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Role of Plant Hormones and Small Signalling Molecules in Nodulation Under P Stress

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Book cover Legume Nitrogen Fixation in Soils with Low Phosphorus Availability

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Abstract

Plant hormones and other mobile signalling elements play key roles in regulating nodulation and N2 fixation in legumes. This includes many hormones associated with regulating general growth and development, such as cytokinin, auxin, gibberellins and strigolactones and plant hormones associated with response to stress, including ethylene. Mobile peptides and microRNAs have also shown to have significant roles in regulating nodule initiation, organogenesis and nutrient response. In this chapter we will discuss the roles of these small signalling molecules in nodulation, highlighting specific examples of their interactions with phosphorous (P) stress. P-induced small peptides and microRNAs have been identified in legumes, but the role of these signals in regulating nodulation response to P stress has not been directly investigated. Similarly, relatively few studies that have specifically examined the role of plant hormones in P response of nodulation and areas for future research are highlighted.

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References

  • Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci 111(50):18084–18089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827

    Article  CAS  PubMed  Google Scholar 

  • Al-Niemi TS, Kahn ML, McDermott TR (1998) Phosphorus uptake by bean nodules. Plant Soil 198:71–78

    Article  CAS  Google Scholar 

  • Balzergue C, Puech-Pagès V, Bécard G, Rochange SF (2010) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 3:1049–1060

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of miR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant-Microbe Interact 23(7):915–926

    Article  CAS  PubMed  Google Scholar 

  • Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64(6):1002–1017

    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(1):241–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1990) Early induction of feedback regulatory responses governing nodulation in soybean. Plant Sci 71(1):69–81

    Article  Google Scholar 

  • Carroll BJ, McNeil DL, Gresshoff PM (1985) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci 82:4162–4166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18(2):412–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82(2):588–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG (2009) Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2:43–58

    Article  CAS  PubMed  Google Scholar 

  • Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol 40(7):770–790

    Article  CAS  PubMed  Google Scholar 

  • Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 110(51):E5025–E5034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234(5):1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013a) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6(1):76–87

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB (2013b) Strigolactones: internal and external signals in plant symbioses? Plant Signal Behav 8(3):e23168

    Article  PubMed  PubMed Central  Google Scholar 

  • Foo E, Ross JJ, Jones WT, Reid JB (2013c) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111(5):769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foo E, McAdam EL, Weller JL, Reid JB (2016) Interactions between ethylene, gibberellins, and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea. J Exp Bot 67:erw047

    Article  Google Scholar 

  • Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J 32:353–360

    Article  CAS  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Funayama-Noguchi S, Noguchi K, Yoshida C, Kawaguchi M (2011) Two CLE genes are induced by phosphate in roots of Lotus japonicus. J Plant Res 124(1):155–156

    Article  CAS  PubMed  Google Scholar 

  • Gentili F, Huss-Danell K (2003) Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J Exp Bot 54(393):2757–2767

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18(10):2680–2693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guinel FC (2015) Ethylene, a hormone at the center-stage of nodulation. Front Plant Sci 6:1121. doi:10.3389/fpls.2015.01121

    Article  PubMed  PubMed Central  Google Scholar 

  • Handa Y, Nishide H, Takeda N, Suzuki Y, Kawaguchi M, Saito K (2015) RNA-seq transcriptional profiling of an arbuscular mycorrhiza provides insights into regulated and coordinated gene expression in Lotus japonicus and Rhizophagus irregularis. Plant Cell Physiol 56(8):pcv071

    Article  Google Scholar 

  • He ZX, Ma Z, Brown KM, Lynch JP (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 

  • Jacobsen E, Feenstra WJ (1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Sci Lett 33(3):337–344

    Article  CAS  Google Scholar 

  • Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet EP, Duc G, Gojon A, Lepetit M, Salon C (2010) Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytol 185:817–828

    Article  CAS  PubMed  Google Scholar 

  • Jiang C, Gao X, Liao L, Harberd NP, Fu X (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 

  • Karmakar K, Rana A, Rajwar A, Sahgal M, Johri BN (2015) Legume-rhizobia symbiosis under stress. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Springer, New Delhi, pp 241–258

    Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosslak RM, Bohlool BB (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol 75(1):125–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420(6914):422–426

    Article  CAS  PubMed  Google Scholar 

  • Krusell L, Sato N, Fukuhara I, Koch BE, Grossmann C, Okamoto S, Oka-Kira E, Otsubo Y, Aubert G, Nakagawa T, Sato S (2011) The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation. Plant J 65(6):861–871

    Article  CAS  PubMed  Google Scholar 

  • Larrainzar E, Riely BK, Kim SC et al (2015) Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between Nod factor and ethylene signals. Plant Physiol 169:233–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KH, LaRue TA (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L.cv Sparkle. Plant Physiol 100:1759–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YS, Mao XT, Tian QY, Li LH, Zhang WH (2009) Phosphorus deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production. Environ Exp Bot 67(1):172–177

    Article  CAS  Google Scholar 

  • Lin YH, Ferguson BJ, Kereszt A, Gresshoff PM (2010) Suppression of hypernodulation in soybean by a leaf-extracted, NARK-and Nod factor-dependent, low molecular mass fraction. New Phytol 85:1074–1086

    Article  Google Scholar 

  • Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F (2013) CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64(7):1967–1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Raez JA, Shirasu K, Foo E (2017) Strigolactones in plant interactions with beneficial and detrimental organisms; The Yin and Yang. TIPS doi.org/10.1016/j.tplants.2017.03.011

    Google Scholar 

  • Ma W, Guinel FC, Glick BR (2003) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69(8):4396–4402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malusà E, Russo MA, Mozzetti C, Belligno A (2006) Modification of secondary metabolism and flavonoid biosynthesis under phosphate deficiency in bean roots. J Plant Nutr 29(2):245–258

    Article  Google Scholar 

  • Martín AC, Del Pozo JC, Iglesias J, Rubio V, Solano R, De La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567

    Article  PubMed  Google Scholar 

  • Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J Exp Bot 52:419–426

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U, Schlaman HR, Spaink HP, Of Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U, Jin J, Noorden GE, Ng LP, Wasson AP (2015) Regulation of nodule development by short-and long-distance auxin transport control. In: de Bruijn FJ (ed) Biological nitrogen fixation. Wiley, Hoboken, pp 465–474

    Chapter  Google Scholar 

  • Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu GJ, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137(24):4317–4325

    Article  CAS  PubMed  Google Scholar 

  • Mori N, Nishiuma K, Sugiyama T, Hayashi H, Akiyama K (2016) Carlactone-type strigolactones and their synthetic analogues as inducers of hyphal branching in arbuscular mycorrhizal fungi. Phytochemistry 130:90–98

    Article  CAS  PubMed  Google Scholar 

  • Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153(1):222–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70(3):367–376

    Article  CAS  PubMed  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315(5808):101–104

    Article  CAS  PubMed  Google Scholar 

  • Nacry P, Canivènc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074

    Article  CAS  PubMed  PubMed Central  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 

  • Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420(6914):426–429

    Article  CAS  PubMed  Google Scholar 

  • Novák K (2010) Early action of pea symbiotic gene NOD3 is confirmed by adventitious root phenotype. Plant Sci 179(5):472–478

    Article  PubMed  Google Scholar 

  • Oka-Kira E, Tateno K, Miura KI, Haga T, Hayashi M, Harada K, Sato S, Tabata S, Shikazono N, Tanaka A, Watanabe Y (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 44(3):505–515

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Kawaguchi M (2015) Shoot HAR1 mediates nitrate inhibition of nodulation in Lotus japonicus. Plant Signal Behav 10(5):e1000138

    Article  PubMed  PubMed Central  Google Scholar 

  • Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50(1):67–77

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M (2013) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat Commun 12:4

    Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53(5):731–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penmetsa RV, Uribe P, Anderson J et al (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J 55:580–595

    Article  CAS  PubMed  Google Scholar 

  • Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G, Liao H (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 159(4):1634–1643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Regnault T, Davière JM, Wild M, Sakvarelidze-Achard L, Heintz D, Bergua EC, Diaz IL, Gong F, Hedden P, Achard P (2015) The gibberellin precursor GA12 acts as a long-distance growth signal in Arabidopsis. Nat Plants. doi:10.1038/nplants.2015.73

