THE NIN-LIKE PROTEIN (NLP) FAMILY IN COMMON BEAN: GENOME-WIDE IDENTIFICATION, EVOLUTION AND EXPRESSION ANALYSIS

Year 2021, , 58 - 84, 30.06.2021

İlker Büyük , Aybüke Okay , Taner Aksoy , Sumer Aras

https://doi.org/10.53447/communc.869501

Cited By: 2

Abstract

One of the plant-specific transcription factor families that play an important role in responses to nitrogen deficiency is NODULE INCEPTION-like (NIN-like) proteins (NLPs). However, the properties and evolutionary relationships of NIN genes in P. vulgaris, which enable nodule formation naturally, have not been studied yet. 12 Pvul-NIN genes have been identified in this study and the approximate positions of these genes have been determined. At the same time, several biochemical and physicochemical properties of NIN-like proteins have been elucidated. Comparisons between both monocot and dicot, but also nodule binding and non-nodule binding species were considered when investigating the evolutionary relationships of NIN genes. 16 duplication events (14 segmental and 2 tandem) have been shown to play a role in the expansion of the NIN gene family in P. vulgaris. In addition, comparative expression analysis of NIN genes was performed by processing publicly available RNAseq data and different levels of Pvul-NIN gene expression under both salt and drought stress were detected, suggesting the roles of Pvul-NIN gene for abiotic stress response. Expression levels of NIN genes have also been investigated in different plant tissues and have been shown to be intensely expressed in nodules and root tissues. This is the first study on the in-silico detection and characterization of Pvul-NIN genes to examine gene expression levels in common bean. The results could therefore provide the basis for future studies of functional characterization of Pvul-NIN genes.

