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Arbuscular Mycorrhizal Fungi and Adaption of P Stress in Plants

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Arbuscular Mycorrhizas and Stress Tolerance of Plants

Abstract

Phosphorus (P) is an essential macronutrient for plant growth. In general, soil P deficiency is a major constraint for plant production because of the excited forms and slow rate of diffusion of P. Several strategies have been systemically applied for plant sensing and adapting P deficiency, especially mycorrhization in most land plants. This chapter reviewed P stress in plant (stress sensing and signaling molecule) and the influence of arbuscular mycorrhizal fungi on host plant P deficiency adaptation.

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References

  • Ai P, Sun S, Zhao J et al (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J 57:798–809

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Hayashi H (2006) Chemical identification of strigolactones as a host-recognition signal for arbuscular mycorrhizal fungi. Regul Plant Growth Dev 41:141–149

    Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alkan N, Gadkar V, Yarden O et al (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microbiol 72:4192–4199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aung K, Lin SI, Wu CC et al (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balzergue C, Chabaud M, Barker DG et al (2013) High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front Plant Sci 4:426

    Article  PubMed  PubMed Central  Google Scholar 

  • Bari R, Pant BD, Stitt M et al (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basu P, Zhang YJ, Lynch JP et al (2007) Ethylene modulates genetic, positional, and nutritional regulation of root plagiogravitropism. Funct Plant Biol 34:41–51

    Article  CAS  Google Scholar 

  • Besserer A, Puech-Pagés V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Besserer A, Becard G, Jauneau A et al (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport and phosphate availability. Annu Rev Plant Physiol 24:225–252

    Article  CAS  Google Scholar 

  • Bitterlich M, Krügel U, Boldt-Burisch K et al (2014) The sucrose transporter SlSUT2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. Plant J 78:877–889

    Article  CAS  PubMed  Google Scholar 

  • Borch K, Bouma TJ, Lynch JP et al (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431

    Article  CAS  Google Scholar 

  • Bothe H, Klingner A, Kaldorf M et al (1994) Biochemical approaches to the study of plant–fungal interactions in arbuscular mycorrhiza. Experientia 50:919–925

    Article  CAS  Google Scholar 

  • Brachmann A, Parniske M (2006) The most widespread symbiosis on earth. PL Biol 4:1111–1112

    CAS  Google Scholar 

  • Breuillin F, Schramm J, Hajirezaei M et al (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017

    Article  CAS  PubMed  Google Scholar 

  • Brinch-Pedersen H, Sørensen LD, Holm PB (2002) Engineering crop plants: getting a handle on phosphate. Trends Plant Sci 7:118–125

    Article  CAS  PubMed  Google Scholar 

  • Bucher M, Hause B, Krajinski F et al (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840

    Article  CAS  PubMed  Google Scholar 

  • Buhtz A, Springer F, Chappell L et al (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749

    Article  CAS  PubMed  Google Scholar 

  • Burleigh SH, Harrison MJ (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119:241–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bustos R, Castrillo G, Linhares F et al (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carbonnel S, Gutjahr C (2014) Control of arbuscular mycorrhiza development by nutrient signals. Front Plant Sci 5:462

    Article  PubMed  PubMed Central  Google Scholar 

  • Carswell C, Grant BR, Theodorou ME et al (1996) The fungicide phosphonate disrupts the phosphate-starvation response in Brassica nigra seedlings. Plant Physiol 110:105–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carswell MC, Grant BR, Plaxton WC (1997) Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide phosphonate. Planta 203:67–74

    Article  CAS  PubMed  Google Scholar 

  • Chapin LJ, Jones ML (2009) Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. J Exp Bot 60:2179–2190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen A, Gu M, Sun S et al (2011) Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol 189:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    Article  CAS  PubMed  Google Scholar 

  • Ciereszko I, Kleczkowski LA (2002) Effects of phosphate deficiency and sugars on expression of rab18 in Arabidopsis: hexokinase-dependent and okadaic acid-sensitive transduction of the sugar signal. Biochim Biophys Acta 1579:43–49

    Article  CAS  PubMed  Google Scholar 

  • Danneberg G, Latus C, Zimmer W et al (1992) Influence of vesicular–arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.) J Plant Physiol 141:33–39

