The ecological genomic basis of salinity adaptation in Tunisian Medicago truncatula
详细信息 查看全文
- 作者：Maren L Friesen (16) (17)
Eric JB von Wettberg (18) (19)
Mounawer Badri (20)
Ken S Moriuchi (21)
Fathi Barhoumi (20)
Peter L Chang (16)
Sonia Cuellar-Ortiz (21)
Matilde A Cordeiro (21) (22)
Wendy T Vu (16)
Soumaya Arraouadi (20)
Naceur Dj茅bali (20)
Kais Zribi (20)
Yazid Badri (20)
Stephanie S Porter (23) (24)
Mohammed Elarbi Aouani (20)
Douglas R Cook (21)
Sharon Y Strauss (23) (24)
Sergey V Nuzhdin (16)
16. Section of Molecular and Computational Biology ; Department of Biological Sciences ; University of Southern California ; Los Angeles ; CA ; 90089 ; USA
17. Department of Plant Biology ; Michigan State University ; East Lansing ; MI ; 48824 ; USA
18. Department of Biological Sciences ; Florida International University ; Miami ; FL ; 33199 ; USA
19. Kushlan Institute for Tropical Science ; Fairchild Tropical Botanic Garden ; Coral Gables ; FL ; 33156 ; USA
20. Centre of Biotechnology of Borj Cedria ; B.P. 901 ; Hammam-Lif ; 2050 ; Tunisia
21. Department of Plant Pathology ; University of California Davis ; Davis ; CA ; 95616 ; USA
22. Instituto de Tecnologia Qu铆mica e Biol贸gica ; Oeiras ; Portugal
23. Department of Evolution and Ecology ; University of California Davis ; Davis ; CA ; 95616 ; USA
24. Center for Population Biology ; University of California Davis ; Davis ; California ; 95616 ; USA - 关键词：Adaptation ; Agriculture ; Ecological genetics ; Population genetics ; Abiotic stress
- 刊名：BMC Genomics
- 出版年：2014
- 出版时间：December 2014
- 年：2014
- 卷：15
- 期：1
- 全文大小：1,325 KB
- 参考文献：1. Levene, H (1953) Genetic equilibrium when more than one ecological niche is available. Am Nat 87: pp. 331-333 CrossRef
2. Hereford, J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173: pp. 579-588 CrossRef
3. Clausen, J, Hiesey, WM (1958) Genetic Structure of Ecological Races (Experimental Studies on the Nature of Species, Vol. 4). Carnegie Institution of Washington, Washington
4. Kawecki, TJ, Ebert, D (2004) Conceptual issues in local adaptation. Ecol Lett 7: pp. 1225-1241 CrossRef
5. Blanquart, F, Kaltz, O, Nuismer, SL, Gandon, S (2013) A practical guide to measuring local adaptation. Ecol Lett 16: pp. 1195-1205 CrossRef
6. Turner, TL, Bourne, EC, Wettberg Von, EJ, Hu, TT, Nuzhdin, SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42: pp. 260-263 CrossRef
7. Ellison, CE, Hall, C, Kowbel, D, Welch, J, Brem, RB, Glass, NL, Taylor, JW (2011) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci U S A 108: pp. 2831-2836 CrossRef
8. Renaut, S, Owens, GL, Rieseberg, LH (2013) Shared selective pressure and local genomic landscape lead to repeatable patterns of genomic divergence in sunflowers. Mol Ecol 23: pp. 311-324 CrossRef
9. Fischer, MC, Rellstab, C, Tedder, A, Zoller, S, Gugerli, F, Shimizu, KK, Holderegger, R, Widmer, A (2013) Population genomic footprints of selection and associations with climate in natural populations of Arabidopsis hallerifrom the Alps. Mol Ecol 22: pp. 5594-5607 CrossRef
10. Axelsson, E, Ratnakumar, A, Arendt, M-L, Maqbool, K, Webster, MT, Perloski, M, Liberg, O, Arnemo, JM, Hedhammar, 脜, Lindblad-Toh, K (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495: pp. 360-364 CrossRef
11. Friesen, M, Wettberg Von, EJ (2010) Adapting genomics to study the evolution and ecology of agricultural systems. Curr Opin Plant Biol 13: pp. 119-125 CrossRef
12. Rozema, J, Flowers, T (2008) Crops for a salinized world. Science 322: pp. 1478-1480 CrossRef
