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Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

Postal Subscription Code 80-906

Front. Agr. Sci. Eng.    2020, Vol. 7 Issue (3) : 296-306    https://doi.org/10.15302/J-FASE-2020347
REVIEW
Arbuscular mycorrhizal associations and the major regulators
Li XUE1(), Ertao WANG2()
1. College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, China
2. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences (CAS), Shanghai 200032, China
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Abstract

Plants growing in natural soils encounter diverse biotic and abiotic stresses and have adapted with sophisticated strategies to deal with complex environments such as changing root system structure, evoking biochemical responses and recruiting microbial partners. Under selection pressure, plants and their associated microorganisms assemble into a functional entity known as a holobiont. The commonest cooperative interaction is between plant roots and arbuscular mycorrhizal (AM) fungi. About 80% of terrestrial plants can form AM symbiosis with the ancient phylum Glomeromycota. A very large network of extraradical and intraradical mycelium of AM fungi connects the underground biota and the nearby carbon and nutrient fluxes. Here, we discuss recent progress on the regulators of AM associations with plants, AM fungi and their surrounding environments, and explore further mechanistic insights.

Keywords AM symbiosis      signal      regulators      nutrients      phosphate      microbiota     
Corresponding Author(s): Li XUE,Ertao WANG   
Just Accepted Date: 11 June 2020   Online First Date: 13 July 2020    Issue Date: 28 July 2020
 Cite this article:   
Li XUE,Ertao WANG. Arbuscular mycorrhizal associations and the major regulators[J]. Front. Agr. Sci. Eng. , 2020, 7(3): 296-306.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2020347
https://academic.hep.com.cn/fase/EN/Y2020/V7/I3/296
Fig.1  Schematic of the development of the arbuscular mycorrhizal (AM) symbiosis and the major regulators involved at different stages. AM development is roughly characterized as four steps: (1) spore germination; (2) hyphal branching; (3) PPA and hyphopodium formation; and (4) arbuscule development. AM fungi facilitate nutrient uptake, meanwhile Pi and N starvation also contribute as master regulators in AM development. Strigolactones secreted from host roots induce fungal spore germination and hyphal branching (steps 1 and 2), while the biosynthesis of strigolactones is controlled by inorganic P (Pi) status, chitooligosaccharides (COs), zaxinone and autoregulation of mycorrhizal symbiosis (AOM) feedback signal CLE53. AM fungi produced chitinaceous molecules (COs and LCOs) to promote pre-symbiosis signaling and effectors/peptides (RiCRN, RiSLM, SIS and RiCLE) to increase fungal colonization (step 3). DELLA, the well-known negative regulator in gibberellin acid (GA) signaling, acts as a positive regulator in arbuscule development. CBX1/WRI5a regulate the gene module related to carbon-Pi exchange between plant and fungi in the arbuscule-containing cells (step 4).
1 S E Smith, F A Smith. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia, 2012, 104(1): 1–13
https://doi.org/10.3852/11-229 pmid: 21933929
2 W Wang, J Shi, Q Xie, Y Jiang, N Yu, E Wang. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Molecular Plant, 2017, 10(9): 1147–1158
https://doi.org/10.1016/j.molp.2017.07.012 pmid: 28782719
3 Y Jiang, W Wang, Q Xie, N Liu, L Liu, D Wang, X Zhang, C Yang, X Chen, D Tang, E Wang. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science, 2017, 356(6343): 1172–1175
https://doi.org/10.1126/science.aam9970 pmid: 28596307
4 L H Luginbuehl, G N Menard, S Kurup, H Van Erp, G V Radhakrishnan, A Breakspear, G E D Oldroyd, P J Eastmond. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science, 2017, 356(6343): 1175–1178
https://doi.org/10.1126/science.aan0081 pmid: 28596311
5 A Keymer, P Pimprikar, V Wewer, C Huber, M Brands, S L Bucerius, P M Delaux, V Klingl, E V Röpenack-Lahaye, T L Wang, W Eisenreich, P Dörmann, M Parniske, C Gutjahr. Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife, 2017, 6: e29107