    PubMed  Google Scholar 

  • Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM (2011a) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108(5):789–795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid DE, Ferguson BJ, Gresshoff PM (2011b) Inoculation-and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant-Microbe Interact 24(5):606–618

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Cho H, Choi D, Hwang I (2012) Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol Cells 34:117–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 19:5

    Google Scholar 

  • Scheible WR, Rojas-Triana M (2015) Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications. In: Plaxton W, Lambers H (eds) Annual plant review, phosphorus metabolism in plants, vol 48. Wiley, Hoboken, p 25

    Google Scholar 

  • Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnabel E, Etienne-Pascal J, de Fernanda C-N, Gérard D, Julia F (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58(6):809–822

    Article  PubMed  Google Scholar 

  • Schnabel EL, Kassaw TK, Smith LS, Marsh JF, Oldroyd GE, Long SR, Frugoli JA (2011) The ROOT DETERMINED NODULATION1 gene regulates nodule number in roots of Medicago truncatula and defines a highly conserved, uncharacterized plant gene family. Plant Physiol 157(1):328–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299(5603):109–112

    Article  CAS  PubMed  Google Scholar 

  • Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci 111(4):1640–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shane MW, De Vos M, de Roock S, Cawthray GR, Lambers H (2003) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R Br. Plant and Soil 248(1–2):209–219

    Article  CAS  Google Scholar 

  • Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42(2):383–385

    Article  CAS  Google Scholar 

  • Soyano T, Kawaguchi M (2014) Systemic regulation of root nodule formation. In: Ohyama T (ed) Advances in biology and ecology of nitrogen fixation. Intech, Rijeka, pp 89–109

    Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    Article  CAS  PubMed  Google Scholar 

  • Staehelin C, Xie ZP, Illana A, Vierheilig H (2011) Long-distance transport of signals during symbiosis: are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal Behav 6(3):372–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulieman S, Van Ha C, Schulze J, Tran LS (2013) Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot 64(10):ert122

    Article  Google Scholar 

  • Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144:594–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315(5808):104–107

    Article  CAS  PubMed  Google Scholar 

  • Valdés-López OS, Arenas-Huertero CA, Ramirez M, Girard L, Sanchez F, Vance CP, Luis Reyes J, Hernandez G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ 31(12):1834–1843

    Article  PubMed  Google Scholar 

  • Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187(3):805–818

    Article  PubMed  Google Scholar 

  • van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long distance auxin transport regulation in the Medicago truncatula super numeric nodulation mutant. Plant Physiol 140:1494–1150

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, YiK ,Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P(2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29: 1924–1935

    Google Scholar 

  • Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyss PE, Mellor RB, Wiemken A (1990) Mutants of soybean (Glycine max) unable to suppress nodulation in the presence of nitrate retain the ability to suppress mycorrhization in the presence of phosphate. J Plant Physiol 136(4):507–509

    Article  CAS  Google Scholar 

  • Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14(1):1

    Article  Google Scholar 

  • Yoneyama K, Kisugi T, Xie X, Arakawa R, Ezawa T, Nomura T, Yoneyama K (2015) Shoot-derived signals other than auxin are involved in systemic regulation of strigolactone production in roots. Planta 241(3):687–698

    Article  CAS  PubMed  Google Scholar 

  • Yu N, Luo D, Zhang X, Liu J, Wang W, Jin Y, Dong W, Liu J, Liu H, Yang W, Zeng L (2014) A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24(1):130

    Article  CAS  PubMed  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(3):192–220

    Article  CAS  PubMed  Google Scholar 

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  1. School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, TAS, 7001, Australia

    Eloise Foo

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  1. Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North, Sudan

    Saad Sulieman

  2. Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science (CSRS), Tsurumi, Yokohama, Japan

    Lam-Son Phan Tran

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Foo, E. (2017). Role of Plant Hormones and Small Signalling Molecules in Nodulation Under P Stress. In: Sulieman, S., Tran, LS. (eds) Legume Nitrogen Fixation in Soils with Low Phosphorus Availability. Springer, Cham. https://doi.org/10.1007/978-3-319-55729-8_8

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