Abstract
Zoysia japonica Steud. (2n = 4× = 40) is a C4 turfgrass well-adapted for the warm-humid and transitional climatic zones of the USA. Its use is limited to warmer climates because of a relative lack of winter hardiness compared to C3 grasses. Molecular markers associated with this trait would be useful for effective selection of winter hardy germplasm before field testing. A pseudo-F2 mapping population of 175 individuals was developed from crosses between Z. japonica cultivars “Meyer” (freeze-tolerant) and “Victoria” (freeze-susceptible) and used to generate a high-density genetic map of 104 SSR markers and 2359 sequencing-derived SNP markers. The map covers 324 Mbp and 2520 cM as well as the 20 chromosomes for the zoysiagrass haploid genome. Phenotypic data on winter injury, establishment, and turf quality collected in North Carolina and Indiana in 2014–2016 were used in conjunction with this map to identify quantitative trait loci (QTL) associated with winter hardiness. Fifty-six QTL associated with winter injury, establishment, and turf quality were identified over six environments. Twelve of those were identified in two or more environments. Furthermore, seven regions of interest were identified on chromosomes 8, 11, and 13 where co-location of QTL for three or more traits occurred. Within these regions, analysis with NCBI basic local alignment search tool (BLAST) identified proteins related to cold and other abiotic stresses tolerance. These QTL and associated markers could be valuable in implementing marker-assisted selection for winter hardiness in zoysiagrass breeding programs.
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References
Afanador L, Haley SD, Kelly JD (1993) Adoption of a mini-prep DNA extraction method for RAPD marker analysis in common bean. Bean Improv Coop 35:10–11
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25(12):1263–1274. https://doi.org/10.1007/s00299-006-0204-8
Blum A (1988) Plant breeding for stress environments. CRC Press, Inc., Boca Raton
Boer MP, Wright D, Feng L, Podlich DW, Luo L, Cooper M, van Eeuwijk FA (2007) A mixed-model quantitative trait loci (QTL) analysis for multiple-environment trial data using environmental covariables for QTL-by-environment interactions, with an example in maize. Genetics 177(3):1801–1813. https://doi.org/10.1534/genetics.107.071068
Brouwer DJ, Duke SH, Osborn TC (2000) Mapping genetic factors associated with winter hardiness, fall growth, and freezing injury in autotetraploid alfalfa. Crop Sci 40(5):1387–1396. https://doi.org/10.2135/cropsci2000.4051387x
Cai HW, Inoue M, Yuyama N, Nakayama S (2004) An AFLP-based linkage map of zoysiagrass (Zoysia japonica). Plant Breed 123(6):543–548. https://doi.org/10.1111/j.1439-0523.2004.01022.x
Cai HW, Inoue M, Yuyama N, Takahashi W, Hirata M, Sasaki T (2005) Isolation, characterization, and mapping of simple sequence repeat markers in zoysiagrass (Zoysia spp.) Theor Appl Genet 112(1):158–166. https://doi.org/10.1007/s00122-005-0118-9
Chandra A, Milla-Lewis SR, Yu Q (2017) An overview of molecular advances in zoysiagrass. Crop Sci 57(supplement1):S1–S12. https://doi.org/10.2135/cropsci2016.09.0822
Clevenger J, Chavarro C, Pearl SA, Ozias-Akins P, Jackson SA (2015) Single nucleotide polymorphism identification in polyploids: a review, example, and recommendations. Mol Plant 8(6):831–846. https://doi.org/10.1016/j.molp.2015.02.002
Dunn JH, Bughrara SS, Warmund MR, Fresenburg BF (1999) Low temperature tolerance of zoysiagrasses. Hortscience 34:96–99
Elshire R, Glaubitz J, Poland J, Kawamoto K, Buckler E, Mitchell S (2011) A robust, simple genotyping-by-sequencing approach for high diversity species. PLoS One 6(5):e19379. https://doi.org/10.1371/journal.pone.0019379
