Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (7): 1832-1848    DOI: 10.1016/S2095-3119(20)63402-5
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Development and application of microsatellite markers within transcription factors in flare tree peony (Paeonia rockii) based on next-generation and single-molecule long-read RNA-seq
LIU Na, CHENG Fang-yun, GUO Xin, ZHONG Yuan
Beijing Advanced Innovation Center for Tree Breeding by Molecular Design/Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding/National Engineering Research Center for Floriculture/Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education/Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

牡丹是起源于中国的具有观赏、药用和食用价值的珍贵作物,其中紫斑牡丹是芍药属中最具代表性的种质之一。EST-SSR标记的开发和应用对于遗传和育种应用具有重要的价值,但芍药属中的EST-SSR资源仍非常有限。在本研究中,我们首先报道了紫斑牡丹中基于下一代(NGS)和单分子长度长(SMLRS)转录组测序的转录因子内SSR标记的开发,从959个与产量相关的候选转录因子内鉴定了包含六种核苷酸重复类型的166个EST-SSR标记,平均每5.83个unigenes包含一个SSR,共有102(61.45 %)对引物在用于RNA-seq的两个品种中产生了扩增产物,其中来自于18个基因家族(AP2、bHLH、HSF等)的58(56.86 %)对引物在连锁作图群体的亲本和8个随机抽选的紫斑牡丹样本中均表现为多态性。通过在37个牡丹样本中的评估,58个 EST-SSR标记表现出了高水平的多态性,PIC值的范围为0.32 到0.91(平均值为0.70),转移性研究表明58对引物在芍药属的7个野生种中的扩增比率为89.66到100%。此外,在62个样本中开展了遗传关系的研究,聚类分析表明主要的聚类和已知的谱系树是基本一致的。综上所述,这些新开发的EST-SSR标记在牡丹种质的保护以及标记辅助选择育种中具有重要的潜在用途。




Abstract  
Tree peonies native to China are a precious crop with ornamental, medicinal and edible oil properties, of which flare tree peony (Paeonia rockii) is one of the most significant germplasms in Paeonia.  The development and application of expressed sequence tag-simple sequence repeat (EST-SSR) markers are very valuable for genetic and breeding applications, but EST-SSR resources for the genus Paeonia are still limited.  In this study, we first reported the development of SSRs within transcription factors (TFs) in P. rockii based on next-generation sequencing (NGS) and single-molecule long-read sequencing (SMLRS).  A total of 166 EST-SSRs containing six nucleotide repeat types were identified from 959 candidate TFs associated with yield, with an average of one SSR per 5.83 unigenes.  In total, 102 (61.45%) pairs of primers produced amplification products in the two RNA-seq cultivars.  Among them, 58 (56.86%) pairs of primers from 18 gene families (AP2, bHLH, HSF, etc.) were identified to be polymorphic both in the parents of a linkage mapping population and in eight randomly selected accessions of P. rockii.  Further, the 58 EST-SSRs indicated a high level of informativeness with PIC values ranging from 0.32 to 0.91 (mean 0.70) after assessment in 37 tree peony accessions.  Transferability studies indicated that the amplification ratio of the 58 pairs of primers ranged from 89.66 to 100% across seven species of Paeonia.  In addition, a genetic relationship study was performed in 62 accessions.  Cluster analysis using the neighbour-joining (NJ) tree demonstrated that major clusters corresponded to the known pedigree trees.  Taken together, these newly developed EST-SSRs have a potential use in the conservation of tree peony germplasm and marker-assisted selection (MAS) breeding.
Keywords:  flare tree peony (Paeonia rockii)        EST-SSR markers        polymorphism        genetic diversity        transferability        genetic relationships  
Received: 06 March 2020   Accepted:
Fund: We gratefully acknowledge Mr. Cheng Xinyun (Beijing Guose Peony Technologies Co., Ltd., China) for his valuable support in maintaining the living plant materials for this study. This work was supported by the National Key Research and Development Project (2019YFD1001500), and the National Natural Science Foundation of China (31471898).
Corresponding Authors:  Correspondence CHENG Fang-yun, E-mail: chengfy8@263.net   
About author:  LIU Na, E-mail: liunapeony@126.com

Cite this article: 

LIU Na, CHENG Fang-yun, GUO Xin, ZHONG Yuan. 2021. Development and application of microsatellite markers within transcription factors in flare tree peony (Paeonia rockii) based on next-generation and single-molecule long-read RNA-seq. Journal of Integrative Agriculture, 20(7): 1832-1848.

