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Symbiosis signaling: Solanaceae symbiotic LCO receptors are functional for rhizobium perception in
legumes
Pascal Ratet
To cite this version:
Pascal Ratet. Symbiosis signaling: Solanaceae symbiotic LCO receptors are functional for rhizobium perception in legumes. Current Biotechnology, 2019, 29 (24), pp.R1312-R1314.
�10.1016/j.cub.2019.10.046�. �hal-03052605�
Title:
Symbiosis signaling: Solanaceae symbiotic LCO receptors are functional for rhizobium perception in legumes.
Pascal Ratet1,2
1 Institute of Plant Sciences Paris-Saclay IPS2, CNRS, INRA, Université Paris-Sud, Université Evry, Université Paris-Saclay, Bâtiment 630, 91405 Orsay, France.
2 Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cité, Bâtiment 630, 91405, Orsay, France.
pascal.ratet@cnrs.fr
Abstract (35 words):
A new study shows that plant receptor genes necessary for the ancient and widespread symbiosis with arbuscular mycorrhizal fungi were co-opted in legume plants without modifications to establish the evolutionary more recent and more specific symbiosis with their bacterial rhizobium partners.
Text (1117 words):
Some plants are able to grow in nitrogen poor soils because they can establish symbiosis with rhizobia or frankia (actinobacteria) bacteria able to reduce the non-limiting atmospheric gaseous nitrogen (N2) to NH3 to the benefit of their host. The capacity to establish this symbiosis also called root nodule symbiosis (RNS) is confined to the Rosid I clade including actinorhizal plants, Parasponia and legumes (1). The RNS was extensively studied using the legume–rhizobia symbiosis and generally requires a specific signaling between both organisms with excretion of flavonoids in the rhizosphere by the plant and production of specific lipo-chitooligosaccharides (LCO or Nod factors for the RNS) by the rhizobia that are recognized by plant specific receptors belonging to the LysM kinase receptor family (LysM-RLK; 2). Genetic studies have highlighted the central role of the Nod factor dependent signaling in most of the legume rhizobia interactions even if variations around this theme exist (3). RNS requires organogenesis and lead to the formation of the nodule organ (generally on the root), hosting the symbiotic bacteria and in which nitrogen reduction takes place. Actinorhizal nodules present a single central vascular bundle that makes them
resembling modified lateral roots (4-5). Legume nodules are divided in two main types depending on the presence or absence of an apical meristem (indeterminate versus determinate nodules) and have peripheral vascular tissues surrounding the central infected tissues.
Genetic studies have suggested that Legume-rhizobia symbiotic signaling evolved from AM symbiosis (6) because some legume mutants are affected in both symbiosis and mycorrhizal fungi are able to produce Nod factor-like (LCO) molecules. It is the mechanism that allowed AM symbiotic genes, and more precisely LCO receptors, to be used for the RNS in legumes that is address in this issue by Girardin et al., (7).
Genes that are common to both symbioses define the common symbiosis signaling pathway (CSSP) (6). However it is now evident that AM symbiosis requires a more complex signaling than the RNS one, because AM fungi produce mixtures of chitooligosaccharides (CO) and LCO molecules (8, 9) perceived by probably different LysM-RLK. This suggests that nodule forming plants have recruited only part of the AM signaling pathway to develop RNS. In agreement with these genetic approaches, phylogenetic studies suggest that RNS has evolved only once, around 100 million years ago (MYA) using components of the AM symbiotic signaling which itself appeared 400 MYA (10 - 12). However, how these AM symbiotic genes and more precisely how the LysM-RLKs were recruited in legume plants to establish the RNS remained unknown. In Legume plants the Nod factor receptors (NFP, Lyk3 in Medicago truncatula and NFR1, NFR5 in Lotus japonicus) are expressed in root epidermis and in the nodule and are thought to recognize specifically the cognate Nod factor. NFP and NFR5 belong to the LysM-RLK LYRIA clade and mutants in these genes are unable to establish RNS but are not affected for AM symbiosis. Paralogs of these genes are expressed in arbuscule containing cells of the root suggesting a role in the fungal symbiosis (13, 14). The presence of two LCO receptors in legume plants suggests a gene duplication in the legume ancestors (or nodule forming plant ancestor) followed by a neo-functionalization of one of them for the RNS. With this hypothesis the receptor protein should have acquired the specificity for the cognate Nod factor perception and the promoter region should have evolved to specifically express in epidermis, in root hairs and during nodule organogenesis.
In contrast to this hypothesis, Girardin et al., (7) elegantly demonstrate that the promoter and the proteins encoded by the LYRIA receptor genes necessary for arbuscular mycorrhiza recognition in Solonaceae plants (AM symbiosis) are functional for the rhizobium recognition in legume and thus were recruited without modification during evolution for the
acquisition of symbiosis with nitrogen fixing bacteria (RNS). The key experiments of this study are described below.
The tomato and petunia SlLYK10 and PhLYK10 genes are unique LYRIA genes (homolog to NFP) and the corresponding sllyk10 and phlyk10 mutants are required for AM symbiosis establishment. Furthermore specific LCOs binding by membrane fractions containing these receptors and the high affinity (Kd in the range of 20 nM) to LCOs compared to COs (Kd higher than 1 M) demonstrate that the Solanaceae receptors are genuine LCO receptors with a LCO affinity comparable to the legume ones (15).
