SSR-Linkage map of interspecific populations derived from Gossypium trilobum and Gossypium thurberi and determination of genes harbored with

Pengcheng, Li; Kirungu, Joy Nyangasi; Lu, Hejun; Odongo Magwanga, Richard; Lu, Pu; Cai, Xiaoyan; Zhou, Zhongli; Wang, Xingxing; Hou, Yuqing; Wang, Yuhong; Yanchao, Xu; Peng, Renhai; Cai, Yingfan; Zhou, Yun; Wang, Kunbo; Liu​​, Fang

doi:10.1371/journal.pone.0207271

Article (Scientific journals)

SSR-Linkage map of interspecific populations derived from Gossypium trilobum and Gossypium thurberi and determination of genes harbored with

Pengcheng, Li; Kirungu, Joy Nyangasi; Lu, Hejun et al.

2018 • In PLoS ONE

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/242204

DOI
10.1371/journal.pone.0207271

PubMed
30419064

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Plos ONE.pdf

Publisher postprint (4.15 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

SSR; Gossypium; segregating distortion regions

Abstract :

[en] Wild cotton species have significant agronomic traits that can be introgressed into elite culti- vated varieties. The use of a genetic map is important in exploring, identification and mining genes which carry significant traits. In this study, 188 F2mapping individuals were developed from Gossypium thurberi (female) and Gossypium trilobum (male), and were genotyped by using simple sequence repeat (SSR) markers. A total of 12,560 simple sequence repeat (SSR) markers, developed by Southwest University, thus coded SWU were screened out of which only 994 were found to be polymorphic, and 849 markers were linked in all the 13 chromosomes. The map had a length of 1,012.458 cM with an average marker distance of 1.193 cM. Segregation distortion regions (SDRs) were observed on Chr01, Chr02, Chr06, Chr07 Chr09, Chr10 and Chr11 with a large proportion of the SDR regions segregating towards the heterozygous allele. There was good syntenic block formation that revealed good collinearity between the genetic and physical map of G. raimondii, compared to the Dt_sub genome of the G. hirsutum and G. barbadense. A total of 2,496 genes were mined within the SSR related regions. The proteins encoding the mined genes within the SDR had varied physiochemical properties; their molecular weights ranged from 6.586 to 252.737 kDa, charge range of -39.5 to 52, grand hydropathy value (GRAVY) of -1.177 to 0.936 and isoelectric (pI) value of 4.087 to 12.206. The low GRAVY values detected showed that the proteins encoding these genes were hydrophilic in nature, a property common among the stress responsive genes. The RNA sequence analysis revealed more of the genes were highly upregulated in various stages of fiber development for instance; Gorai.002G241300 was highly up regulated at 5, 10, 20 and 25 day post anthesis (DPA). Validation through RT-qPCR further revealed that these genes mined within the SDR regions might be playing a significant role under fiber development stages, therefore we infer that Gorai.007G347600 (TFCA), Gorai.012G141600 (FOLB1), Gorai.006G024500 (NMD3), Gorai.002G229900 (LST8) and Gorai.002G235200 (NSA2) are significantly important in fiber development and in turn the quality, and further researches needed to be done to elucidate their exact roles in the fiber development process. The construction of the genetic map between the two wild species paves away for the mapping of quantitative trait loci (QTLs) since the average dis- tance between the markers is small, and mining of genes on the SSR regions will provide an insight in identifying key genes that can be introgressed into the cultivated cotton cultivars.

Disciplines :

Agriculture & agronomy

Author, co-author :

Pengcheng, Li ^✱

Kirungu, Joy Nyangasi ^✱

Lu, Hejun ^✱; Université de Liège - ULiège > Terra

Odongo Magwanga, Richard ^✱

Lu, Pu

Cai, Xiaoyan

Zhou, Zhongli

Wang, Xingxing

Hou, Yuqing

Wang, Yuhong

More authors (6 more)

^✱ These authors have contributed equally to this work.

