Allele diversity for abiotic stress responsive candidate genes in chickpea reference set using gene based SNP markers

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Roorkiwal, Manish ^a,b   Nayak, Spurthi N ^a,c   Thudi, Mahendar ^a   Upadhyaya, Hari D ^a   Brunel, Dominique ^d   Mournet, Pierre ^e   This, Dominique ^e   Sharma, Prakash C ^b   Varshney, Rajeev K ^a  

^a INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

^b GURU GOBIND SINGH INDRAPRASTHA UNIVERSITY   (India)

^c UNIVERSITY OF FLORIDA   (United States)

^d INRA CEA Institut de Génomique   (France)

^e UMR AGAP   (France)

Author keywords

Abiotic stress; Candidate genes; Chickpea; Genetic diversity; Single nucleotide polymorphism

Indexed keywords

EID: 84979500040     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00248     Document Type: Article

References (64)

1. Abdel-latif, A. (2007). Response of maize leaf sucrose phosphate synthase to salinity. Res. J. Agri. Biol. Sci. 3, 930-933.
2. Allagulova, C. R., Gimalov, F. R., Shakirova, F. M., and Vakhitov, V. A. (2003). The plant dehydrins: structure and putative functions. Biochemistry (Mosc.) 68, 1157-1165. doi: 10.1023/A:1026077825584
3. Baud, S., Vaultier, M. N., and Rochat, C. (2004). Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J. Exp. Bot. 55, 397-409. doi: 10.1093/jxb/erh047
4. Biedenkapp, H., Borgmeyer, U., Sippel, A. E., and Klempnauer, K. H. (1988). Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335, 835-837. doi: 10.1038/335835a0
5. Carrari, F., Fernie, A. R., and Iusem, N. D. (2004). Heard it through the grapevine? ABA and sugar cross-talk: the ASR story. Trends Plant Sci. 9, 57-59. doi: 10.1016/j.tplants.2003.12.004
6. Chen, W. J., and Zhu, T. (2004). Networks of transcription factors with roles in environmental stress response. Trends Plant Sci. 9, 591-596. doi: 10.1016/j.tplants.2004.10.007
7. Close, T. J. (1996). Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Plant 97, 795-803. doi: 10.1111/j.1399-3054.1996.tb00546.x
8. Coello, P., Hirano, E., Hey, S. J., Muttucumaru, N., Martinez-Barajas, E., Parry, M. A., et al. (2012). Evidence that abscisic acid promotes degradation of SNF1-related protein kinase (SnRK) 1 in wheat and activation of a putative calcium-dependent SnRK2. J. Exp. Bot. 63, 913-924. doi: 10.1093/jxb/err320
9. Cortés, A. J., Chavarro, M. C., Madriñán, S., This, D., and Blair, M. W. (2012a). Molecular ecology and selection in the drought-related Asr gene polymorphisms in wild and cultivated common bean (Phaseolus vulgaris L.). BMC Genet. 13:58. doi: 10.1186/1471-2156-13-58
10. Cortés, A. J., This, D., Chavarro, C., Madriñán, S., and Blair, M. W. (2012b). Nucleotide diversity patterns at the drought-related DREB2 encoding genes in wild and cultivated common bean (Phaseolus vulgaris L.). Theor. Appl. Genet. 125, 1069-1085. doi: 10.1007/s00122-012-1896-5
11. Cuc, L. M., Mace, E. S., Crouch, J. H., Quang, V. D., Long, T. D., and Varshney, R. K. (2008). Isolation and characterization of novel microsatellite markers and their application for diversity assessment in cultivated groundnut (Arachis hypogaea). BMC Plant Biol. 8:55. doi: 10.1186/1471-2229-8-55
12. Du, H., Yang, S. S., Liang, Z., Feng, B. R., Liu, L., Huang, Y. B., et al. (2012). Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol. 12:106. doi: 10.1186/1471-2229-12-106
13. FAO. (2012). Available online at: http://faostat.fao.org/site/567/default.aspx#ancor
14. 2. J. Exp. Bot. 58, 2983-2992. doi: 10.1093/jxb/erm150
