Population-genetic analysis of HvABCG31 promoter sequence in wild barley (Hordeum vulgare ssp. spontaneum)

BMC Evolutionary Biology

Guoxiong Chen⁵  Abraham Korol²  Takao Komatsuda¹  Eviatar Nevo²  Tamar Krugman²  Shun Sakuma¹  Dmitry Weiner²  Mohammad Pourkheirandish¹  Aidong Wang⁵  Chao Li⁵  Genlin Jiao⁴  Hanan Sela³  Xiaoying Ma⁴ 

[1] National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan;Institute of Evolution and Department of Evolutionary & Environmental Biology, University of Haifa, Mount Carmel, Haifa 31905, Israel;Institute for Cereal Crops Improvement, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel;Shenzhen Fairy Lake Botanical Garden, Chinese Academy of Sciences, Shenzhen, 518004, China;Extreme Stress Resistance and Biotechnology Laboratory, Cold and Arid Regions Environmental and Engineering Institute, Chinese Academy of Sciences, Lanzhou 730000, China

关键词: TFBSs;    Phylogenetic;    Promoter;    HvABCG31;    Wild barley;   

Others  :  1140281
DOI  :  10.1186/1471-2148-12-188

 received in 2012-05-14, accepted in 2012-09-18,  发布年份 2012

【 摘 要 】

Background

The cuticle is an important adaptive structure whose origin played a crucial role in the transition of plants from aqueous to terrestrial conditions. HvABCG31/Eibi1 is an ABCG transporter gene, involved in cuticle formation that was recently identified in wild barley (Hordeum vulgare ssp. spontaneum). To study the genetic variation of HvABCG31 in different habitats, its 2 kb promoter region was sequenced from 112 wild barley accessions collected from five natural populations from southern and northern Israel. The sites included three mesic and two xeric habitats, and differed in annual rainfall, soil type, and soil water capacity.

Results

Phylogenetic analysis of the aligned HvABCG31 promoter sequences clustered the majority of accessions (69 out of 71) from the three northern mesic populations into one cluster, while all 21 accessions from the Dead Sea area, a xeric southern population, and two isolated accessions (one from a xeric population at Mitzpe Ramon and one from the xeric ‘African Slope’ of “Evolution Canyon”) formed the second cluster. The southern arid populations included six haplotypes, but they differed from the consensus sequence at a large number of positions, while the northern mesic populations included 15 haplotypes that were, on average, more similar to the consensus sequence. Most of the haplotypes (20 of 22) were unique to a population. Interestingly, higher genetic variation occurred within populations (54.2%) than among populations (45.8%). Analysis of the promoter region detected a large number of transcription factor binding sites: 121–128 and 121–134 sites in the two southern arid populations, and 123–128,125–128, and 123–125 sites in the three northern mesic populations. Three types of TFBSs were significantly enriched: those related to GA (gibberellin), Dof (DNA binding with one finger), and light.

Conclusions

Drought stress and adaptive natural selection may have been important determinants in the observed sequence variation of HvABCG31 promoter. Abiotic stresses may be involved in the HvABCG31 gene transcription regulations, generating more protective cuticles in plants under stresses.

