Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Impact of arbuscular mycorrhizal fungi (AMF) on cucumber growth and phosphorus uptake under cold stress

Jun Ma A B , Martina Janoušková C , Yansu Li B , Xianchang Yu B , Yan Yan B , Zhirong Zou A D and Chaoxing He B D
+ Author Affiliations
- Author Affiliations

A College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712 100, PR China.

B Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100 081, PR China.

C Institute of Botany, Academy of Sciences of the Czech Republic, 25 243 Pruhonice, Czech Republic.

D Corresponding authors. Emails: zouzhirong2005@hotmail.com; hechaoxing@126.com

Functional Plant Biology 42(12) 1158-1167 https://doi.org/10.1071/FP15106
Submitted: 10 December 2014  Accepted: 30 September 2015   Published: 4 November 2015

Abstract

Symbiosis with root-associated arbuscular mycorrhizal fungi (AMF) can improve plant phosphorus (P) uptake and alleviate environmental stresses. It could be also an effective mean to promote plant performance under low temperatures. The combined effects of arbuscular mycorrhiza and low temperature (15°C/10°C day/night) on cucumber seedlings were investigated in the present study. Root colonisation by AMF, succinate dehydrogenase and alkaline phosphatase activity in the intraradical fungal structures, plant growth parameters, and expression profiles of four cucumber phosphate (Pi) transporters, the fungal Pi transporter GintPT and alkaline phosphatase GintALP were determined. Cold stress reduced plant growth and mycorrhizal colonisation. Inoculation improved cucumber growth under ambient temperatures, whereas under cold stress only root biomass was significantly increased by inoculation. AMF supplied P to the host plant under ambient temperatures and cold stress, as evidenced by the higher P content of mycorrhizal plants compared with non-mycorrhizal plants. Thus, the cold-stressed cucumber seedlings still benefited from mycorrhiza, although the benefit was less than that under ambient temperatures. In accordance with this, a cucumber Pi transporter gene belonging to the Pht1 gene family was strongly induced by mycorrhiza at ambient temperature and to a lesser extent under cold stress. The other three Pi transporters tested from different families were most highly expressed in cold-stressed mycorrhizal plants, suggesting a complex interactive effect of mycorrhiza and cold stress on internal P cycling in cucumber plants.

Additional keywords: Cucumis sativus, low temperature, mycorrhizal growth response, Rhizophagus irregularis, phosphate transporter.


References

Aono T, Maldonado-Mendoza IE, Dewbre GR, Harrison MJ, Saito M (2004) Expression of alkaline phosphatase genes in arbuscular mycorrhizas. New Phytologist 162, 525–534.
Expression of alkaline phosphatase genes in arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVWjurk%3D&md5=2b90e6aca6a546ba8605250c9dcfb343CAS |

Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Molecular Plant-Microbe Interactions 20, 1055–1062.
Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGktbs%3D&md5=8feb8bffb3d204a1dadf98eecc495858CAS | 17849708PubMed |

Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nature Communications 1, 48
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 20975705PubMed |

Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter 4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. The Plant Cell 27, 1352–1366.
Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter 4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosV2qtbY%3D&md5=5e430b9cfbbd1c9ffff457476474d1feCAS | 25841038PubMed |

Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. Forest Ecology and Management 177, 539–557.

Chen SC, Jin WJ, Liu AR, Zhang SJ, Liu DL, Wang FH, Lin XM, He CX (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Scientia Horticulturae 160, 222–229.
Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1eltL%2FL&md5=f34c6c2b1e9c0838f6861025cb1a6e6cCAS |

Chiou TJ, Liu H, Harrison MJ (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. The Plant Journal 25, 281–293.
The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitlKnu7o%3D&md5=4f60fad702f276a6f76708851f09e78cCAS | 11208020PubMed |

Daram P, Brunner S, Persson BL, Amrhein N, Bucher M (1998) Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206, 225–233.
Functional analysis and cell-specific expression of a phosphate transporter from tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltlKhsrw%3D&md5=89d9b534f33bf9621a58435e6701a844CAS | 9737001PubMed |

Fiorilli V, Lanfranco L, Bonfante P (2013) The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability. Planta 237, 1267–1277.
The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsFWlt7c%3D&md5=8eeef66f3cdf3a97a6ed046f45a6346fCAS | 23361889PubMed |