13. Wang, G (2005) Agricultural drought in a future climate: results from 15 global climatemodels participating in the IPCC 4th assessment. Clim Dyn 25: pp. 739-753 CrossRef
14. The state of the world's land and water resources for food and agriculture: Managing systems at risk 2011.http://www.fao.org/docrep/017/i1688e/i1688e.pdf
15. Flowers, TJ, Hajibagheri, MA, Clipson, NJW (1986) Halophytes. Q Rev Biol 61: pp. 313-337 CrossRef
16. Lesins, K, Lesins, I (1979) Genus Medicago (Leguminosae), a Taxogenetic Study. Dr. W. Junk Publishers, The Hague
17. Young, ND, Debell茅, F, Oldroyd, GED, Geurts, R, Cannon, SB, Udvardi, MK, Benedito, VA, Mayer, KFX, Gouzy, J, Schoof, H, Van de Peer, Y, Proost, S, Cook, DR, Meyers, BC, Spannagl, M, Cheung, F, De Mita, S, Krishnakumar, V, Gundlach, H, Zhou, S, Mudge, J, Bharti, AK, Murray, JD, Naoumkina, MA, Rosen, B, Silverstein, KAT, Tang, H, Rombauts, S, Zhao, PX, Zhou, P (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: pp. 520-524 CrossRef
18. Siol, M, Prosperi, JM, Bonnin, I, Ronfort, J (2008) How multilocus genotypic pattern helps to understand the history of selfing populations: a case study in Medicago truncatula. Heredity 100: pp. 517-525 CrossRef
19. Yoder, JB, Briskine, R, Mudge, J, Farmer, A, Paape, T, Steele, K, Weiblen, GD, Bharti, AK, Zhou, P, May, GD, Young, ND, Tiffin, P (2013) Phylogenetic Signal Variation in the Genomes of Medicago (Fabaceae). Syst Biol 62: pp. 424-438 CrossRef
20. Branca, A, Paape, TD, Zhou, P, Briskine, R, Farmer, AD, Mudge, J, Bharti, AK, Woodward, JE, May, GD, Gentzbittel, L, Ben, C, Denny, R, Sadowsky, MJ, Ronfort, J, Bataillon, T, Young, ND, Tiffin, P (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci U S A 108: pp. E864-E870 CrossRef
21. Yoder, JB, Stanton-Geddes, J, Zhou, P, Briskine, R, Young, ND, Tiffin, P (2014) Genomic signature of adaptation to climate in medicago truncatula. Genetics 196: pp. 1263-1275 CrossRef
22. Stanton-Geddes, J, Paape, T, Epstein, B, Briskine, R, Yoder, J, Mudge, J, Bharti, AK, Farmer, AD, Zhou, P, Denny, R, May, GD, Erlandson, S, Yakub, M, Sugawara, M, Sadowsky, MJ, Young, ND, Tiffin, P (2013) Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS One 8: pp. e65688 CrossRef
23. Badri, M, Ilahi, H, Huguet, T, Aouani, ME (2007) Quantitative and molecular genetic variation in sympatric populations of Medicago laciniata and M. truncatula (Fabaceae): relationships with eco-geographical factors. Genet Res 89: pp. 107-122 CrossRef
24. Lazrek, F, Roussel, V, Ronfort, J, Cardinet, G, Chardon, F, Aouani, ME, Huguet, T (2009) The use of neutral and non-neutral SSRs to analyse the genetic structure of a Tunisian collection of Medicago truncatula lines and to reveal associations with eco-environmental variables. Genetica 135: pp. 391-402 CrossRef
25. Arraouadi, S, Badri, M, Zitoun, A, Huguet, T, Aouani, M (2011) Analysis of NaCl stress response in Tunisian and reference lines of Medicago truncatula. Russ J Plant Physiol 58: pp. 316-323 CrossRef
26. Arraouadi, S, Badri, M, Taamalli, W, Huguet, T, Aouani, ME (2011) Variability salt stress response analysis of Tunisian natural populations of Medicago truncatula (Fabaceae) using salt response index (SRI) ratio. Afr J Biotechnol 10: pp. 10636-10647
27. Friesen, M, Cordeiro, MA, Penmetsa, RV, Badri, M, Huguet, T, Aouani, ME, Cook, DR, Nuzhdin, SV (2010) Population genomic analysis of Tunisian Medicago truncatula reveals candidates for local adaptation. Plant J 63: pp. 623-635 CrossRef