https://doi.org/10.7554/eLife.29107 pmid: 28726631
6 C Gutjahr, M Parniske. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology, 2013, 29(1): 593–617
https://doi.org/10.1146/annurev-cellbio-101512-122413 pmid: 24099088
7 M T Waters, C Gutjahr, T Bennett, D C Nelson. Strigolactone signaling and evolution. Annual Review of Plant Biology, 2017, 68(1): 291–322
https://doi.org/10.1146/annurev-arplant-042916-040925 pmid: 28125281
8 K Akiyama, K Matsuzaki, H Hayashi. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 2005, 435(7043): 824–827
https://doi.org/10.1038/nature03608 pmid: 15944706
9 A Besserer, V Puech-Pagès, P Kiefer, V Gomez-Roldan, A Jauneau, S Roy, J C Portais, C Roux, G Bécard, N Séjalon-Delmas. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology, 2006, 4(7): e226
https://doi.org/10.1371/journal.pbio.0040226 pmid: 16787107
10 Y Kobae, H Kameoka, Y Sugimura, K Saito, R Ohtomo, T Fujiwara, J Kyozuka. Strigolactone biosynthesis genes of rice arerequired for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant & Cell Physiology, 2018, 59(3): 544–553
https://doi.org/10.1093/pcp/pcy001 pmid: 29325120
11 W Liu, W Kohlen, A Lillo, R Op den Camp, S Ivanov, M Hartog, E Limpens, M Jamil, C Smaczniak, K Kaufmann, W C Yang, G J E J Hooiveld, T Charnikhova, H J Bouwmeester, T Bisseling, R Geurts. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell, 2011, 23(10): 3853–3865
https://doi.org/10.1105/tpc.111.089771 pmid: 22039214
12 A Genre, M Chabaud, C Balzergue, V Puech-Pagès, M Novero, T Rey, J Fournier, S Rochange, G Bécard, P Bonfante, D G Barker. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist, 2013, 198(1): 190–202
https://doi.org/10.1111/nph.12146 pmid: 23384011
13 M Giovannetti, A Mari, M Novero, P Bonfante. Early Lotus japonicus root transcriptomic responses to symbiotic and pathogenic fungal exudates. Frontiers of Plant Science, 2015, 6: 480
https://doi.org/10.3389/fpls.2015.00480 pmid: 26175746
14 K Abdel-Lateif, D Bogusz, V Hocher. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signaling & Behavior, 2012, 7(6): 636–641
https://doi.org/10.4161/psb.20039 pmid: 22580697
15 J M M Aguilar, A M Ashby, A J M Richards, G J Loake, M D Watson, C H Shaw. Chemotaxis of Rhizobium leguminosarum towards flavonoid inducers of the symbiotic nodulation genes. Journal of General and Applied Microbiology, 1988, 134(10): 2741–2746
16 A J Dharmatilake, W D Bauer. Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Applied and Environmental Microbiology, 1992, 58(4): 1153–1158
https://doi.org/10.1128/AEM.58.4.1153-1158.1992 pmid: 16348685
17 G Bécard, D D Douds, P E Pfeffer. Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal gungi in the presence of CO2 and flavonols. Applied and Environmental Microbiology, 1992, 58(3): 821–825
https://doi.org/10.1128/AEM.58.3.821-825.1992 pmid: 16348673
18 G Nagahashi, D D Douds Jr. The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biology, 2011, 115(4–5): 351–358
https://doi.org/10.1016/j.funbio.2011.01.006 pmid: 21530917
19 E A Fich, N A Segerson, J K C Rose. The plant polyester cutin: biosynthesis, structure, and biological roles. Annual Review of Plant Biology, 2016, 67(1): 207–233
https://doi.org/10.1146/annurev-arplant-043015-111929 pmid: 26865339
20 E Wang, S Schornack, J F Marsh, E Gobbato, B Schwessinger, P Eastmond, M Schultze, S Kamoun, G E D Oldroyd. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology, 2012, 22(23): 2242–2246
https://doi.org/10.1016/j.cub.2012.09.043 pmid: 23122843
21 J Y Wang, I Haider, M Jamil, V Fiorilli, Y Saito, J Mi, L Baz, B A Kountche, K P Jia, X Guo, A Balakrishna, V O Ntui, B Reinke, V Volpe, T Gojobori, I Blilou, L Lanfranco, P Bonfante, S Al-Babili. The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice. Nature Communications, 2019, 10(1): 810
https://doi.org/10.1038/s41467-019-08461-1 pmid: 30778050
22 D C Nelson, G R Flematti, E L Ghisalberti, K W Dixon, S M Smith. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annual Review of Plant Biology, 2012, 63(1): 107–130
https://doi.org/10.1146/annurev-arplant-042811-105545 pmid: 22404467
23 N Morffy, L Faure, D C Nelson. Smoke and hormone mirrors: action and evolution of karrikin and strigolactone signaling. Trends in Genetics, 2016, 32(3): 176–188