Espevig T, DaCosta M, Hoffman L, Aamlid TS, Tronsmo AM, Clarke BB, Huang B (2011) Freezing tolerances and carbohydrate changes of two Agrostis species during cold acclimation. Crop Sci 51(3):1188–1197. https://doi.org/10.2135/cropsci2010.07.0415
Forbes I (1952) Chromosome numbers and hybrids in Zoysia. Agron J 44(4):194–199. https://doi.org/10.2134/agronj1952.00021962004400040008x
Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Toth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’(winter)בTremois’(spring) barley map. Theor Appl Genet 108(4):670–680. https://doi.org/10.1007/s00122-003-1468-9
Grau FV, Radko AM (1951) Meyer (Z-52) zoysia. US Golf Assoc J Turf Manag 4(6):30–31
Guo HL, Xuan JP, Liu JX, Zhang YM, Zheng YQ (2012) Association of molecular markers with cold tolerance and green period in zoysiagrass (Zoysia Willd.) Breed Sci 62(4):320–327. https://doi.org/10.1270/jsbbs.62.320
Guo H, Ding W, Chen J, Chen X, Zheng Y, Wang Z, Liu J (2014) Genetic linkage map construction and QTL mapping of salt tolerance traits in zoysiagrass (Zoysia japonica). PLoS One 9(9):e107249. https://doi.org/10.1371/journal.pone.0107249
Hardie DG (1999) Plant protein serine/threonine kinases: classifications and functions. Annu Rev Plant Physiol Plant Mol Biol 50(1):97–131. https://doi.org/10.1146/annurev.arplant.50.1.97
Harris-Schultz KR, Milla-Lewis SR, Brady JA (2012) Transferability of SSR and RGA markers development in Cynodon spp. to Zoysia spp. Plant Mol Biol Rep 30(5):1264–1269. https://doi.org/10.1007/s11105-012-0417-7
Hinton JD, Livingston DP, Miller GL, Peacock CH, Tuong T (2012) Freeze tolerance of nine zoysiagrass cultivars using natural cold acclimation and freeze chambers. Hortscience 47(1):112–115
Hoffman L, DaCosta M, Ebdon JS, Watkins E (2010) Physiological changes during cold acclimation of perennial ryegrass accessions differing in freeze tolerance. Crop Sci 50(3):1037–1047. https://doi.org/10.2135/cropsci2009.06.0293
Huang X, Wang F, Singh R, Reinert JA, Engelke MC, Genovesi AD, Chandra A, Yu Q (2016) Construction of high-resolution genetic maps of Zoysia matrella (L.) Merrill and applications to comparative genomic analysis and QTL mapping of resistance to fall armyworm. BMC Genomics 17(1):562. https://doi.org/10.1186/s12864-016-2969-7
Jansen J (2005) Construction of linkage maps in full-sib families of diploid outbreeding species by minimizing the number of recombinations in hidden inheritance vectors. Genetics 170(4):2013–2025. https://doi.org/10.1534/genetics.105.041822
Jessup RW, Renganayaki K, Reinert JA, Genovesi AD, Engelke MC, Paterson AH, Kamps TL, Schulze S, Howard AN, Biliberto B, Burson BL (2011) Genetic mapping of fall armyworm resistance in Zoysiagrass. Crop Sci 51(4):1774–1783. https://doi.org/10.2135/cropsci2010.09.0553
Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci U S A 93(20):11274–11279. https://doi.org/10.1073/pnas.93.20.11274
Kahraman A, Kusmenoglu I, Aydin N, Aydogan A, Erskine W, Muehlbauer FJ (2004) QTL mapping of winter hardiness genes in lentil. Crop Sci 44(1):13–22. https://doi.org/10.2135/cropsci2004.1300
Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177(3):309–334. https://doi.org/10.1007/s10681-010-0286-9
Kamps TL, Williams NR, Ortega VM, Chamusco KC, Harris-Shultz K, Scully BT, Chase CD (2011) DNA polymorphisms and bermudagrass microsatellite loci and their use in genotype fingerprinting. Crop Sci 51(3):1122–1131. https://doi.org/10.2135/cropsci2010.08.0478
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10(4):493–507. https://doi.org/10.1007/s10142-010-0181-4
Karcher DE, Richardson MD, Landreth JW, McCalla JH Jr (2005) Recovery of zoysiagrass varieties from divot injury. Appl Turf Sci 2(1). https://doi.org/10.1094/ATS-2005-0728-01-RS