    Google Scholar 

  • Danova-Alt R, Dijkema C, DeWaard P et al (2008) Transport and compartmentation of phosphate in higher plant cells-kinetic and 31P nuclear magnetic resonance studies. Plant Cell Environ 31:1510–1521

    Article  CAS  PubMed  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800

    Article  CAS  Google Scholar 

  • Espinosa F, Garrido I, Ortega A et al (2014) ROS, redox activities and NO production by axenically cultured olive seedling roots after interaction with mycorrhizal and pathogenic fungi. PLoS One 9:e100132

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Espinosa F, Garrido I, Álvarez-Tinaut MC (2015) Reflexions on some aspects of the interactions among ROS, RNS, and Ca2+ in response to a mycorrhizal or a pathogenic fungus. Plant Signal Behav 10:e1049789

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Etemadi M, Gutjahr C, Couzigou JM et al (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ezawa T, Yoshida T (1994) Characterization of phosphatase in marigold roots infected with vesicular-arbuscular mycorrhizal fungi. Soil Sci Plant Nutr 40:255–264

    Article  CAS  Google Scholar 

  • Ezawa T, Saito M, Yoshida T (1995) Comparison of phosphatase localization in the intraradical hyphae of arbuscular mycorrhizal fungi, Glomus spp. and Gigaspora spp. Plant Soil 176:57–63

    Article  CAS  Google Scholar 

  • Fabig B, Vielhauer K, Moawad A et al (1989) Gas-chromatographic separation of organic acids and electrophoretic determination of phosphatases from VA mycorrhizal roots. Z Pflanzenernahr Bodenk 152:261–265

    Article  CAS  Google Scholar 

  • Fan C, Wang X, Hu R et al (2013) The pattern of phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biol 3:48

    Article  CAS  Google Scholar 

  • Fellbaum CR, Gachomo EW, Beesetty Y et al (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149:1929–1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Floss DS, Levy JG, Levesque-Tremblay V et al (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 110:E5025–E5034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foo E, Yoneyama K, Hugill C et al (2012) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87

    Article  PubMed  CAS  Google Scholar 

  • Foo E, Ross JJ, Jones WT et al (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  CAS  PubMed  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B et al (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    Article  CAS  PubMed  Google Scholar 

  • García-Garrido JM, Lendzemo V, Castellanos-Morales V et al (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459

    Article  PubMed  Google Scholar 

  • Genre A, Chabaud M, Balzergue C et al (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:190–202

    Article  PubMed  Google Scholar 

  • Gianinazzi S, Gianinazzi-Pearson V, Dexheimer J (1979) Enzymatic studies on the metabolism of vesicular -arbuscular mycorrhiza. 3. Ultrastructural localization of acid and alkaline phosphatase in onion roots infected by Glomus mosseae (Nicol.&Gerd). New Phytol 82:127–132

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Gianinazzi S (1976) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza. I effect of mycorrhiza formation and phosphorus nutrition on soluble phosphatase activities. Physiol Veg 14:833–841

    CAS  Google Scholar 

  • Gianinazzi-Pearson V, Gianinazzi S (1978) Enzymatic studies on the metabolism of vesicular -arbuscular mycorrhiza. IT. Soluble alkaline phosphatase specific to mycorrhizal infection in onion roots. Physiol. Plant Pathol 12:45–53

    CAS  Google Scholar 

  • Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55:253–264

    Article  CAS  PubMed  Google Scholar 

  • Gilbert GA, Knight JD, Vance CP et al (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 85:921–928

    Article  CAS  Google Scholar 

  • Ginzberg I, David R, Shaul O et al (1998) Glomus intraradices colonization regulates gene expression in tobacco roots. Symbiosis 25:145–157

    CAS  Google Scholar 

  • Giots F, Donaton MCV, Thevelein JM (2003) Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase a pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 47:1163–1181

    Article  CAS  PubMed  Google Scholar 

  • Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Roldan V, Roux C, Girard D et al (2007) Strigolactones: promising plant signals. Plant Signal Behav 2:163–164

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  CAS  PubMed  Google Scholar 

  • Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant-Microbe Interact 24:867–878

    Article  CAS  PubMed  Google Scholar 

  • Grace EJ, Cotsaftis O, Tester M et al (2009) Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytol 181:938–949

