Abstract
Maize was one of the first eukaryotic species in which individual chromosomes can be identified cytologically, which made maize one of the oldest models for genetics and cytogenetics research. Nevertheless, consistent identification of all 10 chromosomes from different maize lines as well as from wild Zea species remains a challenge. We developed a new technique for maize chromosome identification based on fluorescence in situ hybridization (FISH). We developed two oligonucleotide-based probes that hybridize to 24 chromosomal regions. Individual maize chromosomes show distinct FISH signal patterns, which allow universal identification of all chromosomes from different Zea species. We developed karyotypes from three Zea mays subspecies and two additional wild Zea species based on individually identified chromosomes. A paracentric inversion was discovered on the long arm of chromosome 4 in Z. nicaraguensis and Z. luxurians based on modifications of the FISH signal patterns. Chromosomes from these two species also showed distinct distribution patterns of terminal knobs compared with other Zea species. These results support that Z. nicaraguensis and Z. luxurians are closely related species.
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Abbreviations
- BAC:
-
Bacterial artificial chromosome
- DAPI:
-
4,6-Diamidino-2-phenylindole
- FISH:
-
Fluorescence in situ hybridization
- Mb:
-
Megabase
- MY:
-
Million years
- Oligo:
-
Oligonucleotide
References
Adawy SSM, Stupar RM, Jiang J (2004) Fluorescence in situ hybridization of knob-associated DNA elements analysis reveals multiple loci in one-knob and knobless maize lines. J Histochem Cytochem 52:1113–1116
Albert PS, Gao Z, Danilova TV, Birchler JA (2010) Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet Genome Res 129:6–16
Albert PS, Zhang T, Semrau K, Rouillard JM, Kao YH, Wang CJR, Danilova TV, Jiang JM, Birchler JA (2019) Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc Natl Acad Sci U S A 116:1679–1685
Amarillo FIE, Bass HW (2007) A transgenomic cytogenetic sorghum (Sorghum propinquum) bacterial artificial chromosome fluorescence in situ hybridization map of maize (Zea mays L.) pachytene chromosome 9, evidence for regions of genome hyperexpansion. Genetics 177:1509–1526
Bi YF, Zhao QZ, Yan WK, Li MX, Liu YX, Cheng CY, Zhang L, Yu XQ, Li J, Qian CT, Wu YF, Chen JF, Lou QF (2020) Flexible chromosome painting based on multiplex PCR of oligonucleotides and its application for comparative chromosome analyses in Cucumis. Plant J. https://doi.org/10.1111/tpj.14600
Braz GT, He L, Zhao HN, Zhang T, Semrau K, Rouillard JM, Torres GA, Jiang JM (2018) Comparative Oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523
Bridges CB (1935) Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J Hered 26:60–64
Chen CC, Chen CM, Hsu FC, Wang CJ, Yang JT, Kao YY (2000) The pachytene chromosomes of maize as revealed by fluorescence in situ hybridization with repetitive DNA sequences. Theor Appl Genet 101:30–36
Cheng ZK, Buell CR, Wing RA, Jiang JM (2002) Resolution of fluorescence in-situ hybridization mapping on rice mitotic prometaphase chromosomes, meiotic pachytene chromosomes and extended DNA fibers. Chromosom Res 10:379–387
Danilova TV, Birchler JA (2008) Integrated cytogenetic map of mitotic metaphase chromosome 9 of maize: resolution, sensitivity, and banding paint development. Chromosoma 117:345–356
Danilova TV, Friebe B, Gill BS (2014) Development of a wheat single gene FISH map for analyzing homoeologous relationship and chromosomal rearrangements within the Triticeae. Theor Appl Genet 127:715–730
de Carvalho CR, Saraiva LS (1993) A new heterochromatin banding pattern revealed by modified HKG banding technique in maize chromosomes. Heredity 70:515–519
de Carvalho CR, Saraiva LS (1997) High-resolution HKG-banding in maize mitotic chromosomes. J Plant Res 110:417–420
Deaguiarperecin MLR, Vosa CG (1985) C-banding in maize II. Identification of somatic chromosomes. Heredity 54:37–42
Fang Z, Pyhajarvi T, Weber AL, Dawe RK, Glaubitz JC, Gonzalez JDS, Ross-Ibarra C, Doebley J, Morrell PL, Ross-Ibarra J (2012) Megabase-scale inversion polymorphism in the wild ancestor of maize. Genetics 191:883–U426
Figueroa DM, Bass HW (2012) Development of pachytene FISH maps for six maize chromosomes and their integration with other maize maps for insights into genome structure variation. Chromosom Res 20:363–380