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17(3):287–291. https://doi.org/10.1038/7036
Kimball JA, Zuleta MC, Harris-Schultz KR, Kenworthy KE, Lehman VG, Milla-Lewis SR (2013) Genetic relationships in Zoysia and the identification of putative interspecific hybrids using simple sequence repeat markers and inflorescence traits. Crop Sci 53(1):285–295. https://doi.org/10.2135/cropsci2012.04.0218
Lewitt J (1980) Responses of plants to environmental stresses: chilling, freezing, and high temperature stresses, vol 1. Academic Press, New York
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li M, Nana Y, Mariko H, Chen J, Wang Y, Cai HW (2009) Construction of a high-density SSR marker-based linkage map of zoysiagrass (Zoysia japonica Steud). Euphytica 170(3):327–338. https://doi.org/10.1007/s10681-009-9990-8
Ma KH, Jang DH, Dixit A, Chung JW, Lee SY, Lee JR, Kang HK, Kim SM, Park YJ (2007) Characterization of 30 new microsatellite markers, developed from enriched genomic DNA library of zoysiagrass Zoysia japonica Steud. Mol Ecol Notes 7(6):1323–1325. https://doi.org/10.1111/j.1471-8286.2007.01869.x
Margarido GRA, Souza AP, Garcia AAF (2007) OneMap: software for genetic mapping in outcrossing species. Hereditas 144(3):78–79. https://doi.org/10.1111/j.2007.0018-0661.02000.x
Melo AT, Bartaula R, Hale I (2016) GBS-SNP-CROP: a reference-optional pipeline for SNP discovery and plant germplasm characterization using variable length, paired-end genotyping-by-sequencing data. BMC Bioinformatics 17(1):29. https://doi.org/10.1186/s12859-016-0879-y
Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92(5):255–264. https://doi.org/10.1016/j.ygeno.2008.07.001
Mulkey SE, Zuleta MC, Keebler JE, Schaff JE, Milla-Lewis SR (2013) Development and characterization of simple sequence repeat markers for St. Augustinegrass. Crop Sci 54(1):401–412. https://doi.org/10.2135/cropsci2013.04.0246
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10(7):339–346. https://doi.org/10.1016/j.tplants.2005.05.009
National Turfgrass Evaluation Program (NTEP) (2012) National turfgrass evaluation program, Beltsville MD. http://www.ntep.org. Accessed 22 Sept 2016
Ouyang S, Liu Y, Liu P, Lei G, He S, Ma B, Zhang W, Zhang J, Chen S (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62(2):316–329. https://doi.org/10.1111/j.1365-313X.2010.04146.x
Patton AJ, Reicher ZJ (2005) Establishment rates of zoysiagrass cultivars, 2005 Annual Report: Purdue University Turfgrass Science Program, pp 1–7. https://turf.purdue.edu/report/2004/p43.pdf
Patton AJ, Reicher ZJ (2007) Zoysiagrass species and genotypes differ in their winter injury and freeze tolerance. Crop Sci 47(4):1619–1627. https://doi.org/10.2135/cropsci2006.11.0737
Patton AJ, Cunningham S, Volenec J, Reicher Z (2007a) Differences in freeze tolerance of zoysiagrass: I. Role of proteins. Crop Sci 47(5):2162–2169. https://doi.org/10.2135/cropsci2006.11.0739
Patton AJ, Cunningham S, Volenec J, Reicher Z (2007b) Differences in freeze tolerance of zoysiagrasses: II. Carbohydrate and poline accumulation. Crop Sci 47(5):2170–2181. https://doi.org/10.2135/cropsci2006.12.0784
Patton AJ, Schwartz BM, Kenworthy KE (2017) Zoysiagrass (Zoysia spp.) history, utilization, and improvement in the United States: a review. Crop Sci 57:S1–S12. https://doi.org/10.2135/cropsci2017.02.0074
Pinto RS, Lopes MS, Collins NC, Reynolds MP (2016) Modelling and genetic dissection of staygreen under heat stress. Theor Appl Genet 129(11):2055–2074. https://doi.org/10.1007/s00122-016-2757-4
Poland J, Brown PJ, Sorrells ME, Jannink J (2012) Development of high-diversity genetic maps for barley and wheat using a novel two-enzyme genotyping-by sequencing approach. PLoS One 7(2):e32253. https://doi.org/10.1371/journal.pone.0032253