28. Castro, BM, Moriuchi, KS, Friesen, M, Badri, M, Nuzhdin, SV, Strauss, SY, Cook, DR, Wettberg Von, E (2013) Parental environments and interactions with conspecifics alter salinity tolerance of offspring in the annual Medicago truncatula. J Ecol 101: pp. 1281-1287 CrossRef
29. Pritchard, JK, Stephens, M, Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155: pp. 945-959
30. Evanno, G, Regnaut, S, Goudet, J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14: pp. 2611-2620 CrossRef
31. Beerli, P, Palczewski, M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: pp. 313-326 CrossRef
32. Mitchell-Olds, T, Schmitt, J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: pp. 947-952 CrossRef
33. Fournier Level, A, Korte, A, Cooper, MD, Nordborg, M, Schmitt, J, Wilczek, AM (2011) A Map of local adaptation in Arabidopsis thaliana. Sci (New York, NY) 334: pp. 86-89 CrossRef
34. Leimu, R, Fischer, M (2008) A meta-analysis of local adaptation in plants. PLoS One 3: pp. e4010 CrossRef
35. Hoeksema, JD, Forde, SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171: pp. 275-290 CrossRef
36. Lajeunesse, MJ, Forbes, MR (2002) Host range and local parasite adaptation. P R Soc B 269: pp. 703-710 CrossRef
37. Siol, M, Bonnin, I, Olivieri, I, Prosperi, JM, Ronfort, J (2007) Effective population size associated with self-fertilization: lessons from temporal changes in allele frequencies in the selfing annual Medicago truncatula. J Evol Biol 20: pp. 2349-2360 CrossRef
38. Munns, R, Tester, M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: pp. 651-681 CrossRef
39. Hubbard, KE, Nishimura, N, Hitomi, K, Getzoff, ED, Schroeder, JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24: pp. 1695-1708 CrossRef
40. Zhao, R, Sun, H-L, Mei, C, Wang, X-J, Yan, L, Liu, R, Zhang, X-F, Wang, X-F, Zhang, D-P (2011) The Arabidopsis Ca(2+) -dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192: pp. 61-73 CrossRef
41. Cordeiro, MA, Moriuchi, KS, Fotinos, TD, Miller, KE, Nuzhdin, SV, Wettberg Von, EJ, Cook, DR (2014) Population differentiation for germination and early seedling root growth traits under saline conditions in the annual legume Medicago truncatula (Fabaceae). Am J Bot 101: pp. 488-498 CrossRef
42. Howe, GA, Jander, G (2008) Plant Immunity to Insect Herbivores. Annu Rev Plant Biol 59: pp. 41-66 CrossRef
43. Weinl, S, Kudla, J (2009) The CBL-CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytol 184: pp. 517-528 CrossRef
44. Li, R, Zhang, J, Wu, G, Wang, H, Chen, Y, Wei, J (2012) HbCIPK2, a novel CBL-interacting protein kinase from halophyte Hordeum brevisubulatum, confers salt and osmotic stress tolerance. Plant Cell Environ 35: pp. 1582-1600 CrossRef
45. Ge, L-F, Chao, D-Y, Shi, M, Zhu, M-Z, Gao, J-P, Lin, H-X (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. PLANTA 228: pp. 191-201 CrossRef
46. L贸pez, M, Tejera, NA, Iribarne, C, Lluch, C, Herrera-Cervera, JA (2008) Trehalose and trehalase in root nodules of Medicago truncatulaand Phaseolus vulgarisin response to salt stress. Physiol Plant 134: pp. 575-582 CrossRef
47. L贸pez, M, Tejera, NA, Lluch, C (2009) Validamycin A improves the response of Medicago truncatula plants to salt stress by inducing trehalose accumulation in the root nodules. J Plant Physiol 166: pp. 1218-1222 CrossRef
48. Baxter, I, Brazelton, JN, Yu, D, Huang, YS, Lahner, B, Yakubova, E, Li, Y, Bergelson, J, Borevitz, JO, Nordborg, M, Vitek, O, Salt, DE (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 6: pp. e1001193 CrossRef