Keywords

NIN-like proteins (NLPs), in-silico analysis, bioinformatics, bean, RNAseq

References

• Mu, X., Chen, Q., Chen, F., Yuan, L. and Mi, G. Within-leaf nitrogen allocation in adaptation to low nitrogen supply in maize during grain-filling stage. Frontiers in plant science, 7 (2016), 699.
• Mu, X., Chen, Q., Chen, F., Yuan, L. and Mi, G. A RNA-seq analysis of the response of photosynthetic system to low nitrogen supply in maize leaf. International journal of molecular sciences, 18(12) (2017), 2624.
• Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L. and Suzuki, A. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of botany, 105(7) (2010), 1141-1157.
• Tegeder, M. and Masclaux‐Daubresse, C. Source and sink mechanisms of nitrogen transport and use. New Phytologist, 217(1) (2018), 35-53.
• Schroeder, J. I., Delhaize, E., Frommer, W. B., Guerinot, M. L., Harrison, M. J., Herrera-Estrella, L., Horie, T., Kochian, L. V., Munns, R. and Nishizawa, N. K. Using membrane transporters to improve crops for sustainable food production. Nature, 497(7447) (2013), 60-66.
• Mu, X. and Luo, J. Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling. Cellular and Molecular Life Sciences (2019), 1-12.
• Undurraga, S. F., Ibarra-Henríquez, C., Fredes, I., Álvarez, J. M. and Gutiérrez, R. A. Nitrate signaling and early responses in Arabidopsis roots. Journal of Experimental Botany, 68(10) (2017), 2541-2551.
• Luo, J., Zhou, J.-J., Masclaux-Daubresse, C., Wang, N., Wang, H. and Zheng, B. Morphological and physiological responses to contrasting nitrogen regimes in Populus cathayana is linked to resources allocation and carbon/nitrogen partition. Environmental and Experimental Botany, 162 (2019), 247-255.
• Mueller, N. D., West, P. C., Gerber, J. S., MacDonald, G. K., Polasky, S. and Foley, J. A. A tradeoff frontier for global nitrogen use and cereal production. Environmental Research Letters, 9(5) (2014), 054002.
• Wan, T., Xue, H. and TONG, Y.-p. Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops. Journal of integrative agriculture, 16(12) (2017), 2657-2673.
• Chen, Q., Soulay, F., Saudemont, B., Elmayan, T., Marmagne, A. and Masclaux-Daubresse, C. Overexpression of ATG8 in Arabidopsis stimulates autophagic activity and increases nitrogen remobilization efficiency and grain filling. Plant and Cell Physiology, 60(2) (2019), 343-352.
• Mandal, V. K., Sharma, N. and Raghuram, N. Molecular targets for improvement of crop nitrogen use efficiency: current and emerging options. Springer, City, 2018.
• Mu, X., Chen, F., Wu, Q., Chen, Q., Wang, J., Yuan, L. and Mi, G. Genetic improvement of root growth increases maize yield via enhanced post-silking nitrogen uptake. European Journal of Agronomy, 63 (2015), 55-61.
• Luo, J. and Zhou, J.-J. Growth performance, photosynthesis, and root characteristics are associated with nitrogen use efficiency in six poplar species. Environmental and Experimental Botany, 164 (2019), 40-51.
• Wang, Y.-Y., Cheng, Y.-H., Chen, K.-E. and Tsay, Y.-F. Nitrate transport, signaling, and use efficiency. Annual Review of Plant Biology, 69 (2018), 85-122.
• Oldroyd, G. E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology, 11(4) (2013), 252-263.
• Good, A. Toward nitrogen-fixing plants. Science, 359(6378) (2018), 869-870.
• Naulin, P. A., Armijo, G. I., Vega, A. S., Tamayo, K. P., Gras, D. E., de la Cruz, J. and Gutiérrez, R. A. Nitrate Induction of Primary Root Growth Requires Cytokinin Signaling in Arabidopsis thaliana. Plant and Cell Physiology, 61, 2 (2020), 342-352.
• Armijo, G. and Gutiérrez, R. A. Emerging players in the nitrate signaling pathway. Molecular Plant, 10(8) (2017), 1019-1022.
• Zhao, L., Zhang, W., Yang, Y., Li, Z., Li, N., Qi, S., Crawford, N. M. and Wang, Y. The Arabidopsis NLP7 gene regulates nitrate signaling via NRT1. 1–dependent pathway in the presence of ammonium. Scientific reports, 8(1) (2018), 1-13.
• Camargo, A., Llamas, Á., Schnell, R. A., Higuera, J. J., González-Ballester, D., Lefebvre, P. A., Fernández, E. and Galván, A. Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. The Plant Cell, 19(11) (2007), 3491-3503.
• Chardin, C., Girin, T., Roudier, F., Meyer, C. and Krapp, A. The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. Journal of experimental botany, 65(19) (2014), 5577-5587.
• Sharrocks, A. D. The ETS-domain transcription factor family. Nature reviews Molecular cell biology, 2(11) (2001), 827-837.
• Schwechheimer, C., Zourelidou, M. and Bevan, M. Plant transcription factor studies. Annual review of plant biology, 49(1) (1998), 127-150.
• Schauser, L., Wieloch, W. and Stougaard, J. Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. Journal of molecular evolution, 60(2) (2005), 229-237.