Pruitt HM, Bernstein R, Lu J, DaCosta M, Tuong TD, Arellano C, Livingston DP, Milla-Lewis SR (2017) Proteomic analysis of cold acclimation in Zoysiagrass. Proc. Amer. Soc. Agron. Intl. Ann. Mtg., Tampa, FL. October 22–26
Rogers RA, Dunn JH, Nelson CJ (1975) Cold hardening and carbohydrate composition of Meyer zoysia. Agron J 67(6):836–838. https://doi.org/10.2134/agronj1975.00021962006700060029x
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019
Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3(3):217–223. https://doi.org/10.1016/S1369-5266(00)80068-0
Sladek BS, Henry GM, Auld DL (2009) Evaluation of zoysiagrass genotypes for shade tolerance. Hortscience 44:1447–1451
Sonah H, Bastien M, Iquira E, Tardivel A, Legare G, Boyle B, Normandeau E, Laroche J, Larose S, Jean M, Belzile F (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS One 8(1):e54603. https://doi.org/10.1371/journal.pone.0054603
Steel RGD, Torrie JH, Dickey DA (1997) Principles and procedures of statistics: a biometrical approach. WCB/McGraw-Hill, Boston
Sun X, Yu Q, Tang L, Ji W, Gai H, Liu X, Ding X, Zhu Y (2013) GsSRK, a G-type lectin S-receptor-like serine/threonine protein kinase, is a postitive regulator of plant tolerance to salt stress. J Plant Physiol 170(5):505–515. https://doi.org/10.1016/j.jplph.2012.11.017
Tanaka H, Hirakawa H, Kosugi S, Nakayama S, Ono A, Watanabe A, Hashiguchi M, Gondo T, Ishigaki G, Muguerza M, Shimizu K (2016) Sequencing and comparative analyses of the genomes of zoysiagrasses. DNA Res 23(2):171–180. https://doi.org/10.1093/dnares/dsw006
Tsuruta S, Hashiguchi M, Ebina M, Matsu T, Yamamoto T, Kobayashi M, Takahara M, Nakagawa H, Akashi R (2005) Development and characterization of simple sequence repeat markers in Zoysia japonica Steud. Grassl Sci 51(3):249–257. https://doi.org/10.1111/j.1744-697X.2005.00033.x
Vaid N, Pandey PK, Tuteja N (2012) Genome-wise analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Mol Biol 80(4-5):365–388. https://doi.org/10.1007/z11103-012-9952-8
van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, Software for the calculation of genetic linkage maps. Plant Res Internat, Wageningen, 1–51
Verbyla AP, Eckerman PJ, Thompson R, Cullis BR (2003) The analysis of quantitative trait loci in multi-environment trials using a multiplicative mixed model. Aust J Agric Res 54(12):1395–1408. https://doi.org/10.1071/AR02239
Wang D, Shi J, Carlson SR, Cregan PB, Ward RW, Diers BW (2003) A low-cost, high-throughput polyacrylamide gel electrophoresis system for genotyping with microsatellite DNA markers. Crop Sci 43(5):1828–1832. https://doi.org/10.2135/cropsci2003.1828
Wang XS, Zhu J, Mansueto L, Bruskiewich R (2005) Identification of candidate genes for drought stress tolerance in rice by the integration of a genetic (QTL) map with the rice genome physical map. J Zhejiang Univ Sci 6(5):382–388
Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15(3):745–759. https://doi.org/10.1105/tpc.008714
Yamada T, Jones ES, Cogan NOI, Vecchies AC, Nomura T, Hisano H, Shimamoto Y, Smith KF, Hayward MD, Forster JW (2004) QTL analysis of morphological, developmental, and winter hardiness-associated traits in perennial ryegrass. Crop Sci 44(3):925–935. https://doi.org/10.2135/cropsci2004.9250
Yaneshita M, Kaneko S, Sasakuma T (1999) Allotetraploidy of Zoysia species with 2n=40 based on a RFLP genetic map. Theor Appl Genet 98(5):751–756. https://doi.org/10.1007/s001220051131
Zhang Q, Fry J, Pan X, Rajashekar C, Bremer D, Engelke M, Wang X (2009) Acclimation of Zoysia japonica and Z. matrella and changes in rhizome abscisic acid levels. Int Turfgrass Soc Res J 11:883–892
