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Journal of Integrative Agriculture  2021, Vol. 20 Issue (5): 1287-1301    DOI: 10.1016/S2095-3119(20)63416-5
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
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High density genetic map and quantitative trait loci (QTLs) associated with petal number and flower diameter identified in tetraploid rose
YU Chao1*, WAN Hui-hua1*, Peter M. BOURKE2, CHENG Bi-xuan1, LUO Le1, PAN Hui-tang1, ZHANG Qi-xiang1, 3 
1 Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding/National Engineering Research Center for Floriculture/Beijing Laboratory of Urban and Rural Ecological Environment/Engineering Research Center of Landscape Environment of Ministry of Education/Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, P.R.China
2 Plant Breeding, Wageningen University & Research, Wageningen 6700 AJ, The Netherlands
3 Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, P.R.China
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摘要  

月季(Rosa cvs.)是世界上最重要的观赏植物之一。现代月季多为四倍体,其减数分裂过程中存在双减数分裂和优先配对,使得传统的连锁分析方法不能适用四倍体月季。因此,四倍体月季遗传图谱的构建工作既迫切又具挑战性。本研究以四倍体月季F1杂交群体为试验材料,通过简化基因组测序的方法构建遗传图谱。共检测到17,382个SNP标记,加上课题组前期开发的440个SSR和AFLP标记,利用GATK中同源四倍体的模型进行基因分型,最终获得6,885个高质量的标记。然后利用polymapR进行遗传连锁分析,构建了四倍体月季的高密度遗传连锁图谱。该图谱包含7个连锁群,6,842个标记,总图距为1,158.90 cM,标记间平均遗传距离为0.18 cM。随后对花瓣数量和花朵直径进行QTL分析,检测到1个与花瓣数量相关的主效QTL (qpnum-3-1),解释表型变异20.18–22.11%。检测到4个与花朵直径相关的QTLs,连续两年的花朵直径数据检测到1个主效QTL(qfdia-2-2)。本研究为现代月季分子标记辅助育种工作奠定基础,同时为其他同源多倍体的遗传分析提供借鉴。




Abstract  

Rose is one of the most important ornamental and economic plants in the world.  Modern rose cultivars are primarily tetraploid, and during meiosis, they may exhibit double reduction or preferential chromosome pairing.  Therefore, the construction of a high density genetic map of tetraploid rose is both challenging and instructive.  In this study, a tetraploid rose population was used to conduct a genetic analysis using genome sequencing.  A total of 17 382 single nucleotide polymorphism (SNP) markers were selected from 2 308 042 detected SNPs.  Combined with 440 previously developed simple sequence repeats (SSR) and amplified fragment length polymorphism (AFLP) markers, a marker dosage of 6 885 high quality markers was successfully assigned by GATK software in the tetraploid model.  These markers were used in the construction of a high density genetic map, containing the expected seven linkage groups with 6 842 markers, a total map length of 1 158.9 cM, and an average inter-marker distance of 0.18 cM.  Quantitative trait locus (QTL) analysis was subsequently performed to characterize the genetic architecture of petal number and flower diameter.  One major QTL (qpnum-3-1) was detected for petal number in three consecutive years, which explained 20.18–22.11% of the variation in petal number.  Four QTLs were detected for flower diameter; the main locus, qfdia-2-2, was identified in two consecutive years.  Our results will benefit the molecular marker-assisted breeding of modern rose cultivars.  In addition, this study provides a guide for the genetic and QTL analysis of autotetraploid plants using sequencing-based genotyping methods. 

Keywords:   rose        tetraploid        genetic linkage map        QTLs  
Received: 19 January 2020   Accepted:
Fund: This research was supported by grants from the National Natural Science Foundation of China (31600565), the Fundamental Research Funds for the Central Public Welfare Research Institutes, China (ZZ13-YQ-053) and the Special Fund for Beijing Common Construction Project, China.  Dr. Peter M. Bourke from Plant Breeding, Wageningen University & Research, The Netherlands, was partly funded through the TKI polyploids project (BO-26.03-009-004 and BO-50-002-022).
