Abstract
The industrial agriculture has given rise to an excessive use and misuse of agrochemicals causing environmental pollution. Therefore, it is urgent to find alternatives that are more environmentally friendly than chemical fertilizers and pesticides for disease control. The key to achieve successful biological control strategies is the knowledge of the ecological interactions that occur belowground. The rhizosphere constitutes a very dynamic environment harbouring the plant roots and many organisms. Plants communicate and interact with those organisms through the production and release of a large variety of secondary metabolites into the rhizosphere. Thus, they use these metabolites to defend themselves against soil-borne pathogens, which can adversely affect plant growth and fitness, but also to establish mutualistic associations with beneficial soil microorganisms. However, despite the importance of these plant-organism interactions the mechanisms regulating them remain largely unknown.
We review here chemical communication that takes place in the rhizosphere between plants and other soil organisms, and the potential use of this molecular dialogue for developing new biological control strategies against deleterious organisms. We focus on the knowledge of the root parasitic weed germination stimulants – strigolactones – to develop more efficient control methods against this pest. Finally, we illustrate this with an exciting example: the use of the mutualistic arbuscular mycorrhizal symbiosis for controlling root parasitic weeds by reducing the production of strigolactones in the host plant.
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Abbreviations
- AM:
-
arbuscular mycorrhiza
- AHL:
-
N-acyl homoserine lactone
- PGPF:
-
plant growth promoting fungi
- PGPR:
-
plant growth promoting rhizobacteria
- QS:
-
Quorum sensing
References
Agrios GN (2005) Plant pathology. Elsevier, New York
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
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
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650
Bais HP, Walker TS, Schweizer HP, Vivanco JA (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778
Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Becard G, Sejalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. Plos Biol 4:1239–1247
Bird DM, Kaloshian I (2003) Are roots special? Nematodes have their say. Physiol Mol Plant P 62:115–123
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 27(1):1–11
Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364
Bouwmeester HJ, Roux C, López-Ráez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230
Bucher M, Wegmuller S, Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 12:500–507
Caillaud MC, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecornte P, Engler JD, Abad P, Rosso MN, Favery B (2008) Root-knot nematodes manipulate plant cell functions during a compatible interaction. J Plant Physiol 165:104–113
Cook CE, Whichard LP, Wall ME, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. 2. The structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199
Delgado JA (2002) Quantifying the loss mechanisms of nitrogen. J Soil Water Conserv 57:389–398
Ejeta G (2007) Breeding for Striga resistance in sorghum: exploitation of an intricate host-parasite biology. Crop Sci 47:S216–227
Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7
Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303
Fernández-Aparicio M, García-Garrido JM, Ocampo JA, Rubiales D (2010) Colonisation of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 50:262–268
Fitter AH (2005) Darkness visible: reflections on underground ecology. J Ecol 93:231–243
Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44
Garcia VG, Onco MAP, Susan VR (2006) Review. Biology and systematics of the form genus Rhizoctonia. Span J Agric Res 4:55–79
Garg N, Geetanjali (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron Sustain Dev 27:59–68
Genin S, Boucher C (2004) Lessons learned from the genome analysis of Ralstonia solanacearum. Annu Rev Phytopathol 42:107–134
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagés V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194
Gressel J, Hanafi A, Head G, Marasas W, Obilana AB, Ochanda J, Souissi T, Tzotzos G (2004) Major heretofore intractable biotic constraints to African food security that may be amenable to novel biotechnological solutions. Crop Prot 23:661–689
Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110
Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors - controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868
Horiuchi J, Prithiviraj B, Bais HP, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857
Jain R, Foy CL (1992) Nutrient effects on parasitism and germination of Egyptian broomrape (Orobanche aegyptiaca). Weed Technol 6:269–275
Jamil M, Charnikhova T, Verstappen F, Bouwmeester H (2010) Carotenoid inhibitors reduce strigolactone production and Striga hermonthica infection in rice. Arch Biochem Biophys 504:123–131
Joel DM, Hershenhom Y, Eizenberg H, Aly R, Ejeta G, Rich JP, Ransom JK, Sauerborn J, Rubiales D (2007) Biology and management of weedy root parasites. Hortic Rev 33:267–349
Johnson AW, Roseberry G, Parker C (1976) A novel approach to Striga and Orobanche control using synthetic germination stimulants. Weed Res 16:223–227
Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29
Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136
Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962
Lendzemo VW, Kuyper TW, Kropff MJ, van Ast A (2005) Field inoculation with arbuscular mycorrhizal fungi reduces Striga hermonthica performance on cereal crops and has the potential to contribute to integrated Striga management. Field Crops Res 91:51–61
Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ, van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal Behav 2:58–62
López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008a) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874
