Theoretical and Applied Genetics

, Volume 132, Issue 8, pp 2413–2423 | Cite as

The anther-specific CYP704B is potentially responsible for MSG26 male sterility in barley

  • Juan Qi
  • Fei NiEmail author
  • Xiao Wang
  • Meng Sun
  • Yu Cui
  • Jiajie Wu
  • Allan Caplan
  • Daolin FuEmail author
Original Article


Key message

Plant male sterility is a valuable trait in breeding and hybrid seed production. The barley male-sterility gene msg26 was mapped to a 0.02-cM region that anchors to a 506-kb low-quality assembly between two cleaved amplified polymorphic sequence (CAPS) markers, SP1M14 and SP1M49. The barley gene HORVU4Hr1G074840, which encodes a putative cytochrome P450 CYP704B protein, appears to be a strong candidate for the MSG26 trait.


Barley (Hordeum vulgare L.) is an important cereal crop worldwide. Traditional breeding in barley is time-consuming and labor-intensive. The use of male-sterile genotypes may significantly improve the efficacy of hybrid breeding and seed production. The barley accession ‘GSHO745’ is a spontaneous male-sterile mutant from the barley variety, ‘Unitan’. The male sterility in ‘GSHO745’ is controlled by the recessive gene, msg26 (originally named as ms-u). We revealed that the barley plants homozygous for msg26 proceeded normally through Meiosis II until the tetrad stage, but became fully defective in the late uninucleate microspores and developed pollen-less anthers. Using seven barley F2 populations, we mapped MSG26 to a 0.02-cM region that anchored to a 506-kb low-quality assembly between two cleaved amplified polymorphic sequence markers, SP1M14 and SP1M49. The HORVU4Hr1G074840 gene that encodes a putative cytochrome P450 protein (CYP704B) was identified as the most plausible candidate for MSG26. First, HORVU4Hr1G074840 is located in a collinear region of the rice CYP704B2 and the maize CYP704B1. Both of these genes are essential for male gamete production. Second, the male-sterile allele of HORVU4Hr1G074840 in GSHO745 contained a 4-bp deletion in the last exon. The resulting frame shift causes a Gly436Gln substitution, scrambles the sequence of the remainder of the protein, and forms a new termination site at the 70th triplet of the shifted reading frame. We thus called the variant protein CYP704B:p.G436Qfs*70. Third, the barley HORVU4Hr1G074840 gene was specifically expressed in anthers. Altogether, HORVU4Hr1G074840 represents a strong candidate for MSG26 in barley.



This work was supported by the China Research and Development Initiative on Genetically Modified Plants (2016ZX08009003-001-006), the National Key Research and Development Program of China (2016YFD0100604), and by the Hatch project IDA01587 from the USDA National Institute of Food and Agriculture.

Compliance with ethical standards

Conflict of interest

All authors declare no competing financial interests.

Supplementary material

122_2019_3363_MOESM1_ESM.jpg (277 kb)
Fig. S1 Pollen grains of the Msg26 heterozygous plant. Pollen grains of an F1 plant (derived from GSHO745/Morex, genotype Msg26 msg26) were colored by Alexander’s stain (Alexander 1969). Scale bar = 50 μm. (JPEG 276 kb)
122_2019_3363_MOESM2_ESM.jpg (234 kb)
Fig. S2 MSG26 region collinearity between barley, maize, and rice. a-c) Physical map in rice, barley, and maize, respectively. The collinear regions between HORVU4Hr1G074720 and HORVU4Hr1G074810 are 49.3 kb in rice (a), 457.9 kb in barley (b), and 219.6 kb in maize (c). Due to space limitations, a short name of the barley genes was used on the maps, for example 4Hr1G074790 for HORVU4Hr1G074790. The most promising candidate is highlighted by an asterisk symbol. The following genes are collinear: 1) HORVU4Hr1G074720 (or SP1M14), Os03t0167800, Zm00001d027827; 2) HORVU4Hr1G074790, Os03t0168400, and Zm00001d027835; 3) HORVU4Hr1G074830, Os03t0168550, and Zm00001d027843; 4) HORVU4Hr1G074840, Os03t0168600, and Zm00001d027837; 5) HORVU4Hr1G074850, Os03t0168700, and Zm00001d027838; and 6) HORVU4Hr1G074810 (or SP1M4), Os03t0169100, and Zm00001d027841. (JPEG 234 kb)
122_2019_3363_MOESM3_ESM.jpg (187 kb)
Fig. S3 Expression of wheat collinear genes in the MSG26 region. The expression data were extracted from the wheat RNA-Seq databases (Ramírez-González et al. 2018). The X-axis separated different tissues, including roots (at the flag-leaf stage), stems, leaves, and spikes (at the booting stage) and grains (at the milk stage). The Y-axis represented the expression count. Expression counts were normalized using the variance stabilizing transformation in DESeq2 (Love et al. 2014). (JPEG 186 kb)
122_2019_3363_MOESM4_ESM.docx (31 kb)
Supplementary material 4 (DOCX 31 kb)


