- Email: [email protected]
Symbiosis Signaling: Solanaceae Symbiotic LCO Receptors Are Functional for Rhizobium Perception in Legumes
Current Biology
Dispatches recent study in Current Biology found that ambient temperature increases, which we often seek when going to bed, activate preoptic neurons through a multisynaptic excitatory pathway [20]. The pernicious association between lack of sleep and obesity is another one for which subgroups of LHGABA neurons may be ultimately held responsible. Other environmental conditions or bodily states that affect sleep/wake, however, may come as a surprise. We must stay tuned for rapid further developments. REFERENCES 1. Von Economo, C. (1930). Sleep as a problem of localization. J. Nerv. Ment. Dis. 71, 249–259. 2. Nauta, W.J.H. (1946). Hypothalamic regulation of sleep in rats. An experimental study. J. Neurophysiol. 9, 285–316. 3. Liu, D., and Dan, Y. (2019). A motor theory of sleep-wake control: arousal-action circuit. Annu. Rev. Neurosci. 42, 27–46. 4. Luppi, P.H., and Fort, P. (2019). Neuroanatomical and neurochemical bases of vigilance states. Handb. Exp. Pharmacol. 253, 35–58. 5. Venner, A., De Luca, R., Sohn, L.T., Bandaru, S.S., Verstegen, A.M.J., Arrigoni, E., and Fuller, P.M. (2019). An inhibitory lateral hypothalamic-preoptic circuit mediates rapid arousals from sleep. Curr. Biol. 29, 4155–4168.
6. Saper, C.B., and Lowell, B.B. (2014). The hypothalamus. Curr. Biol. 24, R1111–R1116. 7. Arrigoni, E., Chee, M.J.S., and Fuller, P.M. (2019). To eat or to sleep: that is a lateral hypothalamic question. Neuropharmacology 154, 34–49. 8. Mahoney, C.E., Cogswell, A., Koralnik, I.J., and Scammell, T.E. (2019). The neurobiological basis of narcolepsy. Nat. Rev. Neurosci. 20, 83–93. 9. Saper, C.B., Fuller, P.M., Pedersen, N.P., Lu, J., and Scammell, T.E. (2010). Sleep state switching. Neuron 68, 1023–1042. 10. Burdakov, D., Karnani, M.M., and Gonzalez, A. (2013). Lateral hypothalamus as a sensorregulator in respiratory and metabolic control. Physiol. Behav. 121, 117–124. 11. Herrera, C.G., Ponomarenko, A., Korotkova, T., Burdakov, D., and Adamantidis, A. (2017). Sleep and metabolism: the multitasking ability of lateral hypothalamic inhibitory circuitries. Front. Neuroendocrinol. 44, 27–34. 12. Venner, A., Anaclet, C., Broadhurst, R.Y., Saper, C.B., and Fuller, P.M. (2016). A novel population of wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Curr. Biol. 26, 2137–2143. 13. Herrera, C.G., Cadavieco, M.C., Jego, S., Ponomarenko, A., Korotkova, T., and Adamantidis, A. (2016). Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat. Neurosci. 19, 290–298. 14. Szymusiak, R., and McGinty, D. (2008). Hypothalamic regulation of sleep and arousal. Ann. N.Y. Acad. Sci. 1129, 275–286.