• Tedeschi, F., Rizzo, P., Rutten, T., Altschmied, L. and Bäumlein, H. RWP‐RK domain‐containing transcription factors control cell differentiation during female gametophyte development in Arabidopsis. New Phytologist, 213(4) (2017), 1909-1924.
• Konishi, M. and Yanagisawa, S. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nature communications, 4(1) (2013), 1-9.
• Schauser, L., Roussis, A., Stiller, J. and Stougaard, J. A plant regulator controlling development of symbiotic root nodules. Nature, 402(6758) (1999), 191-195.
• Streeter, J. G. Effect of nitrate in the rooting medium on carbohydrate composition of soybean nodules. Plant physiology, 68(4) (1981), 840-844.
• Carroll, B. J., McNeil, D. L. and Gresshoff, P. M. Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proceedings of the National Academy of Sciences, 82(12) (1985), 4162-4166.
• Laeremans, T. and Vanderleyden, J. Infection and nodulation signalling in Rhizobium-Phaseolus vulgaris symbiosis. World Journal of Microbiology and Biotechnology, 14(6) (1998), 787-808.
• Ruschel, A., Salati, E. and Vose, P. Nitrogen enrichment of soil and plant byRhizobium phaseoli-Phaseolus vulgaris symbiosis. Plant and Soil, 51(3) (1979), 425-429.
• Hungria, M., Campo, R. J. and Mendes, I. C. Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils, 39(2) (2003), 88-93.
• Albareda, M., Rodríguez-Navarro, D. N. and Temprano, F. J. Soybean inoculation: Dose, N fertilizer supplementation and rhizobia persistence in soil. Field crops research, 113(3) (2009), 352-356.
• O'hara, G. and Daniel, R. M. Rhizobial denitrification: a review. Soil Biology and Biochemistry, 17(1) (1985), 1-9.
• Zhang, N. N., Sun, Y. M., Wang, E. T., Yang, J. S., Yuan, H. L. and Scow, K. M. Effects of intercropping and Rhizobial inoculation on the ammonia-oxidizing microorganisms in rhizospheres of maize and faba bean plants. Applied Soil Ecology, 85 (2015), 76-85.
• Horiuchi, J.-i., Prithiviraj, B., Bais, H. P., Kimball, B. A. and Vivanco, J. M. Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta, 222(5) (2005), 848-857.
• Anjum, M. S., Ahmed, Z. I. and Rauf, C. A. Effect of Rhizobium inoculation and nitrogen fertilizer on yield and yield components of mungbean. International Journal of Agriculture and Biology (Pakistan) (2006).
• Chabot, R., Antoun, H. and Cescas, M. P. Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar. phaseoli. Plant and soil, 184(2) (1996), 311-321.
• Yanni, Y. G., Rizk, R., Corich, V., Squartini, A., Ninke, K., Philip-Hollingsworth, S., Orgambide, G., De Bruijn, F., Stoltzfus, J. and Buckley, D. Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Springer, City, 1997.
• Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A.-E., Barloy-Hubler, F., Galibert, F. and Kondorosi, A. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium–legume symbiosis. Proceedings of the National Academy of Sciences, 103(13) (2006), 5230-5235.
• Forrester, N. J. and Ashman, T.-L. The direct effects of plant polyploidy on the legume–rhizobia mutualism. Annals of botany, 121(2) (2018), 209-220.
• Maróti, G. and Kondorosi, É. Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? Frontiers in Microbiology, 5 (2014), 326.
• Leboulleux, S., Borget, I., Labro, S., Bidault, S., Vielh, P., Hartl, D., Dauchy, S., Chougnet, C. N., Girard, E. and Azoulay, S. Frequency and intensity of pain related to thyroid nodule fine-needle aspiration cytology. Thyroid, 23(9) (2013), 1113-1118.
• Abaidoo, R. C., George, T., Bohlool, B. B. and Singleton, P. W. Influence of elevation and applied nitrogen on rhizosphere colonization and competition for nodule occupancy by different rhizobial strains on field-grown soybean and common bean. Canadian journal of microbiology, 36(2) (1990), 92-96.
• Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U. and Putnam, N. Phytozome: a comparative platform for green plant genomics. Nucleic acids research, 40, D1 (2012), D1178-D1186.
• Guo, A.-Y., Zhu, Q.-H., Chen, X. and Luo, J.-C. GSDS: a gene structure display server. Yi chuan= Hereditas, 29(8) (2007), 1023-1026.
• Voorrips, R. MapChart: software for the graphical presentation of linkage maps and QTLs. Journal of heredity, 93(1) (2002), 77-78.
• Bailey, T. L., Williams, N., Misleh, C. and Li, W. W. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic acids research, 34(suppl_2) (2006), W369-W373.
• Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular biology and evolution, 28(10) (2011), 2731-2739.
• Letunic, I. and Bork, P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic acids research, 3(suppl_2) (2011), W475-W478.
