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The Role of Strigolactones in Plant–Microbe Interactions

  • Soizic Rochange
  • Sofie Goormachtig
  • Juan Antonio Lopez-Raez
  • Caroline GutjahrEmail author
Chapter

Abstract

Plants associate with an infinite number of microorganisms that interact with their hosts in a mutualistic or parasitic manner. Evidence is accumulating that strigolactones (SLs) play a role in shaping these associations. The best described function of SLs in plant–microbe interactions is in the rhizosphere, where, after being exuded from the root, they activate hyphal branching and enhanced growth and energy metabolism of symbiotic arbuscular mycorrhiza fungi (AMF). Furthermore, an impact of SLs on the quantitative development of root nodule symbiosis with symbiotic nitrogen-fixing bacteria and on the success of fungal and bacterial leaf pathogens is beginning to be revealed. Thus far, the role of SLs has predominantly been studied in binary plant–microbe interactions. It can be predicted that their impact on the bacterial, fungal, and oomycetal communities (microbiomes), which thrive on roots, in the rhizosphere, and on aerial tissues, will be addressed in the near future.

Keywords

Rhizobia Arbuscular mycorrhiza fungi Pathogen Rhizosphere Receptor Plant hormones Plant disease Medicago truncatula Pea Rice Tomato 

Notes

Glossary

ABC transporters

Members of a transmembrane transporter family. They often consist of multiple subunits comprising transmembrane domains and membrane-bound ATPases. Hydrolysis of ATP by the ATPases fuels energy-dependent translocation of substrates across membranes.

Actinomycete

Diverse order of Gram-positive, anaerobic bacteria, which have a mycelium-like, filamentous, and branching growth habit. Some species form root nodule symbiosis with plants of the Fagales, Rosales, and Cucurbitales.

Arbuscules

Tree-shaped hyphal structure, formed by arbuscular mycorrhiza fungi in root cortex cells. These structures release mineral nutrients to apoplast between arbuscule and host cell and take up lipids, delivered by the host.

Arbuscular mycorrhiza

Ancient symbiosis between most land plants and fungi of the Glomeromycotina. Endomycorrhiza, in which the fungus penetrates root cortex cells to form tree-shaped arbuscules. The fungus improves plant mineral nutrition and receives lipids and carbohydrates stemming from photosynthesis in return.

Biotroph

Parasite or symbiont, which colonizes a living host cell and exploits the living cell for. Example for nutrients.

Chitin

N-acetyl-glucosamine polymer, which is the main component of fungal cell walls.

Flavonoids

Family of chemical compounds with several phenyl-rings often containing a keto group. They are widespread in the plant kingdom and act, for example, as flower colors, as toxic deterrents of pathogens, or as attractants of rhizobia in the rhizosphere.

Haber–Bosch process

An industrial process producing ammonium from molecular nitrogen and hydrogen. The process requires a catalyst (e.g., iron) and high temperature and pressure (400–500 °C; 15–25 MPa). It is named after its inventors Fritz Haber and Carl Bosch.

Hemibiotroph

Plant pathogen, which first colonizes the plant in a biotrophic manner and then turns into a necrotroph.

Hyphae

Thread-like structures, which form the body of fungi.

Microbiome

The term microbiome describes the community of microbes colonizing certain niche including bacteria, archaea, protists, fungi, and viruses or their collective genomes.

Mutualism

Interaction between a minimum of two organisms, in which both organisms profit from the collaboration.

Nectrotroph

Parasite, which kills the cell of the host and feeds on the dead material.

Nodule primordia

Root nodule in its earliest recognizable stage, from when cell division has started to a visible small white nodule, before the nodule is mature and functional.

Oomycetes

Oomycota is a group of filamentous protist with c. 500 species. The name derives from their oversized oogonia, which contain the female gametes.

Parasitism

Relationship between at least two species, in which one of the two lives on the cost of its host and causes harm to it.

Spore

Unit of asexual reproduction of fungi used for dispersal and survival (e.g. for plant-interacting fungi through winter, when hosts are unavailable). Spores are an integral part of the fungal life cycle.

Rhizosphere

Narrow region of the soil, which is directly attached to the root and influenced by root exudates and sloughed-off plant cells. The rhizosphere hosts a specific set of microbes, which are influenced by the root activity.