Findley SD, Cannon S, Varala K, Du JC, Ma JX, Hudson ME, Birchler JA, Stacey G (2010) A fluorescence in situ hybridization system for karyotyping soybean. Genetics 185:727–744
Fradkin M, Ferrari MR, Espert SM, Ferreira V, Grassi E, Greizerstein EJ, Poggio L (2013) Differentiation of triticale cultivars through FISH karyotyping of their rye chromosomes. Genome 56:267–272
Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez J, Liu KJ, Buckler ES, Doebley J (2005) Genetic diversity and population structure of teosinte. Genetics 169:2241–2254
Han YH, Zhang T, Thammapichai P, Weng YQ, Jiang JM (2015) Chromosome-specific painting in cucumis species using bulked oligonucleotides. Genetics 200:771–779
He L, Braz GT, Torres GA, Jiang JM (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513
Hilton H, Gaut BS (1998) Speciation and domestication in maize and its wild relatives: evidence from the globulin-1 gene. Genetics 150:863–872
Hou LL, Xu M, Zhang T, Xu ZH, Wang WY, Zhang JX, Yu MM, Ji W, Zhu CW, Gong ZY, Gu MH, Jiang JM, Yu HX (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110
Janda J, Safar J, Kubalakova M, Bartos J, Kovarova P, Suchankova P, Pateyron S, Cihalikova J, Sourdille P, Simkova H, Faivre-Rampant P, Hribova E, Bernard M, Lukaszewski A, Dolezel J, Chalhoub B (2006) Advanced resources for plant genomics: a BAC library specific for the short arm of wheat chromosome 1B. Plant J 47:977–986
Jewell DC, Islam-Faridi N (1994) A technique for somatic chromosome preparation and C-banding of maize. In: Freeling M, Walbot V (eds) The maize handbook. Springer-Verlag, New York, Inc, pp 484–493
Jiang JM (2019) Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosom Res 27:153–165
Jiang JM, Gill BS (1994) Nonisotopic in situ hybridization and plant genome mapping: the first 10 years. Genome 37:717–725
Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068
Kakeda K, Yamagata H, Fukui K, Ohno M, Fukui K, Wei ZZ, Zhu FS (1990) High resolution bands in maize chromosomes by G-banding methods. Theor Appl Genet 80:265–272
Kato A (1999) Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 74:160–166
Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci U S A 101:13554–13559
Kirov I, Khrustaleva L, Laere KV, Soloviev A, Sofie M, Romanov D, Fesenko I (2017) DRAWID: user-friendly java software for chromosome measurements and idiogram drawing. Comp Cytogenet 11:747–757
Koumbaris GL, Bass HW (2003) A new single-locus cytogenetic mapping system for maize (Zea mays L.): overcoming FISH detection limits with marker-selected sorghum (S. propinquum L.) BAC clones. Plant J 35:647–659
Lamb JC, Danilova T, Bauer MJ, Meyer JM, Holland JJ, Jensen MD, Birchler JA (2007a) Single-gene detection and karyotyping using small-target fluorescence in situ hybridization on maize somatic chromosomes. Genetics 175:1047–1058
Lamb JC, Meyer JM, Corcoran B, Kato A, Han FP, Birchler JA (2007b) Distinct chromosomal distributions of highly repetitive sequences in maize. Chromosom Res 15:33–49
Lengerova M, Kejnovsky E, Hobza R, Macas J, Grant SR, Vyskot B (2004) Multicolor FISH mapping of the dioecious model plant, Silene latifolia. Theor Appl Genet 108:1193–1199
Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas-Genetisk A 52:201–220
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760
Li H, Wang CY, Fu SL, Guo X, Yang BJ, Chen CH, Zhang H, Wang YJ, Liu XL, Han FP, Ji WQ (2014) Development and discrimination of 12 double ditelosomics in tetraploid wheat cultivar DR147. Genome 57:89–95
Liu XY, Sun S, Wu Y, Zhou Y, Gu SW, Yu HX, Yi CD, Gu MH, Jiang JM, Liu B, Zhang T, Gong ZY (2020) Dual-color oligo-FISH can reveal chromosomal variations and evolution in Oryza species. Plant J 101:112–121
Mano Y, Omori F (2013) Flooding tolerance in interspecific introgression lines containing chromosome segments from teosinte (Zea nicaraguensis) in maize (Zea mays subsp mays). Ann Bot-London 112:1125–1139
Martins LD, Yu F, Zhao HN, Dennison T, Lauter N, Wang HY, Deng ZH, Thompson A, Semrau K, Rouillard JM, Birchler JA, Jiang JM (2019) Meiotic crossovers characterized by haplotype-specific chromosome painting in maize. Nat Commun 10:4604
McClintock B (1929) Chromosome morphology in Zea mays. Science 69:629–629
Meng Z, Zhang ZL, Yan TY, Lin QF, Wang Y, Huang WY, Huang YJ, Li ZJ, Yu QY, Wang JP, Wang K (2018) Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front Plant Sci 9:1624
