Abstract
Background and aims
Identification of the association between Cd tolerance-related traits and molecular markers facilitates an efficient selection of the tolerant cultivars. The objectives of this study were to analyze the Cd tolerance and the genetic diversity of native bermudagrass accessions in China, and to identify marker-trait association with wild bermudagrass.
Methods
A countrywide collection of 120 bermudagrass [Cynodon dactylon (L.) Pers.] accessions were evaluated for Cd tolerance and genetic diversity with simple sequence repeat (SSR) markers.
Result
Significant variations in 7 physiological parameters were observed among the accessions under Cd conditions. The 104 SSR primers amplified 1474 alleles. The average gene diversity and polymorphic information content (PIC) for the whole sample was 0.2270 and 0.1894, respectively. Clustering analysis showed that the distance of genetic relationship was affected by the cultivars of natural habitats and the edaphic conditions. Thirty one SSR markers were associated with more than one trait (P < 0.01), while 37 markers were identified by corrected P values (P < 3.5 × 10−4).
Conclusion
Thirty one SSR markers were associated with a reduction in 7 traits under Cd stress. These markers can be used for genetic improvement of Cd tolerance of bermudagrass after further validation.
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References
Achleitner A, Tinker NA, Zechner E, Buerstmayr H (2008) Genetic diversity among oat varieties of worldwide origin and associations of AFLP markers with quantitative traits. Theor Appl Genet 117:1041–1053
Aidid SB, Okamoto H (1992) Effects of lead, cadmium and zinc on the electric membrane potential at the xylem/symplast interface and cell elongation of Impatiens balsamina. Environ Exp Bot 32:439–448. doi:10.1016/0098-8472(92)90056-8
Aidid SB, Okamoto H (1993) Responses of elongation growth rate, turgor pressure and cell wall extensibility of stem cells of Impatiens balsamina to lead, cadmium and zinc. Biometals 6:245–249
Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:e60
Archer M, Caldwell R (2004) Response of six Australian plant species to heavy metal contamination at an abandoned mine site. Water Air Soil Pollut 157:257–267
Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631
Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709
Bell J, Tanhuanpää P, Kalendar R, Schulman AH, Kiviharju E (2007) A major gene for grain cadmium accumulation in oat (Avena sativa L.). Genome 50:588–594
Belyaev D, Borodin P (1982) The influence of stress on variation and its role in evolution. Biologisches Zentralblatt 101:705–714
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Bush EJ, Barrett SCH (1993) Genetics of mine invasions by Deschampsia cespitosa (Poaceae). Can J Bot 71:1336–1348. doi:10.1139/b93-159
Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693
Das P, Samantaray S, Rout G (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36
Deng J, Liao B, Ye M, Deng D, Lan C, Shu W (2007) The effects of heavy metal pollution on genetic diversity in zinc/cadmium hyperaccumulator Sedum alfredii populations. Plant Soil 297:83–92. doi:10.1007/s11104-007-9322-5
Deniau A, Pieper B, Ten Bookum W, Lindhout P, Aarts M, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920
Ducousso A, Petit D, Valero M, Vernet P (1990) Genetic variation between and within populations of a perennial grass: Arrhenatherum elatius. Heredity 65:179–188. doi:10.1038/hdy.1990.86
Fedoroff NV (1989) About maize transposable elements and development. Cell 56:181–191. doi:10.1016/0092-8674(89)90891-x
Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064. doi:10.1111/j.1365-313X.2005.02591.x
Gao WW, Li PY, Sun ZJ, Zhang TH, Ti ABL, Huang CF, Li N (2010) Genetic diversity of Cynodon dacty lon germplasm in Xinjiang by SSR molecular markers. Pratacultuarl Sci 27:58–64
Gouyon PH, Lumaret R, Valdeyron G, Vernet P (1983) Reproductive strategies and disturbance by man. In: Mooney H, Godron M (eds) Disturbance and ecosystems. Springer, Berlin
Grant C, Campbell C, Charnock N (2002) Selection of species suitable for derelict mine site rehabilitation in New South Wales, Australia. Water Air Soil Pollut 139:215–235
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hartwig A (2010) Mechanisms in cadmium-induced carcinogenicity: recent insights. Biometals 23:951–960
Hedrick PW, Ginevan ME, Ewing EP (1976) Genetic polymorphism in heterogeneous environments. Annu Rev Ecol Syst 7:1–32. doi:10.1146/annurev.es.07.110176.000245
Hewitt EJ, Bureaux CA (1966) Sand and water culture methods used in the study of plant nutrition. Cambridge Univ Press
Hiscox J, Israelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular California Agricultural Experiment Station 347
Hu T, Hu L, Zhang X, Zhang P, Zhao Z, Fu J (2013) Differential responses of CO2 assimilation, carbohydrate allocation and gene expression to NaCl stress in perennial ryegrass with different salt tolerance. PLoS One 8:e66090. doi:10.1371/journal.pone.0066090
Ishikawa S, Ae N, Yano M (2005) Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol 168:345–350
Ivandic V, Hackett CA, Nevo E, Keith R, Thomas WT, Forster BP (2002) Analysis of simple sequence repeats (SSRs) in wild barley from the Fertile Crescent: associations with ecology, geography and flowering time. Plant Mol Biol 48:511–527