In order to know if the promoters of these Solanaceae genes are still functional in legume plants, the authors first show that promoter::GUS (proSlLYK10 and proPhLYK10) constructs are specifically up-regulated at early stages of arbuscule development in root cortical cells. Secondly they expressed these constructs in legume plants together with the proNFP::GUS construct and showed that the three constructs are similarly expressed. This demonstrates that the AM symbiotic Solanaceae promoters contain all the information (cis- regulatory elements) required for expression in legume nodules. Furthermore the authors expressed the NFP coding sequence from either the NFP or SlLYK10 promoters and could complement the nfp mutant with this construct. This confirms that the cis-regulatory elements from the Solanaceae AM symbiotic promoters are sufficient to express the receptor in the nodules.
The authors also searched for and identified a common cis-regulatory element in the LYRIA promoter region from dicotyledonous plant species including nodule-forming and non-nodule forming plants. A minimal SiLYK10 promoter retaining this sequence is expressed in young nodules suggesting that the recruitment of LYRIA genes for RNS did not require modification of the cis-regulatory sequences in the symbiotic promoters. Lastly the authors expressed the SlSILK10 and PhSILK10 coding sequences under strong promoters in the legume nfp or nfr5 mutants and were able to complement the mutations showing that the Solanaceae proteins have the capacity to support RNS.
This work provides clear genetic evidence via the characterization of petunia and tomato mutants that members of the LysM-RLK (LYRIA phylogenetic group) promote efficient AMF root penetration and are required for proper arbuscule development. In addition it allows proposing an evolutionary scenario in which an ancestral LYRIA gene involved in AM establishment was recruited directly for a role in nodule organogenesis and rhizobial colonization without a need for cis-regulatory elements and protein sequence modification.
In addition, these results raise two hypotheses for the biological role of these proteins.
First, because they participate to intracellular accommodation in the two symbioses, the role of these LYRIA proteins in plants might be to host microbial partners intracellularly.
Secondly the complementation of the nfp and nfr5 mutants by the tomato and petunia proteins raises the question of the specificity of Nod factor recognition by the legume proteins. We can thus suppose that the Solanacea proteins are recognizing specifically the general LCO structure but not the CO molecules as shown in this work. However they probably do not participate to the specific recognition of the LCO decoration, that are responsible for the rhizobium strain specificity. Other LysM-RLK like Lyk3 (M. truncatula) or NFR1 (L.
japonicus) or NF hydrolases (16) might be responsible for this specificity.
References (15)
1. Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., &
Martin P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92, 2647–2651.
2. Buendia, L., Girardin, A., Wang, T., Cottret, L., and Lefebvre, B. (2018). LysM Receptor- Like kinase and LysM receptor-like protein families: an update on phylogeny and functional characterization. Front Plant Sci 9, 1531.
3. Fabre, S., Gully, D., Poitout, A., Patrel, D., Arrighi, J.F., Giraud, E., Czernic, P., Cartieaux, F. (2015) Nod Factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic toolkit. Plant Physiol. 169, 2654-64.
4. Franche, C., Laplaze, L., Duhoux, E., & Bogusz, D. (1998). Actinorhizal symbioses:
Recent advances in plant molecular and genetic transformation studies. Critical Reviews in Plant Sci 17, 1–28.
5. Froussart, E., Bonneau, J., Franche, C., & Bogusz, D. (2016a). Recent advances in actinorhizal symbiosis signaling. Plant Mol Biol 90, 613–622.
6. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6, 763-775.
7. Girardin, A., Wang, T., Ding, Y., Keller, J., Buendia, L., Gaston, M., Ribeyre, C., Gasciolli, V., Auriac, M-C., Vernié, T., Bendahmane, A., Ried, M., Parniske, M., Morel, P., Vandenbussche, M., Schorderet, M., Reinhardt, D., Delaux, P-M;, Bono J-J., Lefebvre B. (2019) LCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biology, this issue.
8. Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Bécard, G., and Dénarié, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63.
9. Genre, A., Chabaud, M., Balzergue, C., Puech-Pages, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Bécard, G., Bonfante, P., and Barker, D.G. (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, 179- 189.
10. Doyle, J. J. (2011). Phylogenetic perspectives on the origins of nodulation. Mol Plant
Microbe Interac 24, 1289–1295.
11. van Velzen, R., Doyle, J. J., & Geurts, R. (2019). A Resurrected Scenario: Single Gain and Massive Loss of Nitrogen-Fixing Nodulation. Trends Plant Sci 24, 49–57.
12. Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J., & Kiers, E. T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Commun 10, 4087.
13. Gomez, S.K., Javot, H., Deewatthanawong, P., Torres-Jerez, I., Tang, Y., Blancaflor, E.B., Udvardi, M.K., and Harrison, M.J. (2009). Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9, 10.
14. Rasmussen, S.R., Füchtbauer, W., Novero, M., Volpe, V., Malkov, N., Genre, A., Bonfante, P., Stougaard, J., and Radutoiu, S. (2016). Intraradical colonization by arbuscular mycorrhizal fungi triggers induction of a lipochitooligosaccharide receptor. Sci Rep 6, 29733.
15. Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J.T., Maolanon, N., Vinther, M., Lorentzen, A., Madsen, E.B., Jensen, K.J., Roepstorff, P., Thirup, S., Ronson, C.W., Thygesen, M.B., and Stougaard, J. (2012). Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci USA 109, 13859-13864.
16. Cai, J., Zhang, L.Y., Liu, W., Tian, Y., Xiong, J.S., Wang, Y.H., Li, R.J., Li, H.M., Wen, J., Mysore, K.S., Boller, T., Xie, Z.P., Staehelin, C. (2018) Role of the Nod Factor hydrolase MtNFH1 in regulating Nod Factor levels during Rhizobial infection and in mature nodules of Medicago truncatula. Plant Cell. 30, 397-414.