15. Zhang, Z., Ferretti, V., Guntan, I., Moro, A., Steinberg, E.A., Ye, Z., Zecharia, A.Y., Yu, X., Vyssotski, A.L., Brickley, S.G., et al. (2015). Neuronal ensembles sufficient for recovery sleep and the sedative actions of a2 adrenergic agonists. Nat. Neurosci. 18, 553–561. 16. Chung, S., Weber, F., Zhong, P., Tan, C.L., Nguyen, T.N., Beier, K.T., Hormann, N., Chang, W.C., Zhang, Z., Do, J.P., et al. (2017). Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545, 477–481. 17. Kroeger, D., Absi, G., Gagliardi, C., Bandaru, S.S., Madara, J.C., Ferrari, L.L., Arrigoni, E., Mu¨nzberg, H., Scammell, T.E., Saper, C.B., and Vetrivelan, R. (2018). Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nat. Commun. 9, 4129. 18. Ma, Y., Miracca, G., Yu, X., Harding, E.C., Miao, A., Yustos, R., Vyssotski, A.L., Franks, N.P., and Wisden, W. (2019). Galanin neurons unite sleep homeostasis and a2-adrenergic sedation. Curr. Biol. 29, 3315–3322.e3. 19. Carter, M.E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., and de Lecea, L. (2010). Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526– 1533. 20. Harding, E.C., Yu, X., Miao, A., Andrews, N., Ma, Y., Ye, Z., Lignos, L., Miracca, G., Ba, W., Yustos, R., et al. (2018). A neuronal hub binding sleep initiation and body cooling in response to a warm external stimulus. Curr. Biol. 28, 2263–2273.e4.
Symbiosis Signaling: Solanaceae Symbiotic LCO Receptors Are Functional for Rhizobium Perception in Legumes Pascal Ratet1,2
Paris-Sud, Universite Evry, Universite Paris-Saclay, Baˆtiment 630, of Plant Sciences Paris-Saclay IPS2, CNRS, INRA, Universite 91405 Orsay, France 2Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cite , Baˆtiment 630, 91405 Orsay, France Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.10.046 1Institute
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 evolutionarily more recent and more specific symbiosis with their bacterial rhizobium partners. Some plants are able to grow in nitrogenpoor soils because they can establish symbiosis with rhizobia or frankia
(actinobacteria) bacteria, which are able to reduce the non-limiting atmospheric gaseous nitrogen (N2) to NH3 to the
R1312 Current Biology 29, R1301–R1325, December 16, 2019 ª 2019 Elsevier Ltd.
benefit of their host. The capacity to establish this symbiosis, also called root nodule symbiosis (RNS), is confined to the
Current Biology
Dispatches Rosid I clade, including actinorhizal plants, Parasponia and legumes [1]. RNS has been extensively studied using legume–rhizobia symbiosis as a model, and generally requires specific signaling between both organisms, with excretion of flavonoids in the rhizosphere by the plant and production of specific lipochitooligosaccharides (LCOs 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 leads to the formation of the nodule organ (generally on the root), which hosts the symbiotic bacteria and in which nitrogen reduction takes place. Actinorhizal nodules present a single central vascular bundle that makes them resemble 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 symbioses and mycorrhizal fungi are able to produce Nod factor-like (LCO) molecules. This is the mechanism that allowed AM symbiotic genes — and more precisely LCO receptors — to be used for the RNS in legumes, which is addressed in this issue of Current Biology 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], which are probably perceived by different LysM-RLKs. This suggests that nodule-forming plants have recruited only part of the AM signaling pathway to develop RNS. In agreement with these genetic results, 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 specifically recognize 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 neofunctionalization of one of them for the RNS. Under 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 be expressed 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 nitrogenfixing bacteria (RNS). The key experiments of this study are described below. The authors found that tomato and petunia SlLYK10 and PhLYK10 genes are unique LYRIA genes (homologous to NFP), and the corresponding sllyk10 and phlyk10 mutants are required for AM symbiosis establishment. Furthermore, membrane fractions containing the Solanaceae LYRIA receptors bind specific LCOs with high affinity (Kd in the range of 20 nM) compared with COs (Kd higher than 1 mM), which demonstrates that the Solanaceae receptors are genuine LCO receptors with an 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 upregulated 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 result 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 nonnodule-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 the proposal of 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.