Language :

English

Title :

SSR-Linkage map of interspecific populations derived from Gossypium trilobum and Gossypium thurberi and determination of genes harbored with

Publication date :

29 October 2018

Journal title :

PLoS ONE

eISSN :

1932-6203

Publisher :

Public Library of Science, United States - California

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 12 December 2019

Statistics

Number of views

57 (10 by ULiège)

Number of downloads

13 (6 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Magwanga RO, Lu P, Kirungu JN, Lu H, Wang X, Cai X, et al. Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet. 2018;19. https://doi.org/10.1186/s12863-018-0608-9
Guo W. Gene cloning and molecular breeding to improve fiber qualities in cotton. Chinese Sci Bull. 2003; 48: 709. https://doi.org/10.1360/02wc0463
Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, et al. Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics. 2008; 92: 478–487. https://doi.org/10.1016/j.ygeno.2008.07.013 PMID: 18801424
Wegier A, Piñeyro-Nelson A, Alarcón J, Gálvez-Mariscal A, Álvarez-Buylla ER, Piñero D. Recent long-distance transgene flow into wild populations conforms to historical patterns of gene flow in cotton (Gossypium hirsutum) at its centre of origin. Mol Ecol. 2011; 20: 4182–4194. https://doi.org/10.1111/j.1365294X.2011.05258.x PMID: 21899621
Basbag S, Gencer O. Investigation of some yield and fibre quality characteristics of interspecific hybrid (Gossypium hirsutum L. ?? G. barbadense L.) cotton varieties. Hereditas. 2007; 144: 33–42. https://doi.org/10.1111/j.2007.0018-0661.01962.x PMID: 17567438
Singh C, Kumar V, Prasad I, Patil VR, Rajkumar BK. Response of upland cotton (G.Hirsutum L.) genotypes to drought stress using drought tolerance indices. J Crop Sci Biotechnol. 2016; 19: 53–59. https://doi.org/10.1007/s12892-015-0073-1
Brubaker CL, Brown AHD, Stewart JMD, Kilby MJ, Grace JP. Production of fertile hybrid germplasm with diploid Australian Gossypium species for cotton improvement. Euphytica. 1999; 108: 199–213. https://doi.org/10.1023/A:1003641217653
Wendel JF, Grover CE. Taxonomy and Evolution of the Cotton Genus, Gossypium. 2015; 1–20. https://doi.org/10.2134/agronmonogr57.2013.0020
Kunbo W F WJ, Jinping HUA. Designations for individual genomes and chromosomes in Gossypium. Journal of Cotton Research; 2018; 3–7. https://doi.org/10.1186/s42397-018-0002-1
Kirungu JN, Deng Y, Cai X, Magwanga RO, Zhou Z, Wang X, et al. Simple sequence repeat (SSR) genetic linkage map of D genome diploid cotton derived from an interspecific cross between Gossypium davidsonii and Gossypium klotzschianum. Int J Mol Sci. 2018;19. https://doi.org/10.3390/ijms19010204 PMID: 29324636
Magwanga R, Lu P, Kirungu J, Diouf L, Dong Q, Hu Y, et al. GBS Mapping and Analysis of Genes Conserved between Gossypium tomentosum and Gossypium hirsutum Cotton Cultivars that Respond to Drought Stress at the Seedling Stage of the BC2F2 Generation. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2018; 19: 1614. https://doi.org/10.3390/ijms19061614 PMID: 29848989
Qin H, Guo W, Zhang YM, Zhang T. QTL mapping of yield and fiber traits based on a four-way cross population in Gossypium hirsutum L. Theor Appl Genet. 2008; 117: 883–894. https://doi.org/10.1007/s00122-008-0828-x PMID: 18604518
Sun FD, Zhang JH, Wang SF, Gong WK, Shi YZ, Liu AY, et al. QTL mapping for fiber quality traits across multiple generations and environments in upland cotton. Mol Breed. 2012; 30: 569–582. https://doi.org/10.1007/s11032-011-9645-z
Wang H, Huang C, Guo H, Li X, Zhao W, Dai B. QTL Mapping for Fiber and Yield Traits in Upland Cotton under Multiple Environments. 2015; 1–14. https://doi.org/10.1371/journal.pone.0130742 PMID: 26110526