Root nodule symbiosis

Symbiosis between plants of most legumes and bacteria belonging to the rhizobia or less frequent members of the Fagales, Cucurbitales, and Rosales and actinomycetes. The bacteria are hosted in membrane-surrounded compartments in cells of root nodules, which are lateral organs derived from cell division. The bacteria fix atmospheric nitrogen and provide the plant with ammonium in exchange for organic carbon.

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Akiyama K, Ogasawara S, Ito S, Hayashi H (2010a) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51(7):1104–1117PubMedPubMedCentralCrossRefGoogle Scholar
  3. Akiyama K, Tanigawa F, Kashihara T, Hayashi H (2010b) Lupin pyranoisoflavones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry 71(16):1865–1871PubMedCrossRefPubMedCentralGoogle Scholar
  4. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186PubMedCrossRefGoogle Scholar
  5. 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 62(3):1049–1060PubMedPubMedCentralCrossRefGoogle Scholar
  6. Belmondo S, Marschall R, Tudzynski P, López Ráez JA, Artuso E, Prandi C, Lanfranco L (2017) Identification of genes involved in fungal responses to strigolactones using mutants from fungal pathogens. Curr Genet 63(2):201–213PubMedCrossRefPubMedCentralGoogle Scholar
  7. Besserer A, Puech-Pagés V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4(7):e226.  https://doi.org/10.1371/journal.pbio.0040226 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Besserer A, Becard G, Jauneau A, Roux C, Sejalon-Delmas N (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(1):402–413PubMedPubMedCentralCrossRefGoogle Scholar
  9. Blake SN, Barry KM, Gill WM, Reid JB, Foo E (2016) The role of strigolactones and ethylene in disease caused by Pythium irregulare. Mol Plant Pathol 17(5):680–690PubMedCrossRefPubMedCentralGoogle Scholar
  10. Boyer F-D, de Saint Germain A, Pillot J-P, Pouvreau J-B, Chen VX, Ramos S, Stévenin A, Simier P, Delavault P, Beau J-M et al (2012) Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol 159(4):1524–1544PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bravo A, York T, Pumplin N, Mueller L, Harrison M (2016) Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2:15208PubMedCrossRefPubMedCentralGoogle Scholar
  12. Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GED et al (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26(12):4680–4701PubMedPubMedCentralCrossRefGoogle Scholar
  13. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E et al (2010) Phosphate systemically inhibits development of arbuscular mycorrhizal in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64(6):1002–1017PubMedCrossRefGoogle Scholar
  14. Broughton W, Jabbouri S, Peret X (2000) Keys to symbiotic harmony. J Bacteriol 182(20):5641–5652PubMedPubMedCentralCrossRefGoogle Scholar
  15. Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from from plant root exudates. Mol Plant Microbe Interact 13(6):693–698PubMedCrossRefGoogle Scholar
  16. Carbonnel S, Gutjahr C (2014) Control of arbuscular mycorrhiza development by nutrient signals. Front Plant Sci 5:462PubMedPubMedCentralCrossRefGoogle Scholar
  17. Charpentier M, Sun J, Wen J, Mysore KS, Oldroyd GED (2014) Abscisic acid promotion of arbuscular mycorrhizal colonization requires a component of the PROTEIN PHOSPHATASE 2A complex. Plant Physiol 166(4):2077–2090PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154(3753):1189–1190PubMedCrossRefPubMedCentralGoogle Scholar
  19. De Cuyper C, Fromentin J, Yocgo RE, De Keyser A, Guillotin B, Kunert K, Boyer FD, Goormachtig S (2015) From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J Exp Bot 66(1):137–146PubMedCrossRefPubMedCentralGoogle Scholar
  20. Decker EL, Alder A, Hunn S, Ferguson J, Lehtonen MT, Scheler B, Kerres KL, Wiedemann G, Safavi-Rizi V, Nordzieke S et al (2017) Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytol 216(2):455–468PubMedCrossRefPubMedCentralGoogle Scholar
  21. Delaux P-M, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané J-M (2014) Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 10(7):e1004487PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dor E, Joel DM, Kapulnik Y, Koltai H, Hershenhorn J (2011) The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta 234(2):419–427PubMedCrossRefPubMedCentralGoogle Scholar
