eISSN: 2221-6197 DOI: 10.31301/2221-6197

Symbiotic genes of legumes detected by transcriptomic analysis

Year: 2022

Pages: 285-294

Number: Volume 14, issue 3

Type: scientific article

Summary:

Legumes form symbioses with nodule bacteria (NB) and arbuscular mycorrhiza fungi(AM). The formation of symbioses increases the resistance of plants to stress and contributes to obtaining a stable harvest even in conditions of global climate change. The study of the molecular basis of symbioses formed by legumes is necessary to increase the effectiveness of these symbioses when they are used in modern agriculture. Previously, individual regulatory genes (so-called Sym genes) controlling some stages of symbiosis development were studied for model legumes using mutation analysis. Currently, high throughput sequencing technologies allow us to study a complete set of genes encoding the "molecular symbiosis machine" and necessary for ensuring the metabolic integration of symbionts. Among them, there are genes encoding nodulins (from the “nodule”), proteins specific for legume-rhizobial symbiosis (LRS), and mycorrhizins specific for arbuscular-mycorrhizal (AM) symbiosis. The products of genes whose expression is induced during the development of both LRS and AMS are called symbiosins. The genes encoding symbiosins, nodulins and mycorrhizins have been studied on the model legumes Medicago truncatula Gaertn., Lotus japonicus (Regel.) K. Larsen and Glycine max (L.) Merr., while the symbiosis-specific genes of non-model legumes, as well as the features of their expression, have not been sufficiently studied to date. The use of transcriptomics approaches (i.e., the study of the entire set of expressed genes, the so-called transcriptome) makes it possible to fill this knowledge gap. In this paper, we have summarized the results of research of the expression of the above groups of genes in legumesin recent years.

Keywords:

legumes, root symbiosis, next-generation sequencing, gene expression, transcriptomics

References:

1. Alunni, B., Kevei, Z., Redondo-Nieto, M., Kondorosi, A., Mergaert, P., and Kondorosi, E. Genomic Organization and Evolutionary Insights on GRP and NCR Genes, Two Large Nodule-Specific Gene Families in Medicago truncatula. MPMI. 2007. V. 20. P. 1138–
1148. doi: 10.1094/MPMI-20-9-1138

2. Boscari, A., Del Giudice, J., Ferrarini, A., Venturini, L., Zaffini, A.-L., Delledonne, M., et al. Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol. 2013. V. 161. P. 425–439. doi: 10.1104/pp.112.208538

3. Deguchi, Y., Banba, M., Shimoda, Y., Chechetka, S. A., Suzuri, R., Okusako, Y., et al. Transcriptome Profiling of Lotus japonicus Roots During Arbuscular Mycorrhiza Development and Comparison with that of Nodulation. DNA Research. 2007. V. 14. P. 117–133. doi: 10.1093/dnares/dsm014

4. Gao, Y., Selee, B., Schnabel, E.L., Poehlman, W. L., Chavan, S.A., Frugoli, J.A., et al. Time Series Transcriptome Analysis in Medicago truncatula Shoot and Root Tissue During Early Nodulation. Front. Plant Sci. 2022. V. 13. P. 861639. doi: 10.3389/fpls.2022.861639

5. Gaude, N., Bortfeld, S., Duensing, N., Lohse, M., Krajinski, F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development: Arbuscule-containing and non-colonized cortical cells. The Plant Journal. 2012. V. 69. P. 510– 528. doi: 10.1111/j.1365-313X.2011.04810.x

6. Guefrachi, I., Nagymihaly, M., Pislariu, C.I., Van de Velde, W., Ratet, P., Mars, M., et al. Extreme specificity of NCR gene expression in Medicago truncatula. BMC Genomics. 2014. V. 15. P. 712. doi: 10.1186/1471-2164-15-712

7. Handa, Y., Nishide, H., Takeda, N., Suzuki, Y., Kawaguchi, M., Saito, K. RNA-seq Transcriptional Profiling of an Arbuscular Mycorrhiza Provides Insights into Regulated and Coordinated Gene Expression in Lotus japonicus and Rhizophagus irregularis. Plant Cell Physiol. 2015. V. 56. P. 1490–1511. doi: 10.1093/pcp/pcv071

8. Høgslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M. A., Goffard, N., et al. Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS One. 2009. V. 4. e6556. doi: 10.1371/journal.pone.0006556

9. Ho-Plágaro, T., García-Garrido, J.M. Molecular Regulation of Arbuscular Mycorrhizal Symbiosis. Int J Mol Sci. 2022. V. 23. P. 5960. doi: 10.3390/ijms23115960