    Article  CAS  PubMed  Google Scholar 

  • Grunwald U, Guo W, Fischer K et al (2009) Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta 229:1023–1034

    Google Scholar 

  • Gryndler M, Hrselova H, Chvatalova I et al (1998) The effect of selected plant hormones on in vitro proliferation of hyphae of Glomus Fistulosum. Biol Plant 41:255–263

    Article  CAS  Google Scholar 

  • Gutjahr C (2014) Phytohormone signaling in arbuscular mycorhiza development. Curr Opin Plant Biol 20:26–34

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Radovanovic D, Geoffroy J et al (2012) The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J 69:906–920

    Article  CAS  PubMed  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Maier W, Miersch O et al (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S et al (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110

    Article  CAS  PubMed  Google Scholar 

  • He Z, Ma Z, Brown KM et al (2005) Assessment of inequality of root hair density in Arabidopsis thaliana using the Gini coefficient: a close look at the effect of phosphorus and its interaction with ethylene. Ann Bot 95:287–293

    Article  CAS  PubMed  Google Scholar 

  • Hernández G, Ramirez M, Valdés-López O et al (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Herrera-Medina M, Gagnon H, Piche Y et al (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164:993–998

    Article  CAS  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H et al (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Google Scholar 

  • Ho CH, Lin SH, Hu HC et al (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  CAS  PubMed  Google Scholar 

  • Holsbeeks I, Lagatie O, Van Nuland A et al (2004) The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem Sci 29:556–564

    Article  CAS  PubMed  Google Scholar 

  • Illana A, Garcia-Garrido J, Sampedro I et al (2011) Strigolactones seem not to be involved in the nonsusceptibilty of arbuscular mycorrhizal (AM) nonhost plants to AM fungi. Botany 89:285–288

    Article  Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I et al (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa S, Adu-Gyamfi JJ, Nakamura T et al (2002) Genotypic variability in phosphorus solubilizing activity of root exudates by pigeonpea grown in low-nutrient environments. Plant Soil 245:71–81

    Article  CAS  Google Scholar 

  • Jabaji-Hare SH, Therien J, Charest PM (1990) High resolution cytochemical study of the vesicular-arbuscular mycorrhizal association, Glomus clarum -Allium porrum. New Phytol 114:481–496

    Article  Google Scholar 

  • Jain A, Poling MD, Karthikeyan AS et al (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Javot H, Pumplin N, Harrison M (2007a) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    Article  CAS  PubMed  Google Scholar 

  • Javot H, Varma Penmetsa R, Terzaghi N et al (2007b) A Medicago truncatula phosphate transporter indispensible for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeanmaire C, Dexheimer J, Marx C et al (1985) Effect of vesicular -arbuscular mycorrhizal infection on the distribution of neutral phosphatase activities in root cortical cells. J. Plant Physiol 119:285–293

    Article  CAS  Google Scholar 

  • Jeschke WD, Peuke AD, Pate JS et al (1997) Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. J Exp Bot 48:1737–1747

    Article  CAS  Google Scholar 

  • Jiang C, Gao X, Liao L et al (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karandashov V, Nagy R, Wegmuller S et al (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 101:6285–6290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karthikeyan A, Varadarajan D, Jain A et al (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918

    Article  CAS  PubMed  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Masuda T, Ki T et al (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47:238–248

    Article  CAS  PubMed  Google Scholar 

  • Kohlen W, Charnikhova T, Lammers M et al (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547

    Article  CAS  PubMed  Google Scholar 

  • Kojima T, Hayatsu M, Saito M (1998) Intraradical hyphae phosphatase of the arbuscular mycorrhizal fungus, Gigaspora margarita. Biol Fertil Soils 26:331–335

    Article  CAS  Google Scholar 

  • Koltai H, Kapulnik Y (eds) (2010) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht/New York

    Google Scholar 

  • Koltai H, Dor E, Hershenhorn J et al (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136

    Article  CAS  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J et al (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    Article  CAS  PubMed  Google Scholar 

  • Kuiper D, Schuit J, Kuiper P (1988) Effects of internal and external cytokinin concentrations on root growth and shoot to root ratio of Plantago major ssp. pleiosperma at different nutrient conditions. Plant Soil 111:231–236