https://doi.org/10.1016/j.tig.2016.01.002 pmid: 26851153
24 C Gutjahr, E Gobbato, J Choi, M Riemann, M G Johnston, W Summers, S Carbonnel, C Mansfield, S Y Yang, M Nadal, I Acosta, M Takano, W B Jiao, K Schneeberger, K A Kelly, U Paszkowski. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science, 2015, 350(6267): 1521–1524
https://doi.org/10.1126/science.aac9715 pmid: 26680197
25 J A Villaécija-Aguilar, M Hamon-Josse, S Carbonnel, A Kretschmar, C Schmidt, C Dawid, T Bennett, C Gutjahr. SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis. PLOS Genetics, 2019, 15(8): e1008327
https://doi.org/10.1371/journal.pgen.1008327 pmid: 31465451
26 P N McGuiness, J B Reid, E Foo. The role of gibberellins and brassinosteroids in nodulation and arbuscular mycorrhizal associations. Frontiers of Plant Science, 2019, 10: 269
https://doi.org/10.3389/fpls.2019.00269 pmid: 30930916
27 C Jiang, X Gao, L Liao, N P Harberd, X Fu. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiology, 2007, 145(4): 1460–1470
https://doi.org/10.1104/pp.107.103788 pmid: 17932308
28 D S Floss, J G Levy, V Lévesque-Tremblay, N Pumplin, M J Harrison. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(51): E5025–E5034
https://doi.org/10.1073/pnas.1308973110 pmid: 24297892
29 N Yu, D Luo, X Zhang, J Liu, W Wang, Y Jin, W Dong, J Liu, H Liu, W Yang, L Zeng, Q Li, Z He, G E D Oldroyd, E Wang. A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Research, 2014, 24(1): 130–133
https://doi.org/10.1038/cr.2013.167 pmid: 24343576
30 Y Jin, H Liu, D Luo, N Yu, W Dong, C Wang, X Zhang, H Dai, J Yang, E Wang. DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications, 2016, 7(1): 12433
https://doi.org/10.1038/ncomms12433 pmid: 27514472
31 P Pimprikar, S Carbonnel, M Paries, K Katzer, V Klingl, M J Bohmer, L Karl, D S Floss, M J Harrison, M Parniske, C Gutjahr. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Current Biology, 2016, 26(8): 987–998
https://doi.org/10.1016/j.cub.2016.01.069 pmid: 27020747
32 D S Floss, S K Gomez, H J Park, A M MacLean, L M Müller, K K Bhattarai, V Lévesque-Tremblay, I E Maldonado-Mendoza, M J Harrison. A transcriptional program for arbuscule degeneration during AM symbiosis is regulated by MYB1. Current Biology, 2017, 27(8): 1206–1212
https://doi.org/10.1016/j.cub.2017.03.003 pmid: 28392110
33 C Heck, H Kuhn, S Heidt, S Walter, N Rieger, N Requena. Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Current Biology, 2016, 26(20): 2770–2778
https://doi.org/10.1016/j.cub.2016.07.059 pmid: 27641773
34 D S Floss, V Lévesque-Tremblay, H J Park, M J Harrison. DELLA proteins regulate expression of a subset of AM symbiosis-induced genes in Medicago truncatula. Plant Signaling & Behavior, 2016, 11(4): e1162369
https://doi.org/10.1080/15592324.2016.1162369 pmid: 26984507
35 L Xue, H Cui, B Buer, V Vijayakumar, P M Delaux, S Junkermann, M Bucher. Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiology, 2015, 167(3): 854–871
https://doi.org/10.1104/pp.114.255430 pmid: 25560877
36 S Hirsch, J Kim, A Muñoz, A B Heckmann, J A Downie, G E D Oldroyd. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell, 2009, 21(2): 545–557
https://doi.org/10.1105/tpc.108.064501 pmid: 19252081
37 E Gobbato, J F Marsh, T Vernié, E Wang, F Maillet, J Kim, J B Miller, J Sun, S A Bano, P Ratet, K S Mysore, J Dénarié, M Schultze, G E D Oldroyd. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Current Biology, 2012, 22(23): 2236–2241
https://doi.org/10.1016/j.cub.2012.09.044 pmid: 23122845
38 F Liaqat, R Eltem. Chitooligosaccharides and their biological activities: a comprehensive review. Carbohydrate Polymers, 2018, 184: 243–259
https://doi.org/10.1016/j.carbpol.2017.12.067 pmid: 29352917
39 Y Cao, M K Halane, W Gassmann, G Stacey. The role of plant innate immunity in the legume-rhizobium symbiosis. Annual Review of Plant Biology, 2017, 68(1): 535–561
https://doi.org/10.1146/annurev-arplant-042916-041030 pmid: 28142283
40 F Maillet, V Poinsot, O André, V Puech-Pagès, A Haouy, M Gueunier, L Cromer, D Giraudet, D Formey, A Niebel, E A Martinez, H Driguez, G Bécard, J Dénarié. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 2011, 469(7328): 58–63