Jamers A, Blust R, De Coen W, Griffin JL, Jones OA (2013) An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 126:355–364
Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Jegadeesan S, Yu K, Poysa V, Gawalko E, Morrison M, Shi C, Cober E (2010) Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [Glycine max (L.) Merr]. Theor Appl Genet 121:283–294. doi:10.1007/s00122-010-1309-6
Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol 238:272–279
Kresovich S, Szewc-McFadden A, Bliek S, McFerson J (1995) Abundance and characterization of simple-sequence repeats (SSRs) isolated from a size-fractionated genomic library of Brassica napus L. (rapeseed). Theor Appl Genet 91:206–211
Larsson EH, Bornman JF, Asp H (1998) Influence of UV-B radiation and Cd2+ on chlorophyll fluorescence, growth and nutrient content in Brassica napus. J Exp Bot 49:1031–1039
Lefebre C, Vernet P (1990) Microevolutionary processes on contaminated deposits. Heavy Metal Tolerance in Plants: Evolutionary Aspects., Boca Raton
Ling Y, Zhang XQ, Ma X, Chen SY, Chen TT, Liu W (2012) Analysis of genetic diversity among wild bermudagrass germplasm from southwest China using SSR markers. Genet Mol Res 11:4598–4608. doi:10.4238/2012.October.17.5
Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot:1420-1425
Luo H, Li H, Zhang X, Fu J (2011) Antioxidant responses and gene expression in perennial ryegrass (Lolium perenne L.) under cadmium stress. Ecotoxicology 20:770–778
Madejón P, Murillo J, Marañón T, Cabrera F (2006) Bioaccumulation of trace elements in a wild grass three years after the Aznalcóllar mine spill (South Spain). Environ Monit Assess 114:169–189
Matus I, Hayes P (2002) Genetic diversity in three groups of barley germplasm assessed by simple sequence repeats. Genome 45:1095–1106
Mengoni A, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random amplified polymorphic DNA analysis. Mol Ecol 9:1319–1324. doi:10.1046/j.1365-294x.2000.01011.x
Nei M (1972) Genetic distance between populations. Am Nat:283-292
Overnell J (1975) The effect of some heavy metal ions on photosynthesis in a freshwater alga. Pestic Biochem Physiol 5:19–26. doi:10.1016/0048-3575(75)90039-5
Padmaja K, Prasad D, Prasad A (1990) Inhibition of chlorophyll synthesis in Phaseolus vulgaris L. seedlings by cadmium acetate. Photosynthetica 24:399–405
Pakniyat H, Powell W, Baird E, Handley L, Robinson D, Scrimgeour C, Hackett C, Forster B, Nevo E, Caligari P (1997) AFLP variation in wild barley (Hordeum spontaneum C. Koch) with reference to salt tolerance and associated ecogeography. Genome 40:332–341
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Roosens N, Verbruggen N, Meerts P, Ximenez-Embun P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672. doi:10.1046/j.1365-3040.2003.01084.x
Rosielle AA, Hamblin J (1981) Theoretical aspects of selection for yield in stress and non-stress environments. Crop Sci 21:943–946
Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol 13:468–474
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Shavrukov Y, Langridge P, Tester M, Nevo E (2010) Wide genetic diversity of salinity tolerance, sodium exclusion and growth in wild emmer wheat, Triticum dicoccoides. Breed Sci 60:426–435. doi:10.1270/jsbbs.60.426
Shi G, Cai Q (2009) Cadmium tolerance and accumulation in eight potential energy crops. Biotechnol Adv 27:555–561
Skøt L, Sackville Hamilton N, Mizen S, Chorlton K, Thomas I (2002) Molecular genecology of temperature response in Lolium perenne: 2. Association of AFLP markers with ecogeography. Mol Ecol 11:1865–1876
Skøt L, Humphreys MO, Armstead I, Heywood S, Skøt KP, Sanderson R, Thomas ID, Chorlton KH, Hamilton NRS (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.). Mol Breeding 15:233–245
Skøt L, Humphreys J, Humphreys MO, Thorogood D, Gallagher J, Sanderson R, Armstead IP, Thomas ID (2007) Association of candidate genes with flowering time and water-soluble carbohydrate content in Lolium perenne (L.). Genetics 177:535–547
Sun X, Zhang J, Zhang H, Ni Y, Zhang Q, Chen J, Guan Y (2010) The responses of Arabidopsis thaliana to cadmium exposure explored via metabolite profiling. Chemosphere 78:840–845
Sun D, Ren W, Sun G, Peng J (2011) Molecular diversity and association mapping of quantitative traits in Tibetan wild and worldwide originated barley (Hordeum vulgare L.) germplasm. Euphytica 178:31–43
Tan C, Wu Y, Taliaferro CM, Anderson MP, Tauer C, Samuels T (2012) Development of simple sequence repeat markers for bermudagrass from its expressed sequence tag sequences and preexisting sorghum SSR markers. Mol Breeding 29:23–30
Tan C, Wu Y, Taliaferro CM, Bell GE, Martin DL, Smith MW (2014) Development and characterization of genomic SSR markers in Cynodon transvaalensis Burtt-Davy. Mol Genet Genomics 289:523–531. doi:10.1007/s00438-014-0829-1
Tazib T, Kobayashi Y, Ikka T, Zhao C-R, Iuchi S, Kobayashi M, Kimura K, Koyama H (2009) Association mapping of cadmium, copper and hydrogen peroxide tolerance of roots and translocation capacities of cadmium and copper in Arabidopsis thaliana. Physiol Plant 137:235–248. doi:10.1111/j.1399-3054.2009.01286.x
Turgeon AJ (1991) Turfgrass management. Prentice-Hall Inc.