  23. Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13(1):162PubMedPubMedCentralCrossRefGoogle Scholar
  24. Favre P, Bapaume L, Bossolini E, Delorenzi M, Falquet L, Reinhardt D (2014) A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC Plant Biol 14(1):333PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol 40(7):770–790PubMedCrossRefPubMedCentralGoogle Scholar
  26. Flematti GR, Scaffidi A, Waters MT, Smith SM (2016) Stereospecificity in strigolactone biosynthesis and perception. Planta 243(6):1361–1373PubMedCrossRefPubMedCentralGoogle Scholar
  27. Fliegmann J, Bono JJ (2015) Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors. Glycoconj J 32(7):455–464PubMedCrossRefPubMedCentralGoogle Scholar
  28. Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234:1073–1081PubMedCrossRefPubMedCentralGoogle Scholar
  29. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17(2):464–474PubMedPubMedCentralCrossRefGoogle Scholar
  30. Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87PubMedCrossRefGoogle Scholar
  31. Foo E, Ferguson BJ, Reid JB (2014) The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway. Ann Bot 113(6):1037–1045PubMedPubMedCentralCrossRefGoogle Scholar
  32. Foo E, Blake SN, Fisher BJ, Smith JA, Reid JB (2016) The role of strigolactones during plant interactions with the pathogenic fungus Fusarium oxysporum. Planta 243(6):1387–1396PubMedCrossRefGoogle Scholar
  33. Fusconi A (2014) Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation? Ann Bot 113(1):19–33PubMedCrossRefGoogle Scholar
  34. Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P 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(1):190–202PubMedCrossRefGoogle Scholar
  35. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C et al (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194PubMedCrossRefGoogle Scholar
  36. Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24(8):867–878PubMedCrossRefGoogle Scholar
  37. Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG, Summers W, Carbonnel S, Mansfield C, Yang S-Y, Nadal M et al (2015) Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350(6267):1521–1524PubMedCrossRefGoogle Scholar
  38. Ha CV, Leyva-Gonzalez MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV et al (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci U S A 111(2):851–856PubMedCrossRefPubMedCentralGoogle Scholar
  39. Haq BU, Ahmad MZ, Ur Rehman N, Wang J, Li P, Li D, Zhao J (2017) Functional characterization of soybean strigolactone biosynthesis and signaling genes in Arabidopsis max mutants and GmMAX3 in soybean nodulation. BMC Plant Biol 17:259PubMedPubMedCentralCrossRefGoogle Scholar
  40. Herrera-Medina M, Steinkellner S, Vierheilig H, Ocampo Bote J, García Garrido J (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564.  https://doi.org/10.1111/j.1469-8137.2007.02107.x CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, Yajima S, Kyozuka J, Ueguchi-Tanaka M, Matsuoka M et al (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol 174(2):1250–1259PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kamel L, Tang N, Malbreil M, San Clemente H, Le Marquer M, Roux C, Frei Dit Frey N (2017) The comparison of expressed candidate secreted proteins from two arbuscular mycorrhizal fungi unravels common and specific molecular tools to invade different host plants. Front Plant Sci 8:124PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kaori Y, Xiaonan X, Hitoshi S, Yasutomo T, Shin O, Kohki A, Hideo H, Koichi Y (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179(2):484–494CrossRefGoogle Scholar
  44. Keymer A, Gutjahr C (2018) Cross-kingdom lipid transfer in arbuscular mycorrhizal symbiosis and beyond. Curr Opin Plant Biol 44:137–144.  https://doi.org/10.1016/j.pbi.2018.1004.1005 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kobae Y, Kameoka H, Sugimura Y, Saito K, Ohtomo R, Fujiwara T, Kyozuka J (2018) Strigolactone biosynthesis genes of rice are required for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant Cell Physiol 59(3):544–553PubMedCrossRefPubMedCentralGoogle Scholar
  46. Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P, Haider I, Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ et al (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196(2):535–547PubMedCrossRefGoogle Scholar