https://doi.org/10.1038/nature09622 pmid: 21209659
41 F Feng, J Sun, G V Radhakrishnan, T Lee, Z Bozsóki, S Fort, A Gavrin, K Gysel, M B Thygesen, K R Andersen, S Radutoiu, J Stougaard, G E D Oldroyd. A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula. Nature Communications, 2019, 10(1): 5047
https://doi.org/10.1038/s41467-019-12999-5 pmid: 31695035
42 J Dénarié, F Debellé, J C Promé. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry, 1996, 65(1): 503–535
https://doi.org/10.1146/annurev.bi.65.070196.002443 pmid: 8811188
43 C Zipfel, G E D Oldroyd. Plant signalling in symbiosis and immunity. Nature, 2017, 543(7645): 328–336
https://doi.org/10.1038/nature22009 pmid: 28300100
44 E B Madsen, L H Madsen, S Radutoiu, M Olbryt, M Rakwalska, K Szczyglowski, S Sato, T Kaneko, S Tabata, N Sandal, J Stougaard. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature, 2003, 425(6958): 637–640
https://doi.org/10.1038/nature02045 pmid: 14534591
45 S Radutoiu, L H Madsen, E B Madsen, H H Felle, Y Umehara, M Grønlund, S Sato, Y Nakamura, S Tabata, N Sandal, J Stougaard. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 2003, 425(6958): 585–592
https://doi.org/10.1038/nature02039 pmid: 14534578
46 Y Cao, Y Liang, K Tanaka, C T Nguyen, R P Jedrzejczak, A Joachimiak, G Stacey. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife, 2014, 3: e03766
https://doi.org/10.7554/eLife.03766 pmid: 25340959
47 M Hayafune, R Berisio, R Marchetti, A Silipo, M Kayama, Y Desaki, S Arima, F Squeglia, A Ruggiero, K Tokuyasu, A Molinaro, H Kaku, N Shibuya. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(3): E404–E413
https://doi.org/10.1073/pnas.1312099111 pmid: 24395781
48 X Zhang, W Dong, J Sun, F Feng, Y Deng, Z He, G E D Oldroyd, E Wang. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant Journal, 2015, 81(2): 258–267
https://doi.org/10.1111/tpj.12723 pmid: 25399831
49 K Miyata, T Kozaki, Y Kouzai, K Ozawa, K Ishii, E Asamizu, Y Okabe, Y Umehara, A Miyamoto, Y Kobae, K Akiyama, H Kaku, Y Nishizawa, N Shibuya, T Nakagawa. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant & Cell Physiology, 2014, 55(11): 1864–1872
https://doi.org/10.1093/pcp/pcu129 pmid: 25231970
50 J Sun, J B Miller, E Granqvist, A Wiley-Kalil, E Gobbato, F Maillet, S Cottaz, E Samain, M Venkateshwaran, S Fort, R J Morris, J M Ané, J Dénarié, G E D Oldroyd. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell, 2015, 27(3): 823–838
https://doi.org/10.1105/tpc.114.131326 pmid: 25724637
51 J He, C Zhang, H Dai, H Liu, X Zhang, J Yang, X Chen, Y Zhu, D Wang, X Qi, W Li, Z Wang, G An, N Yu, Z He, Y F Wang, Y Xiao, P Zhang, E Wang. A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Molecular Plant, 2019, 12(12): 1561–1576
https://doi.org/10.1016/j.molp.2019.10.015 pmid: 31706032
52 R Huang, Z Li, C Mao, H Zhang, Z Sun, H Li, C Huang, Y Feng, X Shen, M Bucher, Z Zhang, Y Lin, Y Cao, D Duanmu. Natural variation at OsCERK1 regulates arbuscular mycorrhizal symbiosis in rice. New Phytologist, 2020, 225(4): 1762–1776
https://doi.org/10.1111/nph.16158 pmid: 31484206
53 A Girardin, T M Wang, Y Ding, J Keller, L Buendia, M Gaston, C Ribeyre, V Gasciolli, M C Auriac, T Vernie, A Bendahmane, M K Ried, M Parniske, P Morel, M Vandenbussche, M Schorderet, D Reinhardt, P M Delaux, J J Bono, B. LefebvreLCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biology, 2019, 29(24): 4249–4259. e5
54 Y Kobae, M Kawachi, K Saito, Y Kikuchi, T Ezawa, M Maeshima, S Hata, T Fujiwara. Up-regulation of genes involved in N-acetylglucosamine uptake and metabolism suggests a recycling mode of chitin in intraradical mycelium of arbuscular mycorrhizal fungi. Mycorrhiza, 2015, 25(5): 411–417
https://doi.org/10.1007/s00572-014-0623-2 pmid: 25564438
55 M Nadal, R Sawers, S Naseem, B Bassin, C Kulicke, A Sharman, G An, K An, K R Ahern, A Romag, T P Brutnell, C Gutjahr, N Geldner, C Roux, E Martinoia, J B Konopka, U Paszkowski. An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nature Plants, 2017, 3(6): 17073
https://doi.org/10.1038/nplants.2017.73 pmid: 28548655
56 L Kamel, N Tang, M Malbreil, H San Clemente, M Le Marquer, C Roux, N Frei Dit Frey. The comparison of expressed candidate secreted proteins from two arbuscular mycorrhizal fungi unravels common and specific molecular tools to invade different host plants. Frontiers of Plant Science, 2017, 8: 124