【 授权许可】

   
2012 Ma et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Nevo E: Evolution under environmental stress at macro-and microscales. Genome Biol Evol 2011, 2:1039-1052.
• [2]Wright SI, Gaut BS: Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 2005, 22:506-519.
• [3]Leino MW, Hagenblad J: Nineteenth century seeds reveal the population genetics of landrace barley (Hordeum vulgare). Mol Biol Evol 2010, 27:964-973.
• [4]Samuels L, Kunst L, Jetter R: Sealing plant surfaces: cuticular wax formation by epidermal cells. Plant Biol 2008, 59:683-707.
• [5]Raven JA, Edwards D: Physiological evolution of lower embryophytes: adaptations to the terrestrial environment. In The evolution of plant physiology: from whole plants to ecosystems. Edited by Alan R. Amsterdam: Elsevier; 2004:17-41.
• [6]Nawrath C: Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 2006, 9:281-287.
• [7]Riederer M, Schreiber L: Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 2001, 52:2023-2032.
• [8]Kunst L, Jetter R, Samuels AL: Biosynthesis and transport of plant cuticular waxes. Annual Plant Reviews Volume 23: Biology of the Plant Cuticle 2006, 182-215.
• [9]Li C, Wang AD, Ma XY, Nero E, Chen GX: Consensus maps of cloned plant cuticle genes. Sci Cold Arid Regi 2010, 2:465-476.
• [10]Chen G, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li X, Zhao X: An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci U S A 2011, 108:12354-12359.
• [11]Chen G, Sagi M, Weining S, Krugman T, Fahima T, Korol AB, Nevo E: Wild barley eibi1 mutation identifies a gene essential for leaf water conservation. Planta 2004, 219:684-693.
• [12]Chen GX, Komatsudu T, Pourkheirandish M, Sameri M, Sato K, Krugman T, Fahima T, Korol AB, Nevo E: Mapping of the eibi1 gene responsible for the drought hypersensitive cuticle in wild barley (Hordeum spontaneum). Breed Sci 2009, 59:21-26.
• [13]Nevo E: Origin, evolution, population genetics and resources for breeding of wild barley, Hordeum spontaneum, in the Fertile Crescent. Barley: Genetics, Molecular Biology and Biotechnology, Shewry, P (ed) CAB International 1992, 19-43.
• [14]Zohary D, Hopf M, Weiss E: Domestication of Plants in the Old World: The Origin and Spread of Domesticated Plants in Southwest Asia, Europe, and the Mediterranean Basin. New York: Oxford University Press; 2012.
• [15]Doebley JF, Gaut BS, Smith BD: The molecular genetics of crop domestication. Cell 2006, 127:1309-1321.
• [16]Ross-Ibarra J, Morrell PL, Gaut BS: Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc Natl Acad Sci U S A 2007, 104:8641-8648.
• [17]Burger JC, Chapman MA, Burke JM: Molecular insights into the evolution of crop plants. Am J Bot 2008, 95:113-122.
• [18]Buckler ES, Thornsberry JM, Kresovich S: Molecular diversity, structure and domestication of grasses. Genet Res 2001, 77:213-218.
• [19]Nevo E: Genome evolution of wild cereal diversity and prospects for crop improvement. Plant Genet Resour 2006, 4:36-46.
• [20]Nevo E, Beiles A, Zohary D: Genetic resources of wild barley in the Near East: structure, evolution and application in breeding. Biol J Linn Soc 1986, 27:355-380.
• [21]Vanhala T, Van Rijn C, Buntjer J, Stam P, Nevo E, Poorter H, Van Eeuwijk F: Environmental, phenotypic and genetic variation of wild barley (Hordeum spontaneum) from Israel. Euphytica 2004, 137:297-309.
• [22]Nevo E, Chen G: Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant Cell Environ 2010, 33:670-685.
• [23]Nevo E: Evolution of wild barley and barley improvement. In Advance in Barley Sciences. 15-20 April 2012; Hangzhou, China. Edited by Li C, Zhang G, Liu X, Eglinton J. Hangzhou: Zhejiang University Press- Springer; 2012:1-16. [Proceedings of 11th Int. Barley Genetics Symposium] Volume