Abdel-Ghany S E, Hamilton M, Jacobi J L, Ngam P, Devitt N, Schikey F, Ben-Hur A, Reddy A S N. 2016. A survey of the sorghum transcriptome using single-molecule long reads. Nature Communications, 7, 1–11.
Agarwal M, Shrivastava N, Padh H. 2008. Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Reports, 27, 617–631.
Agarwal S, Khan S. 2019. Genetic diversity of 18 male and 18 female accessions of Jojoba [Simmondsia chinensis (link) Schneider] using EST-SSRs. Meta Gene, 19, 134–141.
Bazzo B R, de Carvalho L M, Carazzolle M F, Pereira G A G, Colombo C A. 2018. Development of novel EST-SSR markers in the macaúba palm (Acrocomia aculeata) using transcriptome sequencing and cross-species transferability in Arecaceae species. BMC Plant Biology, 18, 276.
Biswas M K, Nath U K, Howlader J, Bagchi M, Natarajan S, Kayum M A, Kim H T, Park J I, Kang J G, Nou I S. 2018. Exploration and exploitation of novel SSR markers for candidate transcription factor genes in Lilium Species. Genes, 9, 97.
Blair M W, González L F, Kimani P M, Butare L. 2010. Genetic diversity, inter-gene pool introgression and nutritional quality of common beans (Phaseolus vulgaris L.) from Central Africa. Theoretical and Applied Genetics, 121, 237–248.
Botstein D, White R L, Skolnick M, Davis R W. 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32, 314-331.
Boudchicha R H, Hormaza J I, Benbouza H. 2018. Diversity analysis and genetic relationships among local Algerian fig cultivars (Ficus carica l.) using SSR markers. South African Journal of Botany, 116, 207–215.
Boureima S, Zakaria K, Pauline B K, Mariam K, Ernest T R, Nerbéwendé S, Romaric N K, Hamed O M, Boukaré K, Issa et A, Mahamadou S. 2018. Evaluation of genetic diversity of African eggplant [Solanum aethiopicum (L.) sub sp Kumba] using EST-SSR molecular markers. International Journal of Current Microbiology and Applied Sciences, 7, 2470–2479.
Burow G, Chopra R, Hughes H, Xin Z G, Burke J. 2019. Marker assisted selection in Sorghum using KASP assay for the detection of single nucleotide polymorphism/insertion deletion. Methods in Molecular Biology, 1931, 75–84.
Cai C F, Cheng F Y, Wu J, Zhong Y, Liu G X. 2015. The first high-density genetic map construction in tree peony (Paeonia Sect. Moutan) using genotyping by specific-locus amplified fragment sequencing. PLoS ONE, 10, e0128584.
Cai K, Zhu L F, Zhang K K, Li L, Zhao Z Y, Zeng W, Lin X C. 2019. Development and characterization of EST-SSR markers from RNA-Seq data in Phyllostachys violascens. Frontiers in Plant Science, 10, 50.
Chen C, Begcy K, Liu K, Folsom J J, Wang Z, Zhang C, Walia H. 2016. Heat stress yields a unique MADS box transcription factor in determining seed size and thermal sensitivity. Plant Physiology, 171, 606–622.
Cheng F Y. 2007. Advances in the breeding of tree peonies and a cultivar system for the cultivar group. International Journal of Plant Breeding, 1, 89–104.
Dong M L, Wang Z W, He Q W, Zhao J, Fan Z R, Zhang J F. 2018. Development of EST-SSR markers in Larix principis-rupprechtii Mayr and evaluation of their polymorphism and cross-species amplification. Trees, 32, 1559–1571.
Du Q Z, Gong C R, Pan W, Zhang D Q. 2012a. Development and application of microsatellites in candidate genes related to wood properties in the Chinese white poplar (Populus tomentosa Carr.). DNA Research, 20, 31–44.
Du Q Z, Zhang D Q, Li B L. 2012b. Development of 15 novel microsatellite markers from cellulose synthase genes in Populus tomentosa (Salicaceae). American Journal of Botany, 99, e46–e48.