https://doi.org/10.3389/fpls.2017.00124 pmid: 28223991
57 M Le Marquer, H San Clemente, C Roux, B Savelli, N Frei Dit Frey. Identification of new signalling peptides through a genome-wide survey of 250 fungal secretomes. BMC Genomics, 2019, 20(1): 64
https://doi.org/10.1186/s12864-018-5414-2 pmid: 30658568
58 K Sędzielewska Toro, A Brachmann. The effector candidate repertoire of the arbuscular mycorrhizal fungus Rhizophagus clarus. BMC Genomics, 2016, 17(1): 101
https://doi.org/10.1186/s12864-016-2422-y pmid: 26861502
59 T Zeng, R Holmer, J Hontelez, B Te Lintel-Hekkert, L Marufu, T de Zeeuw, F Wu, E Schijlen, T Bisseling, E Limpens. Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant Journal, 2018, 94(3): 411–425
https://doi.org/10.1111/tpj.13908 pmid: 29570877
60 S Kloppholz, H Kuhn, N Requena. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Current Biology, 2011, 21(14): 1204–1209
https://doi.org/10.1016/j.cub.2011.06.044 pmid: 21757354
61 S Voß, R Betz, S Heidt, N Corradi, N Requena. RiCRN1, a crinkler effector from the arbuscular mycorrhizal fungus Rhizophagus irregularis, functions in arbuscule development. Frontiers in Microbiology, 2018, 9: 2068
https://doi.org/10.3389/fmicb.2018.02068 pmid: 30233541
62 S Tsuzuki, Y Handa, N Takeda, M Kawaguchi. Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Molecular Plant-Microbe Interactions, 2016, 29(4): 277–286
https://doi.org/10.1094/MPMI-10-15-0234-R pmid: 26757243
63 T Zeng, L Rodriguez-Moreno, A Mansurkhodzaev, P Wang, W van den Berg, V Gasciolli, S Cottaz, S Fort, B P H J Thomma, J J Bono, T Bisseling, E Limpens. A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytologist, 2020, 225(1): 448–460
https://doi.org/10.1111/nph.16245 pmid: 31596956
64 A M Schmitz, T E Pawlowska, M J Harrison. A short LysM protein with high molecular diversity from an arbuscular mycorrhizal fungus, Rhizophagus irregularis. Mycoscience, 2019, 60(1): 63–70
https://doi.org/10.1016/j.myc.2018.09.002
65 S E Smith, F A Smith. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 2011, 62(1): 227–250
https://doi.org/10.1146/annurev-arplant-042110-103846 pmid: 21391813
66 C Santi, D Bogusz, C Franche. Biological nitrogen fixation in non-legume plants. Annals of Botany, 2013, 111(5): 743–767
https://doi.org/10.1093/aob/mct048 pmid: 23478942
67 B J Ferguson, C Mens, A H Hastwell, M Zhang, H Su, C H Jones, X Chu, P M Gresshoff. Legume nodulation: the host controls the party. Plant, Cell & Environment, 2019, 42(1): 41–51
https://doi.org/10.1111/pce.13348 pmid: 29808564
68 S E Smith, F A Smith, I Jakobsen. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology, 2003, 133(1): 16–20
https://doi.org/10.1104/pp.103.024380 pmid: 12970469
69 S E Smith, F A Smith, I Jakobsen. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist, 2004, 162(2): 511–524
https://doi.org/10.1111/j.1469-8137.2004.01039.x
70 L Nussaume, S Kanno, H Javot, E Marin, N Pochon, A Ayadi, T M Nakanishi, M C Thibaud. Phosphate import in plants: focus on the PHT1 transporters. Frontiers of Plant Science, 2011, 2: 83
https://doi.org/10.3389/fpls.2011.00083 pmid: 22645553
71 M Bucher. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 2007, 173(1): 11–26
https://doi.org/10.1111/j.1469-8137.2006.01935.x pmid: 17176390
72 V Loth-Pereda, E Orsini, P E Courty, F Lota, A Kohler, L Diss, D Blaudez, M Chalot, U Nehls, M Bucher, F Martin. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiology, 2011, 156(4): 2141–2154
https://doi.org/10.1104/pp.111.180646 pmid: 21705655
73 F Walder, D Brulé, S Koegel, A Wiemken, T Boller, P E Courty. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytologist, 2015, 205(4): 1632–1645
https://doi.org/10.1111/nph.13292 pmid: 25615409
74 C Rausch, M Bucher. Molecular mechanisms of phosphate transport in plants. Planta, 2002, 216(1): 23–37
https://doi.org/10.1007/s00425-002-0921-3 pmid: 12430011
75 V Karandashov, M Bucher. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science, 2005, 10(1): 22–29
https://doi.org/10.1016/j.tplants.2004.12.003 pmid: 15642520