    Article  CAS  Google Scholar 

  • Kulik A, Noirot E, Grandperret V et al (2015) Interplays between nitric oxide and reactive oxygen species in cryptogein signalling. Plant Cell Environ 38:331–348

    Article  CAS  PubMed  Google Scholar 

  • Lai F, Thacker J, Li Y et al (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Finnegan PM, Laliberte E et al (2011) Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156:1058–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288

    Article  CAS  PubMed  Google Scholar 

  • Lendzemo V, Kuyper TW, Urban A et al (2009) The arbuscular mycorrhizal host status of plants cannot be linked with the striga seed-germination-activity of plant root exudates. J Plant Dis Protect 11:86–89

    Article  Google Scholar 

  • Li K, Xu C, Li Z et al (2008) Comparative proteome analyses of phosphorus responses in maize (Zea mays L.) roots of wild-type and a low-P-tolerant mutant reveal root characteristics associated with phosphorus efficiency. Plant J 55:927–939

    Article  CAS  PubMed  Google Scholar 

  • Li S, Dong L (2015) Ethylene and plant responses to phosphate deficiency. Front Plant Sci 6:796

    Google Scholar 

  • Lian B, Zhou X, Miransari M et al (2000) Effects of salicylic acid on the development and root nodulation of soybean seedlings. J Agron Crop Sci 185:187–192

    Article  CAS  Google Scholar 

  • Liang C, Tian J, Lam HM et al (2010) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152:854–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao H, Yan X, Rubio G et al (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31:959–970

    Article  CAS  Google Scholar 

  • Lin SI, Chiang SF, Lin WY et al (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Trieu AT, Blaylock LA et al (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. Mol Plant-Microbe Interact 11:14–22

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Samac DA, Bucciarelli B et al (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–268

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Versaw WK, Pumplin N et al (2008) Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. J Biol Chem 283:24673–24681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu TY, Chang CY, Chiou TJ (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319

    Article  CAS  PubMed  Google Scholar 

  • Liu JQ, Allan DL, Vance CP (2010) Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Mol Plant 3:428–437

    Article  CAS  PubMed  Google Scholar 

  • Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • López-Arredondo DL, Leyva-González MA, González-Morales SI et al (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • López-Ráez JA, Charnikhova T, Gómez-Roldán V et al (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540

    Article  CAS  PubMed  Google Scholar 

  • Lota F, Wegmüller S, Buer B et al (2013) The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12, a Qb-SNARE protein gene, required for arbuscule formation in Lotus japonicus. Plant J 74:280–293

    Article  CAS  PubMed  Google Scholar 

  • Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long – distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Groover A, Lichtenberger R et al (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388

    Article  CAS  PubMed  Google Scholar 

  • Ludwig-Muller J (2000) Hormonal balance in plants during colonization by mycorrhizal fungi. In: Kapulnik Y, Douds D (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Amsterdam, pp 263–283

    Chapter  Google Scholar 

  • Ludwig-Muller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Kapulnik Y, Koltai H (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Dordrecht, p 169

    Chapter  Google Scholar 

  • Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Müller J, Güther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2:194–196

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56

    Article  CAS  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabood F, Smith DL (2005) Pre-incubation of Bradyrhizobium japonicum with jasmonates accelerates nodulation and nitrogen fixation in soybean (Glycine max) at optimal and suboptimal root zone temperatures. Physiol Plant 125:311–323

    Article  CAS  Google Scholar 

  • Maeda D, Ashida K, Iguchi K et al (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47:807–817

    Article  CAS  PubMed  Google Scholar 

  • Martín-Rodríguez JÁ, León-Morcillo R, Vierheilig H et al (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205

    Article  PubMed  CAS  Google Scholar 

  • Martín-Rodríguez JÁ, Ocampo JA, Molinero-Rosales N et al (2014) Role of gibberellins during arbuscular mycorrhizal formation in tomato: new insights revealed by endogenous quantification and genetic analysis of their metabolism in mycorrhizal roots. Physiol Plant 154:66–81

    Article  PubMed  CAS  Google Scholar 

  • Matusova R, Rani K, Verstappen FW et al (2005) The strigolactone germination stimulants of the plant-parasitic striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maucher H, Hause B, Feussner I et al (2000) Allene oxide synthases of barley (Hordeum vulgare cv. Salome): tissue specific regulation in seedling development. Plant J 21:199–213