Current Biology 29, R1301–R1325, December 16, 2019 R1313
Current Biology
Dispatches In addition, these results raise two hypotheses for the biological role of these proteins. First, because they participate in 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 Solanaceae proteins are specifically recognizing the general LCO structure, but not the CO molecules, as shown in this work. However, they probably do not participate in the specific recognition of the LCO decoration, which is 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 1. Soltis, D.E., Soltis, P.S., Morgan, D.R., Swensen, S.M., Mullin, B.C., Dowd, J.M., and 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., and Cartieaux, F. (2015). Nod factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic toolkit. Plant Physiol. 169, 2654–2664. 4. Franche, C., Laplaze, L., Duhoux, E., and Bogusz, D. (1998). Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies. Crit. Rev. Plant Sci. 17, 1–28. 5. Froussart, E., Bonneau, J., Franche, C., and Bogusz, D. (2016). 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, , T., et al. (2019). LCO V., Auriac, M.-C., Vernie receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Curr. Biol. 29, 4249–4259. , O., Puech8. Maillet, F., Poinsot, V., Andre Page`s, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63. 9. Genre, A., Chabaud, M., Balzergue, C., PuechPages, V., Novero, M., Rey, T., Fournier, J., card, G., Bonfante, P., et al. Rochange, S., Be (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., and 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., and Kiers, E.T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat. 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., Fu¨chtbauer, 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., et al. (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., et al. (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.
Neuroscience: Reevaluating the Role of Orbitofrontal Cortex Brianna J. Sleezer1 and Benjamin Yost Hayden2,* 1Department
of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA of Neuroscience, Center for Magnetic Resonance Research, Center for Neuroengineering, University of Minnesota, Minneapolis, MN 55455, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.10.063 2Department
A new optogenetic lesion study shows that the orbitofrontal cortex is essential for integrating information about recent rewards — which may either increase or decrease demand for more — with learned preferences to drive behavior. To behave effectively, humans and other foragers must constantly incorporate new information about the external world and
their internal desires with previously learned information about values, tradeoffs, and structures in the world [1].
R1314 Current Biology 29, R1301–R1325, December 16, 2019 ª 2019 Elsevier Ltd.
For example, one may normally enjoy eating a turkey sandwich for lunch, but after eating turkey leftovers at every meal
Dispatches recent study in Current Biology found that ambient temperature increases, which we often seek when going to bed, activate preoptic neurons through a multisynaptic excitatory pathway [20]. The pernicious association between lack of sleep and obesity is another one for which subgroups of LHGABA neurons may be ultimately held responsible. Other environmental conditions or bodily states that affect sleep/wake, however, may come as a surprise. We must stay tuned for rapid further developments. REFERENCES 1. Von Economo, C. (1930). Sleep as a problem of localization. J. Nerv. Ment. Dis. 71, 249–259. 2. Nauta, W.J.H. (1946). Hypothalamic regulation of sleep in rats. An experimental study. J. Neurophysiol. 9, 285–316. 3. Liu, D., and Dan, Y. (2019). A motor theory of sleep-wake control: arousal-action circuit. Annu. Rev. Neurosci. 42, 27–46. 4. Luppi, P.H., and Fort, P. (2019). Neuroanatomical and neurochemical bases of vigilance states. Handb. Exp. Pharmacol. 253, 35–58. 5. Venner, A., De Luca, R., Sohn, L.T., Bandaru, S.S., Verstegen, A.M.J., Arrigoni, E., and Fuller, P.M. (2019). An inhibitory lateral hypothalamic-preoptic circuit mediates rapid arousals from sleep. Curr. Biol. 29, 4155–4168.