Corresponding Authors:  Correspondence ZHANG Qi-xiang, Tel/Fax: +86-10-62336321, E-mail: zqxbjfu@126.com    
About author:  YU Chao, E-mail: yuchao@bjfu.edu.cn; * These authors contributed equally to this study.

Cite this article: 

YU Chao, WAN Hui-hua, Peter M. BOURKE, CHENG Bi-xuan, LUO Le, PAN Hui-tang, ZHANG Qi-xiang . 2021. High density genetic map and quantitative trait loci (QTLs) associated with petal number and flower diameter identified in tetraploid rose. Journal of Integrative Agriculture, 20(5): 1287-1301.

Bajgain P, Rouse M N, Anderson J A. 2016. Comparing genotyping-by-sequencing and single nucleotide polymorphism chip genotyping for quantitative trait loci mapping in wheat. Crop Science, 56, 232–248.
Barabaschi D, Tondelli A, Desiderio F, Volante A, Vaccino P, Vale G, Cattivelli L. 2016. Next generation breeding. Plant Science, 242, 3–13.
Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2134.
Bourke P M, Arens P, Voorrips R E, Esselink G D, Koning-Boucoiran C F, Van’t Westende W P, Santos Leonardo T, Wissink P, Zheng C, van Geest G, Visser R G, Krens F A, Smulders M J, Maliepaard C. 2017. Partial preferential chromosome pairing is genotype dependent in tetraploid rose. The Plant Journal, 90, 330–343.
Bourke P M, Gitonga V W, Voorrips R E, Visser R G F, Krens F A, Maliepaard C. 2018a. Multi-environment QTL analysis of plant and flower morphological traits in tetraploid rose. Theoretical and Applied Genetics, 131, 2055–2069.
Bourke P M, Van G G, Voorrips R E, Jansen J, Kranenburg T, Shahin A, Rgf V, Arens P, Mjm S, Maliepaard C. 2018b. polymapR - linkage analysis and genetic map construction from F1 populations of outcrossing polyploids. Bioinformatics, 34, 3496–3502.
Bourke P M, Voorrips R E, Kranenburg T, Jansen J, Visser R G, Maliepaard C. 2016. Integrating haplotype-specific linkage maps in tetraploid species using SNP markers. Theoretical and Applied Genetics, 129, 1–16.
Bourke P M, Voorrips R E, Visser R G F, Maliepaard C. 2018c. Tools for genetic studies in experimental populations of polyploids. Frontiers in Plant Science, 9, 513.
Carvalho D R A, Koning-Boucoiran C F S, Fanourakis D, Vasconcelos M W, Carvalho S M P, Heuvelink E, Krens F A, Maliepaard C. 2015. QTL analysis for stomatal functioning in tetraploid Rosa×hybrida grown at high relative air humidity and its implications on postharvest longevity. Molecular Breeding, 35, 172.
Chang Y, Ding J, Xu Y, Li D, Zhang W, Li L, Song J. 2018. SLAF-based high-density genetic map construction and QTL mapping for major economic traits in sea urchin Strongylocentrotus intermedius. Scientific Reports, 8, 820.
Crespel L, Chirollet M, Durel C, Zhang D, Meynet J, Gudin S. 2002. Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theoretical and Applied Genetics, 105, 1207–1214.
Debener T, Mattiesch L. 1999. Construction of a genetic linkage map for roses using RAPD and AFLP markers. Theoretical and Applied Genetics, 99, 891–899.
Dugo M L, Satovic Z, Millan T, Cubero J I, Rubiales D, Cabrera A, Torres A M. 2005. Genetic mapping of QTLs controlling horticultural traits in diploid roses. Theoretical and Applied Genetics, 111, 511–520.
