Transcriptome analyses reveal candidate genes potentially involved in al stress response in alfalfa

Frontiers in Plant Science

Volumn 8, Issue FEBRUARY, 2017, Pages

  Liu, Wenxian ^a   Xiong, Conghui ^a   Yan, Longfeng ^a   Zhang, Zhengshe ^a   Ma, Lichao ^a   Wang, Yanrong ^a   Liu, Yajie ^a   Liu, Zhipeng ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Alfalfa; Aluminum stress; Differentially expressed genes; Internal detoxification mechanism; RNA Seq; Transcriptome

Indexed keywords

EID: 85011901242     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00026     Document Type: Article

References (68)

1. Anoop, V. M., Basu, U., McCammon, M. T., McAlister-Henn, L., and Taylor, G. J. (2003). Modulation of citrate metabolismalters aluminumtolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol. 132, 2205–2217. doi: 10.1104/pp.103.023903
2. Arenhart, R. A., Bai, Y., Valter de Oliveira, L. F., Bucker Neto, L., Schunemann, M., Maraschin Fdos, S., et al. (2014). Newinsights into aluminumtolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol. Plant 7, 709–721. doi: 10.1093/mp/sst160
3. Arenhart, R. A., Lima, J. C., Pedron, M., Carvalho, F. E., Silveira, J. A., Rosa, S. B., et al. (2013). Involvement of ASR genes in aluminiumtolerance mechanisms in rice. Plant Cell Environ. 36, 52–67. doi: 10.1111/j.1365-3040.2012.02553.x
4. Barone, P., Rosellini, D., Lafayette, P., Bouton, J., Veronesi, F., and Parrott, W. (2008). Bacterial citrate synthase expression and soil aluminum tolerance in transgenic alfalfa. Plant Cell Rep. 27, 893–901. doi: 10.1007/s00299-008-0517-x
5. Casati, P., and Walbot, V. (2003). Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol. 132, 1739–1754. doi: 10.1104/pp.103.022871
6. Chandran, D., Sharopova, N., Ivashuta, S., Gantt, J. S., VandenBosch, K. A., and Samac, D. A. (2008). Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta 228, 151–166. doi: 10.1007/s00425-008-0726-0
7. Chen, H. X., Lu, C. P., Jiang, H., and Peng, J. H. (2015). Global transcriptome analysis reveals distinct aluminum-tolerance pathways in the Al-accumulating species Hydrangea macrophylla and marker identification. PLoS ONE 10:e0144927. doi: 10.1371/journal.pone.0144927
8. Chen, L., Wang, T., Zhao, M., Tian, Q., and Zhang, W. H. (2012). Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235, 375–386. doi: 10.1007/s00425-011-1514-9
9. Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676. doi: 10.1093/bioinformatics/bti610
10. de la Fuente, J. M., Ramírez-Rodríguez, V., Cabrera-Ponce, J. L., and Herrera-Estrella, L. (1997). Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276, 1566–1568. doi: 10.1126/science.276.5318.1566
11. Delhaize, E., Ma, J. F., and Ryan, P. R. (2012). Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci. 17, 341–348. doi: 10.1016/j.tplants.2012.02.008
12. Delhaize, E., Ryan, P. R., Hebb, D. M., Yamamoto, Y., Sasaki, T., and Matsumoto, H. (2004). Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc. Natl. Acad. Sci. U.S.A. 101, 15249–15254. doi: 10.1073/pnas.0406258101
13. Delhaize, E., Ryan, P. R., and Randall, P. J. (1993). Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiol. 103, 695–702. doi: 10.1104/pp.103.3.695
14. Dharmasiri, N., and Estelle, M. (2004). Auxin signaling and regulated protein degradation. Trends Plant Sci. 9, 302–308. doi: 10.1016/j.tplants.2004.04.003
15. Du, Z., Zhou, X., Ling, Y., Zhang, Z. H., and Su, Z. (2010). agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64–W70. doi: 10.1093/nar/gkq310