    Article  CAS  PubMed  Google Scholar 

  • McArthur DA, Knowles NR (1992) Resistance responses of potato to vesicular-arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiol 100:341–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O et al (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutantnts1007. Planta 222:709–715

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Miransari M (2010b) Arbuscular mycorrhiza and soil microbes. In: Thangadurai D, Busso CA, Hijri M (eds) Mycorrhizal biotechnology. Science Publishers/CRC Press/Taylor & Francis Group, Enfield/Boca Raton/USA, p 226

    Google Scholar 

  • Miransari M, Bahrami HA, Rejali F et al (2007) Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on corn (Zea mays L.) growth. Soil Biol Biochem 39:2014–2026

    Article  CAS  Google Scholar 

  • Miransari M, Bahrami HA, Rejali F et al (2008) Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206

    Article  CAS  Google Scholar 

  • Miransari M, Abrishamchi A, Khoshbakht K et al (2014) Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit Rev Biotechnol 34:123–133

    Article  CAS  PubMed  Google Scholar 

  • Morcuende R, Bari R, Gibon Y et al (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  CAS  PubMed  Google Scholar 

  • Muchhal US, Liu C, Raghothama K (1997) Ca2+-ATPase is expressed differentially in phosphate starved roots of tomato. Physiol Plant 101:540–544

    Article  CAS  Google Scholar 

  • Mukherjee A, Ané JM (2011) Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol Plant-Microbe Interact 24:260–270

    Article  CAS  PubMed  Google Scholar 

  • Nagarajan VK, Smith AP (2012) Ethylene’s role in phosphate starvation signaling: more than just a root growth regulator. Plant Cell Physiol 53:277–286

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Karandashov V, Chague V et al (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. Plant J 42:236–250

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Vasconcelos MJV, Zhao S et al (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.) Plant Biol 8:186–197

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Drissner D, Amrhein N et al (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959

    Article  CAS  PubMed  Google Scholar 

  • Nakano-Hylander A, Olsson PA (2007) Carbon allocation in mycelia of arbuscular mycorrhizal fungi during colonisation of plant seedlings. Soil Biol Biochem 39:1450–1458

    Google Scholar 

  • Narise T, Kobayashi K, Baba S et al (2010) Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol Biol 72:533–544

    Article  CAS  PubMed  Google Scholar 

  • Nielsen KL, Eshel A, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. J Exp Bot 52:329–339

    Article  CAS  PubMed  Google Scholar 

  • Nukui N, Ezura H, Minamisawa K (2004) Transgenic Lotus japonicus with an ethylene receptor gene Cm-ERS1/H70A enhances formation of infection threads and nodule primordia. Plant Cell Physiol 45:427–435

    Article  CAS  PubMed  Google Scholar 

  • O’Rourke JA, Yang SS, Miller SS et al (2013) An RNA-Seq transcriptome analysis of orthophosphate deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161:705–724

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd GE, Engstrom EM, Long SR (2001) Ethylene inhibits the nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13:1835–1849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pant BD, Buhtz A, Kehr J et al (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paszkowski U, Kroken S, Roux C et al (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 99:13324–13329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A et al (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272

    Article  PubMed  PubMed Central  Google Scholar 

  • Popova Y, Thayumanavan P, Lonati E et al (2010) Transport and signaling through the phosphate – binding site of the yeast Pho84 phosphate transceptor. Proc Natl Acad Sci U S A 107:2890–2895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pozo MJ, Loon LCV, Pieterse CMJ (2004) Jasmonates signals in plant microbe interactions. J Plant Growth Regul 23:211–222

    CAS  Google Scholar 

  • Pratt J, Boisson AM, Gout E et al (2009) Phosphate (Pi) starvation effect on the cytosolic Pi concentration and Pi exchanges across the tonoplast in plant cells: an in vivo 31P-nuclear magnetic resonance study using methylphosphonate as a Pi analog. Plant Physiol 151:1646–1657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama KG (1999) Molecular regulation of phosphate acquisition in plants. In: Gissel-Nielsen G, Jensen A (eds) Plant nutrition—molecular biology and genetics. Springer, Netherlands, pp 95–103

    Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Ramaekers L, Remans R, Rao IM et al (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176