  1. Ahokas H (1979) Cytoplasmic male sterility in barley. III. Maintenance of sterility and restoration of fertility in the msm1 cytoplasm. Euphytica 28:409–419CrossRefGoogle Scholar
  2. Ahokas H (1980) Cytoplasmic male sterility in barley. VII. Nuclear genes for restoration. Theor Appl Genet 57:193–202CrossRefGoogle Scholar
  3. Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122CrossRefGoogle Scholar
  4. Amiruzzaman M, Bhuiyan MSA, Uddin S (2003) Heterosis and genetic variability in relation to genetic divergence in barley (Hordeum vulgare L.). Bangladesh J Bot 32:33–37Google Scholar
  5. Andrews S (2010) FASTQC: A quality control tool for high throughput sequence data.
  6. Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J, Pozniak CJ, Choulet F, Distelfeld A, Poland J, Ronen G, Sharpe AG, Barad O, Baruch K, Keeble-Gagnère G, Mascher M, Ben-Zvi G, Josselin A-A, Himmelbach A, Balfourier F, Gutierrez-Gonzalez J, Hayden M, Koh C, Muehlbauer G, Pasam RK, Paux E, Rigault P, Tibbits J, Tiwari V, Spannagl M, Lang D, Gundlach H, Haberer G, Mayer KFX, Ormanbekova D, Prade V, Šimková H, Wicker T, Swarbreck D, Rimbert H, Felder M, Guilhot N, Kaithakottil G, Keilwagen J, Leroy P, Lux T, Twardziok S, Venturini L, Juhász A, Abrouk M, Fischer I, Uauy C, Borrill P, Ramirez-Gonzalez RH, Arnaud D, Chalabi S, Chalhoub B, Cory A, Datla R, Davey MW, Jacobs J, Robinson SJ, Steuernagel B, van Ex F, Wulff BBH, Benhamed M, Bendahmane A, Concia L, Latrasse D, Bartoš J, Bellec A, Berges H, Doležel J, Frenkel Z, Gill B, Korol A, Letellier T, Olsen O-A, Singh K, Valárik M, van der Vossen E, Vautrin S, Weining S, Fahima T, Glikson V, Raats D, Číhalíková J, Toegelová H, Vrána J, Sourdille P, Darrier B, Barabaschi D, Cattivelli L, Hernandez P, Galvez S, Budak H, Jones JDG, Witek K, Yu G, Small I, Melonek J, Zhou R, Belova T, Kanyuka K, King R, Nilsen K, Walkowiak S, Cuthbert R, Knox R, Wiebe K, Xiang D, Rohde A, Golds T, Čížková J, Akpinar BA, Biyiklioglu S, Gao L, N’Daiye A, Kubaláková M, Šafář J, Alfama F, Adam-Blondon A-F, Flores R, Guerche C, Loaec M, Quesneville H, Condie J, Ens J, Maclachlan R, Tan Y, Alberti A, Aury J-M, Barbe V, Couloux A, Cruaud C, Labadie K, Mangenot S, Wincker P, Kaur G, Luo M, Sehgal S, Chhuneja P, Gupta OP, Jindal S, Kaur P, Malik P, Sharma P, Yadav B, Singh NK, Khurana JP, Chaudhary C, Khurana P, Kumar V, Mahato A, Mathur S, Sevanthi A, Sharma N, Tomar RS, Holušová K, Plíhal O, Clark MD, Heavens D, Kettleborough G, Wright J, Balcárková B, Hu Y, Salina E, Ravin N, Skryabin K, Beletsky A, Kadnikov V, Mardanov A, Nesterov M, Rakitin A, Sergeeva E, Handa H, Kanamori H, Katagiri S, Kobayashi F, Nasuda S, Tanaka T, Wu J, Cattonaro F, Jiumeng M, Kugler K, Pfeifer M, Sandve S, Xun X, Zhan B, Batley J, Bayer PE, Edwards D, Hayashi S, Tulpová Z, Visendi P, Cui L, Du X, Feng K, Nie X, Tong W, Wang L (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191CrossRefGoogle Scholar
  7. Bernhard T, Friedt W, Snowdon RJ, Wittkop B (2017a) New insights into genotypic thermodependency of cytoplasmic male sterility for hybrid barley breeding. Plant Breed 136:8–17CrossRefGoogle Scholar
  8. Bernhard T, Friedt W, Voss-Fels KP, Frisch M, Snowdon RJ, Wittkop B (2017b) Heterosis for biomass and grain yield facilitates breeding of productive dual-purpose winter barley hybrids. Crop Sci 57:2405–2418CrossRefGoogle Scholar
  9. Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112CrossRefGoogle Scholar
  10. Bohra A, Jha UC, Adhimoolam P, Bisht D, Singh NP (2016) Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep 35:967–993CrossRefGoogle Scholar