16. Duressa, D., Soliman, K., and Chen, D. (2010). Identification of aluminum responsive genes in Al-tolerant soybean line PI 416937. Int. J. Plant Genomics 2010, 1–13. doi: 10.1155/2010/164862
17. Duressa, D., Soliman, K. M., Taylor, R. W., and Chen, D. (2011). Gene expression profiling in soybean under aluminum stress: genes differentially expressed between Al-tolerant and Al-sensitive genotypes. Am. J. Cell Mol. 1, 156. doi: 10.4236/ajmb.2011.13016
18. Ernst, J., and Bar-Joseph, Z. (2006). STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:191. doi: 10.1186/1471-2105-7-191
19. Gould, B., McCouch, S., and Geber, M. (2015). De novo transcriptome assembly and identification of gene candidates for rapid evolution of soil Al tolerance in Anthoxanthum odoratum at the long-term park grass experiment. PLoS ONE 10:e0124424. doi: 10.1371/journal.pone.0124424
20. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., et al. (2011). Full-length transcriptome assembly fromRNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652. doi: 10.1038/nbt.1883
21. Houde, M., and Diallo, A. O. (2008). Identification of genes and pathways associated with aluminumstress and tolerance using transcriptome profiling of wheat near-isogenic lines. BMC Genomics 9:400. doi: 10.1186/1471-2164-9-400
22. Huang, C. F., Yamaji, N., Chen, Z. C., and Ma, J. F. (2012). A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J. 69, 857–867. doi: 10.1111/j.1365-313X.2011.04837.x
23. Iseli, C., Jongeneel, C. V., and Bucher, P. (1999). “ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences,” in Proceeding of the Seventh International Conference on Intelligent Systems for Molecular Biology, eds T. Lengauer, P. Bork, D. Brutlag, J. Glasgow, H.-W. Mewes, and R. Zimmer (Menlo park, CA: AAAI press), 138–148.
24. Jiang, Y. Q., and Deyholos, M. K. (2006). Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol. 6:25. doi: 10.1186/1471-2229-6-25
25. Kant, S., Bi, Y. M., Zhu, T., and Rothstein, S. J. (2009). SAUR39, a small auxin-up RNA gene, acts as a negative regulator of auxin synthesis and transport in rice. Plant Physiol. 151, 691–701. doi: 10.1104/pp.109.143875
26. Khu, D.-M., Reyno, R., Han, Y., Zhao, P. X., Bouton, J. H., Brummer, E. C., et al. (2013). Identification of aluminumtolerance quantitative trait loci in tetraploid alfalfa. Crop Sci. 53, 148–163. doi: 10.2135/cropsci2012.03.0181
27. Kochian, L. V., Pineros, M. A., and Hoekenga, O. A. (2005). The physiology, genetics and molecular biology of plant aluminumresistance and toxicity. Plant Soil. 274, 175–195. doi: 10.1007/s11104-004-1158-7
28. Kochian, L. V., Piñeros, M. A., Liu, J. P., and Magalhaes, J. V. (2015). Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu. Rev. Plant Biol. 66, 571–598. doi: 10.1146/annurev-arplant-043014-114822
29. Koyama, H., Kawamura, A., Kihara, T., Hara, T., Takita, E., and Shibata, D. (2000). Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol. 41, 1030–1037. doi: 10.1093/pcp/pcd029
30. Koyama, H., Takita, E., Kawamura, A., Hara, T., and Shibata, D. (1999). Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium. Plant Cell Physiol. 40, 482–488. doi: 10.1093/oxfordjournals.pcp.a029568
31. Kumari, M., Taylor, G. J., and Deyholos, M. K. (2008). Transcriptomic responses to aluminumstress in roots of Arabidopsis thaliana. Mol. Genet. Genomics 279, 339–357. doi: 10.1007/s00438-007-0316-z