76 H Javot, R V Penmetsa, N Terzaghi, D R Cook, M J Harrison. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(5): 1720–1725
https://doi.org/10.1073/pnas.0608136104 pmid: 17242358
77 S Y Yang, M Grønlund, I Jakobsen, M S Grotemeyer, D Rentsch, A Miyao, H Hirochika, C S Kumar, V Sundaresan, N Salamin, S Catausan, N Mattes, S Heuer, U Paszkowski. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell, 2012, 24(10): 4236–4251
https://doi.org/10.1105/tpc.112.104901 pmid: 23073651
78 M Willmann, N Gerlach, B Buer, A Polatajko, R Nagy, E Koebke, J Jansa, R Flisch, M Bucher. Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Frontiers of Plant Science, 2013, 4: 533
https://doi.org/10.3389/fpls.2013.00533 pmid: 24409191
79 L Xue, L Klinnawee, Y Zhou, G Saridis, V Vijayakumar, M Brands, P Dörmann, T Gigolashvili, F Turck, M Bucher. AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(39): E9239–E9246
https://doi.org/10.1073/pnas.1812275115 pmid: 30209216
80 Y Jiang, Q Xie, W Wang, J Yang, X Zhang, N Yu, Y Zhou, E Wang. Medicago AP2-domain transcription factor WRI5a is a master regulator of lipid biosynthesis and transfer during mycorrhizal symbiosis. Molecular Plant, 2018, 11(11): 1344–1359
https://doi.org/10.1016/j.molp.2018.09.006 pmid: 30292683
81 F Krajinski, P E Courty, D Sieh, P Franken, H Zhang, M Bucher, N Gerlach, I Kryvoruchko, D Zoeller, M Udvardi, B Hause. The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell, 2014, 26(4): 1808–1817
https://doi.org/10.1105/tpc.113.120436 pmid: 24781114
82 E Wang, N Yu, S A Bano, C Liu, A J Miller, D Cousins, X Zhang, P Ratet, M Tadege, K S Mysore, J A Downie, J D Murray, G E D Oldroyd, M Schultze. A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell, 2014, 26(4): 1818–1830
https://doi.org/10.1105/tpc.113.120527 pmid: 24781115
83 J Liu, J Chen, K Xie, Y Tian, A Yan, J Liu, Y Huang, S Wang, Y Zhu, A Chen, G Xu. A mycorrhiza-specific H+-ATPase is essential for arbuscule development and symbiotic phosphate and nitrogen uptake. Plant, Cell & Environment, 2020, 43(4): 1069–1083
https://doi.org/10.1111/pce.13714 pmid: 31899547
84 M Govindarajulu, P E Pfeffer, H Jin, J Abubaker, D D Douds, J W Allen, H Bücking, P J Lammers, Y Shachar-Hill. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 2005, 435(7043): 819–823
https://doi.org/10.1038/nature03610 pmid: 15944705
85 D Wipf, F Krajinski, D van Tuinen, G Recorbet, P E Courty. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytologist, 2019, 223(3): 1127–1142
https://doi.org/10.1111/nph.15775 pmid: 30843207
86 M Guether, R Balestrini, M Hannah, J He, M K Udvardi, P Bonfante. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist, 2009, 182(1): 200–212
https://doi.org/10.1111/j.1469-8137.2008.02725.x pmid: 19192192
87 Y Handa, H Nishide, N Takeda, Y Suzuki, M Kawaguchi, K Saito. RNA-seq transcriptional profiling of an arbuscular mycorrhiza provides insights into regulated and coordinated gene expression in Lotus japonicus and Rhizophagus irregularis. Plant & Cell Physiology, 2015, 56(8): 1490–1511
https://doi.org/10.1093/pcp/pcv071 pmid: 26009592
88 Y Sugimura, K Saito. Comparative transcriptome analysis between Solanum lycopersicum L. and Lotus japonicus L. during arbuscular mycorrhizal development. Soil Science and Plant Nutrition, 2017, 63(2): 127–136
https://doi.org/10.1080/00380768.2017.1280378
89 J Liu, J Liu, J Liu, M Cui, Y Huang, Y Tian, A Chen, G Xu. The potassium transporter SlHAK10 is involved in mycorrhizal potassium uptake. Plant Physiology, 2019, 180(1): 465–479
https://doi.org/10.1104/pp.18.01533 pmid: 30760639
90 E Nouri, F Breuillin-Sessoms, U Feller, D Reinhardt. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS One, 2014, 9(6): e90841
https://doi.org/10.1371/journal.pone.0090841 pmid: 24608923
91 F Breuillin, J Schramm, M Hajirezaei, A Ahkami, P Favre, U Druege, B Hause, M Bucher, T Kretzschmar, E Bossolini, C Kuhlemeier, E Martinoia, P Franken, U Scholz, D Reinhardt. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant Journal, 2010, 64(6): 1002–1017
https://doi.org/10.1111/j.1365-313X.2010.04385.x pmid: 21143680
92 V Blanke, C Renker, M Wagner, K Füllner, M Held, A J Kuhn, F Buscot. Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytologist, 2005, 166(3): 981–992