Ellis J R, Burke J M. 2007. EST-SSRs as a resource for population genetic analyses. Heredity, 99, 125.
Eujayl I, Sledge M K, Wang L, May G D, Chekhovskiy K, Zwonitzer J C, Mian M A R. 2004. Medicago truncatula EST-SSRs reveal cross-species genetic markers for Medicago spp. Theoretical and Applied Genetics, 108, 414–422.
Feller A, Machemer K, Braun E L, Grotewold E. 2011. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. The Plant Journal, 66, 94–116.
Gai S P, Zhang Y X, Mu P, Liu C Y, Liu S, Dong L, Zheng G S. 2012. Transcriptome analysis of tree peony during chilling requirement fulfillment: assembling, annotation and markers discovering. Gene, 497, 256–262.
Gonzaga Z J, Aslam K, Septiningsih E M, Collard B C Y. 2015. Evaluation of SSR and SNP markers for molecular breeding in rice. Plant Breeding and Biotechnology, 3, 139–152.
Guo S Y, Dai S J, Singh P K, Wang H Y, Wang Y N, Tan J L H, Wee W Y, Ito T. 2018. A membrane-bound NAC-like transcription factor OsNTL5 represses the flowering in Oryza sativa. Frontiers in Plant Science, 9, 555.
Gupta S K, Bansal R, Gopalakrishna T. 2014. Development and characterization of genic SSR markers for mungbean (Vigna radiata (L.) Wilczek). Euphytica, 195, 245–258.
Heang D, Sassa H. 2012. Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS ONE, 7, e31325.
He X, Qu B Y, Li W J, Zhao X Q, Teng W, Ma W Y, Ren Y Z, Li B, Li Z S, Tong Y P. 2015. The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiology, 169, 1991–2005.
Hirsch S, Oldroyd G E D. 2009. GRAS-domain transcription factors that regulate plant development. Plant Signaling & Behavior, 4, 698–700.
Hisano H, Sato S, Isobe S, Sasamoto S, Wada T, Matsuno A, Fujishiro T, Yamada M, Nakayama S, Nakamura Y, Watanabe S, Harada K, Tabata S. 2007. Characterization of the soybean genome using EST-derived microsatellite markers. DNA Research, 14, 271–281.
Iorizzo M, Senalik D A, Grzebelus D, Bowman M, Cavagnaro P F, Matvienko M, Ashrafi H, Deynze A V, Simon P W. 2011. De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity. BMC Genomics, 12, 389.
Jofuku K D, Omidyar P K, Gee Z, Okamuro J K. 2005. Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proceedings of the National Academy of Sciences of the United States of America, 102, 3117–3122.
Kantety R V, La Rota M, Matthews D E, Sorrells M E. 2002. Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Molecular Biology, 48, 501–510.
Kaplan-Levy R N, Brewer P B, Quon T, Smyth D R. 2012. The trihelix family of transcription factors - light, stress and development. Trends in Plant Science, 17, 163–171.
Kim H J, Lee H R, Han J H, Yeom S I, Harn C H, Kim B D. 2008. Marker production by PCR amplification with primer pairs from conserved sequences of WRKY genes in chili pepper. Molecules & Cells, 25, 196.
Lande R, Thompson R. 1990. Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics, 124, 743–756.
Li B, Li Q R, Mao X G, Li A, Wang J Y, Chang X P, Hao C Y, Zhang X Y, Jing R L. 2016. Two novel AP2/EREBP transcription factor genes TaPARG have pleiotropic functions on plant architecture and yield-related traits in common wheat. Frontiers in Plant Science, 7, 1191.
Li S S, Yuan R Y, Chen L G, Wang L S, Hao X H, Wang L J, Zheng X C, Du H. 2015. Systematic qualitative and quantitative assessment of fatty acids in the seeds of 60 tree peony (Paeonia section Moutan DC.) cultivars by GC-MS. Food Chemistry, 173, 133–140.
Li S X, Yin T M, Wang M X, Gerald A T. 2011. Characterization of microsatellites in the coding regions of the Populus genome. Molecular Breeding, 27, 59–66.
Li Z X, Qin G W, He J H, Cao X Y. 2010. Comparative analysis of fatty acid composition in seed kernel and coat of Paeonia rockii Seeds. Seed, 29, 34–36. (in Chinese)
Liu H, Sun M, Du D L, Pan H T, Cheng T R, Wang J, Zhang Q X. 2015. Whole-transcriptome analysis of differentially expressed genes in the vegetative buds, floral buds and buds of Chrysanthemum morifolium. PLoS ONE, 10, e0128009.