  11. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  12. Browne RG, Iacuone S, Li SF, Dolferus R, Parish RW (2018) Anther morphological development and stage determination in Triticum aestivum. Front Plant Sci 9:228CrossRefGoogle Scholar
  13. Carr DH, Walker JE (1961) Carbol fuchsin as a stain for human chromosomes. Stain Technol 36:233–236CrossRefGoogle Scholar
  14. Chang Z, Chen Z, Wang N, Xie G, Lu J, Yan W, Zhou J, Tang X, Deng XW (2016) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci 113:14145–14150CrossRefGoogle Scholar
  15. Chayut N, Yuan H, Ohali S, Meir A, Yeselson Y, Portnoy V, Zheng Y, Fei Z, Lewinsohn E, Katzir N, Schaffer AA, Gepstein S, Burger J, Li L, Tadmor Y (2015) A bulk segregant transcriptome analysis reveals metabolic and cellular processes associated with Orange allelic variation and fruit -carotene accumulation in melon fruit. BMC Plant Biol 15:274CrossRefGoogle Scholar
  16. Cigan AM, Singh M, Benn G, Feigenbutz L, Kumar M, Cho M-J, Svitashev S, Young J (2017) Targeted mutagenesis of a conserved anther-expressed P450 gene confers male sterility in monocots. Plant Biotechnol J 15:379–389CrossRefGoogle Scholar
  17. Dai F, Wang X, Zhang X-Q, Chen Z, Nevo E, Jin G, Wu D, Li C, Zhang G (2018) Assembly and analysis of a qingke reference genome demonstrate its close genetic relation to modern cultivated barley. Plant Biotechnol J 16:760–770CrossRefGoogle Scholar
  18. den Dunnen JT, Dalgleish R, Maglott DR, Hart RK, Greenblatt MS, McGowan-Jordan J, Roux A-F, Smith T, Antonarakis SE, Taschner PEM (2016) HGVS recommendations for the description of sequence variants: 2016 update. Hum Mutat 37:564–569CrossRefGoogle Scholar
  19. Deng J, Gao Z (1980) The use of a dominant male-sterile gene in wheat breeding. Acta Agron Sin 6:85–98 (in Chinese) Google Scholar
  20. Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Carl Falco S, Jantz D, Alexander Lyznik L (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76:888–899CrossRefGoogle Scholar
  21. Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Møller BL, Preuss D (2009) CYP704B1 is a long-chain fatty acid ω-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589CrossRefGoogle Scholar
  22. Einfeldt CHP, Ceccarelli S, Grando S, Gland-Zwerger A, Geiger HH (2005) Heterosis and mixing effects in barley under drought stress. Plant Breed 124:350–355CrossRefGoogle Scholar
  23. Falk DE (2010) Generating and maintaining diversity at the elite level in crop breeding. Genome 53:982–991CrossRefGoogle Scholar
  24. Fox T, DeBruin J, Haug Collet K, Trimnell M, Clapp J, Leonard A, Li B, Scolaro E, Collinson S, Glassman K, Miller M, Schussler J, Dolan D, Liu L, Gho C, Albertsen M, Loussaert D, Shen B (2017) A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnol J 15:942–952CrossRefGoogle Scholar
  25. Franckowiak JD (1988) Mapping four male sterile genes on chromosome 1. Barley Newsl 31:111Google Scholar
  26. Franckowiak JD (1995) Notes on linkage drag in Bowman backcross derived lines of spring barley. Barley Genet Newsl 24:63–70Google Scholar
  27. Franckowiak JD, Lundqvist U (2010) Descriptions of barley genetic stocks for 2010. Barley Genet Newsl 40:45–177Google Scholar
  28. Gebrekidan B, Rasmusson DC (1970) Evaluating parental cultivars for use in hybrids and heterosis in barley. Crop Sci 10:500–502CrossRefGoogle Scholar
  29. Hagberg A (1953) Heterosis in barley. Hereditas 39:325–348CrossRefGoogle Scholar
  30. Hockett EA (1974) The genetic male sterile barley collection. Barley Genet Newsl 4:121–123Google Scholar