15. Gonzalez, E. M., Gordon, A. J., James, C. L., and Arrese-Igor, C. (1995). The role of sucrose synthase in the response of soybean nodules to drought. J. Exp. Bot. 46, 1515-1523. doi: 10.1093/jxb/46.10.1515
16. Halford, N. G., and Hey, S. J. (2009). Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signaling in plants. Biochem. J. 419, 247-259. doi: 10.1042/BJ20082408
17. Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S., and Masmoudi, K. (2011). Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal. Behav. 6, 1503-1509. doi: 10.4161/psb.6.10.17088
18. Hara, M., Terashima, S., Fukaya, T., and Kuboi, T. (2003). Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217, 290-298. doi: 10.1007/s00425-003-0986-7
19. Hardie, D. G. (2007). AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell. Biol. 8, 774-785. doi: 10.1038/nrm2249
20. Jayashree, B., Bhanuprakash, A., Jami, A., Reddy, S. P., Nayak, S., and Varshney, R. K. (2009). Perl module and PISE wrappers for the integrated analysis of sequence data and SNP features. BMC Res. Notes 2:92. doi: 10.1186/1756-0500-2-92
21. Joo, J., Lee, Y. H., Kim, Y. K., Nahm, B. H., and Song, S. I. (2013). Abiotic stress responsive rice ASR1 and ASR3 exhibit different tissue-dependent sugar and hormone-sensitivities. Mol. Cells 35, 421-435. doi: 10.1007/s10059-013-0036-7
22. Kalifa, Y., Perlson, E., Gilad, A., Konrad, Z., Scolnik, P. A., and Bar-Zvi, D. (2004). Over-expression of the water and salt stress-regulated Asr1 gene confers an increased salt tolerance. Plant Cell Environ. 27, 1459-1468. doi: 10.1111/j.1365-3040.2004.01251.x
23. Kleines, M., Elster, R.-C., Rodrigo, M.-J., Blervacq, A.-S., Salamini, F., and Bartels, D. (1999). Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum Hochst. Planta 209, 13-24. doi: 10.1007/s004250050602
24. Konishi, S., Izawa, T., Lin, S. Y., Ebana, K., Fukuta, Y., Sasaki, T., et al. (2006). An SNP caused loss of seed shattering during rice domestication. Science 312, 1392-1396. doi: 10.1126/science.1126410
25. Kovach, M. J., Sweeney, M. T., and McCouch, S. R. (2007). New insights into the history of rice domestication. Trends Genet. 23, 578-587. doi: 10.1016/j.tig.2007.08.012
26. Kudapa, H., Ramalingam, A., Nayakoti, S., Chen, X., Zhuang, W., Liang, X., et al. (2013). Functional genomics to study stress responses in crop legumes: progress and prospects. Funct. Plant Biol. 40, 1221-1233. doi: 10.1071/FP13191
27. Kumar, A., and Turner, N. C. (2009). Growth and sucrose synthase activity of developing chickpea (Cicer arietinum L.) seeds under field conditions. Austr. J. Crop Sci. 3, 20-27.
28. Londo, J. P., Chiang, Y. C., Hung, K. H., Chiang, T. Y., and Schaal BA. (2006). Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc. Natl. Acad. Sci. U.S.A. 103, 9578-9583. doi: 10.1073/pnas.0603152103
29. Mallikarjuna, G., Mallikarjuna, K., Reddy, M. K., and Kaul, T. (2011). Expression of OsDREB2A transcription factor confers enhanced dehydration and salt stress tolerance in rice (Oryza sativa L.). Biotechnol. Lett. 33, 1689-1697. doi: 10.1007/s10529-011-0620-x
30. Masle, J., Gilmore, S. R., and Farquhar, G. D. (2005). The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866-870. doi: 10.1038/nature03835
31. Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., et al. (2010). Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genomics 283, 185-196. doi: 10.1007/s00438-009-0506-y