Tan Z, Zhang Z, Sun X, Li Q, Sun Y, Yang P, et al. Genetic Map Construction and Fiber Quality QTL Mapping Using the CottonSNP80K Array in Upland Cotton. Front Plant Sci. 2018; 9. https://doi.org/10.3389/fpls.2018.00225 PMID: 29535744
Bowman DT, May OL, Calhoun DS. Genetic base of upland cotton cultivars released between 1970 and 1990. Crop Sci. 1996; 36: 577–581. https://doi.org/10.2135/cropsci1996.0011183X003600030008x
Linos AA, Bebeli PJ, Kaltsikes PJ. Cultivar identification in upland cotton using RAPD markers. Aust J Agric Res. 2002; 53: 637–642. https://doi.org/10.1071/AR01129
Magwanga RO, Lu P, Kirungu JN, Diouf L, Dong Q, Hu Y, et al. GBS mapping and analysis of genes conserved between gossypium tomentosum and gossypium hirsutum cotton cultivars that respond to drought stress at the seedling stage of the BC2F2generation. Int J Mol Sci. 2018; 19. https://doi.org/10.3390/ijms19061614 PMID: 29848989
Zhao F, Fang W, Xie D, Zhao Y, Tang Z, Li W, et al. Proteomic identification of differentially expressed proteins in Gossypium thurberi inoculated with cotton Verticillium dahliae. Plant Sci. 2012; 185–186: 176–184. https://doi.org/10.1016/j.plantsci.2011.10.007 PMID: 22325879
Walker GP, Natwick ET. Resistance to silverleaf whitefly, Bemisia argentifolii (Hem., Aleyrodidae), in Gossypium thurberi, a wild cotton species. J Appl Entomol. 2006; 130: 429–436. https://doi.org/10.1111/j.1439-0418.2006.01083.x
Miyazaki J, Stiller WN, Wilson LJ. Identification of host plant resistance to silverleaf whitefly in cotton: Implications for breeding. F Crop Res. 2013; 154: 145–152. https://doi.org/10.1016/j.fcr.2013.08.001
Yu JZ, Kohel RJ, Fang DD, Cho J, Van Deynze a., Ulloa M, et al. A High-Density Simple Sequence Repeat and Single Nucleotide Polymorphism Genetic Map of the Tetraploid Cotton Genome. G3: Genes|Genomes|Genetics. 2012; 2: 43–58. https://doi.org/10.1534/g3.111.001552 PMID: 22384381
Guo Y, Saha S, Yu JZ, Jenkins JN, Kohel RJ, Scheffler BE, et al. BAC-derived SSR markers chromosome locations in cotton. Euphytica. 2008; 161: 361–370. https://doi.org/10.1007/s10681-007-9585-1
Qureshi SN, Saha S, Kantety R V, Jenkins JN. EST-SSR: A New Class of Genetic Markers in Cotton. J Cotton Sci. 2004; 8: 112–123.
Zhang J, Stewart J, Mac. Economical and rapid method for extracting cotton genomic DNA. J Cott Sci. 2000; 4: 193–201.
Boopathi NM, Thiyagu K, Urbi B, Santhoshkumar M, Gopikrishnan A, Aravind S, et al. Marker-assisted breeding as next-generation strategy for genetic improvement of productivity and quality: Can it be realized in cotton? Int J Plant Genomics. 2011;2011. https://doi.org/10.1155/2011/670104 PMID: 21577317
Creste S, Tulmann Neto A, Figueira A. Detection of Single Sequence Repeat Polymorphisms in Denaturing Polyacrylamide Sequencing Gels by Silver Staining. Plant Mol Biol Report. 2001; 19: 299–306. https://doi.org/10.1007/BF02772828
Stam P. Construction of integrated genetic linkage maps by means of a new computer package: Join Map. Plant J. 1993; 3: 739–744. https://doi.org/10.1111/j.1365-313X.1993.00739.x
Voorrips RE. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002; 93: 77–78. https://doi.org/10.1093/jhered/93.1.77 PMID: 12011185
Li W, Lin Z, Zhang X. A Novel Segregation Distortion in Intraspecific Population of Asian Cotton (Gossypium arboretum L.) Detected by Molecular Markers. J Genet Genomics. 2007; 34: 634–640. https://doi.org/10.1016/S1673-8527(07)60072-1 PMID: 17643949
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21: 3674–3676. https://doi.org/10.1093/bioinformatics/bti610 PMID: 16081474
Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol. 2015; 33: 531–537. https://doi.org/10.1038/nbt.3207 PMID: 25893781
Liu X, Zhao B, Zheng HJ, Hu Y, Lu G, Yang CQ, et al. Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Sci Rep. 2015; 5. https://doi.org/10.1038/srep14139 PMID: 26420475
Chabane K, Varshney RK, Graner A, Valkoun J. Generation and exploitation of EST-derived SSR markers for assaying molecular diversity in durum wheat populations. Genet Resour Crop Evol. 2008; 55: 869–881. https://doi.org/10.1007/s10722-007-9292-8
Liang X, Chen X, Hong Y, Liu H, Zhou G, Li S, et al. Utility of EST-derived SSR in cultivated peanut (Arachis hypogaea L.) and Arachis wild species. BMC Plant Biol. 2009; 9. https://doi.org/10.1186/1471-2229-9-35 PMID: 19309524
Kantety R V., La Rota M, Matthews DE, Sorrells ME. Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol. 2002; 48: 501–510. https://doi.org/10.1023/A:1014875206165 PMID: 11999831
Frelichowski JE, Palmer MB, Main D, Tomkins JP, Cantrell RG, Stelly DM, et al. Cotton genome mapping with new microsatellites from Acala “Maxxa” BAC-ends. Mol Genet Genomics. 2006; 275: 479–491. https://doi.org/10.1007/s00438-006-0106-z PMID: 16501995
Liang Z, Yuanda L, Caiping C, Xiangchao T, Xiangdong C, Wei Z, et al. Toward allotetraploid cotton genome assembly: integration of a high-density molecular genetic linkage map with DNA sequence information. BMC Genomics. 2012; 13: 539. https://doi.org/10.1186/1471-2164-13-539 PMID: 23046547
Yu Y, Yuan D, Liang S, Li X, Wang X, Lin Z, et al. Genome structure of cotton revealed by a genome-wide SSR genetic map constructed from a BC1 population between gossypium hirsutum and G. barbadense. BMC Genomics. 2011; 12: 15. https://doi.org/10.1186/1471-2164-12-15 PMID: 21214949
Hu J, Wang L, Li J. Comparison of genomic SSR and EST-SSR markers for estimating genetic diversity in cucumber. Biol Plant. 2011; 55: 577–580. https://doi.org/10.1007/s10535-011-0129-0
Langebartels C, Wohlgemuth H, Kschieschan S, Grün S, Sandermann H. Oxidative burst and cell death in ozone-exposed plants. Plant Physiology and Biochemistry. 2002. pp. 567–575. https://doi.org/10.1016/S0981-9428(02)01416-X
Vanderauwera S, Hoeberichts FA, Breusegem F Van. Hydrogen Peroxide-Responsive Genes in Stress Acclimation and Cell Death. Reactive Oxygen Species in Plant Signaling: Springer. 2009. pp. 149–164. https://doi.org/10.1007/978-3-642-00390-5_9
Liu K, Sun J, Yao L, Yuan Y. Transcriptome analysis reveals critical genes and key pathways for early cotton fiber elongation in Ligon lintless-1 mutant. Genomics. 2012; 100: 42–50. https://doi.org/10.1016/j.ygeno.2012.04.007 PMID: 22576057
Saha B, Borovskii G, Panda SK. Alternative oxidase and plant stress tolerance. Plant signaling & behavior. 2016. p. e1256530. https://doi.org/10.1080/15592324.2016.1256530 PMID: 27830987
Gonzalez FJ, Gelboin H V. Human cytochromes p450: Evolution and cDNA-directed expression. Environmental Health Perspectives. 1992. pp. 81–85. https://doi.org/10.1289/ehp.929881 PMID: 1486867
Schuler MA, Werck-Reichhart D. Functional genomics of P450s. Annu Rev Plant Biol. 2003; 54: 629–667. https://doi.org/10.1146/annurev.arplant.54.031902.134840 PMID: 14503006
Mizutani M, Sato F. Unusual P450 reactions in plant secondary metabolism. Arch Biochem Biophys. 2011; 507: 194–203. https://doi.org/10.1016/j.abb.2010.09.026 PMID: 20920462
Córdoba JM, Chavarro C, Schlueter JA, Jackson SA, Blair MW. Integration of physical and genetic maps of common bean through BAC-derived microsatellite markers. BMC Genomics. 2010; 11. https://doi.org/10.1186/1471-2164-11-436 PMID: 20637113