10. Hwang, B., Lee, J.H., Bang, D. Single-cell RNA sequencing technologies and bioinformatics pipelines. Exp Mol Med. 2018. V. 50. P. 1–14. doi: 10.1038/s12276-018-0071-8

11. Jardinaud, M.-F., Boivin, S., Rodde, N., Catrice, O., Kisiala, A., Lepage, A., et al. A Laser DissectionRNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis. Plant Physiol. 2016. V. 171. P. 2256–2276. doi: 10.1104/pp.16.00711

12. Kouchi, H., Hata, S. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Molec. Gen. Genet. 1993. V. 238. P. 106–119. doi: 10.1007/BF00279537

13. Krajinski, F., Frenzel, A. Towards the elucidation of AM-specific transcription in Medicago truncatula. Phytochemistry. 2007. V. 68. P. 75–81. doi: 10.1016/j.phytochem.2006.09.035 

14. Küster, H., Vieweg, M.F., Manthey, K., Baier, M.C., Hohnjec, N., and Perlick, A.M. Identification and expression regulation of symbiotically activated legume genes. Phytochemistry. 2007. V. 68. P. 8–18. doi: 10.1016/j.phytochem.2006.09.029

15. Laporte, P., Satiat-Jeunemaître, B., Velasco, I., Csorba, T., Van de Velde, W., Campalans, A., et al. A novel RNA-binding peptide regulates the establishment of the Medicago truncatula – Sinorhizobium meliloti nitrogen-fixing symbiosis: Small RNA-binding proteins in nodulation. The Plant Journal. 2010. V. 62. P. 24–38. doi: 10.1111/j.1365-313X.2009.04121.x

16. Legocki, R.P., and Verma, D.P.S. Identification of “nodule-specific” host proteins (nodulins) involved in the development of Rhizobium-Legume symbiosis. Cell. 1980. V. 20. P. 153–163. doi: 10.1016/0092-8674(80)90243-3

17. Libault, M. Transcriptional Reprogramming of Legume Genomes: Perspective and Challenges Associated With Single-Cell and Single Cell-Type Approaches During Nodule Development. Front. Plant Sci. 2018. V. 9. P. 1600. doi: 10.3389/fpls.2018.01600

18. Liu, J., Miller, S. S., Graham, M., Bucciarelli, B., Catalano, C. M., Sherrier, D. J., et al. Recruitment of Novel Calcium-Binding Proteins for Root Nodule Symbiosis in Medicago truncatula. Plant Physiology. 2006. V. 141. P. 167–177. doi: 10.1104/pp.106.076711

19. Manthey, K., Krajinski, F., Hohnjec, N., Firnhaber, C., Pühler, A., Perlick, A. M., et al. Transcriptome Profiling in Root Nodules and Arbuscular Mycorrhiza Identifies a Collection of Novel Genes Induced During Medicago truncatula Root Endosymbioses. MPMI. 2004. V. 17. P. 1063–1077. doi: 10.1094/MPMI.2004.17.10.1063

20. Mergaert, P., Kereszt, A., Kondorosi, E. Gene Expression in Nitrogen-Fixing Symbiotic Nodule Cells in Medicago truncatula and Other Nodulating Plants. Plant Cell. 2020. V. 32. P. 42–68. doi: 10.1105/tpc.19.00494

21. Mergaert, P., Nikovics, K., Kelemen, Z., Maunoury, N., Vaubert, D., Kondorosi, A., et al. A Novel Family in Medicago truncatula Consisting of More Than 300 Nodule-Specific Genes Coding for Small, Secreted Polypeptides with Conserved Cysteine Motifs. Plant Physiology. 2003. V. 132. P. 161–173. doi: 10.1104/pp.102.018192

22. Montiel, J., Downie, J.A., Farkas, A., Bihari, P., Herczeg, R., Bálint, B., et al. Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides. Proc Natl Acad Sci USA. 2017. V. 114. P. 5041–5046. doi: 10.1073/pnas.1704217114

23. Mortier, V., Den Herder, G., Whitford, R., Van de Velde, W., Rombauts, S., D’haeseleer, K., et al. CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically. Plant Physiology. 2010. V. 153. P. 222–237. doi: 10.1104/pp.110.153718

24. Nanjareddy, K., Arthikala, M.-K., Gómez, B.-M., Blanco, L., Lara, M. Differentially expressed genes in mycorrhized and nodulated roots of common bean are associated with defense, cell wall architecture, N metabolism, and P metabolism. PLoS One. 2017. V. 12.P. e0182328. doi: 10.1371/journal.pone.0182328

