Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species

Autoři: Mireille Chabaud aff001;  Joëlle Fournier aff001;  Lukas Brichet aff001;  Iltaf Abdou-Pavy aff001;  Leandro Imanishi aff002;  Laurent Brottier aff003;  Elodie Pirolles aff003;  Valérie Hocher aff003;  Claudine Franche aff004;  Didier Bogusz aff004;  Luis G. Wall aff002;  Sergio Svistoonoff aff003;  Hassen Gherbi aff003;  David G. Barker aff001
Působiště autorů: Laboratory of Plant-Microbe Interactions (INRA/CNRS/University of Toulouse), Castanet-Tolosan, France aff001;  Laboratory of Biochemistry, Microbiology and Soil Biological Interactions, Department of Science and Technology, National University of Quilmes, CONICET, Bernal, Argentina aff002;  Laboratory of Tropical and Mediterranean Symbioses (IRD/INRA/CIRAD/University of Montpellier/Supagro), Montpellier, France aff003;  Plant Diversity, Adaptation and Development (IRD/University of Montpellier), Montpellier, France aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223149


Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.

Klíčová slova:

Fungi – Genetically modified plants – Chitin – Legumes – Plants – Symbiosis – Root hairs – Acetonitrile


1. Bonfante P, Genre A. Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science. 2008;13:492–8. doi: 10.1016/j.tplants.2008.07.001 18701339

2. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology. 2008;6:763–75. doi: 10.1038/nrmicro1987 18794914

3. Martin FM, Uroz S, Barker DG. Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. Science. 2017;356:aad4501.

4. Ibañez F, Wall L, Fabra A. Starting points in plant-bacteria nitrogen-fixing symbioses: intercellular invasion of the roots. Journal of Experimental Botany. 2017;68:1905–18. doi: 10.1093/jxb/erw387 27756807

5. Fournier J, Timmers ACJ, Sieberer BJ, Jauneau A, Chabaud M, Barker DG. Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiology. 2008;148:1985–95. doi: 10.1104/pp.108.125674 18931145

6. Gage DJ. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews. 2004;68:280–300. doi: 10.1128/MMBR.68.2.280-300.2004 15187185

7. Svistoonoff S, Hocher V, Gherbi H. Actinorhizal root nodule symbioses: what is signalling telling about the origins of nodulation? Current Opinion in Plant Biology. 2014;20:11–18. doi: 10.1016/j.pbi.2014.03.001 24691197

8. Liu Q, Berry AM. The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis–a structural and histochemical study. Protoplasma. 1991;163:82–92.

9. Miller IM, Baker DD. The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma. 1985;128:107–119.

10. Valverde C, Wall LG. Time course of nodule development in the Discaria trinervis (Rhamnaceae) Frankia symbiosis. New Phytologist. 1999;141:345–54.

11. Gutjahr C, Parniske M. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology. 2013;29:593–617. doi: 10.1146/annurev-cellbio-101512-122413 24099088

12. Oldroyd GED. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology. 2013;11:252–63. doi: 10.1038/nrmicro2990 23493145

13. Barker DG, Chabaud M, Russo G, Genre A. Nuclear Ca2+ signalling in arbuscular mycorrhizal and actinorhizal endosymbioses: on the trail of novel underground signals. New Phytologist. 2017;214:533–8. doi: 10.1111/nph.14350 27918078

14. Miwa H, Sun J, Oldroyd GED, Downie JA. Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant Journal. 2006;48:883–94. doi: 10.1111/j.1365-313X.2006.02926.x 17227545

15. Antolin-Llovera M, Petutsching EK, Ried MK, Lipka V, Nurnberger T, Robatzek S, et al. Knowing your friends and foes—plant receptor-like kinases as initiators of symbiosis or defence. New Phytologist. 2014;204:791–802. doi: 10.1111/nph.13117 25367611

16. Zipfel C, Oldroyd GED. Plant signalling in symbiosis and immunity. Nature. 2017;543:328–36. doi: 10.1038/nature22009 28300100

17. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature. 2011;469:58–63. doi: 10.1038/nature09622 21209659

18. Genre A, Chabaud M, Balzergue C, Puech-Pages V, Novero M, Rey T, et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist. 2013;198:179–89. doi: 10.1111/nph.12120

19. Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, et al. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell. 2015;27:823–38. doi: 10.1105/tpc.114.131326 25724637

20. Carotenuto G, Chabaud M, Miyata K, Capozzi M, Takeda N, Kaku H, et al. The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling. New Phytologist. 2017;214:1440–6. doi: 10.1111/nph.14539 28369864

21. Cérémonie H, Debellé F, Fernandez MP. Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Canadian Journal of Botany. 1999;77:1293–301.