• [24]Wunderlich Z, Mirny LA: Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 2009, 25:434-440.
• [25]Behrens S, Vingron M: Studying the evolution of promoter sequences: a waiting time problem. J Comput Biol 2010, 17:1591-1606.
• [26]Stone JR, Wray GA: Rapid evolution of cis-regulatory sequences via local point mutations. Mol Biol Evol 2001, 18:1764-1770.
• [27]Maeso I, Roy SW, Irimia M: Widespread recurrent evolution of genomic features. Genome Biol Evol 2012, 4:486-500.
• [28]Kim TM, Park PJ: Advances in analysis of transcriptional regulatory networks. Wiley Interdiscip Rev Syst Biol Med 2011, 3:21-35.
• [29]Fu YX: New statistical tests of neutrality for DNA samples from a population. Genetics 1996, 143:557-570.
• [30]Tajima F: The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 1996, 143:1457-1465.
• [31]Yang Z, Zhang T, Bolshoy A, Beharav A, Nevo E: Adaptive microclimatic structural and expressional dehydrin 1 evolution in wild barley, Hordeum spontaneum, at 'Evolution Canyon', Mount Carmel, Israel. Mol Ecol 2009, 18:2063-2075.
• [32]Nevo E: Evolution of genome–phenome diversity under environmental stress. Proc Natl Acad Sci U S A 2001, 98:6233-6240.
• [33]Cronin JK, Bundock PC, Henry RJ, Nevo E: Adaptive climatic molecular evolution in wild barley at the Isa defense locus. Proc Natl Acad Sci U S A 2007, 104:2773-2778.
• [34]Nevo E: Molecular evolution and ecological stress at global, regional and local scales: The Israeli perspective. J Exp Zool 1998, 282:95-119.
• [35]Owuor E, Beharav A, Fahima T, Kirzhner V, Korol A, Nevo E: Microscale ecological stress causes RAPD molecular selection in wild barley, Neve Yaar microsite, Israel. Genet Resour Crop Ev 2003, 50:213-224.
• [36]Zongyun F, Lili Z, Yizheng Z, Hongqing L: Further molecular evidence for the Hordeum vulgare ssp. spontaneum in Tibet as ultimate progenitor of Chinese cultivated barley. High Technology Letters 2005, 11:20-324.
• [37]Nevo E: Population genetic structure of wild barley and wheat in the Near East Fertile Crescent: regional and local adaptive patterns. In Cereal Genomics. Edited by Gupta PK, Varshney RK. Dordrecht: Kluwer Academic Publishers; 2004:135-163.
• [38]Lee CR, Mitchell-olds T: Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Mol Ecol 2011, 20:4631-4642.
• [39]Chen G, Krugman T, Fahima T, Chen K, Hu Y, Röder M, Nevo E, Korol A: Chromosomal regions controlling seedling drought resistance in Israeli wild barley, Hordeum spontaneum. Genet Resour Crop Ev 2010, 57:85-99.
• [40]Owuor ED, Fahima T, Beharav A, Korol A, Nevo E: RAPD divergence caused by microsite edaphic selection in wild barley. Genetica 1999, 105:177-192.
• [41]Nosil P, Funk DJ, O-B D: Divergent selection and heterogeneous genomic divergence. Mol Ecol 2009, 18:375-402.
• [42]Ivandic V, Hackett C, Zhang Z, Staub J, Nevo E, Thomas W, Forster B: Phenotypic responses of wild barley to experimentally imposed water stress. J Exp Bot 2000, 51:2021-2029.
• [43]Tajima F: Evolutionary relationship of DNA sequences in finite populations. Genetics 1983, 105:437.
• [44]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
• [45]Fu YX: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
• [46]Nevo E: "Evolution Canyon", a potential microscale monitor of global warming across life. Proc Natl Acad Sci U S A 2012, 109:2960-2965.
• [47]Nevo E: Asian, African and European biota meet at "Evolution Canyon" Israel: local tests of global biodiversity and genetic diversity patterns. Proc R Soc Lond B Biol Sci 1995, 262:149-155.
• [48]Hofinger BJ, Russell JR, Bass CG, Baldwin T, Dos Reis M, Hedley PE, Li Y, Macaulay M, Waugh R, Hammond-Kosack KIME: An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Mol Ecol 2011, 20:3653-3668.