  31. Hockett EA, Eslick RF (1969) Genetic male-sterile genes useful in hybrid barley production. In: Nilan RA (ed) Barley genetics II: proceedings of second international barley genetics symposium. Washington State University Press, Pullman, pp 298–307Google Scholar
  32. Hockett EA, Eslick RF, Reid DA, Wiebe GA (1968) Genetic male sterility in barley. II. Available spring and winter stocks. Crop Sci 8:754–755CrossRefGoogle Scholar
  33. IBSC (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716CrossRefGoogle Scholar
  34. Ji X, Shiran B, Wan J, Lewis DC, Jenkins CLD, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ 33:926–942CrossRefGoogle Scholar
  35. Ji J, Yang L, Fang Z, Zhuang M, Zhang Y, Lv H, Liu Y, Li Z (2017) Recessive male sterility in cabbage (Brassica oleracea var. capitata) caused by loss of function of BoCYP704B1 due to the insertion of a LTR-retrotransposon. Theor Appl Genet 130:1441–1451CrossRefGoogle Scholar
  36. Kaul MLH (ed) (1988) Male sterility in higher plants. Springer, BerlinGoogle Scholar
  37. Kawahara Y, de la Bastide M, Hamilton J, Kanamori H, McCombie W, Ouyang S, Schwartz D, Tanaka T, Wu J, Zhou S, Childs K, Davidson R, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee S, Kim J, Numa H, Itoh T, Buell C, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:1–10CrossRefGoogle Scholar
  38. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357CrossRefGoogle Scholar
  39. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190CrossRefGoogle Scholar
  40. Linde-Laursen I, Heslop-Harrison JS, Shepherd KW, Taketa S (1997) The barley genome and its relationship with the wheat genomes. A survey with an internationally agreed recommendation for barley chromosome nomenclature. Hereditas 126:1–16CrossRefGoogle Scholar
  41. Liu S, Yeh C-T, Tang HM, Nettleton D, Schnable PS (2012) Gene mapping via bulked segregant RNA-Seq (BSR-Seq). PLoS ONE 7:e36406CrossRefGoogle Scholar
  42. Liu X, Bi B, Xu X, Li B, Tian S, Wang J, Zhang H, Wang G, Han Y, McElroy JS (2019) Rapid identification of a candidate nicosulfuron sensitivity gene (Nss) in maize (Zea mays L.) via combining bulked segregant analysis and RNA-seq. Theor Appl Genet 132:1351–1361CrossRefGoogle Scholar
  43. Longin C, Mühleisen J, Maurer H, Zhang H, Gowda M, Reif J (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096CrossRefGoogle Scholar
  44. Martín AC, Atienza SG, Ramírez MC, Barro F, Martín A (2009) Chromosome engineering in wheat to restore male fertility in the msH1 CMS system. Mol Breed 24:397–408CrossRefGoogle Scholar
  45. Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang X-Q, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427CrossRefGoogle Scholar
  46. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefGoogle Scholar
  47. Metzker ML (2009) Sequencing technologies—the next generation. Nat Rev Genet 11:31CrossRefGoogle Scholar
  48. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88:9828–9832CrossRefGoogle Scholar
  49. Mühleisen J, Maurer HP, Stiewe G, Bury P, Reif JC (2013) Hybrid breeding in barley. Crop Sci 53:819–824CrossRefGoogle Scholar
  50. Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615CrossRefGoogle Scholar
  51. Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant, Cell Environ 28:1534–1551CrossRefGoogle Scholar
  52. Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203CrossRefGoogle Scholar
  53. Ramage RT (1983) Heterosis and hybrid seed production in barley. In: Frankel R (ed) Heterosis: reappraisal of theory and practice. Springer, Berlin, pp 71–93CrossRefGoogle Scholar
  54. Ramirez-Gonzalez RH, Segovia V, Bird N, Fenwick P, Holdgate S, Berry S, Jack P, Caccamo M, Uauy C (2015) RNA-Seq bulked segregant analysis enables the identification of high-resolution genetic markers for breeding in hexaploid wheat. Plant Biotechnol J 13:613–624CrossRefGoogle Scholar