6. Saper, C.B., and Lowell, B.B. (2014). The hypothalamus. Curr. Biol. 24, R1111–R1116. 7. Arrigoni, E., Chee, M.J.S., and Fuller, P.M. (2019). To eat or to sleep: that is a lateral hypothalamic question. Neuropharmacology 154, 34–49. 8. Mahoney, C.E., Cogswell, A., Koralnik, I.J., and Scammell, T.E. (2019). The neurobiological basis of narcolepsy. Nat. Rev. Neurosci. 20, 83–93. 9. Saper, C.B., Fuller, P.M., Pedersen, N.P., Lu, J., and Scammell, T.E. (2010). Sleep state switching. Neuron 68, 1023–1042. 10. Burdakov, D., Karnani, M.M., and Gonzalez, A. (2013). Lateral hypothalamus as a sensorregulator in respiratory and metabolic control. Physiol. Behav. 121, 117–124. 11. Herrera, C.G., Ponomarenko, A., Korotkova, T., Burdakov, D., and Adamantidis, A. (2017). Sleep and metabolism: the multitasking ability of lateral hypothalamic inhibitory circuitries. Front. Neuroendocrinol. 44, 27–34. 12. Venner, A., Anaclet, C., Broadhurst, R.Y., Saper, C.B., and Fuller, P.M. (2016). A novel population of wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Curr. Biol. 26, 2137–2143. 13. Herrera, C.G., Cadavieco, M.C., Jego, S., Ponomarenko, A., Korotkova, T., and Adamantidis, A. (2016). Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat. Neurosci. 19, 290–298. 14. Szymusiak, R., and McGinty, D. (2008). Hypothalamic regulation of sleep and arousal. Ann. N.Y. Acad. Sci. 1129, 275–286.
15. Zhang, Z., Ferretti, V., Guntan, I., Moro, A., Steinberg, E.A., Ye, Z., Zecharia, A.Y., Yu, X., Vyssotski, A.L., Brickley, S.G., et al. (2015). Neuronal ensembles sufficient for recovery sleep and the sedative actions of a2 adrenergic agonists. Nat. Neurosci. 18, 553–561. 16. Chung, S., Weber, F., Zhong, P., Tan, C.L., Nguyen, T.N., Beier, K.T., Hormann, N., Chang, W.C., Zhang, Z., Do, J.P., et al. (2017). Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545, 477–481. 17. Kroeger, D., Absi, G., Gagliardi, C., Bandaru, S.S., Madara, J.C., Ferrari, L.L., Arrigoni, E., Mu¨nzberg, H., Scammell, T.E., Saper, C.B., and Vetrivelan, R. (2018). Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nat. Commun. 9, 4129. 18. Ma, Y., Miracca, G., Yu, X., Harding, E.C., Miao, A., Yustos, R., Vyssotski, A.L., Franks, N.P., and Wisden, W. (2019). Galanin neurons unite sleep homeostasis and a2-adrenergic sedation. Curr. Biol. 29, 3315–3322.e3. 19. Carter, M.E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., and de Lecea, L. (2010). Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526– 1533. 20. Harding, E.C., Yu, X., Miao, A., Andrews, N., Ma, Y., Ye, Z., Lignos, L., Miracca, G., Ba, W., Yustos, R., et al. (2018). A neuronal hub binding sleep initiation and body cooling in response to a warm external stimulus. Curr. Biol. 28, 2263–2273.e4.
Symbiosis Signaling: Solanaceae Symbiotic LCO Receptors Are Functional for Rhizobium Perception in Legumes Pascal Ratet1,2
Paris-Sud, Universite Evry, Universite Paris-Saclay, Baˆtiment 630, of Plant Sciences Paris-Saclay IPS2, CNRS, INRA, Universite 91405 Orsay, France 2Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cite , Baˆtiment 630, 91405 Orsay, France Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.10.046 1Institute
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 evolutionarily more recent and more specific symbiosis with their bacterial rhizobium partners. Some plants are able to grow in nitrogenpoor soils because they can establish symbiosis with rhizobia or frankia
(actinobacteria) bacteria, which are able to reduce the non-limiting atmospheric gaseous nitrogen (N2) to NH3 to the
R1312 Current Biology 29, R1301–R1325, December 16, 2019 ª 2019 Elsevier Ltd.