Van Assche F, Clijsters H (1990) A biological test system for the evaluation of the phytotoxicity of metal-contaminated soils. Environ Pollut 66:157–172. doi:10.1016/0269-7491(90)90118-V
Virk PS, Ford-Lloyd BV, Jackson MT, Pooni HS, Clemeno TP, Newbury HJ (1996) Predicting quantitative variation within rice germplasm using molecular markers. Heredity 76:296–304
Wang Z, Yuan X, Zheng Y, Liu J (2009) Molecular identification and genetic analysis for 24 turf-type Cynodon cultivars by Sequence-Related Amplified Polymorphism markers. Sci Hortic 122:461–467
Wang Z, Wu Y, Martin DL, Gao H, Samuels T, Tan C (2010) Identification of vegetatively propagated turf bermudagrass cultivars using simple sequence repeat markers. Crop Sci 50:2103–2111
Wang Z, Liao L, Yuan X, Guo H, Guo A, Liu J (2013) Genetic diversity analysis of Cynodon dactylon (bermudagrass) accessions and cultivars from different countries based on ISSR and SSR markers. Biochem Syst Ecol 46:108–115. doi:10.1016/j.bse.2012.09.001
Xie Y, Liu L, Fu J, Li H (2012) Genetic diversity in Chinese natural zoysiagrass based on inter-simple sequence repeat (ISSR) analysis. Afr J Biotechnol 11:7659–7669
Xie Y, Hu L, Du Z, Sun X, Amombo E, Fan J, Fu J (2014a) Effects of cadmium exposure on growth and metabolic profile of bermudagrass [Cynodon dactylon (L.) Pers.]. PLoS One 9:e115279
Xie Y, Luo H, Hu L, Sun X, Lou Y, Fu J (2014b) Classification of genetic variation for cadmium tolerance in Bermudagrass [Cynodon dactylon (L.) Pers.] using physiological traits and molecular markers. Ecotoxicology 23:1030–1043. doi:10.1007/s10646-014-1247-1
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160
Yu X, Bai G, Luo N, Chen Z, Liu S, Liu J, Warnke SE, Jiang Y (2011) Association of simple sequence repeat (SSR) markers with submergence tolerance in diverse populations of perennial ryegrass. Plant Sci 180:391–398
Acknowledgments
This work was financially supported by the Young Scientists Fund of the National Natural Science Foundation of China (Grant no. 31101563) and National Natural Science Foundation of China (Grant No. 31272194, 31401915).
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Responsible Editor: Juan Barcelo.
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Table S1
The code, name, origin and status of 120 bermudagrass accessions used in this study (PDF 24 kb)
Table S2
Heavy metal concentrations of polluted areas in Hunan province (PDF 13 kb)
Table S3
Characteristics of the 104 SSR primers used for the genetic relationship analysis in 120 bermudagrass accessions (PDF 37 kb)
Table S4
Range of turf quality (TQ), growth rate (GR), total chlorophyll content (Chl t), chlorophyll a content (Chl a), chlorophyll b content (Chl b), transpiration rate (TR) and leaf water content (LWC) for 120 bermudagrass accessions under control (CK) and Cd treatment (Cd) (PDF 19 kb)
Table S5
Cadmium concentrations in 12 bermudagrass accessions (PDF 17 kb)
Figure S1
An example of amplification profiles of SSR marker CDCA693-694 (PDF 234 kb)
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Xie, Y., Sun, X., Ren, J. et al. Genetic diversity and association mapping of cadmium tolerance in bermudagrass [Cynodon dactylon (L.) Pers.]. Plant Soil 390, 307–321 (2015). https://doi.org/10.1007/s11104-015-2391-y
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DOI: https://doi.org/10.1007/s11104-015-2391-y