  55. Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Bräutigam A, Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361:eaar6089CrossRefGoogle Scholar
  56. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh C-T, Emrich SJ, Jia Y, Kalyanaraman A, Hsia A-P, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia J-M, Deragon J-M, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefGoogle Scholar
  57. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jørgensen J-E, Weigel D, Andersen SU (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6:550CrossRefGoogle Scholar
  58. Singh SP, Srivastava R, Kumar J (2015) Male sterility systems in wheat and opportunities for hybrid wheat development. Acta Physiol Plant 37:1713CrossRefGoogle Scholar
  59. Singh M, Kumar M, Thilges K, Cho M-J, Cigan AM (2017) MS26/CYP704B is required for anther and pollen wall development in bread wheat (Triticum aestivum L.) and combining mutations in all three homeologs causes male sterility. PLoS ONE 12:e0177632CrossRefGoogle Scholar
  60. Søgaard B, von Wettstein-Knowles P (1987) Barley: genes and chromosomes. Carlsberg Res Commun 52:123–196CrossRefGoogle Scholar
  61. Suneson CA (1940) A male sterile character in barley: a new tool for the plant breeder. J Hered 31:213–214CrossRefGoogle Scholar
  62. Tang H, Krishnakuar V, Li J (2015) jcvi: JCVI utility libraries. Zenodo.
  63. United-Nations (2015) World population prospects: the 2015 revision, key findings and advance tables. In: Department of Economic and Social Affairs PD (ed). United Nations, New YorkGoogle Scholar
  64. Wan X, Wu S, Li Z, Dong Z, An X, Ma B, Tian Y, Li J (2019) Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Mol Plant 12:321–342CrossRefGoogle Scholar
  65. Wanjugi H, Coleman-Derr D, Huo N, Kianian SF, Luo M-C, Wu J, Anderson O, Gu YQ (2009) Rapid development of PCR-based genome-specific repetitive DNA junction markers in wheat. Genome 52:576–587CrossRefGoogle Scholar
  66. Wiebe GA (1960) A proposal for hybrid barley. Agron J 52:181–182CrossRefGoogle Scholar
  67. Xu J, X-y Wang, W-z Guo (2015) The cytochrome P450 superfamily: key players in plant development and defense. J Integr Agric 14:1673–1686CrossRefGoogle Scholar
  68. Yang L, Liu B, Zhai H, Wang S, Liu H, Zhou Y, Meng F, Yang J, Zhu G, Chui S, Zhang Q, Wei Y (2009) Dwarf male-sterile wheat: a revolutionary breeding approach to wheat. In: Shu QY (ed) Induced plant mutations in the genomics era. Food and Agriculture Organization of the United Nations, Rome, pp 370–372Google Scholar
  69. Yuan C, Jiang H, Wang H, Li K, Tang H, Li X, Fu D (2012) Distribution, frequency and variation of stripe rust resistance loci Yr10, Lr34/Yr18 and Yr36 in Chinese wheat cultivars. J Genet Genom 39:587–592CrossRefGoogle Scholar
  70. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  71. Zhang X, Lu C, Xu R, Zhou M (2015) Development of molecular markers linked to barley heterosis. Euphytica 203:309–319CrossRefGoogle Scholar
  72. Zhou MX (2010) Barley production and consumption. In: Zhang G, Li C (eds) Genetics and improvement of barley malt quality. Springer, Berlin, pp 1–17Google Scholar
  73. Zhuang J-Y, Du J-H, Cao L-Y, Fan Y-Y, Cheng S-H (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Crop BiologyShandong Agricultural UniversityTai’anChina
  2. 2.Department of Plant SciencesUniversity of IdahoMoscowUSA
  3. 3.Center for Reproductive BiologyWashington State UniversityPullmanUSA

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