Liu K J, Muse S V. 2005. PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics, 21, 2128–2129.
Liu N, Cheng F Y. 2020. Association mapping for yield traits in Paeonia rockii based on SSR markers within transcription factors of comparative transcriptome. BMC Plant Biology, 20, 245.
Liu N, Cheng F Y, Zhong Y, Guo X. 2019. Comparative transcriptome and coexpression network analysis of carpel quantitative variation in Paeonia rockii. BMC Genomics, 20, 683.
Liu W X, Jia X T, Liu Z M, Zhang Z S, Wang Y R, Liu Z P, Xie W G. 2015. Development and characterization of transcription factor gene-derived microsatellite (TFGM) markers in Medicago truncatula and their transferability in leguminous and non-leguminous species. Molecules, 20, 8759–8771.
Lu G W, Casaretto J A, Ying S, Mahmood K, Liu F, Bi Y M, Rothstein S J. 2017. Overexpression of OsGATA12 regulates chlorophyll content, delays plant senescence and improves rice yield under high density planting. Plant Molecular Biology, 94, 215–227.
Man W, Zhang L Y, Li X H, Xie X B, Pei W F, Yu J W, Yu S X, Zhang J F. 2016. A comparative transcriptome analysis of two sets of backcross inbred lines differing in lint-yield derived from a Gossypium hirsutum×Gossypium barbadense population. Molecular Genetics Genomics, 291, 1749–1767.
Mishra A K, Puranik S, Prasad M. 2012. Structure and regulatory networks of WD40 protein in plants. Journal of Plant Biochemistry and Biotechnology, 21, 32–9. (in Chinese)
Nelson D E, Repetti P P, Adams T R, Creelman R A, Wu J R, Warner D C, Anstrom D C, Bensen R J, Castiglioni P P, Donnarummo M G, Hinchey B S, Kumimoto R W, Maszie D R, Canales R D, Krolikowski K A, Dotson S B, Gutterson N, Ratcliffe O J, Heard J E. 2007. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences of the United States of America, 104, 16450–16455.
Ning Y S, Liu W D, Wang G L. 2017. Balancing immunity and yield in crop plants. Trends in Plant Science, 22, 1069–1079.
Oh S J, Kim Y S, Kwon C W, Park H K, Jeong J S, Kim J K. 2009. Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiology, 150, 1368–1379.
Van Oosterhout C, Hutchinson W F, Wills D P M, Shipley P. 2004. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538.
Parita B, Kumar S N, Darshan D, Karen P. 2018. Elucidation of genetic diversity among ashwagandha [Withania somnifera (L.) Dunal] genotypes using EST-SSR markers. Research Journal of Biotechnology, 13, 52–59.
Parthiban S, Govindaraj P, Senthilkumar S. 2018. Comparison of relative efficiency of genomic SSR and EST-SSR markers in estimating genetic diversity in sugarcane. 3 Biotech, 8, 144.
Peakall R, Smouse P E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
Peng L P, Cai C F, Zhong Y, Xu X X, Xian H L, Cheng F Y, Mao J F. 2017. Genetic analyses reveal independent domestication origins of the emerging oil crop Paeonia ostii, a tree peony with a long-term cultivation history. Scientific Reports, 7, 5340.
Qu B, He X, Wang J, Zhao Y Y, Teng W, Shao A, Zhao X Q, Ma W Y, Wang J Y, Li B, Li Z S, Tong Y P. 2015. A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiology, 167, 411–423.
Rahaie M, Xue G P, Schenk P M. 2013. The role of transcription factors in wheat under different abiotic stresses. Abiotic Stress-Plant Responses and Applications in Agriculture, 2, 367–385.
Ren D Y, Li Y F, He G H, Qian Q. 2019. Multi-floret spikelet improves rice yield. New Phytologist, doi: 10.1111/NPH.16303.
Reuber T L, Ratcliffe O, Heard J, Riechmann J L, Pineda O, Adam L. 2010. Transcription factors for increasing yield. U.S. Patent, Application No. 7,858,848. Patent and Trademark Office, Washington, D.C., USA.