32. Larsen, P. B., Geisler, M. J. B., Jones, C. A., Williams, K. M., and Cancel, J. D. (2005). ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 41, 353–363. doi: 10.1111/j.1365-313x.2004.02306.x
33. Li, R. Q., Yu, C., Li, Y. R., Lam, T. W., Yiu, S. M., Kristiansen, K., et al. (2009). SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967. doi: 10.1093/bioinformatics/btp336
34. Li, X. F., Ma, J. F., and Matsumoto, H. (2000). Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol. 123, 513–523. doi: 10.1104/pp.123.4.1537
35. Liu, W. X., Zhang, Z. S., Chen, S. Y., Ma, L. C., Wang, H. C., Dong, R., et al. (2016). Global transcriptome profiling analysis reveals insight into saliva-responsive genes in alfalfa. Plant Cell Rep. 35, 561–571. doi: 10.1007/s00299-015-1903-9
36. Ma, J. F. (2005). Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit. Rev. Plant Sci. 24, 267–281. doi: 10.1080/07352680500196017
37. Ma, J. F., Ryan, P. R., and Delhaize, E. (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273–278. doi: 10.1016/s1360-1385(01)01961-6
38. Ma, J. F., Zheng, S. J., and Matsumoto, H. (1997a). Specific secretion of citric acid Induced by Al stress in Cassia tora L. Plant Cell Physiol. 38, 1019–1025. doi: 10.1093/oxfordjournals.pcp.a029266
39. Ma, J. F., Zheng, S. J., Matsumoto, H., and Hiradate, S. (1997b). Detoxifying aluminumwith buckwheat. Nature 390, 569–570. doi: 10.1038/37518
40. Ma, Z. (1998). Oxalate exudation by taro in response to Al. Plant Physiol. 118, 861–865. doi: 10.1104/pp.118.3.861
41. Makhloufi, E., Yousfi, F. E., Marande, W., Mila, I., Hanana, M., Bèrges, H., et al. (2014). Isolation and molecular characterization of ERF1, an ethylene response factor gene from durum wheat (Triticum turgidum L. subsp durum), potentially involved in salt-stress responses. J. Exp. Bot. 65, 6359–6371. doi: 10.1093/jxb/eru352
42. Maron, L. G., Kirst, M., Mao, C., Milner, M. J., Menossi, M., and Kochian, L. V. (2008). Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytol. 179, 116–128. doi: 10.1111/j.1469-8137.2008.02440.x
43. 3+. Mol. Biol. Rep. 41, 8107–8116. doi: 10.1007/s11033-014-3709-1
44. Miyasaka, S. C., Buta, J. G., Howell, R. K., and Foy, C. D. (1991). Mechanism of aluminum tolerance in snapbean. Root exudation of citric acid. Plant Physiol. 96, 737–743. doi: 10.1104/pp.96.3.737
45. Mortazavi, A., Williams, B. A., Mccue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628. doi: 10.1038/nmeth.1226
46. Pellet, D. M., Grunes, D. L., and Kochian, L. V. (1995). Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196, 788–795. doi: 10.1007/bf01106775
47. Ponce, G., Barlow, P. W., Feldman, L. J., and Cassab, G. I. (2005). Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant Cell Environ. 28, 719–732. doi: 10.1111/j.1365-3040.2005.01318.x
48. Postnikova, O. A., Shao, J., and Nemchinov, L. G. (2013). Analysis of the alfalfa root transcriptome in response to salinity stress. Plant Cell Physiol. 54, 1041–1055. doi: 10.1093/pcp/pct056
49. Rahman, M. A., Kim, Y.-G., and Lee, B.-H. (2014). Proteomic response of alfalfa subjected to aluminum (Al) stress at low pH soil. J. Korean Soc. Grassland Forage Sci. 34, 262–268. doi: 10.5333/kgfs.2014.34.4.262
50. Sun, P., Tian, Q. Y., Zhao, M. G., Dai, X. Y., Huang, J. H., Li, L. H., et al. (2007). Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol. 48, 1229–1235. doi: 10.1093/pcp/pcm077
51. Sung, D. Y., Vierling, E., and Guy, C. L. (2001). Comprehensive expression profile analysis of the Arabidopsis hsp70 gene family. Plant Physiol. 126, 789–800. doi: 10.1104/Pp.126.2.789
52. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G. T. S., Sandberg, G., et al. (2007). Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 19, 2186–2196. doi: 10.1105/tpc.107.052100
53. Tesfaye, M., Temple, S. J., Allan, D. L., Vance, C. P., and Samac, D. A. (2001). Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol. 127, 1836–1844. doi: 10.1104/pp.127.4.1836
54. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., et al. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578. doi: 10.1038/nprot.2012.016
55. Wang, J. Y., Lan, P., Gao, H. M., Zheng, L., Li, W. F., and Schmidt, W. (2013). Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 14:783. doi: 10.1186/1471-2164-14-783
56. Wang, L. K., Feng, Z. X., Wang, X., Wang, X. W., and Zhang, X. G. (2010). DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136–138. doi: 10.1093/bioinformatics/btp612
57. Wang, Y., Tao, X., Tang, X. M., Xiao, L., Sun, J. L., Yan, X. F., et al. (2013). Comparative transcriptome analysis of tomato (Solanum lycopersicum) in response to exogenous abscisic acid. BMC Genomics 14:841. doi: 10.1186/1471-2164-14-841
58. Xie, C., Mao, X. Z., Huang, J. J., Ding, Y., Wu, J. M., Dong, S., et al. (2011). KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316–W322. doi: 10.1093/nar/gkr483
59. Xu, M. Y., You, J. F., Hou, N. N., Zhang, H. M., Chen, G., and Yang, Z. M. (2010). Mitochondrial enzymes and citrate transporter contribute to the aluminium-induced citrate secretion from soybean (Glycine max) roots. Funct. Plant Biol. 37, 285–295. doi: 10.1071/FP09223
60. Xu, W. R., Li, R. M., Zhang, N. B., Ma, F. L., Jiao, Y. T., and Wang, Z. P. (2014). Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress. Plant Mol. Biol. 86, 527–541. doi: 10.1007/s11103-014-0245-2
61. Yang, Z. B., Geng, X. Y., He, C. M., Zhang, F., Wang, R., Horst, W. J., et al. (2014). TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell 26, 2889–2904. doi: 10.1105/tpc.114.127993
62. Yang, Z. M., Sivaguru, M., Horst, W. J., and Matsumoto, H. (2000). Aluminium tolerance is achieved by exudation of citric acid fromroots of soybean (Glycine max L. Merr.). Physiol. Plant. 110, 72–77. doi: 10.1034/j.1399-3054.2000.11 0110.x
63. Ye, J., Fang, L., Zheng, H. K., Zhang, Y., Chen, J., Zhang, Z. J., et al. (2006). WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 34, W293–W297. doi: 10.1093/nar/gkl031
64. Yin, L., Wang, S., Eltayeb, A. E., Uddin, M. I., Yamamoto, Y., Tsuji, W., et al. (2010). Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231, 609–621. doi: 10.1007/s00425-009-1075-3
65. Yokosho, K., Yamaji, N., and Ma, J. F. (2014). Global transcriptome analysis of Al-induced genes in an Al-accumulating species, common buckwheat (Fagopyrum esculentum Moench). Plant Cell Physiol. 55, 2077–2091. doi: 10.1093/pcp/pcu135
66. You, J. F., Zhang, H. M., Liu, N., Gao, L. L., Kong, L. N., Yang, Z. M., et al. (2011). Transcriptomic responses to aluminum stress in soybean roots. Genome 54, 923–933. doi: 10.1139/g11-060
67. Zeng, H. Q., Wang, G. P., Zhang, Y. Q., Hu, X. Y., Pi, E., Zhu, Y. Y., et al. (2015). Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil. 398, 207–227. doi: 10.1007/s11104-015-2657-4
68. Zhu, H. F., Wang, H., Zhu, Y. F., Zou, J. W., Zhao, F. J., and Huang, C. F. (2015). Genome-wide transcriptomic and phylogenetic analyses reveal distinct aluminum-tolerance mechanisms in the aluminum-accumulating species buckwheat (Fagopyrum tataricum). BMC Plant Biol. 15:16. doi: 10.1186/s12870-014-0395-z