  47. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483(7389):341–344PubMedCrossRefGoogle Scholar
  48. Lanfranco L, Fiorilli V, Venice F, Bonfante P (2018) Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J Exp Bot 69(9):2175–2188PubMedCrossRefPubMedCentralGoogle Scholar
  49. Li W, Kien Huu N, Ha Duc C, Chien Van H, Watanabe Y, Osakabe Y, Leyva-Gonzalez MA, Sato M, Toyooka K, Voges L et al (2017) The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana. PLoS Genet 13(11):e1007076PubMedPubMedCentralCrossRefGoogle Scholar
  50. Liu C, Murray J (2016) The role of flavonoids in nodulation host-range specificity: an update. Plants 5:33PubMedCentralCrossRefGoogle Scholar
  51. Liu W, Kohlen W, Lillo A (2011) Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell 23:3853–3865PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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):1967–1981PubMedPubMedCentralCrossRefGoogle Scholar
  53. Lopez-Raez J (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243:1375–1385PubMedCrossRefPubMedCentralGoogle Scholar
  54. López-Ráez J, Charnikhovab T, Fernández I, Bouwmeester H, Pozo M (2010a) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297CrossRefGoogle Scholar
  55. López-Ráez J, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TD, Thompson AJ, Ruyter‐Spira C, Bouwmeester H (2010b) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187(2):343–354PubMedCrossRefPubMedCentralGoogle Scholar
  56. López-Ráez JA, Shirasu K, Foo E (2017) Strigolactones in plant interactions with beneficial and detrimental organisms: the yin and yang. Trends Plant Sci 22(6):527–537PubMedCrossRefPubMedCentralGoogle Scholar
  57. Marzec M, Muszynska A (2015) In silico analysis of the genes encoding proteins that are involved in the biosynthesis of the RMS/MAX/D pathway revealed new roles of strigolactones in plants. Int J Mol Sci 16(4):6757–6782PubMedPubMedCentralCrossRefGoogle Scholar
  58. McAdam EL, Hugill C, Fort S, Samain E, Cottaz S, Davies NW, Reid JB, Foo E (2017) Determining the site of action of strigolactones during nodulation. Plant Physiol 175(1):529–542PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 130:90–98PubMedCrossRefPubMedCentralGoogle Scholar
  60. Moscatiello R, Sello S, Novero M, Negro A, Bonfante P, Navazio L (2014) The intracellular delivery of TAT-aequorin reveals calcium-mediated sensing of environmental and symbiotic signals by the arbuscular mycorrhizal fungus Gigaspora margarita. New Phytol 203(3):1012–1020PubMedCrossRefPubMedCentralGoogle Scholar
  61. 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):101–104PubMedCrossRefPubMedCentralGoogle Scholar
  62. Nagata M, Yamamoto N, Shigeyama T, Terasawa Y, Anai T, Sakai T, Inada S, Arima S, Hashiguchi M, Akashi R et al (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid and strigolactone signaling. Plant Cell Physiol 56(11):2100–2109PubMedPubMedCentralGoogle Scholar
  63. Oancea F, Georgescu E, Matusova R, Georgescu F, Nicolescu A, Raut I, Jecu ML, Vladulescu MC, Vladulescu L, Deleanu C (2017) New strigolactone mimics as exogenous signals for rhizosphere organisms. Molecules 22(6):1–15CrossRefGoogle Scholar
  64. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59(1):519–546PubMedCrossRefPubMedCentralGoogle Scholar
  65. GED O, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144CrossRefGoogle Scholar
  66. Peláez-Vico MA, Bernabéu-Roda L, Kohlen W, Soto MJ, López-Ráez JA (2016) Strigolactones in the Rhizobium-legume symbiosis: stimulatory effect on bacterial surface motility and down-regulation of their levels in nodulated plants. Plant Sci 245:119–127PubMedCrossRefPubMedCentralGoogle Scholar
  67. Piisilä M, Keceli MA, Brader G, Jakobson L, Jöesaar I, Sipari N, Kollist H, Palva ET, Kariola T (2015) The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol 15(1):53PubMedPubMedCentralCrossRefGoogle Scholar
  68. Radutoiu S, Madsen L, Madsen E, Jurkiewicz A, Fukai E, Quistgaard E, Albrektsen A, James E, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935PubMedPubMedCentralCrossRefGoogle Scholar
  69. Rehman NU, Ali M, Ahmad MZ, Liang G, Zhao J (2018) Strigolactones promote rhizobia interaction and increase nodulation in soybean (Glycine max). Microb Pathog 114:420–430PubMedCrossRefPubMedCentralGoogle Scholar