Gavito ME, Olsson PA, Rouhier H, Medina-Peñafiel A, Jakobsen I, Bago A, Azcón-Aguilar C (2005) Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytologist 168, 179–188.
Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeksLfJ&md5=0d85cd934c78f91d3c562ab0288d6072CAS | 16159332PubMed |

Gianinazzi S, Vosátka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Canadian Journal of Botany 82, 1264–1271.
Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business.Crossref | GoogleScholarGoogle Scholar |

Hamburger D, Rezzonico E, Petétot JMC, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell 14, 889–902.
Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWktro%3D&md5=d0e6070bdd1974edb55dfa4f8d8f5000CAS | 11971143PubMed |

Hanway JJ, Heidel H (1952) Soil analysis methods as used in lowa state college soil testing laboratory. Lowa Agriculture 7, 364–374.

Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 626–629.
A phosphate transporter from the mycorrhizal fungus Glomus versiforme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVChsbo%3D&md5=b420418a9d1b12503959fa01e7111c97CAS | 8524398PubMed |

Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell 14, 2413–2429.
A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFels7Y%3D&md5=f4d6ea0d0fa147679379842772f2e190CAS | 12368495PubMed |

Hawkes CV, Hartley IP, Ineson P, Fitter AH (2008) Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Global Change Biology 14, 1181–1190.
Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus.Crossref | GoogleScholarGoogle Scholar |

Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. The Plant Cell 23, 3812–3823.
A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1eku7vN&md5=085a3b3f26310dd9337026830ff652c0CAS | 21972259PubMed |

Hetrick BAD, Bloom J (1984) The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76, 953–956.
The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297–299.
An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1Kit7g%3D&md5=ded4abc78e4758b9b1f3dd638ef6bf35CAS | 11565029PubMed |

Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2012) Response of plasma membrane H+-ATPase to low temperature in cucumber roots. Journal of Plant Research 125, 291–300.
Response of plasma membrane H+-ATPase to low temperature in cucumber roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVCrs7o%3D&md5=8fed944b0d8fc7aa46268f695857b777CAS | 21638005PubMed |

Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant, Cell & Environment 30, 310–322.
Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlemu7o%3D&md5=1f3b4e0160e87f7a739093c360a0dfb3CAS |

Joner EJ, Jakobsen I (1994) Contribution by two arbuscular mycorrhizal fungi to P uptake by cucumber (Cucumis sativus L.) from32P-labelled organic matter during mineralization in soil. Plant and Soil 163, 203–209.
Contribution by two arbuscular mycorrhizal fungi to P uptake by cucumber (Cucumis sativus L.) from32P-labelled organic matter during mineralization in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXislWmtrc%3D&md5=dd050b950bc23407bd8790a994eaf71eCAS |

Kachurina OM, Zhang H, Raun WR, Krenzer EG (2000) Simultaneous determination of soil aluminum, ammonium- and nitrate-nitrogen using 1 M potassium chloride extraction. Communications in Soil Science and Plant Analysis 31, 893–903.
Simultaneous determination of soil aluminum, ammonium- and nitrate-nitrogen using 1 M potassium chloride extraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVKktbY%3D&md5=f1995709eac0ccf28189626f0ad7aad2CAS |

Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10, 22–29.
Symbiotic phosphate transport in arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFaruw%3D%3D&md5=9256804de8491aaeb386cb4170861143CAS | 15642520PubMed |

Karasawa T, Hodge A, Fitter AH (2012) Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant, Cell & Environment 35, 819–828.
Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFWlsL8%3D&md5=27426b3773fdac4fda1f851aa86de18bCAS |

Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882.
Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFWlt7o%3D&md5=4e32667df1a2da978c6dc9f1279c3183CAS | 21836016PubMed |

Kytöviita MM (2005) Asymmetric symbiont adaptation to Arctic conditions could explain why high Arctic plants are non-mycorrhizal. FEMS Microbiology Ecology 53, 27–32.
Asymmetric symbiont adaptation to Arctic conditions could explain why high Arctic plants are non-mycorrhizal.Crossref | GoogleScholarGoogle Scholar | 16329926PubMed |

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) CLUSTAL W and CLUSTAL X version 2.0. Bioinformatics 23, 2947–2948.
CLUSTAL W and CLUSTAL X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=59c4d2bb184b0f087e373b4c28757e14CAS | 17846036PubMed |