22. Chabaud M, Gherbi H, Pirolles E, Vaissayre V, Fournier J, Moukouanga D, et al. Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytologist. 2016;209:86–93. doi: 10.1111/nph.13732 26484850

23. Cissoko M, Hocher V, Gherbi H, Gully D, Carre-Mlouka A, Sane S, et al. Actinorhizal signaling molecules: Frankia root hair deforming factor shares properties with NIN-inducing factor. Frontiers in Plant Science. 2018;9:1494. doi: 10.3389/fpls.2018.01494 30405656

24. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, Barker DG. A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiology. 2009;151:1197–206. doi: 10.1104/pp.109.142851 19700563

25. Fournier J, Imanishi L, Chabaud M, Abdou-Pavy I, Genre A, Brichet L, et al. Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization. New Phytologist. 2018;219:1018–30. doi: 10.1111/nph.15216 29790172

26. Svistoonoff S, Sy MO, Diagne N, Barker DG, Bogusz D, Franche C. Infection-specific activation of the Medicago truncatula Enod11 early nodulin gene promoter during actinorhizal root nodulation. Molecular Plant-Microbe Interactions. 2010;23:740–7. doi: 10.1094/MPMI-23-6-0740 20459313

27. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MD, Goker M, Meier-Kolthoff JP, Schumann P, et al. Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp nov and Frankia elaeagni sp nov. International Journal of Systematic and Evolutionary Microbiology. 2016;66:5201–10. doi: 10.1099/ijsem.0.001496 27624710

28. Nouioui I, Montero-Calasanz MD, Ghodhbane-Gtari F, Rohde M, Tisa LS, Klenk HP, et al. Frankia discariae sp nov.: an infective and effective microsymbiont isolated from the root nodule of Discaria trinervis. Archives of Microbiology. 2017;199(5):641–7. doi: 10.1007/s00203-017-1337-6 28105505

29. Clavijo F, Diedhiou I, Vaissayre V, Brottier L, Acolatse J, Moukouanga D, et al. The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytologist. 2015;208:887–903. doi: 10.1111/nph.13506 26096779

30. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proceedings of the National Academy of Sciences of the United States of America. 2008;105:4928–32. doi: 10.1073/pnas.0710618105 18316735

31. Diagne N, Escoute J, Lartaud M, Verdeil JL, Franche C, Kane A, et al. Uvitex2B: a rapid and efficient stain for detection of arbuscular mycorrhizal fungi within plant roots. Mycorrhiza. 2011;21:315–21. doi: 10.1007/s00572-010-0357-8 21225294

32. Svistoonoff S, Benabdoun FM, Nambiar-Veetil M, Imanishi L, Vaissayre V, Cesari S, et al. The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PloS One. 2013;8:e64515. doi: 10.1371/journal.pone.0064515 23741336

33. Obertello M, Wall LG. Interactions between Frankia BCU110501 (actinorhiza) and Gigaspora rosea (arbuscular mycorrhiza) with Discaria trinervis studied by spot inoculation. Symbiosis. 2015;66:13–20.

34. Smith SE, Reed DJ. Mycorrhizal Symbiosis. London, UK: Elsevier. 2008.

35. Bonfante P, Genre A, Faccio A, Martini I, Schauser L, Stougaard J, et al. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Molecular Plant-Microbe Interactions. 2000;13:1109–20. doi: 10.1094/MPMI.2000.13.10.1109 11043472

36. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell. 2005;17:3489–99. doi: 10.1105/tpc.105.035410 16284314

37. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell. 2008;20:1407–20. doi: 10.1105/tpc.108.059014 18515499

38. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, et al. Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and non-legume root epidermis. New Phytologist. 2011;189:347–55. doi: 10.1111/j.1469-8137.2010.03464.x 20880223

39. Imanishi L, Vayssieres A, Franche C, Bogusz D, Wall L, Svistoonoff S. Transformed hairy roots of Discaria trinervis: A valuable tool for studying actinorhizal symbiosis in the context of intercellular infection. Molecular Plant-Microbe Interactions. 2011;24:1317–24. doi: 10.1094/MPMI-03-11-0078 21585269

40. Goormachtig S, Capoen W, James EK, Holsters M. Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:6303–8. doi: 10.1073/pnas.0401540101 15079070

41. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Communications. 2010;1:10. doi: 10.1038/ncomms1009 20975672

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