Gar O, Sargent D J, Tsai C J, Pleban T, Shalev G, Byrne D H, Zamir D. 2011. An autotetraploid linkage map of rose (Rosa hybrida) validated using the strawberry (Fragaria vesca) genome sequence. PLoS ONE, 6, e20463.
van Geest G, Bourke P M, Voorrips R E, Marasek-Ciolakowska A, Liao Y, Post A, van Meeteren U, Visser R G F, Maliepaard C, Arens P. 2017. An ultra-dense integrated linkage map for hexaploid chrysanthemum enables multi-allelic QTL analysis. Theoretical and Applied Genetics, 130, 2527–2541.
Gerard D, Ferrão L F V, Garcia A A F, Stephens M. 2018. Genotyping polyploids from messy sequencing data. Genetics, 210, 789–807.
Gitonga V W, Stolker R, Koning-Boucoiran C F, Aelaei M, Visser R G, Maliepaard C, Krens F A. 2016. Inheritance and QTL analysis of the determinants of flower color in tetraploid cut roses. Molecular Breeding, 36, 143.
Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, Shalev G, Bar E, Davydov O, Ovadis M, Emanuel M, Wang J, Adam Z, Pichersky E, Lewinsohn E, Zamir D, Vainstein A, Weiss D. 2002. Rose scent: Genomics approach to discovering novel floral fragrance-related genes. The Plant Cell, 14, 2325–2338.
Hackett C A, Boskamp B, Vogogias A, Preedy K F, Milne I. 2017. TetraploidSNPMap: Software for linkage analysis and QTL mapping in autotetraploid populations using SNP dosage data. Journal of Heredity, 108, 438–442.
Hackett C A, Bradshaw J E, Bryan G J. 2014. QTL mapping in autotetraploids using SNP dosage information. Theoretical and Applied Genetics, 127, 1885–1904.
Hackett C A, McLean K, Bryan G J. 2013. Linkage analysis and QTL mapping using SNP dosage data in a tetraploid potato mapping population. PLoS ONE, 8, e63939.
Hibrand Saint-Oyant L, Ruttink T, Hamama L, Kirov I, Lakhwani D, Zhou N N, Bourke P M, Daccord N, Leus L, Schulz D, Van de Geest H, Hesselink T, Van Laere K, Debray K, Balzergue S, Thouroude T, Chastellier A, Jeauffre J, Voisine L, Gaillard S, et al. 2018. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nature Plants, 4, 473–484.
Jiang B, Liu W, Xie D, Peng Q, He X, Lin Y, Liang Z. 2015. High-density genetic map construction and gene mapping of pericarp color in wax gourd using specific-locus amplified fragment (SLAF) sequencing. BMC Genomics, 16, 1035.
Koning-Boucoiran C F S, Esselink G, Vukosavljev M, Westende W P C V T, Gitonga V W, Krens F A, Voorrips R E, Weg W E V D, Schulz D, Debener T, Arens P F P, Smulders M J M. 2015. Using RNA-Seq to assemble a rose transcriptome with more than 13,000 full-length expressed genes and to develop the WagRhSNP 68k Axiom SNP array for rose (Rosa L.). Frontiers in Plant Science, 6, 249.
Koning-Boucoiran C F S, Gitonga V W, Yan Z, Dolstra O, van der Linden C G, van der Schoot J, Uenk G E, Verlinden K, Smulders M J, Krens F A, Maliepaard C. 2012. The mode of inheritance in tetraploid cut roses. Theoretical and Applied Genetics, 125, 591–607.
Lachance J, Tishkoff S A. 2013. SNP ascertainment bias in population genetic analyses: Why it is important, and how to correct it. BioEssays, 35, 780–786.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25, 1754–1760.
Li X, Wei Y, Acharya A, Jiang Q, Kang J, Brummer E C. 2014. A saturated genetic linkage map of autotetraploid alfalfa (Medicago sativa L.) developed using genotyping-by-sequencing is highly syntenous with the Medicago truncatula genome. G3 (Bethesda), 4, 1971–1979.