32. Missihoun, T. D., Schmitz, J., Klug, R., Kirch, H. H., and Bartels, D. (2011). Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses. Planta 233, 369-382. doi: 10.1007/s00425-010-1297-4
33. Nayak, S. N., Jayashree, B., Upadhyaya, H. D., Hash, C. T., Kavi Kishor, P. B., Chattopadhyay, D., et al. (2009). Isolation and sequence analysis of DREB2A homologues in three cereals and two legume species. Plant Sci. 117, 460-467. doi: 10.1016/j.plantsci.2009.07.009
34. Petit, R. J., El Mousadik, A., and Pons, O. (1998). Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12, 844-855. doi: 10.1046/j.1523-1739.1998.96489.x
35. Petrivalský, M., Brauner, F., Luhová, L., Gagneul, D., and Sebela, M. (2007). Aminoaldehyde dehydrogenase activity during wound healing of mechanically injured pea seedlings. J. Plant Physiol. 164, 1410-1418. doi: 10.1016/j.jplph.2007.01.018
36. Philippe, R., Courtois, B., McNally, K. L., Mournet, P., El-Malki, R., Paslier, M. C. L., et al. (2010). Structure, allelic diversity and selection of Asr genes, candidate for drought tolerance, in Oryza sativa L. and wild relatives. Theor. Appl. Genet. 121, 769-787. doi: 10.1007/s00122-010-1348-z
37. Puhakainen, T., Hess, M. W., Mäkelä, P., Svensson, J., Heino, P., and Palva, E. T. (2004). Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol. Biol. 54, 743-753. doi: 10.1023/B:PLAN.0000040903.66496.a4
38. Rafalski, A. (2002). Applications of single nucleotide polymorphisms in crop genetics. Curr. Opin. Plant Biol. 5, 94-100. doi: 10.1016/S1369-5266(02)00240-6
39. Riechmann, J. L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., et al. (2000). Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105-2110. doi: 10.1126/science.290.5499.2105
40. Romero, I., Fuertes, A., Benito, M. J., Malpica, J. M., Leyva, A., and Paz-Ares, J. (1998). More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J. 14, 273-284. doi: 10.1046/j.1365-313X.1998.00113.x
41. Roorkiwal, M., and Sharma, P. C. (2012). Sequence similarity based identification of abiotic stress responsive genes in chickpea. Bioinformation 8, 92-97. doi: 10.6026/97320630008092
42. Ross-Ibarra, J., Morrell, P. L., and Gaut, B. S. (2007). Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc. Natl. Acad. Sci. USA 15:104. doi: 10.1073/pnas.0700643104
43. Ruelland, E., Cantrel, C., Gawer, M., Kader, J. C., and Zachowski, A. (2002). Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol. 130, 999-1007. doi: 10.1104/pp.006080
44. Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K., et al. (2006). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292-1309. doi: 10.1105/tpc.105.035881
45. Schena, M., Shalon, D., Davis, R. W., and Brown, P. O. (1995). Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467-470. doi: 10.1126/science.270.5235.467
46. Shpak, E. D., Berthiaume, C. T., Hill, E. J., and Torii, K. U. (2004). Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131, 1491-1501. doi: 10.1242/dev.01028
47. Shukla, R. K., Raha, S., Tripathi, V., and Chattopadhyay, D. (2006). Expression of CAP2, an AP2-family transcription factor from chickpea enhances growth and tolerance to dehydration and salt tress in transgenic tobacco. Plant Physiol. 142, 113-123. doi: 10.1104/pp.106.081752
48. Skibbe, D. S., Liu, F., Wen, T. J., Yandeau, M. D., Cui, X., Cao, J., et al. (2002). Characterization of the aldehyde dehydrogenase gene families of Zea mays and Arabidopsis. Plant Mol. Biol. 48, 751-764. doi: 10.1023/A:1014870429630