López-Ráez JA, Charnikhova T, Mulder P, Kohlen W, Bino R, Levin I, Bouwmeester H (2008b) Susceptibility of the tomato mutant high pigment-2 (hp-2 dg) to Orobanche spp infection. J AgricFood Chem 56:6326–6332
López-Ráez JA, Matusova R, Cardoso C, Jamil M, Charnikhova T, Kohlen W, Ruyter-Spira C, Verstappen F, Bouwmeester H (2009) Strigolactones: ecological significance and use as a target for parasitic plant control. Pest Manag Sci 64:471–477
López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular mycorhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297
Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63
Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466
Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139: 920–934
Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739
Nagahashi G, Douds DD (2004) Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantea. Mycol Res 108:1079–1088
Otten W, Gilligan CA (2006) Soil structure and soil-borne diseases: using epidemiological concepts to scale from fungal spread to plant epidemics. Eur J Soil Sci 57:26–37
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172:35–46
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201
Perry RN, Moens M (2006) Plant nematology. CABI publishing, London
Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398
Priest FG, Campbell I (2003) Brewing microbiology. Kluwer, New York
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361
Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187
Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626
Reddy PM, Rendon-Anaya M, de los Dolores Soto del Rio M (2007) Flavonoids as signaling molecules and regulators of root nodule development. Dyn Soil Dyn Plant 1:83–94
Requena N, Serrano E, Ocon A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68:33–40
Rispail N, Dita MA, Gonzalez-Verdejo C, Perez-de-Luque A, Castillejo MA, Prats E, Roman B, Jorrin J, Rubiales D (2007) Plant resistance to parasitic plants: molecular approaches to an old foe. New Phytol 173:703–711
Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeij A, van Bezouwen L, de Ruijter N, Cardoso C, López-Ráez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analogue GR24 on root system architecture in Arabidopsis: Another below-ground role of strigolactones? Plant Physiol 155:721–734
Sbrana C, Giovannetti M (2005) Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15:539–545
Schenk H, Driessen RAJ, de Gelder R, Goubitz K, Nieboer H, Bruggemann-Rotgans IEM, Diepenhorst P (1999) Elucidation of the structure of Solanoeclepin A, a natural hatching factor of potato and tomato cyst nematodes, by single-crystal x-ray diffraction. Croatica Chemica Acta 72:593–606
Scholes JD, Press MC (2008) Striga infestation of cereal crops - an unsolved problem in resource limited agriculture. Curr Opin Plant Biol 11:180–186
Siegler DS (1998) Plant secondary metabolism. Kluwer, Boston
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Smith SE, Barker SJ, Zhu YG (2006) Fast moves in arbuscular mycorrhizal symbiotic signalling. Trends Plant Sci 11:369–371
Soto MJ, Fernandez-Aparicio M, Castellanos-Morales V, Garcia-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 42:383–385
Sprent JI (2009) Legume nodulation. A global perspective. Wiley-Blackwell, Chichester
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 12:1290–1306
Sun Z, Matusova R, Bouwmeester H (2007) Germination of Striga and chemical signaling involved: a target for control methods. In: Gressel J, Ejeta G (eds) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific, Nairobi, pp 47–60
Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FWA, Ming Z, van Echtelt E, Strack D, Bisseling T, Bouwmeester HJ (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801
Thompson JN (2005) Coevolution: the geographic mosaic of coevolutionary arms races. Curr Biol 15:R992–R994
Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200
Varma A, Verma S, Sudha, Sahay N, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311
Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci U S A 102:3147–3152
Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479
Wigchert SCM, Kuiper E, Boelhouwer GJ, Nefkens GHL, Verkleij JAC, Zwanenburg B (1999) Dose-response of seeds of the parasitic weeds Striga and Orobanche toward the synthetic germination stimulants GR24 and Nijmegen 1. J Agric Food Chem 47:1705–1710
Williamson VM, Gleason CA (2003) Plant-nematode interactions. Curr Opin Plant Biol 6:327–333
Yoneyama K, Takeuchi Y, Yokota T (2001) Production of clover broomrape seed germination stimulants by red clover requires nitrate but it inhibited by phosphate and ammonium. Physiol Plant 112:25–30
Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038
Yoneyama K, Xie XN, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494
Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones: structures and biological activities. Pest Manag Sci 65:467–470
Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65:478–491
Acknowledgements
Our research is supported by grants PERG-02-2007-224751 from the Marie Curie program from the European Commission, AGL2009-07691 from the National R&D Plan of the MINCIN, and The Netherlands Organisation for Scientific Research (NWO; VICI-grant to HB). HB is also (co) financed by the Centre for BioSystems Genomics (CBSG), a part of the Netherlands Genomics Initiative/Netherlands Organisation for Scientific Research. JAL-R is supported by a postdoctoral contract (JAE-Doc) from the Spanish Research Council (CSIC).
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López-Ráez, J.A., Bouwmeester, H., Pozo, M.J. (2012). Communication in the Rhizosphere, a Target for Pest Management. In: Lichtfouse, E. (eds) Agroecology and Strategies for Climate Change. Sustainable Agriculture Reviews, vol 8. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1905-7_5
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