49. Toomajian, C, Hu, TT, Aranzana, MJ, Lister, C, Tang, C, Zheng, H, Zhao, K, Calabrese, P, Dean, C, Nordborg, M (2006) A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biol 4: pp. e137 CrossRef
50. Mungu铆a-Rosas, MA, Ollerton, J, Parra-Tabla, V, De-Nova, JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol Lett 14: pp. 511-521 CrossRef
51. Valverde, F (2011) CONSTANS and the evolutionary origin of photoperiodic timing of flowering. J Exp Bot 62: pp. 2453-2463 CrossRef
52. Laurie, RE, Diwadkar, P, Jaudal, M, Zhang, L, Hecht, V, Wen, J, Tadege, M, Mysore, KS, Putterill, J, Weller, JL, Macknight, RC (2011) The medicago FLOWERING LOCUS T homolog, MtFTa1, is a Key regulator of flowering time. Plant Physiol 156: pp. 2207-2224 CrossRef
53. Pierre, J-B, Huguet, T, Barre, P, Huyghe, C, Julier, B (2008) Detection of QTLs for flowering date in three mapping populations of the model legume species Medicago truncatula. Theoret Appl Genetics 117: pp. 609-620 CrossRef
54. Pierre, J-B, Bogard, M, Herrmann, D, Huyghe, C, Julier, B (2010) A CONSTANS-like gene candidate that could explain most of the genetic variation for flowering date in Medicago truncatula. Mol Breeding 28: pp. 25-35 CrossRef
55. Yeoh, CC, Balcerowicz, M, Zhang, L, Jaudal, M, Brocard, L, Ratet, P, Putterill, J (2013) Fine mapping links the FTa1 flowering time regulator to the dominant Spring1 locus in medicago. PLoS One 8: pp. e53467 CrossRef
56. Stanton, ML, Roy, BA, Thiede, DA (2007) Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution 54: pp. 93-111 CrossRef
57. Triky-Dotan, S, Yermiyahu, U, Katan, J, Gamliel, A (2005) Development of crown and root rot disease of tomato under irrigation with saline water. Phytopathology 95: pp. 1438-1444 CrossRef
58. Bari, R, Jones, J (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: pp. 473-488 CrossRef
59. Jones, JDG, Dangl, JL (2006) The plant immune system. Nature 444: pp. 323-329 CrossRef
60. Seeholzer, S, Tsuchimatsu, T, Jordan, T, Bieri, S, Pajonk, S, Yang, W, Jahoor, A, Shimizu, KK, Keller, B, Schulze-Lefert, P (2010) Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol Plant Microbe Interact 23: pp. 497-509 CrossRef
61. Benedito, V, Torres Jerez, I, Murray, J, Andriankaja, A, Allen, S, Kakar, K, Wandrey, M, Verdier, J, Zuber, H, Ott, T, Moreau, S, Niebel, A, Frickey, T, Weiller, G, He, J, Dai, X, Zhao, P, Tang, Y, Udvardi, M (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55: pp. 504-513 CrossRef
62. Li, D, Zhang, Y, Hu, X, Shen, X, Ma, L, Su, Z, Wang, T, Dong, J (2011) Transcriptional profiling of Medicago truncatula under salt stress identified a novel CBF transcription factor MtCBF4 that plays an important role in abiotic stress responses. Bmc Plant Biol 11: pp. 109 CrossRef
63. Kawecki, TJ (1994) Accumulation of deleterious mutations and the evolutionary cost of being a generalist. Am Nat 144: pp. 833-838 CrossRef
64. Bierne, N, Welch, J, Loire, E, Bonhomme, F, David, P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20: pp. 2044-2072 CrossRef
65. Hoekstra, HE, Coyne, JA (2007) The locus of evolution: Evo devo and the genetics of adaptation. Evolution 61: pp. 995-1016 CrossRef
66. Lande, R, Arnold, S (1983) The measurement of selection on correlated characters. Evolution 37: pp. 1210-1226 CrossRef