Liu H, Trieu AT, Blaylock LA, Harrison MJ (1998) Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Molecular Plant-Microbe Interactions 11, 14–22.
Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFertw%3D%3D&md5=9a9b324d2e9c0a847195d154f2483260CAS | 9425684PubMed |

Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14, 93–101.
Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7ptFynsQ%3D%3D&md5=49f7a8157982711698162494eb850595CAS | 12748840PubMed |

Liu Q, Parsons AJ, Xue H, Jones CS, Rasmussen S (2013) Functional characterisation and transcript analysis of an alkaline phosphatase from the arbuscular mycorrhizal fungus Funneliformis mosseae. Fungal Genetics and Biology 54, 52–59.
Functional characterisation and transcript analysis of an alkaline phosphatase from the arbuscular mycorrhizal fungus Funneliformis mosseae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFOnur0%3D&md5=4c59a947fd3b74727d64a660f02ea433CAS | 23474124PubMed |

Liu A, Chen S, Chang R, Liu D, Chen H, Ahammed G, Lin X, He C (2014) Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2 accumulation and ATPase activity. Journal of Plant Research 127, 775–785.
Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2 accumulation and ATPase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVOnurrM&md5=0791b274b7a78701f78cf4e8dbf2505aCAS | 25160659PubMed |

Lu MH, Lou QF, Chen JF (2004) A review on chilling injury and cold tolerance in Cucumis sativus L. Chinese Bulletin of Botany 21, 578–586.

Malcová R, Gryndler M (2003) Amelioration of Pb and Mn toxicity to arbuscular mycorrhizal fungus Glomus intraradices by maize root exudates. Biologia Plantarum 47, 297–299.
Amelioration of Pb and Mn toxicity to arbuscular mycorrhizal fungus Glomus intraradices by maize root exudates.Crossref | GoogleScholarGoogle Scholar |

McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biology 12, 563–569.

Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. The Plant Journal 42, 236–250.
The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFSrtro%3D&md5=9899d110732aeb96e014ab5354526be4CAS | 15807785PubMed |

Olsen SR, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture, Circular 939.

Paradis R, Dalpé Y, Charest C (1995) The combined effect of arbuscular mycorrhizas and short-term cold exposure on wheat. New Phytologist 129, 637–642.
The combined effect of arbuscular mycorrhizas and short-term cold exposure on wheat.Crossref | GoogleScholarGoogle Scholar |

Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews. Microbiology 6, 763–775.
Arbuscular mycorrhiza: the mother of plant root endosymbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWitL3J&md5=675604eafc7c77ae8fae65cfc8b1e3f1CAS | 18794914PubMed |

Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 99, 13324–13329.
Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvFGgsLw%3D&md5=45e965e0971dde39bf4b7efeef158e1dCAS | 12271140PubMed |

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–160.
Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Crossref | GoogleScholarGoogle Scholar |

Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414, 462–470.
A phosphate transporter expressed in arbuscule-containing cells in potato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFamtro%3D&md5=1b7258e03744779e3e54177c917ea4eeCAS | 11719809PubMed |

Rausch C, Zimmermann P, Amrhein N, Bucher M (2004) Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis. The Plant Journal 39, 13–28.
Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1yktbg%3D&md5=761f265dd5f8f072acbdada37a1e9649CAS | 15200639PubMed |

Ross JP (1971) Effect of phosphate fertilization on yield of mycorrhizal and nonmycorrhizal soybeans. Phytopathology 61, 1400–1403.
Effect of phosphate fertilization on yield of mycorrhizal and nonmycorrhizal soybeans.Crossref | GoogleScholarGoogle Scholar |

Ruotsalainen AL, Kytöviita MM (2004) Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. Oecologia 140, 226–233.
Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum.Crossref | GoogleScholarGoogle Scholar | 15138882PubMed |

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=a1c9730ef5dcf836df932bdd43dae470CAS | 18546601PubMed |

Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera [M]. Botanische Staatssammlung Munich. (Royal Botanic Garden Edinburgh: Kew, UK)

Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421.
A new fungal phylum, the Glomeromycota: phylogeny and evolution.Crossref | GoogleScholarGoogle Scholar |

Secco D, Baumann A, Poirier Y (2010) Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiology 153, 1693–1704.
Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons.Crossref | GoogleScholarGoogle Scholar |

Smith S, Read D (1997) Mycorrhizal symbiosis. In ‘Mycorrhizal symbiosis’. (2nd edn) (Academic Press: London.)

Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16–20.
Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlait7o%3D&md5=5fa355d095be0aa3cb3f96816cfa9f57CAS | 12970469PubMed |

Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist 182, 347–358.
More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVOhtLk%3D&md5=674e1dd2ddcca67ad990c239c67371c9CAS | 19207688PubMed |

Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology 156, 1050–1057.
Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWlurc%3D&md5=2065b1a4f048ca3b83055621cf994928CAS | 21467213PubMed |

Takabatake R, Hata S, Taniguchi M, Kouchi H, Sugiyama T, Izui K (1999) Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice and Arabidopsis. Plant Molecular Biology 40, 479–486.
Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVylsb8%3D&md5=c61c8dcaa489de3b071d11ccb4695eb2CAS | 10437831PubMed |

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=14f8674a92ef964b3e4fd8614ff7318fCAS | 21546353PubMed |

Tawaraya K, Hirose R, Wagatsuma T (2012) Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition. Biology and Fertility of Soils 48, 839–843.
Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition.Crossref | GoogleScholarGoogle Scholar |

Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycological Research 97, 245–250.
In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvFWnt70%3D&md5=a044b9fdff95e5c3d068e3fda54cfe40CAS |

Tisserant E, Kohler A, Dozolme‐Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez S, Koul R (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytologist 193, 755–769.
The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVejtr8%3D&md5=ff5caf86205e8d8aa714eb543a2ad15aCAS | 22092242PubMed |

Valentine AJ, Osborne BA, Mitchell DT (2001) Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber. Scientia Horticulturae 88, 177–189.
Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitVOiu78%3D&md5=8702f92b9bd7560ec59f305add58602bCAS |

Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. The Plant Cell 14, 1751–1766.
A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslChu7w%3D&md5=480da5d85f842c319a2eef21daa4c858CAS | 12172020PubMed |

Walder F, Ruré D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytologist 205, 1632–1645.
Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFehsLc%3D&md5=55064e7361a99bd86fdec8fb387d6215CAS | 25615409PubMed |

Wang B, Funakoshi DM, Dalpé Y, Hamel C (2002) Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12, 93–96.
Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature.Crossref | GoogleScholarGoogle Scholar | 12035733PubMed |

Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiology 135, 400–411.
Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12nu7Y%3D&md5=f9e1d07143aff2e8389c261316f0346cCAS | 15122012PubMed |

Wu QS, Zou YN (2010) Beneficial roles of arbuscular mycorrhizas in citrus seedlings at temperature stress. Scientia Horticulturae 125, 289–293.
Beneficial roles of arbuscular mycorrhizas in citrus seedlings at temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntVGjtbg%3D&md5=347cc2706ce505910c94ca9d226c516fCAS |

Young CC, Juang TC, Guo HY (1986) The effect of inoculation with vesicular-arbuscular mycorrhizal fungi on soybean yield and mineral phosphorus utilization in subtropical-tropical soils. Plant and Soil 95, 245–253.
The effect of inoculation with vesicular-arbuscular mycorrhizal fungi on soybean yield and mineral phosphorus utilization in subtropical-tropical soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xmt1Ghtrg%3D&md5=890d3e5021a2e3c12e4d047a61bf8e09CAS |

Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Scientia Horticulturae 122, 200–208.
Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVamt70%3D&md5=f9812da8dd028a0d4ee72d626643fe1eCAS |

Zhao B, Trouvelot A, Gianinazzi S, Gianinazzi-Pearson V (1997) Influence of two legume species on hyphal production and activity of two arbuscular mycorrhizal fungi. Mycorrhiza 7, 179–185.
Influence of two legume species on hyphal production and activity of two arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Zhao L, Versaw WK, Liu J, Harrison MJ (2003) A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. New Phytologist 157, 291–302.
A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFygs7w%3D&md5=354d55bd5cdc255fcdd82050329b5cf8CAS |

Zhu XC, Song FB, Xu HW (2010) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant and Soil 331, 129–137.
Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVOhs7k%3D&md5=9918aee8ebda9284ef67ee63bdcba365CAS |