25. Nap, J.-P., Bisseling, T. Developmental Biology of a Plant-Prokaryote Symbiosis: The Legume Root Nodule. Science. 1990a. V. 250. P. 948–954. doi: 10.1126/science.250.4983.948

26. Nap, J.-P., Bisseling, T. The roots of nodulins. Physiol Plant. 1990b . V. 79. P. 407–414. doi: 10.1111/j.1399-3054.1990.tb06760.x 27. Okamoto, S., Ohnishi, E., Sato, S., Takahashi, H., Nakazono, M., Tabata, S., et al. Nod Factor/NitrateInduced CLE Genes that Drive HAR1-Mediated Systemic Regulation of Nodulation. Plant and Cell Physiology. 2009. V. 50. P. 67–77. doi: 10.1093/pcp/pcn194

28. Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol. 2008. V. 6. P. 763–775. doi: 10.1038/nrmicro1987

29. Sakamoto, K., Ogiwara, N., Kaji, T., Sugimoto, Y., Ueno, M., Sonoda, M., et al. Transcriptome analysis of soybean (Glycine max) root genes differentially expressed in rhizobial, arbuscular mycorrhizal, and dual symbiosis. J Plant Res. 2019. V. 132. P. 541–568. doi: 10.1007/s10265-019-01117-7

30. Sańko-Sawczenko, I., Łotocka, B., Mielecki, J., Rekosz-Burlaga, H., and Czarnocka, W. Transcriptomic Changes in Medicago truncatula and Lotus japonicus Root Nodules during Drought Stress. Int J Mol Sci. 2019. V. 20. P. E1204. doi: 10.3390/ijms20051204

31. Sprent, J. I. Nodulation in legumes. Annals of Botany. 2002. V. 89(6). P. 797-798. doi: 10.1093/aob/mcf128

32. Tikhonovich, I.A., Provorov, N.A. Simbiogenetics of microbe-plant interactions. Ecological Genetics. V. 1. P. 36–46. doi: 10.17816/ecogen1036-46

33. Tominaga, T., Miura, C., Sumigawa, Y., Hirose, Y., Yamaguchi, K., Shigenobu, S., et al. Conservation and Diversity in Gibberellin-Mediated Transcriptional Responses Among Host Plants Forming Distinct Arbuscular Mycorrhizal Morphotypes. Front Plant Sci. 2021. V. 12. P. 795695. doi: 10.3389/fpls.2021.795695

34. Tromas, A., Parizot, B., Diagne, N., Champion, A., Hocher, V., Cissoko, M., et al. Heart of Endosymbioses: Transcriptomics Reveals a Conserved Genetic Program among Arbuscular Mycorrhizal, Actinorhizal and Legume-Rhizobial Symbioses. PLoS ONE. 2012. V. 7.P. e44742. doi: 10.1371/journal.pone.0044742

35. Verma, D.P.S., Fortin, M.G., Stanley, J., Mauro, V.P., Purohit, S., Morrison, N. Nodulins and nodulin genes of Glycine max. Plant Mol Biol. 1986. V. 7. P. 51–61. doi: 10.1007/BF00020131

36. Wang, L., Zhou, Y., Li, R., Liang, J., Tian, T., Ji, J., et al. Single cell‐type transcriptome profiling reveals genes that promote nitrogen fixation in the infected and uninfected cells of legume nodules. Plant Biotechnology Journal. 2022. V. 20. P. 616–618. doi:
10.1111/pbi.13778

37. Wyss, P., Mellor, Robert B., Wiemken, A. Vesicular-arbuscular mycorrhizas of wild-type soybean and non-nodulating mutants with Glomus mosseae contain symbiosis-specific polypeptides (mycorrhizins), immunologically cross-reactive with nodulins. Planta. 1990. V. 182. doi: 10.1007/BF00239978

38. Yokota, K., Hayashi, M. Function and evolution of nodulation genes in legumes. Cell. Mol. Life Sci. 2011. V. 68. P. 1341–1351. doi: 10.1007/s00018-011-0651-4

39. Zorin, E.A., Kliukova, M.S., Afonin, A.M., Gribchenko, E.S., Gordon, M.L., Sulima, A.S., et al. A variable gene family encoding nodule-specific cysteinerich peptides in pea (Pisum sativum L.). Front. Plant Sci. 2022. V. 13. P. 884726. doi: 10.3389/fpls.2022.884726

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eISSN: 2221-6197 DOI: 10.31301/2221-6197