• Zhang, Y. miRU: an automated plant miRNA target prediction server. Nucleic acids research, 33(suppl_2) (2005), W701-W704.
• Suyama, M., Torrents, D. and Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic acids research, 34(suppl_2) (2006), W609-W612.
• Yang, Z. and Nielsen, R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular biology and evolution, 17(1) (2000), 32-43.
• Hiz, M. C., Canher, B., Niron, H. and Turet, M. Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PloS one, 9(3) (2014).
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N. and Bourne, P. E. The protein data bank. Nucleic acids research, 28(1) (2000), 235-242.
• Kelley, L. A. and Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nature protocols, 4(3) (2009), 363.
• Liu, M., Chang, W., Fan, Y., Sun, W., Qu, C., Zhang, K., Liu, L., Xu, X., Tang, Z. and Li, J. Genome-wide identification and characterization of nodule-inception-like protein (nlp) family genes in Brassica napus. International journal of molecular sciences, 19(8) (2018), 2270.
• Ohno, S. Evolution by gene duplication. Springer Science & Business Media, 2013.
• Lynch, M. Gene duplication and evolution. Science, 297(5583) (2002), 945-947.
• Ruse, M. The Cambridge encyclopedia of Darwin and evolutionary thought (2013).
• Cao, B. P. Genome-wide analysis of NIN-like protein (NLP) family in maize (Zea mays L.) by using bioinformatic methods. Science and Technology Development Journal-Natural Sciences, 1(T2) (2017), 39-47.
• Wu, Z., Liu, H., Huang, W., Yi, L., Qin, E., Yang, T., Wang, J. and Qin, R. Genome-Wide Identification, Characterization, and Regulation of RWP-RK Gene Family in the Nitrogen-Fixing Clade. Plants, 9(9) (2020), 1178.
• Mangan, S. and Alon, U. Structure and function of the feed-forward loop network motif. Proceedings of the National Academy of Sciences, 100, 21 (2003), 11980-11985.
• Cassan, M. and Rousset, J.-P. UAG readthrough in mammalian cells: effect of upstream and downstream stop codon contexts reveal different signals. BMC molecular biology, 2(1) (2001), 3.
• Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J. and Schwede, T. Protein structure homology modeling using SWISS-MODEL workspace. Nature protocols, 4(1) (2009), 1.
• Schwede, T., Kopp, J., Guex, N. and Peitsch, M. C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic acids research, 31(13) (2003), 3381-3385.
• Arnold, F. H. and Haymore, B. L. Engineered metal-binding proteins: purification to protein folding. Science, 252(5014) (1991), 1796-1798.
• Wittkopp, P. J. and Kalay, G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nature Reviews Genetics, 13(1) (2012), 59-69.
• Schiavon, M., Ertani, A. and Nardi, S. Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of the tricarboxylic acid (TCA) cycle and nitrogen metabolism in Zea mays L. Journal of Agricultural and Food Chemistry, 56(24) (2008), 11800-11808.
• Xie, Z., Nolan, T. M., Jiang, H. and Yin, Y. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Frontiers in plant science, 10 (2019), 228.
• Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D. and Shinozaki, K. Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. The Plant Cell, 9(10) (1997), 1859-1868.
• Hausser, J., Syed, A. P., Bilen, B. and Zavolan, M. Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome research, 23, 4 (2013), 604-615.
• Holt, D. B., Gupta, V., Meyer, D., Abel, N. B., Andersen, S. U., Stougaard, J. and Markmann, K. micro RNA 172 (miR172) signals epidermal infection and is expressed in cells primed for bacterial invasion in Lotus japonicus roots and nodules. New Phytologist, 208(1) (2015), 241-256.
• Yao, X., Chen, J., Zhou, J., Yu, H., Ge, C., Zhang, M., Gao, X., Dai, X., Yang, Z.-N. and Zhao, Y. An essential role for miRNA167 in maternal control of embryonic and seed development. Plant physiology, 180(1) (2019), 453-464.
• Pegler, J. L., Oultram, J. M., Grof, C. P. and Eamens, A. L. Profiling the abiotic stress responsive microRNA landscape of Arabidopsis thaliana. Plants, 8(3) (2019), 58.
• Debernardi, J. M., Rodriguez, R. E., Mecchia, M. A. and Palatnik, J. F. Functional specialization of the plant miR396 regulatory network through distinct microRNA–target interactions. PLoS Genet, 8(1) (2012), e1002419.
• Wan, P., Wu, J., Zhou, Y., Xiao, J., Feng, J., Zhao, W., Xiang, S., Jiang, G. and Chen, J. Y. Computational analysis of drought stress-associated miRNAs and miRNA co-regulation network in Physcomitrella patens. Genomics, proteomics & bioinformatics, 9(1-2) (2011), 37-44.
• Grieco, G. E., Brusco, N., Licata, G., Nigi, L., Formichi, C., Dotta, F. and Sebastiani, G. Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes. International Journal of Molecular Sciences, 20(24) (2019), 6358.