49. Stiti, N., Missihoun, T. D., Kotchoni, S. O., Kirch, H. H., and Bartels, D. (2011). Aldehyde dehydrogenases in Arabidopsis thaliana: biochemical requirements, metabolic pathways, and functional analysis. Front. Plant Sci. 2:65. doi: 10.3389/fpls.2011.00065
50. Tsuji, G., Fujii, S., Fujihara, N., Hirose, C., Tsuge, S., Shiraishi, T., et al. (2003). Agrobacterium tumefaciens-mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium. J. Gen. Plant Pathol. 69, 230-239. doi: 10.1007/s10327-003-0040-4
51. Upadhyaya, H. D., Bramel, P. J., and Singh, S. (2001). Development of a chickpea core subset using geographic distribution and quantitative traits. Crop Sci. 41, 206-210. doi: 10.2135/cropsci2001.411206x
52. Upadhyaya, H. D., Dwivedi, S. L., Baum, M., Varshney, R. K., Udupa, S. M., Gowda, C. L. L., et al. (2008). Genetic structure, diversity, and allelic richness in composite collection and reference set in chickpea (Cicer arietinum L.). BMC Plant Biol. 8:106. doi: 10.1186/1471-2229-8-106
53. Upadhyaya, H. D., Furman, B. J., Dwivedi, S. L., Udupa, S. M., Gowda, C. L. L., Baum, M., et al. (2006). Development of a composite collection for mining germplasm possessing allelic variation for beneficial traits in chickpea. Plant Genet. Resour. 4, 13-19. doi: 10.1079/PGR2005101
54. Upadhyaya, H. D., and Ortiz, R. (2001). A mini core subset for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement. Theor. Appl. Genet. 102, 1292-1298. doi: 10.1007/s00122-001-0556-y
55. Varshney, R. K., Hiremath, P. J., Lekha, P., Kashiwagi, J., Balaji, J., Deokar, A. A., et al. (2009). A comprehensive resource of drought-and salinity-responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC Genomics 10:523. doi: 10.1186/1471-2164-10-523
56. Varshney, R. K., Song, C., Saxena, R. K., Azam, S., Yu, S., Sharpe, A. G., et al. (2013). Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat. Biotechnol. 31, 240-246. doi: 10.1038/nbt.2491
57. Velasco-Conde, T., Yakovlev, I., Majada, J. P., Aranda, I., and Johnsen, Ø. (2012). Dehydrins in maritime pine (Pinus pinaster) and their expression related to drought stress response. Tree Genet. Gen. 8, 957-973. doi: 10.1007/s11295-012-0476-9
58. Volpe, V., Dell'Aglio, E., Giovannetti, M., Ruberti, C., Costa, A., Genre, A., et al. (2013). An AM-induced, MYB-family gene of Lotus japonicus (LjMAMI) affects root growth in an AM-independent manner. Plant J. 73, 442-455. doi: 10.1111/tpj.12045
59. Wise, M. J., and Tunnacliffe, A. (2004). POPP the question: what do LEA proteins do? Trends Plant Sci. 9, 13-17. doi: 10.1016/j.tplants.2003.10.012
60. Wood, A. J., Saneoka, H., Rhodes, D., Joly, R. J., and Goldsbrough, P. B. (1996). Betaine aldehyde dehydrogenase in sorghum. Plant Physiol. 110, 1301-1308. doi: 10.1104/pp.110.4.1301
61. Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high salt stress. Plant Cell 6, 251-264. doi: 10.1105/tpc.6.2.251
62. Yang, C. Y., Chen, Y. C., Jauh, G. Y., and Wang, C. S. (2005). A Lily ASR protein involves abscisic acid signaling and confers drought and salt resistance in Arabidopsis. Plant Physiol. 139, 836-846. doi: 10.1104/pp.105.065458
63. Yokotani, N., Ichikawa, T., Kondou, Y., Iwabuchi, M., Matsui, M., Hirochika, H., et al. (2013). Role of the rice transcription factor JAmyb in abiotic stress response. J. Plant Res. 126, 131-139. doi: 10.1007/s10265-012-0501-y
64. Zhu, C., Gore, M., Buckler, E. S., and Yu, J. (2008). Status and prospects of association mapping in plants. Plant Genome 1, 5-20. doi: 10.3835/plantgenome2008.02.0089