Rogers A. 1995. Peonies. Timber Press, Portland, USA.
Sahni S, Prasad B D, Liu Q, Grbic B, Sharpe A, Singh S P, Krishna P. 2016. Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Scientific Reports, 6, 28298.
Saini P, Kamboj D, Yadav R C, Yadav N R. 2019. SRAPs and EST-SSRs provide useful molecular diversity for targeting drought and salinity tolerance in Indian mustard. Molecular Biology Reports, 46, 1213–1225.
Shimray P W, Bajaj D, Srivastava R, Daware A, Upadhyaya H D, Kumar R, Bharadwaj C, Tyagi A K, Parida S K. 2017. Identifying transcription factor genes associated with yield traits in chickpea. Plant Molecular Biology Reporter, 35, 562–574.
Singh N, Choudhury D R, Singh A K, Kumar S, Srinivasan K, Tyagi R K, Singh N K, Singh R. 2013. Comparison of SSR and SNP markers in estimation of genetic diversity and population structure of Indian rice varieties. PLoS ONE, 8, e84136.
Slate J, David P, Dodds K G, Veenvliet B A, Glass B C, Broad T E, McEwan J C. 2004. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity, 93, 255.
Srivastava R, Rai K M, Srivastava R. 2018. Plant biosynthetic engineering through transcription regulation: An insight into molecular mechanisms during environmental stress.  In: Varjani S, Parameswaran B, Kumar S, Khare S, eds., Biosynthetic Technology and Environmental Challenges. Energy, Environment, and Sustainability. Springer, Singapore. pp. 51–72.
Stern F C. 1946. A Study of the Genus Paeonia. Royal Horticulture Society, London, England.
Su J, Hu C, Yan X, Jin Z, Chen Q, Guan Q, Wang Y, Zhong D, Jansson C, Wang F, Schnürer A, Sun C. 2015. Expression of barley SUSIBA2 transcription factor yields high-starch low-methane rice. Nature, 523, 602.
Sun J J, Zhou T, Zhang R T, Jia Y, Zhao Y M, Yang J, Zhao G F. 2019. Comparative transcriptome and development of expressed sequence tag-simple sequence repeat markers for two closely related oak species. Journal of Systematics and Evolution, 57, 440–450.
Taheri S, Abdullah T L, Rafii M Y, Harikrishna J A, Werbrouck S P O, Teo C H, Sahebi M, Azizi P. 2019. De novo assembly of transcriptomes, mining, and development of novel EST-SSR markers in Curcuma alismatifolia (Zingiberaceae family) through Illumina sequencing. Scientific Reports, 9, 3047.
Tan C C, Wu Y Q, Taliaferro C M, Anderson M P, Tauer C, Samuels T. 2012. Development of simple sequence repeat markers for bermudagrass from its expressed sequence tag sequences and preexisting sorghum SSR markers. Molecular Breeding, 29, 23–30.
Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S. 2001. Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Research, 11, 1441–1452.
Temnykh S, Park W D, Ayres N, Cartinhour S, Hauck N, Lipovich L, Cho Y G, Ishii T, McCouch S R. 2000. Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theoretical and Applied Genetics, 100, 697–712.
Tian J G, Wang C L, Xia J L, Wu L S, Xu G H, Wu W H, Li D, Qin W C, Han X, Chen Q Y, Jin W W, Tian F. 2019. Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science, 365, 658–664.
Tian X Y, Zheng J W, Jiao Z Y, Zhou J, He K Y, Wang B S, He X D. 2019. Transcriptome sequencing and EST-SSR marker development in Salix babylonica and S. suchowensis. Tree Genetics & Genomes, 15, 9.
Torokeldiev N, Ziehe M, Gailing O, Finkeldey R. 2019. Genetic diversity and structure of natural Juglans regia L. populations in the southern Kyrgyz Republic revealed by nuclear SSR and EST-SSR markers. Tree Genetics & Genomes, 15, 5.
Ukoskit K, Posudsavang G, Pongsiripat N, Chatwachirawong P, Klomsa-ard P, Poomipant P, Tragoonrung S. 2019. Detection and validation of EST-SSR markers associated with sugar-related traits in sugarcane using linkage and as sociation mapping. Genomics, 111, 1–9.