https://doi.org/10.1111/j.1469-8137.2005.01374.x pmid: 15869657
93 F Breuillin-Sessoms, D S Floss, S K Gomez, N Pumplin, Y Ding, V Levesque-Tremblay, R D Noar, D A Daniels, A Bravo, J B Eaglesham, V A Benedito, M K Udvardi, M J Harrison. Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell, 2015, 27(4): 1352–1366
https://doi.org/10.1105/tpc.114.131144 pmid: 25841038
94 J Dong, G Ma, L Sui, M Wei, V Satheesh, R Zhang, S Ge, J Li, T E Zhang, C Wittwer, H J Jessen, H Zhang, G Y An, D Y Chao, D Liu, M Lei. Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Molecular Plant, 2019, 12(11): 1463–1473
https://doi.org/10.1016/j.molp.2019.08.002 pmid: 31419530
95 C H Ho, S H Lin, H C Hu, Y F Tsay. CHL1 functions as a nitrate sensor in plants. Cell, 2009, 138(6): 1184–1194
https://doi.org/10.1016/j.cell.2009.07.004 pmid: 19766570
96 K H Liu, C Y Huang, Y F Tsay. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell, 1999, 11(5): 865–874
https://doi.org/10.1105/tpc.11.5.865 pmid: 10330471
97 Y F Tsay, J I Schroeder, K A Feldmann, N M Crawford. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell, 1993, 72(5): 705–713
https://doi.org/10.1016/0092-8674(93)90399-B pmid: 8453665
98 K Garcia, D Chasman, S Roy, J M Ané. Physiological responses and gene co-expression network of mycorrhizal roots under K+ deprivation. Plant Physiology, 2017, 173(3): 1811–1823
https://doi.org/10.1104/pp.16.01959 pmid: 28159827
99 J F Briat, H Rouached, N Tissot, F Gaymard, C Dubos. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Frontiers of Plant Science, 2015, 6: 290
https://doi.org/10.3389/fpls.2015.00290 pmid: 25972885
100 X Xie, W Hu, X Fan, H Chen, M Tang. Interactions between phosphorus, zinc, and iron homeostasis in nonmycorrhizal and mycorrhizal plants. Frontiers of Plant Science, 2019, 10: 1172
https://doi.org/10.3389/fpls.2019.01172 pmid: 31616454
101 Y Hirakawa, S Sawa. Diverse function of plant peptide hormones in local signaling and development. Current Opinion in Plant Biology, 2019, 51: 81–87
https://doi.org/10.1016/j.pbi.2019.04.005 pmid: 31132657
102 T C de Bang, P K Lundquist, X Dai, C Boschiero, Z Zhuang, P Pant, I Torres-Jerez, S Roy, J Nogales, V Veerappan, R Dickstein, M K Udvardi, P X Zhao, W R Scheible. Genome-wide identification of Medicago peptides involved in macronutrient responses and nodulation. Plant Physiology, 2017, 175(4): 1669–1689
https://doi.org/10.1104/pp.17.01096 pmid: 29030416
103 V Mortier, G Den Herder, R Whitford, W Van de Velde, S Rombauts, K D’Haeseleer, M Holsters, S Goormachtig. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiology, 2010, 153(1): 222–237
https://doi.org/10.1104/pp.110.153718 pmid: 20348212
104 D Tsikou, Z Yan, D B Holt, N B Abel, D E Reid, L H Madsen, H Bhasin, M Sexauer, J Stougaard, K Markmann. Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA. Science, 2018, 362(6411): 233–236
https://doi.org/10.1126/science.aat6907 pmid: 30166437
105 T Sasaki, T Suzaki, T Soyano, M Kojima, H Sakakibara, M Kawaguchi. Shoot-derived cytokinins systemically regulate root nodulation. Nature Communications, 2014, 5(1): 4983
https://doi.org/10.1038/ncomms5983 pmid: 25236855
106 D Morandi, M Sagan, E Prado-Vivant, G Duc. Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza, 2000, 10(1): 37–42
https://doi.org/10.1007/s005720050285
107 M Z Solaiman, K Senoo, M Kawaguchi, H Imaizumi-Anraku, S Akao, A Tanaka, H Obata. Characterization of mycorrhizas fglomus sp. on roots of hypernodulating mutants of Lotus japonicus. Journal of Plant Research, 2000, 113(4): 443–448
https://doi.org/10.1007/PL00013953
108 K Sakamoto, Y Nohara. Soybean (Glycine max [L.] Merr.) shoots systemically control arbuscule formation in mycorrhizal symbiosis. Soil Science and Plant Nutrition, 2009, 55(2): 252–257
https://doi.org/10.1111/j.1747-0765.2009.00358.x
109 L M Müller, K Flokova, E Schnabel, X Sun, Z Fei, J Frugoli, H J Bouwmeester, M J Harrison. A CLE-SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza. Nature Plants, 2019, 5(9): 933–939
https://doi.org/10.1038/s41477-019-0501-1 pmid: 31477892
110 M Le Marquer, G Bécard, N Frei Dit Frey. Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis. New Phytologist, 2019, 222(2): 1030–1042