Hinze LL, Gazave E, Gore MA, Fang DD, Scheffler BE, Yu JZ, et al. Genetic diversity of the two commercial tetraploid cotton species in the gossypium diversity reference set. J Hered. 2016; 107: 274–286. https://doi.org/10.1093/jhered/esw004 PMID: 26774060
Chee P, Draye X, Jiang CX, Decanini L, Delmonte TA, Bredhauer R, et al. Molecular dissection of interspecific variation between Gossypium hirsutum and Gossypium barbadense (cotton) by a backcross-self approach: I. Fiber elongation. Theor Appl Genet. 2005; 111: 757–763. https://doi.org/10.1007/s00122-005-2063-z PMID: 15983756
Dixon DC, Seagull RW, Triplett BA. Changes in the Accumulation of [alpha]- and [beta]-Tubulin Isotypes during Cotton Fiber Development. Plant Physiol. 1994; 105: 1347–1353. https://doi.org/10.1104/PP.105.4.1347 PMID: 12232289
Whittaker DJ, Triplett B a. Gene-specific changes in alpha-tubulin transcript accumulation in developing cotton fibers. Plant Physiol. 1999; 121: 181–8. https://doi.org/10.1104/pp.121.1.181 PMID: 10482673
Li Y, Sun J, Li C, Zhu Y, Xia G. Specific expression of a beta-tubulin gene (GhTub1) in developing cotton fibers. Sci China C Life Sci. 2003; 46: 235–242. https://doi.org/10.1360/03yc9025 ET—2008/09/03 LA—eng PMID: 18763138
Frey M, Chomet P, Glawischnig E, Stettner C, Grün S, Winklmair A, et al. Analysis of a chemical plant defense mechanism in grasses. Science. 1997; 277: 696–9. https://doi.org/10.1126/science.277.5326.696 PMID: 9235894
Magwanga RO, Lu P, Kirungu JN, Dong Q, Hu Y, Zhou Z, et al. Cotton Late Embryogenesis Abundant (LEA2) Genes Promote Root Growth and Confers Drought Stress Tolerance in Transgenic Arabidopsis thaliana. G3 (Bethesda). 2018; g3.200423.2018. https://doi.org/10.1534/g3.118.200423 PMID: 29934376
Magwanga R, Lu P, Kirungu J, Cai X, Zhou Z, Wang X, et al. Whole Genome Analysis of Cyclin Dependent Kinase (CDK) Gene Family in Cotton and Functional Evaluation of the Role of CDKF4 Gene in Drought and Salt Stress Tolerance in Plants. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2018; 19: 2625. https://doi.org/10.3390/ijms19092625 PMID: 30189594
Lu P, Magwanga RO, Lu H, Kirungu JN, Wei Y, Dong Q, et al. A novel G-protein-coupled receptors gene from upland cotton enhances salt stress tolerance in transgenic Arabidopsis. Genes (Basel). 2018; 9. https://doi.org/10.3390/genes9040209 PMID: 29649144
Xu J, Liu L, Xu Y, Chen C, Rong T, Ali F, et al. Development and characterization of simple sequence repeat markers providing genome-wide coverage and high resolution in maize. DNA Res. 2013; 20: 497–509. https://doi.org/10.1093/dnares/dst026 PMID: 23804557
Badigannavar A, Myers GO. Construction of genetic linkage map and QTL analysis for fiber traits in diploid cotton (Gossypium arboreum x Gossypium herbaceum). J Cotton Sci. 2015; 19: 15–26.
Han Z, Wang C, Song X, Guo W, Gou J, Li C, et al. Characteristics, development and mapping of Gossypium hirsutum derived EST-SSRs in allotetraploid cotton. Theor Appl Genet. 2006; 112: 430–439. https://doi.org/10.1007/s00122-005-0142-9 PMID: 16341684
Ma XX, Zhou BL, Lü YH, Guo WZ, Zhang TZ. Simple sequence repeat genetic linkage maps of A-genome diploid cotton (Gossypium arboreum). J Integr Plant Biol. 2008; 50: 491–502. https://doi.org/10.1111/j.1744-7909.2008.00636.x PMID: 18713384
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK. An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts. Euphytica. 2005. pp. 169–196. https://doi.org/10.1007/s10681-005-1681-5
Zhan H, Xu S. Generalized linear mixed model for segregation distortion analysis. BMC Genet. 2011;12. https://doi.org/10.1186/1471-2156-12-12