Varshney R K, Graner A, Sorrells M E. 2005. Genic microsatellite markers in plants: features and applications. Trends in Biotechnology, 23, 48–55.
Wang B, Tseng E, Regulski M, Clark T A, Hon T, Jiao Y Y, Lu Z Y, Olson A, Stein J C, Ware D. 2016. Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing. Nature Communications, 7, 11708.
Wang B L, Wang B W, Chen Q Q, Li B L, Zhang D Q. 2011. Identification of SSR loci from transcription factor genes expressed under abiotic stresses in Populus. Scientia Silvae Sinicae, 47, 67–74.
Wang D X, Ma H, Zhang Y L, Duan A A, Li W J, Li Z H. 2013. Paeonia (Paeoniaceae) expressed sequence tag-derived microsatellite markers transferred to Paeonia delavayi. Genetics and Molecular Research, 12, 1278.
Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J J, Zhu X B, Li Y, Li W T, Liu J L, Wang J C, Chen X Q, Qing H, Wang Y P, Liu G F, Wang W M, Li P, Wu X J, et al. 2018. A single transcription factor promotes both yield and immunity in rice. Science, 361, 1026–1028.
Wang Y L, Gao L Y, Yang S Y, Xu Y B, Zhu H Y, Yang L M, Li Q, Hu J B, Sun S R, Ma C S. 2018. Molecular diversity and population structure of oriental thin-skinned melons, Cucumis melo subsp. agrestis, revealed by a set of core SSR markers. Scientia Horticulturae, 229, 59–64.
Wang Z, Yan H W, Fu X N, Li X H, Gao H W. 2013. Development of simple sequence repeat markers and diversity analysis in alfalfa (Medicago sativa L.). Molecular Biology Reports, 40, 3291–3298.
Wang Z Y, Li J, Luo Z X, Huang L F, Chen X L, Fang B P, Li Y J, Chen J Y, Zhang X J. 2011. Characterization and development of EST-derived SSR markers in cultivated sweetpotato (Ipomoea batatas). BMC Plant Biology, 11, 139.
Wright S. 1992. Coefficients of inbreeding and relationship. The American Naturalist, 56, 330–338.
Wu J, Cai C F, Cheng F Y, Cui H L, Zhou H. 2014. Characterisation and development of EST-SSR markers in tree peony using transcriptome sequences. Molecular Breeding, 34, 853–1866.
Wu J, Cheng F Y, Cai C F, Zhong Y, Jie X. 2017. Association mapping for floral traits in cultivated Paeonia rockii based on SSR markers. Molecular Genetics and Genomics, 292, 187–200.
Xiang C G, Duan Y, Li H B, Ma W, Huang S W, Sui X L, Zhang Z H, Wang C L. 2018. A high-density EST-SSR-based genetic map and QTL analysis of dwarf trait in Cucurbita pepo L. International Journal of Molecular Sciences, 19, 3140.
Xu X Y, Zhou C P, Zhang Y, Zhang W Q, Gan X H, Zhang H X, Guo Y, Gan S M. 2018. A novel set of 223 EST-SSR markers in Casuarina L. ex Adans.: polymorphisms, cross-species transferability, and utility for commercial clone genotyping. Tree Genetics & Genomes, 14, 30.
Xu Z C, Peters R J, Weirather J, Luo H M, Liao B S, Zhang X, Zhu Y J, Ji A J, Zhang B, Hu S N, Au K F, Song J Y, Chen S L. 2015. Full-length transcriptome sequences and splice variants obtained by a combination of sequencing platforms applied to different root tissues of Salvia miltiorrhiza and tanshinone biosynthesis. The Plant Journal, 82, 951–961.
Xu Z S, Chen M, Li L C, Ma Y Z. 2011. Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology, 53, 570–585.
Yang J B, Wang M Y, Li W J, He X, Teng W, Ma W Y, Zhao X Q, Hu M Y, Li H, Zhang Y J, Tong Y P. 2019. Reducing expression of a nitrate-responsive bZIP transcription factor increases grain yield and N use in wheat. Plant Biotechnology Journal, 17, 1823–1833.
Yeh F C, Yang R C, Boyle T B, Ye Z H, Mao J X. 1999. POPGENE Version 1.32: The user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Edmonton, AB, Canada.
You X H, Li W, Tao Q C, Sun X F, Tang K X. 2011. At1g65030, a WD40-repeat protein gene regulating seed mass and size in Arabidopsis. Plant Physiology Communications, 47, 715–725.