https://doi.org/10.1111/nph.15643 pmid: 30554405
111 J A Vorholt, C Vogel, C I Carlström, D B Müller. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host & Microbe, 2017, 22(2): 142–155
https://doi.org/10.1016/j.chom.2017.07.004 pmid: 28799900
112 T Thiergart, R Zgadzaj, Z Bozsóki, R Garrido-Oter, S Radutoiu, P Schulze-Lefert. Lotus japonicus symbiosis genes impact microbial interactions between symbionts and multikingdom commensal communities. mBio, 2019, 10(5): e01833-19
https://doi.org/10.1128/mBio.01833-19 pmid: 31594815
113 L Xue, J Almario, I Fabiańska, G Saridis, M Bucher. Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus. New Phytologist, 2019, 224(1): 409–420
https://doi.org/10.1111/nph.15958 pmid: 31125425
114 E Wang, S Schornack, J F Marsh, E Gobbato, B Schwessinger, P Eastmond, M Schultze, S Kamoun, G E D Oldroyd. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology, 2012, 22(23): 2242–2246
https://doi.org/10.1016/j.cub.2012.09.043 pmid: 23122843
115 A Banhara, Y Ding, R Kühner, A Zuccaro, M Parniske. Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes. Frontiers of Plant Science, 2015, 6: 667
https://doi.org/10.3389/fpls.2015.00667 pmid: 26441999
116 R Huisman, K Bouwmeester, M Brattinga, F Govers, T Bisseling, E Limpens. Haustorium formation in Medicago truncatula roots infected by Phytophthora palmivora does not involve the common endosymbiotic program shared by arbuscular mycorrhizal fungi and rhizobia. Molecular Plant-Microbe Interactions, 2015, 28(12): 1271–1280
https://doi.org/10.1094/MPMI-06-15-0130-R pmid: 26313411
117 T Rey, A Chatterjee, M Buttay, J Toulotte, S Schornack. Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytologist, 2015, 206(2): 497–500
https://doi.org/10.1111/nph.13233 pmid: 25495186
118 X L Wang, M X Wang, X G Xie, S Y Guo, Y Zhou, X B Zhang, N Yu, E T Wang. An amplification-selection model for quantified rhizosphere microbiota assembly. Science Bulletin, 2020, 65(12): 983–986
https://doi.org/10.1016/j.scib.2020.03.005
119 I Fabiańska, N Gerlach, J Almario, M Bucher. Plant-mediated effects of soil phosphorus on the root-associated fungal microbiota in Arabidopsis thaliana. New Phytologist, 2019, 221(4): 2123–2137
https://doi.org/10.1111/nph.15538 pmid: 30317641
120 J A López-Ráez, K Shirasu, E Foo. Strigolactones in plant interactions with beneficial and detrimental organisms: the Yin and Yang. Trends in Plant Science, 2017, 22(6): 527–537
https://doi.org/10.1016/j.tplants.2017.03.011 pmid: 28400173
121 I Fabiańska, E Sosa-Lopez, M Bucher. The role of nutrient balance in shaping plant root-fungal interactions: facts and speculation. Current Opinion in Microbiology, 2019, 49: 90–96
https://doi.org/10.1016/j.mib.2019.10.004 pmid: 31733616
122 G Castrillo, P J P L Teixeira, S H Paredes, T F Law, L de Lorenzo, M E Feltcher, O M Finkel, N W Breakfield, P Mieczkowski, C D Jones, J Paz-Ares, J L Dangl. Root microbiota drive direct integration of phosphate stress and immunity. Nature, 2017, 543(7646): 513–518
https://doi.org/10.1038/nature21417 pmid: 28297714
123 J Almario, G Jeena, J Wunder, G Langen, A Zuccaro, G Coupland, M Bucher. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(44): E9403–E9412
https://doi.org/10.1073/pnas.1710455114 pmid: 28973917
124 K Hiruma, N Gerlach, S Sacristán, R T Nakano, S Hacquard, B Kracher, U Neumann, D Ramírez, M Bucher, R J O’Connell, P Schulze-Lefert. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell, 2016, 165(2): 464–474
https://doi.org/10.1016/j.cell.2016.02.028 pmid: 26997485
125 M Bakshi, K Vahabi, S Bhattacharya, I Sherameti, A Varma, K W Yeh, I Baldwin, A K Johri, R Oelmüller. WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biology, 2015, 15(1): 305
https://doi.org/10.1186/s12870-015-0673-4 pmid: 26718529
126 P Frey-Klett, J Garbaye, M Tarkka. The mycorrhiza helper bacteria revisited. New Phytologist, 2007, 176(1): 22–36
https://doi.org/10.1111/j.1469-8137.2007.02191.x pmid: 17803639
127 A Salvioli, S Ghignone, M Novero, L Navazio, F Venice, P Bagnaresi, P Bonfante. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME Journal, 2016, 10(1): 130–144
https://doi.org/10.1038/ismej.2015.91 pmid: 26046255
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