  70. Roth R, Paszkowski U (2017) Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr Opin Plant Biol 39:50–56PubMedCrossRefGoogle Scholar
  71. Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P (2016) Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10(1):130–144PubMedCrossRefGoogle Scholar
  72. Sasse J, Simon S, Gübeli C, Liu G-W, Cheng X, Friml J, Bouwmeester H, Martinoia E, Borghi L (2015) Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr Biol 25(5):647–655PubMedCrossRefGoogle Scholar
  73. Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165(3):1221–1232PubMedPubMedCentralCrossRefGoogle Scholar
  74. Schlemper TR, Leite MFA, Lucheta AR, Shimels M, Bouwmeester HJ, van Veen JA, Kuramae EE (2017) Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol Ecol 93(8):1–11CrossRefGoogle Scholar
  75. Sharda JN, Koide RT (2008) Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? New Phytol 180(3):696–701PubMedCrossRefGoogle Scholar
  76. Smith SM, Li J (2014) Signalling and responses to strigolactones and karrikins. Curr Opin Plant Biol 21:23–29PubMedCrossRefGoogle Scholar
  77. Smith S, Read D (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  78. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62(1):227–250PubMedCrossRefGoogle Scholar
  79. Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Ocampo JA, Delgado MJ (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385CrossRefGoogle Scholar
  80. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12(7):1290–1306PubMedPubMedCentralCrossRefGoogle Scholar
  81. Stes E, Francis I, Pertry I, Dolzblasz A, Depuydt S, Vereecke D (2013) The leafy gall syndrome induced by Rhodococcus fascians. FEMS Microbiol Lett 342(2):187–195PubMedCrossRefPubMedCentralGoogle Scholar
  82. Stes E, Depuydt S, De Keyser A, Matthys C, Audenaert K, Yoneyama K, Werbrouck S, Goormachtig S, Vereecke D (2015) Strigolactones as an auxiliary hormonal defence mechanism against leafy gall syndrome in Arabidopsis thaliana. J Exp Bot 66(16):5123–5134PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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):104–107PubMedCrossRefPubMedCentralGoogle Scholar
  84. Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15(2):211–216PubMedCrossRefGoogle Scholar
  85. Tsuzuki S, Handa Y, Takeda N, Kawaguchi M (2016) Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mol Plant Microbe Interact 29(4):277–286PubMedCrossRefPubMedCentralGoogle Scholar
  86. van Zeijl A, Liu W, Xiao TT, Kohlen W, Yang WC, Bisseling T, Geurts R (2015) The strigolactone biosynthesis gene DWARF27 is co-opted in Rhizobium symbiosis. BMC Plant Biol 15:260PubMedPubMedCentralCrossRefGoogle Scholar
  87. Visentin I, Vitali M, Ferrero M, Zhang Y, Ruyter-Spira C, Novak O, Strnad M, Lovisolo C, Schubert A, Cardinale F (2016) Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol 212(4):954–963PubMedCrossRefPubMedCentralGoogle Scholar
  88. Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68(1):291–322PubMedCrossRefPubMedCentralGoogle Scholar
  89. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207PubMedCrossRefPubMedCentralGoogle Scholar
  90. Yoneyama K, Xie X, Yoneyama K, Kisugi T, Nomura T, Nakatani Y, Akiyama K, McErlean CSP (2018) Which are the major players, canonical or non-canonical strigolactones? J Exp Bot 69(9):2231–2239PubMedCrossRefPubMedCentralGoogle Scholar
  91. Yoshida S, Kameoka H, Tempo M, Akiyama K, Umehara M, Yamaguchi S, Hayashi H, Kyozuka J, Shirasu K (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol 196(4):1208–1216PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Soizic Rochange
    • 1
  • Sofie Goormachtig
    • 2
    • 3
  • Juan Antonio Lopez-Raez
    • 4
  • Caroline Gutjahr
    • 5
    Email author
  1. 1.Laboratoire de Recherche en Sciences Végétales (LRSV), UMR5546Université de Toulouse and CNRR, UPSCastanet-TolosanFrance
  2. 2.Department of Plant Biotechnology and BioinformaticsGhent UniversityGentBelgium
  3. 3.Center for Plant Systems Biology, VIBGentBelgium
  4. 4.Department of Soil Microbiology and Symbiotic SystemsEstación Experimental del Zaidín-Consejo Superior de Investigaciones Científicas (EEZ-CSIC)GranadaSpain
  5. 5.Plant Genetics, School of Life Sciences WeihenstephanTechnical University of Munich (TUM)FreisingGermany

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