGTCGCGGACGAA Yoshihiro et al., 2015
NAG1 GGCGTTAGCTCTTGCCAAGT CGCCGAAACGGTAAACATG Yoshihiro et al., 2015
GiPT CTGCTGTTGATTATTGTTGGC GAACGGTTCCCATAATAGTG Maldonado-Mendoza et al., 2001

Appendix III

Two-way ANOVA of shoot and root dry mass, P concentrations and expression of genes related to C and P metabolisms as influenced by mycorrhizal inoculation and soil P levels"

地上部干质量
Shoot dry mass
根系干质量
Root dry mass
地上部磷浓度
Shoot P concentration
根系磷浓度
Root P concentration
Pht1;2 Pht1;6 G3PT PEPC TC289 MAS1
供体植物 Donor
接种处理 Inoculation treatment (I) * ** * ** ** ** ** ** ns **
磷水平 P levels (P) ** ns ** ** ** ** ** ** ** ns
交互作用 I × P ** ** ns * ** ** ** ** ns **
受体植物 Receiver
接种处理 Inoculation treatment (I) ns ns ns ns ** ** ** ** ** **
磷水平 P levels (P) * * * * ** ** ** ** ** **
交互作用 I × P ns ns ns ns ns ** ** ** ** **
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