Xu Y, Zhu L, Xiao J, Huang N, McCouch SR. Chromosomal regions associated with segregation distortion of molecular markers in F2, backcross, doubled haploid, and recombinant inbred populations in rice (Oryza sativa L.). Mol Gen Genet. 1997; 253: 535–545. https://doi.org/10.1007/s004380050355 PMID: 9065686
Liu X, You J, Guo L, Liu X, He Y, Yuan J, et al. Genetic Analysis of Segregation Distortion of SSR Markers in F2 Population of Barley. J Agric Sci. 2011; 3: 172–177. https://doi.org/10.5539/jas.v3n2p172
Manrique-Carpintero NC, Coombs JJ, Veilleux RE, Buell CR, Douches DS. Comparative Analysis of Regions with Distorted Segregation in Three Diploid Populations of Potato. G3: Genes|Genomes|Genetics. 2016; 6: 2617–2628. https://doi.org/10.1534/g3.116.030031 PMID: 27342736
Shi Y, Li W, Li A, Ge R, Zhang B, Li J, et al. Constructing a high-density linkage map for Gossypium hirsutum×Gossypium barbadense and identifying QTLs for lint percentage. J Integr Plant Biol. 2015; 57: 450–467. https://doi.org/10.1111/jipb.12288 PMID: 25263268
Li X, Jin X, Wang H, Zhang X, Lin Z. Structure, evolution, and comparative genomics of tetraploid cotton based on a high-density genetic linkage map. DNA Res. 2016; 23: 283–293. https://doi.org/10.1093/dnares/dsw016 PMID: 27084896
Khan MK, Chen H, Zhou Z, Ilyas MK, Wang X, Cai X, et al. Genome Wide SSR High Density Genetic Map Construction from an Interspecific Cross of Gossypium hirsutum x Gossypium tomentosum. Front Plant Sci. 2016; 7: 436. https://doi.org/10.3389/fpls.2016.00436 PMID: 27148280
Bovill WD, Ma W, Ritter K, Collard BCY, Davis M, Wildermuth GB, et al. Identification of novel QTL for resistance to crown rot in the doubled haploid wheat population “W21MMT70” x “Mendos.” Plant Breed. 2006; 125: 538–543. https://doi.org/10.1111/j.1439-0523.2006.01251.x
Tsilo TJ, Jin Y, Anderson JA. Diagnostic microsatellite markers for the detection of stem rust resistance gene Sr36 in diverse genetic backgrounds of wheat. Crop Sci. 2008; 48: 253–261. https://doi.org/10.2135/cropsci2007.04.0204
Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982; 157: 105–132. https://doi.org/10.1016/0022-2836(82)90515-0 PMID: 7108955
Flagfeldt DB, Siewers V, Huang L, Nielsen J. Characterization of chromosomal integration sites for heterologous gene expression in Saccharomyces cerevisiae. Yeast. 2009; 26: 545–551. https://doi.org/10.1002/yea.1705 PMID: 19681174
Riviere JL, Cabanne F. Animal and plant cytochrome P-450 systems. Biochimie. 1987; 69: 743–752. https://doi.org/10.1016/0300-9084(87)90195-7 PMID: 3120808
Capdevila JH, Falck JR, Dishman E, Karara A. Cytochrome P-450 arachidonate oxygenase. Methods Enzymol. 1990; 187: 385–394. https://doi.org/10.1016/0076-6879(90)87045-5 PMID: 2233355
Van Hans M. DB, Van Robert F. M. GVan Cees A. M. J. J. DH, Punt PJ. Cytochrome P450 enzyme systems in fungi. Fungal Genet Biol. 1998; 23: 1–17. https://doi.org/10.1006/fgbi.1997.1021 PMID: 9501474
Ninsin KD, Tanaka T. Synergism and stability of acetamiprid resistance in a laboratory colony of Plutella xylostella. Pest Manag Sci. 2005; 61: 723–727. https://doi.org/10.1002/ps.1043 PMID: 15776405
Osborn TC, Brouwer DJ, Kidwell KK, Tavoletti S, Bingham ET. Molecular Marker Applications to Genetics and Breeding of Alfalfa. Mol Cell Technol Forage Improv. 1998;cssaspecia: 25–31. https://doi.org/10.2135/cssaspecpub26.c3
Li X, Wang X, Wei Y, Brummer EC. Prevalence of segregation distortion in diploid alfalfa and its implications for genetics and breeding applications. Theor Appl Genet. 2011; 123: 667–679. https://doi.org/10.1007/s00122-011-1617-5 PMID: 21625992
Xu X, Li L, Dong X, Jin W, Melchinger AE, Chen S. Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize. J Exp Bot. 2013; 64: 1083–1096. https://doi.org/10.1093/jxb/ers393 PMID: 23349137