Lin H, Leng H, Guo Y S, Kondo S, Zhao Y H, Shi G L, Guo X W. 2019. QTLs and candidate genes for downy mildew resistance conferred by interspeci?c grape (V. vinifera L. × V. amurensis Rupr.) crossing. Scientia Horticulturae, 244, 200–207.
Linde M, Debener T. 2003. Isolation and identification of eight races of powdery mildew of roses (Podosphaera pannosa) (Wallr.: Fr.) de Bary and the genetic analysis of the resistance gene Rpp1. Theoretical and Applied Genetics, 107, 256–262.
Linde M, Hattendorf A, Kaufmann H, Debener T. 2006. Powdery mildew resistance in roses: QTL mapping in different environments using selective genotyping. Theoretical and Applied Genetics, 113, 1081–1092.
Malek B V, Weber W, Debener T. 2000. Identification of molecular markers linked to Rdr1, a gene conferring resistance to blackspot in roses. Theoretical and Applied Genetics, 101, 977–983.
Mccouch S R, Chen X, Panaud O, Temnykh S, Xu Y, Yong G C, Ning H, Ishii T, Blair M. 1997. Microsatellite marker development, mapping and applications in rice genetics and breeding. In: Sasaki T, Moore G, eds., Oryza: From Molecule to Plant. Springer, Dordrecht. pp. 89–99.
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M A. 2010. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297–1303.
Peace C, Bassil N, Main D, Ficklin S, Rosyara U R, Stegmeir T, Sebolt A, Gilmore B, Lawley C, Mockler T C. 2012. Development and evaluation of a genome-wide 6K SNP array for diploid sweet cherry and tetraploid sour cherry. PLoS ONE, 7, e48305.
Preedy K F, Hackett C A. 2016. A rapid marker ordering approach for high-density genetic linkage maps in experimental autotetraploid populations using multidimensional scaling. Theoretical and Applied Genetics, 129, 2117–2132.
R Development Core Team. 2013. R: A language and environment for statistical computing. Version 3.5.1. R Foundation for Statistical Computing, Vienna, Austria.
Rajapakse S, Byrne D H, Zhang L, Anderson N, Arumuganathan K, Ballard R E. 2001. Two genetic linkage maps of tetraploid roses. Theoretical and Applied Genetics, 103, 575–583.
Scheben A, Batley J, Edwards D. 2016. Genotyping by sequencing approaches to characterise crop genomes: Choosing the right tool for the right application. Plant Biotechnology Journal, 15, 149–161.
Senthilvel S, Ghosh A, Shaik M, Shaw R K, Bagali P G. 2019. Development and validation of an SNP genotyping array and construction of a high-density linkage map in castor. Scientific Reports, 9, 3003.
Shupert D A, Byrne D H, Pemberton H B. 2007. Inheritance of flower traits, leaflet number and prickles in roses. Acta Horticulturae, 751, 331–335.
Smulders M J M, Arens P, Bourke P M, Debener T, Linde M, Riek J, Leus L, Ruttink T, Baudino S, Hibrand-Saint Oyant L, Clotault J, Foucher F. 2019. In the name of the rose: A roadmap for rose research in the genome era. Horticulture Research, 6, 65.
Spiller M, Linde M, Hibrand-Saint Oyant L, Tsai C J, Byrne D H, Smulders M J, Foucher F, Debener T. 2011. Towards a unified genetic map for diploid roses. Theoretical and Applied Genetics, 122, 489–500.
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H. 2013. SLAF-seq: An efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS ONE, 8, e58700.
UitdeWilligen J G, Wolters A A, Dhoop B B, Borm T J, Visser R G, Van Eck H J. 2013. A next-generation sequencing method for genotyping-by sequencing of highly heterozygous autotetraploid potato. PLoS ONE, 8, e62355.