benefit of their host. The capacity to establish this symbiosis, also called root nodule symbiosis (RNS), is confined to the
Current Biology
Dispatches Rosid I clade, including actinorhizal plants, Parasponia and legumes [1]. RNS has been extensively studied using legume–rhizobia symbiosis as a model, and generally requires specific signaling between both organisms, with excretion of flavonoids in the rhizosphere by the plant and production of specific lipochitooligosaccharides (LCOs 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 leads to the formation of the nodule organ (generally on the root), which hosts the symbiotic bacteria and in which nitrogen reduction takes place. Actinorhizal nodules present a single central vascular bundle that makes them resemble 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 symbioses and mycorrhizal fungi are able to produce Nod factor-like (LCO) molecules. This is the mechanism that allowed AM symbiotic genes — and more precisely LCO receptors — to be used for the RNS in legumes, which is addressed in this issue of Current Biology 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], which are probably perceived by different LysM-RLKs. This suggests that nodule-forming plants have recruited only part of the AM signaling pathway to develop RNS. In agreement with these genetic results, 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 specifically recognize 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 neofunctionalization of one of them for the RNS. Under 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 be expressed 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 nitrogenfixing bacteria (RNS). The key experiments of this study are described below. The authors found that tomato and petunia SlLYK10 and PhLYK10 genes are unique LYRIA genes (homologous to NFP), and the corresponding sllyk10 and phlyk10 mutants are required for AM symbiosis establishment. Furthermore, membrane fractions containing the Solanaceae LYRIA receptors bind specific LCOs with high affinity (Kd in the range of 20 nM) compared with COs (Kd higher than 1 mM), which demonstrates that the Solanaceae receptors are genuine LCO receptors with an 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 upregulated 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 result 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 nonnodule-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 the proposal of 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.
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Current Biology
Dispatches In addition, these results raise two hypotheses for the biological role of these proteins. First, because they participate in 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 Solanaceae proteins are specifically recognizing the general LCO structure, but not the CO molecules, as shown in this work. However, they probably do not participate in the specific recognition of the LCO decoration, which is 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 1. Soltis, D.E., Soltis, P.S., Morgan, D.R., Swensen, S.M., Mullin, B.C., Dowd, J.M., and 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., and Cartieaux, F. (2015). Nod factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic toolkit. Plant Physiol. 169, 2654–2664. 4. Franche, C., Laplaze, L., Duhoux, E., and Bogusz, D. (1998). Actinorhizal symbioses: recent advances in plant molecular and genetic transformation studies. Crit. Rev. Plant Sci. 17, 1–28. 5. Froussart, E., Bonneau, J., Franche, C., and Bogusz, D. (2016). 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, , T., et al. (2019). LCO V., Auriac, M.-C., Vernie receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Curr. Biol. 29, 4249–4259. , O., Puech8. Maillet, F., Poinsot, V., Andre Page`s, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63. 9. Genre, A., Chabaud, M., Balzergue, C., PuechPages, V., Novero, M., Rey, T., Fournier, J., card, G., Bonfante, P., et al. Rochange, S., Be (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., and 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., and Kiers, E.T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat. 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., Fu¨chtbauer, 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., et al. (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., et al. (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.
Neuroscience: Reevaluating the Role of Orbitofrontal Cortex Brianna J. Sleezer1 and Benjamin Yost Hayden2,* 1Department
of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA of Neuroscience, Center for Magnetic Resonance Research, Center for Neuroengineering, University of Minnesota, Minneapolis, MN 55455, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.10.063 2Department
A new optogenetic lesion study shows that the orbitofrontal cortex is essential for integrating information about recent rewards — which may either increase or decrease demand for more — with learned preferences to drive behavior. To behave effectively, humans and other foragers must constantly incorporate new information about the external world and
their internal desires with previously learned information about values, tradeoffs, and structures in the world [1].
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For example, one may normally enjoy eating a turkey sandwich for lunch, but after eating turkey leftovers at every meal