Yu H P, Cheng F Y, Zhong Y, Cai C F, Wu J, Cui H L. 2013. Development of simple sequence repeat (SSR) markers from Paeonia ostii to study the genetic relationships among tree peonies (Paeoniaceae). Scientia Horticulturae, 164, 58–64.
Yuan J H, Cornille A, Giraud T, Cheng F Y, Hu Y H. 2014. Independent domestications of cultivated tree peonies from different wild peony species. Molecular Ecology, 23, 82–95.
Zeng S H, Xiao G, Guo J, Fei Z J, Xu Y Q, Roe B A, Wang Y. 2010. Development of a EST dataset and characterization of EST-SSRs in a traditional Chinese medicinal plant, Epimedium sagittatum (Sieb. Et Zucc.) Maxim. BMC Genomics, 11, 94.
Zhai L L, Xu L, Wang Y, Cheng H, Chen Y L, Gong Y Q, Liu L W. 2014. Novel and useful genic-SSR markers from de novo transcriptome sequencing of radish (Raphanus sativus L.). Molecular Breeding, 33, 611–624.
Zhang J, Yong H, Xu L, He Q, Fan X W, Xing Y Z. 2017. The CCT domain-containing gene family has large impacts on heading date, regional adaptation, and grain yield in rice. Journal of Integrative Agriculture, 16, 2686–2697.
Zhang J J, Shu Q Y, Liu Z A, Ren H X, Wang L S, Keyser E D. 2012. Two EST-derived marker systems for cultivar identification in tree peony. Plant Cell Reports, 31, 299–310.
Zhang M Y, Fan L, Liu Q Z, Song Y, Wei S W, Zhang S L, Wu J. 2014. A novel set of EST-derived SSR markers for pear and cross-species transferability in Rosaceae. Plant Molecular Biology Reporter, 32, 290–302.
Zhang Y X, Li Y E, Zhang Y, Guan S M, Liu C Y, Zheng G S, Gai S P. 2015. Isolation and characterization of a SOC1-Like gene from tree peony (Paeonia suffruticosa). Plant Molecular Biology Reporter, 33, 855–866.
Zhang Y X, Yu C S, Lin J Z, Liu J, Liu B, Wang J, Huang A B, Li H Y, Zhao T. 2017. OsMPH1 regulates plant height and improves grain yield in rice. PLoS ONE, 12, e0180825.
Zhang Z S, Liu W X, Qi X, Liu Z P, Xie W G, Wang Y R. 2015. Genome-wide identification, expression profiling, and SSR marker development of the bZIP transcription factor family in Medicago truncatula. Biochemical Systematics & Ecology, 61, 218–228.
Zhao X, Zhou Z Q, Lin Q B, Pan K Y, Li M Y. 2008. Phylogenetic analysis of Paeonia sect. Moutan (Paeoniaceae) based on multiple DNA fragments and morphological data. Journal of Systematics and Evolution, 46, 563–572.
Zhou C P, He X D, Li F G, Weng Q J, Yu X L, Wang Y, Li M, Shi J S, Gan S M. 2014. Development of 240 novel EST-SSRs in Eucalyptus L’Hérit. Molecular Breeding, 33, 221–225.
Zhou H, Cheng F Y, Wang R, Zhong Y, He C Y. 2013. Transcriptome comparison reveals key candidate genes responsible for the unusual reblooming trait in tree peonies. PLoS ONE, 8, e79996.
Zhou S F, Wang C R, Yin G H, Zhang Y, Shen X Y, Pennerman K K, Zhang J B, Yan H D, Zhang C L, Zhang X Q, Ren S P, Guo T F, Peng Y, Ma X, Liu W, Yan Y H, Huang L K. 2019. Phylogenetics and diversity analysis of Pennisetum species using Hemarthria EST-SSR markers. Grassland Science, 65, 13–22.
[1] ZHANG Ying, CAO Yu-fen, HUO Hong-liang, XU Jia-yu, TIAN Lu-ming, DONG Xing-guang, QI Dan, LIU Chao. An assessment of the genetic diversity of pear (Pyrus L.) germplasm resources based on the fruit phenotypic traits[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2275-2290.