Zhang W, Chen J, Yang Y, Tang Y, Shang J, Shen B (2011) A practical comparison of de novo genome assembly software tools for next-generation sequencing technologies. PLoS One 6(3):e17915. https://doi.org/10.1371/journal.pone.0017915
Acknowledgements
The authors would like to thank the personnel at the Upper Mountain Research Station (Laurel Springs, NC) and the William H. Daniel Turfgrass Research and Diagnostic Center (West Lafayette, IN) for the help in maintaining research plots. The authors would also like to thank the NCSU Genomic Sciences Laboratory for generation and assembly of zoysiagrass sequencing data. This research was supported in part with funding provided by the North Carolina State University Plant Breeding Consortium, the NCSU Center for Turfgrass Environmental Research and Education, and the United States Golf Association.
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Supplementary Table 1
Analysis of variance for winter injury, establishment, pre-freeze turf quality, and post-freeze turf quality in the Meyer × Victoria mapping population in Laurel Springs, NC and West Lafayette, IN environments from 2014 – 2016 (DOCX 12.9 kb)
Supplementary Table 2
Phenotypic correlations between winter injury, establishment, pre-freeze turf quality, and post-freeze turf quality evaluated in a Meyer × Victoria zoysiagrass mapping population at Laurel Springs, NC and West Lafayette, IN from 2014 – 2016 (DOCX 12.1 kb)
Supplementary Table 3
Single nucleotide polymorphism (SNP) and simple sequence repeat (SSR) marker distribution and coverage in the Meyer × Victoria mapping population. These markers cover all 20 Zoysia japonica chromosomes, totaling 2,463 markers, 324 Mbp and 2520 cM (DOCX 13.6 kb)
Supplementary Table 4
All QTL for zoysiagrass winter injury, establishment, pre-freeze turf quality, and post-freeze turf quality in environments in Laurel Spring, NC and West Lafayette, IN and the combined environments. All QTL were detected at a LOD threshold of 3.5 (DOCX 19.0 kb)
Supplementary Table 5
Distribution of QTL for zoysiagrass winter injury, establishment, pre-freeze turf quality, and post-freeze turf quality in environments in Laurel Spring, NC and West Lafayette, IN and the combined environments over the 20 chromosomes of the Z. japonica map. All QTL were detected at a LOD threshold of 3.5 (DOCX 13.8 kb)
Supplementary Table 6
QTL for zoysiagrass winter injury, establishment, pre-freeze turf quality, and post-freeze turf quality identified in two or more environments in Laurel Spring, NC and West Lafayette, IN or combined environments (DOCX 15.5 kb)
Supplementary Table 7
Annotated sequences identified using the NCBI’s basic local alignment search tool (BLAST) in regions on Z. japonica chromosomes 8, 11, and 13. These regions of interest on were examined using the BLASTx program, and protein coding sequences were identified in all of these regions with total score > 200, E values <10-20, and at least two BLAST hits (DOCX 35.2 kb)
Supplementary Figure 1
Physical map of 2359 SNP markers and 104 SSR markers covering 324 Mbp over the 20 chromosomes of the zoysiagrass genome. Positions (kbp) with multiple markers are condensed to single position (color reference) for better visualization. This condensed map contains 1008 markers (JPEG 155 kb)
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Holloway, H.M.P., Yu, X., Dunne, J.C. et al. A SNP-based high-density linkage map of zoysiagrass (Zoysia japonica Steud.) and its use for the identification of QTL associated with winter hardiness. Mol Breeding 38, 10 (2018). https://doi.org/10.1007/s11032-017-0763-0
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DOI: https://doi.org/10.1007/s11032-017-0763-0