67. Stinchcombe, JR, Rutter, MT, Burdick, DS, Tiffin, P, Rausher, MD, Mauricio, R (2002) Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice. Am Nat 160: pp. 511-523 CrossRef
68. Dunham, JP, Friesen, M (2013) A cost-effective method for high-throughput construction of illumina sequencing libraries. Cold Spring Harbor Protocols 2013: pp. 820-834 CrossRef
69. Li, H, Durbin, R (2009) Fast and accurate short read alignment with Burrows鈥揥heeler transform. Bioinformatics 25: pp. 1754-1760 CrossRef
70. McKenna, A, Hanna, M, Banks, E, Sivachenko, A, Cibulskis, K, Kernytsky, A, Garimella, K, Altshuler, D, Gabriel, S, Daly, M, DePristo, MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: pp. 1297-1303 CrossRef
71. Team, R (2009) R: a language and environment for statistical computing.
72. Goudet, J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5: pp. 184-186 CrossRef
73. Storey, JD, Tibshirani, R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: pp. 9440-9445 CrossRef
74. Krishnamurthy, N, Brown, DP, Kirshner, D, Sj枚lander, K (2006) PhyloFacts: an online structural phylogenomic encyclopedia for protein functional and structural classification. Genome Biol 7: pp. R83 CrossRef
75. Datta, RS, Meacham, C, Samad, B, Neyer, C, Sjolander, K (2009) Berkeley PHOG: PhyloFacts orthology group prediction web server. Nucleic Acids Res 37: pp. W84-W89 CrossRef - 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
- 出版者：BioMed Central
- ISSN：1471-2164
文摘
Background As our world becomes warmer, agriculture is increasingly impacted by rising soil salinity and understanding plant adaptation to salt stress can help enable effective crop breeding. Salt tolerance is a complex plant phenotype and we know little about the pathways utilized by naturally tolerant plants. Legumes are important species in agricultural and natural ecosystems, since they engage in symbiotic nitrogen-fixation, but are especially vulnerable to salinity stress. Results Our studies of the model legume Medicago truncatula in field and greenhouse settings demonstrate that Tunisian populations are locally adapted to saline soils at the metapopulation level and that saline origin genotypes are less impacted by salt than non-saline origin genotypes; these populations thus likely contain adaptively diverged alleles. Whole genome resequencing of 39 wild accessions reveals ongoing migration and candidate genomic regions that assort non-randomly with soil salinity. Consistent with natural selection acting at these sites, saline alleles are typically rare in the range-wide species' gene pool and are also typically derived relative to the sister species M. littoralis. Candidate regions for adaptation contain genes that regulate physiological acclimation to salt stress, such as abscisic acid and jasmonic acid signaling, including a novel salt-tolerance candidate orthologous to the uncharacterized gene AtCIPK21. Unexpectedly, these regions also contain biotic stress genes and flowering time pathway genes. We show that flowering time is differentiated between saline and non-saline populations and may allow salt stress escape. Conclusions This work nominates multiple potential pathways of adaptation to naturally stressful environments in a model legume. These candidates point to the importance of both tolerance and avoidance in natural legume populations. We have uncovered several promising targets that could be used to breed for enhanced salt tolerance in crop legumes to enhance food security in an era of increasing soil salinization.