Voorrips R E, Gort G, Vosman B. 2011. Genotype calling in tetraploid species from bi-allelic marker data using mixture models. BMC Bioinformatics, 12, 172.
Vukosavljev M, Arens P, Voorrips R E, van’t Westende W P, Esselink G D, Bourke P M, Cox P, van de Weg W E, Visser R G, Maliepaard C, Smulders M J. 2016. High-density SNP-based genetic maps for the parents of an outcrossed and a selfed tetraploid garden rose cross, inferred from admixed progeny using the 68k rose SNP array. Horticulture Research, 3, 16052.
Xu Q, Wen X, Deng X. 2005. Isolation of TIR and nonTIR NBS–LRR resistance gene analogues and identification of molecular markers linked to a powdery mildew resistance locus in chestnut rose (Rosa roxburghii Tratt). Theoretical and Applied Genetics, 111, 819–830.
Yan M, Byrne D H, Klein P E, Yang J, Dong Q, Anderson N. 2018. Genotyping-by-sequencing application on diploid rose and a resulting high-density SNP-based consensus map. Horticulture Research, 5, 17.
Yan Z, Bai Y L, Silva J A T D, Teixeira D S J A. 2006. Molecular markers and their use in genetic studies in rose. In: Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues. Global Science Books, Japan. pp. 498–503.
Yan Z, Denneboom C, Hattendorf A, Dolstra O, Debener T, Stam P, Visser P B. 2005. Construction of an integrated map of rose with AFLP, SSR, PK, RGA, RFLP, SCAR and morphological markers. Theoretical and Applied Genetics, 110, 766–77.
Ying J Z, Ma M, Bai C, Huang X H, Liu J L, Fan Y Y, Song X J. 2018. TGW3, a major QTL that negatively modulates grain length and weight in rice. Molecular Plant, 11, 750–753.
Yu C. 2015. Construction of a genetic linkage map and qtls analysis for phenotypic traits in tetraploid roses. Ph D thesis, Beijing Forestry University, China. (in Chinese)
Yu C, Luo L, Pan H, Guo X, Wan H, Zhang Q. 2014. Filling gaps with construction of a genetic linkage map in tetraploid roses. Frontiers in Plant Science, 5, 796.
Zhang J, Zhang Q, Cheng T, Yang W, Pan H, Zhong J, Huang L, Liu E. 2015. High-density genetic map construction and identification of a locus controlling weeping trait in an ornamental woody plant (Prunus mume Sieb. et Zucc). DNA Research, 22, 183–191.
Zhang L H, Byrne D H, Ballard R E, Rajapakse S. 2006. Microsatellite marker development in rose and its application in tetraploid mapping. Journal of the American Society for Horticultural Science, 131, 380–387.
Zhao J H, Xu Y H, Li H X, Yin Y, An W, Li Y L, Wang Y J, Fan Y F, Wan R, Guo X, Cao Y L. 2019. A SNP-based high-density genetic map of leaf and fruit related quantitative trait loci in wolfberry (Lycium Linn.). Frontiers in Plant Science, 10, 977.
Zhao X, Huang L, Zhang X, Wang J, Yan D, Li J, Tang L, Li X, Shi T. 2016. Construction of high-density genetic linkage map and identification of flowering-time QTLs in orchardgrass using SSRs and SLAF-seq. Scientific Reports, 6, 29345.
Zheng C, Voorrips R, Jansen J, Hackett C A, Ho J, Bink M C A M. 2016. Probabilistic multilocus haplotype reconstruction in outcrossing tetraploids. Genetics, 203, 119–131.
Zhuang W J, Chen H, Yang M, Wang J P, Pandey M K, Zhang C, Chang W C, Zhang L S, Zhang X T, Tang R H, Garg V, Wang X J, Tang H B, Chow C N, Wang J P, Deng Y, Wang D P, Khan A W, Yang Q, Cai T C, et al . 2019. The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nature Genetics, 51, 865–876.
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