    Article  Google Scholar 

  • Rausch C, Daram P, Brunner S et al (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  CAS  PubMed  Google Scholar 

  • Rochange S (2010) Strigolactones and their role in arbuscular mycorrhizal symbiosis. In: Kapulnik Y, Douds D (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Amsterdam, pp 73–92

    Chapter  Google Scholar 

  • Rouached H, Arpat AB, Poirier Y (2010) Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 3:288–299

    Article  CAS  PubMed  Google Scholar 

  • Ruan HH, Shen WB, Xu LL (2004) Nitric oxide involved in the abscisic acid induced proline accumulation in wheat seedling leaves under salt stress. Acta Bot Sin 46:1307–1315

    Google Scholar 

  • Rubio V, Linhares F, Solano R et al (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio V, Bustos R, Irigoyen ML et al (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69:361–373

    Article  CAS  PubMed  Google Scholar 

  • Ruyter-Spira C, Al-Babili S, van der Krol S et al (2013) The biology of strigolactones. Trends Plant Sci 18:72–83

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Delhaize E (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Biol 52:527–560

    Article  CAS  Google Scholar 

  • Saito M (1995) Enzyme activities of the internal hyphae and germinated spores of an arbuscular mycorrhizal fungus, Gigaspora margarita Becker & Hall. New Phytol 129:425–431

    Article  CAS  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  CAS  PubMed  Google Scholar 

  • Schmidt W, Schikora A (2001) Control of root epidermal patterning: Effects of Fe- and P-deficiency. In: Horst WJ, Schenk MK, Bürkert A et al (Eds.), Plant Nutrition. Springer Netherlands, pp. 538–539

    Google Scholar 

  • Schünmann PHD, Richardson AE, Smith FW et al (2004) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.) J Exp Bot 55:855–865

    Article  PubMed  CAS  Google Scholar 

  • Shekoofeh E, Sepideh H, Roya R (2012) Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. Afr J Biotechnol 11:2223–2235

    CAS  Google Scholar 

  • Shin R (2011) Transcriptional regulatory components responding to macronutrient limitation. J Plant Biol 54:286–293

    Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci U S A 101:8827–8832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357

    Article  CAS  PubMed  Google Scholar 

  • Shin H, Shin HS, Chen R et al (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726

    Article  CAS  PubMed  Google Scholar 

  • Shu B, Xia RX, Wang P (2012) Differential regulation of Pht1 phosphate transporters from trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Sci Hortic-Amsterdam 146:115–123

    Article  CAS  Google Scholar 

  • Shu B, Wang P, Xia RX (2014) Effects of mycorrhizal fungi on phytate-phosphorus utilization in trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Acta Physiol Plant 36:1023–1032

    Article  CAS  Google Scholar 

  • Shu B, Wang P, Xia RX (2015) Characterisation of the phytase gene in trifoliate orange (Poncirus trifoliata (L.) Raf.) seedlings. Sci Hortic-Amsterdam 194:222–229

    Article  CAS  Google Scholar 

  • Shu B, Li WC, Liu LQ et al (2016a) Transcriptomes of arbuscular mycorrhizal fungi and litchi host interaction after tree girdling. Front Microbiol 7:408

    PubMed  PubMed Central  Google Scholar 

  • Shu B, Li WC, Liu LQ et al (2016b) Effects of girdling on arbuscular mycorrhizal colonization and root hair development of litchi seedlings. Sci Hortic-Amsterdam 210:25–33

    Article  Google Scholar 

  • Singh S, Katzer K, Lambert J et al (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:139–152

    Article  CAS  PubMed  Google Scholar 

  • Sobkowiak L, Bielewicz D, Malecka EM et al (2012) The role of the P1BS element containing promoter-driven genes in Pi transport and homeostasis in plants. Front Plant Sci 3:58

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song F, Song G, Dong A et al (2011) Regulatory mechanisms of host plant defense responses to arbuscular mycorrhiza. Acta Ecol Sin 31:322–327

    Article  Google Scholar 

  • Steinkellner S, Lendzemo V, Langer I et al (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306

    Article  CAS  PubMed  Google Scholar 

  • Stenzel I, Hause B, Maucher H et al (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato amplification in wound signalling. Plant J 33:577–589