Meng Z, Han J, Lin Y, Zhao Y, Lin Q, Ma X, Wang J, Zhang M, Zhang L, Yang Q, Wang K (2020) Characterization of a Saccharum spontaneum with a basic chromosome number of x = 10 provides new insights on genome evolution in genus Saccharum. Theor Appl Genet 133:187–199
Mukai Y, Nakahara Y, Yamamoto M (1993) Simultaneous discrimination of the three genomes in hexaploid wheat by multicolor fluorescence insitu hybridization using total genomic and highly repeated DNA probes. Genome 36:489–494
Poggio L, Gonzalez G, Confalonieri V, Comas C, Naranjo CA (2005) The genome organization and diversification of maize and its allied species revisited: evidences from classical and FISH-GISH cytogenetic analysis. Cytogenet Genome Res 109:259–267
Qu MM, Li KP, Han YL, Chen L, Li ZY, Han YH (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164
Rayburn AL, Price HJ, Smith JD, Gold JR (1985) C-band heterochromatin and DNA content in Zea mays. Am J Bot 72:1610–1617
Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosom Res 4:507–516
Ross-Ibarra J, Tenaillon M, Gaut BS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181:1397–1409
Sadder MT, Weber G (2001) Karyotype of maize (Zea mays L.) mitotic metaphase chromosomes as revealed by fluorescence in situ hybridization (FISH) with cytogenetic DNA markers. Plant Mol Biol Rep 19:117–123
Sarkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214
Schnable PS, Ware D, Fulton RS, Stein JC, Wei FS, Pasternak S, Liang CZ, Zhang JW, 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 CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann M, 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 W, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Simonikova D, Nemeckova A, Karafiatova M, Uwimana B, Swennen R, Dolezel J, Hribova E (2019) Chromosome painting facilitates anchoring reference genome sequence to chromosomes in situ and integrated karyotyping in Banana (Musa Spp.). Front Plant Sci 10:1503
Song XY, Song RR, Zhou JW, Yan WK, Zhang T, Sun HJ, Xiao J, Wu YF, Xi ML, Lou QF, Wang HY, Wang X (2020) Development and application of oligonucleotide-based chromosome painting for chromosome 4D of Triticum aestivum L. Chromosome Res. https://doi.org/10.1007/s10577-10020-09627-10570
Swigonova Z, Lai JS, Ma JX, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923
Sybenga J (1972) General Cytogenetics. American Elsevier Publishing Co., INC, New York
Ting YC (1965) Spontaneous chromosome inversions of Guatemalan teosintes (Zea mexicana). Genetica 36:229–242
Wang CJR, Harper L, Cande WZ (2006) High-resolution single-copy gene fluorescence in situ hybridization and its use in the construction of a cytogenetic map of maize chromosome 9. Plant Cell 18:529–544
Wang Y, Diehl A, Wu FN, Vrebalov J, Giovannoni J, Siepel A, Tanksley SD (2008) Sequencing and comparative analysis of a conserved syntenic segment in the solanaceae. Genetics 180:391–408
Ward EJ (1980) Banding patterns in maize mitotic chromosomes. Can J Genet Cytol 22:61–67
Wu FN, Tanksley SD (2010) Chromosomal evolution in the plant family Solanaceae. BMC Genomics 11:182
Xin HY, Zhang T, Han YH, Wu YF, Shi JS, Xi ML, Jiang JM (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321
Xin HY, Zhang T, Wu YF, Zhang WL, Zhang PD, Xi ML, Jiang JM (2020) An extraordinarily stable karyotype of the woody Populus species revealed by chromosome painting. Plant J 101:253–264
Xiong ZY, Pires JC (2011) Karyotype and identification of all homoeologous chromosomes of allopolyploid Brassica napus and its diploid progenitors. Genetics 187:37–49
Zhang P, Li WL, Fellers J, Friebe B, Gill BS (2004) BAC-FISH in wheat identifies chromosome landmarks consisting of different types of transposable elements. Chromosoma 112:288–299
Zhao HN, Zhu XB, Wang K, Gent JI, Zhang WL, Dawe RK, Jiang JM (2016) Gene expression and chromatin modifications associated with maize centromeres. G3-Genes Genom Genet 6:183–192
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This research is supported by NSF grant IOS-1444514 and MSU startup funds to J.J.
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Braz, G.T., do Vale Martins, L., Zhang, T. et al. A universal chromosome identification system for maize and wild Zea species. Chromosome Res 28, 183–194 (2020). https://doi.org/10.1007/s10577-020-09630-5
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DOI: https://doi.org/10.1007/s10577-020-09630-5