• [49]Raz S, Retzkin S, Pavlicek T, Hoffman A, Kimchi H, Zehavi D, Beiles A, Nevo E: Scorpion Biodiversity and Interslope Divergence at "Evolution Canyon", Lower Nahal Oren Microsite, Mt. Carmel, Israel. PLoS One 2009, 4:e5214.
• [50]Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu SH: Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2011, 108:14992-14997.
• [51]Kosma DK, Jenks MA: Eco-physiological and molecular-genetic determinants of plant cuticle function in drought and salt stress tolerance. In Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. Edited by Paul M, Hasegawa , Matthew A, Jenks S, Mohan Jain . Dordrecht: Springer; 2007:91-120.
• [52]Luo B, Xue XY, Hu WL, Wang LJ, Chen XY: An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol 2007, 48:1790-1802.
• [53]Kunst L, Samuels AL: Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 2003, 42:51-80.
• [54]Yanagisawa S: The Dof family of plant transcription factors. Trends Plant Sci 2002, 7:555-560.
• [55]Yamaguchi S: Gibberellin metabolism and its regulation. Annu Rev Plant Biol 2008, 59:225-251.
• [56]Krugman T, Peleg Z, Quansah L, Chagué V, Korol AB, Nevo E, Saranga Y, Fait A, Chalhoub B, Fahima T: Alteration in expression of hormone-related genes in wild emmer wheat roots associated with drought adaptation mechanisms. Funct Integr Genomics 2011, 11:565-583.
• [57]Vettakkorumakankav NN, Falk D, Saxena P, Fletcher RA: A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol 1999, 40:542.
• [58]Huang W, Nevins JR, Ohler U: Phylogenetic simulation of promoter evolution: estimation and modeling of binding site turnover events and assessment of their impact on alignment tools. Genome Biol 2007, 8:R225. BioMed Central Full Text
• [59]Tirosh I, Weinberger A, Bezalel D, Kaganovich M, Barkai N: On the relation between promoter divergence and gene expression evolution. Mol Syst Biol 2008, 4:159-170.
• [60]Nevo E: " Evolution Canyon": a microcosm of life's evolution focusing on adaptation and speciation. Israel Journal of Ecology and Evolution 2006, 52:485-506.
• [61]Goldreich Y: The climate of Israel: observation, research, and application. Us: Springer; 2003.
• [62]Komatsuda T, Nakamura I, Takaiwa F, Oka S: Development of STS markers closely linked to the vrs1 locus in barley, Hordeum vulgare. Genome 1998, 41:680-685.
• [63]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [64]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
• [65]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [66]Excoffier LL, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 2005, 1:47-50.
• [67]Weir B, Cockerham CC: Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
• [68]Del Cerro I, Marmi J, Ferrando A, Chashchin P, Taberlet P, Bosch M: Nuclear and mitochondrial phylogenies provide evidence for four species of Eurasian badgers (Carnivora). Zool Scr 2010, 39:415-425.
• [69]Malysheva-Otto LV, Ganal MW, der MS R: Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm(Hordeum vulgare L.). BMC Genet 2006, 7:6.
• [70]Lin JZ, Brown AHD, Clegg MT: Heterogeneous geographic patterns of nucleotide sequence diversity between two alcohol dehydrogenase genes in wild barley (Hordeum vulgare subspecies spontaneum). Proc Natl Acad Sci U S A 2001, 98:531-536.
• [71]Jakob SS, Martinez-Meyer E, Blattner FR: Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Mol Biol Evol 2009, 26:907-923.
• [72]Chang WC, Lee TY, Huang HD, Huang HY, Pan RL: PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 2008, 9:561-575. BioMed Central Full Text
• [73]Reineke AR, Bornberg-Bauer E, Gu J: Evolutionary divergence and limits of conserved non-coding sequence detection in plant genomes. Nucleic Acids Res 2011, 39:6029-6043.