    Article  CAS  PubMed  Google Scholar 

  • Stumpe M, Carsjens JG, Stenzel I et al (2005) Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula. Phytochemistry 66:781–791

    Article  CAS  PubMed  Google Scholar 

  • Svistoonoff S, Creff A, Reymond M et al (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796

    Article  CAS  PubMed  Google Scholar 

  • Teale WD, Ditengou FA, Dovzhenko AD et al (2008) Auxin as a model for the integration of hormonal signal processing and transduction. Mol Plant 1:229–237

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphate in Arabidopsis. Plant Physiol 127:963–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trull MC, Guiltinan MJ, Lynch JP et al (1997) The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant Cell Environ 20:85–92

    Article  CAS  Google Scholar 

  • Turner BL, Papházy MJ, Haygarth PM et al (2002) Inositol phosphates in the environment. Philos Trans R Soc Lond B 357:449–469

    Article  CAS  Google Scholar 

  • Uhde-Stone C, Gilbert G, Johnson JMF et al (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 2048:99–116

    Article  Google Scholar 

  • Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Magome H et al (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valdés-LÓpez O, Arenas-Huertero C, Ramírez M et al (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ 31:1834–1843

    Article  PubMed  CAS  Google Scholar 

  • Van der Ent S, Van Wees SC, Pieterse CM (2009) Jasmonate signaling in plant interactions with resistance inducing beneficial microbes. Phytochemistry 70:1581–1588

    Article  CAS  PubMed  Google Scholar 

  • Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  CAS  PubMed  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Varadarajan DK, Karthikeyan AS, Matilda PD et al (2002) Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129:1232–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. Adv Exp Med Biol 505:23–39

    Article  CAS  PubMed  Google Scholar 

  • Vieweg MF, Hohnjec N, Kuster H (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220:757–766

    Google Scholar 

  • Wang X, Yi K, Tao Y et al (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29:1924–1935

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang Y, Tian J et al (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151:233–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasaki J, Shinano T, Onishi K et al (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57:2049–2059

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wegmüller S, Svistoonoff S, Reinhardt D et al (2008) A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia. Plant J 54:1115–1127

    Article  PubMed  CAS  Google Scholar 

  • Xiao K, Liu J, Dewbre G et al (2006) Isolation and characterization of root-specific phosphate transporter promoters from Medicago truncatula. Plant Biol 8:439–449

    Article  CAS  PubMed  Google Scholar 

  • Yang SY, Paszkowski U (2011) Phosphate import at the arbuscule: just a nutrient? Mol Plant-Microbe Interact 24:1296–1299

    Article  CAS  PubMed  Google Scholar 

  • Yang SY, Grønlund M, Jakobsen I et al (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D et al (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Sekimoto H et al (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kisugi T et al (2011) Characterization of strigolactones exuded by Asteraceae plants. Plant Growth Regul 65:495–504

    Article  CAS  Google Scholar 

  • Yoshida S, Kameoka H, Tempo M et al (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol 196:1208–1216

    Article  CAS  PubMed  Google Scholar 

  • Yu N, Luo D, Zhang X et al (2014) A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24:130–133

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Meng S, Li M et al (2016) Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Front Plant Sci 7:1398

    Google Scholar 

  • Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Liao H, Lucas WJ (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56:192–220

    Article  CAS  PubMed  Google Scholar 

  • Zhou K, Yamagishi M, Osaki M et al (2008a) Sugar signalling mediates cluster root formation and phosphorus starvation-induced gene expression in white lupin. J Exp Bot 59:2749–2756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Jiao F, Wu Z et al (2008b) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zsögön A, Lambais MR, Benedito VA et al (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Sci Agric 65:259–267

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Fund of China (Project No. 31401818), the Fund on Basic Scientific Research project of Nonprofit Central Research Institutions (No. SSCRI-1630062014006), Germplasm Resource Protection of Ministry of Agriculture (2016NWB053), China Litchi and Longan Industry Technology Research System (Project No.CARS-33-11), and the Plan in Scientific and Technological Innovation Team of Outstanding Young, Hubei Provincial Department of Education (T201604).

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Shu, B., Wu, QS. (2017). Arbuscular Mycorrhizal Fungi and Adaption of P Stress in Plants. In: Wu, QS. (eds) Arbuscular Mycorrhizas and Stress Tolerance of Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-4115-0_5

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