[2] XU Xin, YE Jun-hua, YANG Ying-ying, LI Ruo-si, LI Zhen, WANG Shan, SUN Yan-fei, ZHANG Meng-chen, XU Qun, FENG Yue, WEI Xing-hua, YANG Yao-long. Genetic diversity analysis and GWAS reveal the adaptive loci of milling and appearance quality of japonica (oryza sativa L.) in Northeast China[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1539-1550.
[3] GUO Yi, GONG Ying, HE Yong-meng, YANG Bai-gao, ZHANG Wei-yi, CHEN Bo-er, HUANG Yong-fu, ZHAO Yong-ju, ZHANG Dan-ping, MA Yue-hui, CHU Ming-xing, E Guang-xin. Investigation of Mitochondrial DNA genetic diversity and phylogeny of goats worldwide[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1830-1837.
[4] May Oo kHINE, brozenká MICHAELA, LIU Yan, Jiban kumar kUNDU, WANG Xi-feng. Molecular diversity of barley yellow dwarf virus-PAV from China and the Czech Republic[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2736-2745.
[5] WU Huai-heng, WAN Peng, HUANG Min-song, LEI Chao-liang. Microsatellites reveal strong genetic structure in the common cutworm, Spodoptera litura[J]. >Journal of Integrative Agriculture, 2019, 18(3): 636-643.
[6] WANG Chen, CHEN Yao-sheng, HAN Jian-lin, MO De-lin, LI Xiu-jin, LIU Xiao-hong. Mitochondrial DNA diversity and origin of indigenous pigs in South China and their contribution to western modern pig breeds[J]. >Journal of Integrative Agriculture, 2019, 18(10): 2338-2350.
[7] SONG Xiao-xia, ZHAO Yan, SONG Chun-yan, LI Chuan-hua, CHEN Ming-jie, HUANG Jian-chun, TAN Qi. Intergenic spacer 1 (IGS1) polymorphism map: A marker for the initial classification of cultivated Lentinula edodes strains in China[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2458-2466.
[8] YANG Hai-long, DONG Le, WANG Hui, LIU Chang-lin, LIU Fang, XIE Chuan-xiao. A simple way to visualize detailed phylogenetic tree of huge genomewide SNP data constructed by SNPhylo[J]. >Journal of Integrative Agriculture, 2018, 17(09): 1972-1978.
[9] LIU Tai-guo, GE Run-jing, MA Yu-tong, LIU Bo, GAO Li, CHEN Wan-quan. Population genetic structure of Chinese Puccinia triticina races based on multi-locus sequences[J]. >Journal of Integrative Agriculture, 2018, 17(08): 1779-1789.
[10] Engin Yol, Seymus Furat, Hari D Upadhyaya, Bulent Uzun. Characterization of groundnut (Arachis hypogaea L.) collection using quantitative and qualitative traits in the Mediterranean Basin[J]. >Journal of Integrative Agriculture, 2018, 17(01): 63-75.
[11] WANG Bao-hua, Daniel J. Ebbole, WANG Zong-hua. The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes[J]. >Journal of Integrative Agriculture, 2017, 16(12): 2746-2760.
[12] WANG Jian, HOU Lu, WANG Ruo-yu, HE Miao-miao, LIU Qing-chang. Genetic diversity and population structure of 288 potato (Solanum tuberosum L.) germplasms revealed by SSR and AFLP markers[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2434-2443.
[13] SHENG Fang, CHEN Shu-ying, TIAN Jia, LI Peng, QIN Xue, WANG Lei, LUO Shu-ping, LI Jiang. Morphological and ISSR molecular markers reveal genetic diversity of wild hawthorns (Crataegus songorica K. Koch.) in Xinjiang, China[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2482-2498.
[14] ZHOU Yu, CHAO Gui-mei, LIU Jia-jia, ZHU Ming-qi, WANG Yang, FENG Bai-li. Genetic diversity of Ustilago hordei in Tibetan areas as revealed by RAPD and SSR[J]. >Journal of Integrative Agriculture, 2016, 15(10): 2299-2308.
[15] Alireza Tarang, Anahita Bakhshizadeh Gashti. The power of microsatellite markers and AFLPs in revealing the genetic diversity of Hashemi aromatic rice from Iran[J]. >Journal of Integrative Agriculture, 2016, 15(06): 1186-1197.
No Suggested Reading articles found!