Abstract
Apomixis is defined as asexual reproduction through seeds, although this outcome can be achieved by multiple pathways. Since little is known about the molecular control of these pathways, how they might intersect is also a mystery. Two of these pathways in the grass family, diplospory and apospory, are receiving attention from molecular biologists. Apospory in Pennisetum/Cenchrus, two genera of panicoid grasses, results in the formation of four-nucleate embryo sacs that lack antipodals. Sexual reproduction frequently aborts so that the resulting seed is composed of (1) a parthenogenetically derived embryo that is genetically identical to the mother and (2) endosperm formed through pseudogamy. The transmission of apomixis is associated with the transfer of a linkage block on a single chromosome. This linkage block contains repetitive sequences as well as hemizygous, low-copy DNA sequences. Fluorescence in situ hybridization has demonstrated that these DNA regions occur on only a single chromosome, but not its homologs, in the polyploid apomicts studied. Features of the apomixis-associated region resemble those of other chromosomal segments isolated from recombination and replete with "selfish" DNAs.
Similar content being viewed by others
References
Albertini E, Porceddu A, Ferranti F, Reale L, Barcaccia G, Romano B, Falcinelli M (2001) Apospory and parthenogenesis may be uncoupled in Poa pratensis: a cytological investigation. Sex Plant Reprod 14:213–217
Arthur L, Ozias-Akins P, Hanna WW (1993) Female sterile mutant in pearl millet—evidence for initiation of apospory. J Hered 84:112–115
Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton, Fla.
Barcaccia G, Mazzucato A, Albertini E, Zethof J, Gerats A, Pezzotti M, Falcinelli M (1998) Inheritance of parthenogenesis in Poa pratensis L.: auxin test and AFLP linkage analyses support monogenic control. Theor Appl Genet 97:74–82
Baulcombe (2002) RNA silencing. Curr Biol 12:R82–R84
Birari SP (1981) Mechanism of apomixis in Pennisetum polystachyon Schult. J Maharashtra Agric Univ 6:208–212
Burow GB, Jessup RW, Bowers JE, Schulze SR, Li Z, Wang YW, Burson BB, Hussey MA, Paterson AH (2001) Alignment of Pennisetum ciliare and Sorghum bicolor chromosomes based on EST-enriched genetic maps. http://www.intl-pag.org/pag/9/abstracts/W25_03.html
Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond Ser B 355:163–178
Chapman GP, Busri N (1994) Apomixis in Pennisetum: an ultrastructural study. Int J Plant Sci 155:492–497
Charlesworth D, Wright SI (2001) Breeding systems and genome evolution. Curr Opin Genet Dev 11:685–690
Chen L, Miyazaki C, Kojima A, Saito A, Adachi T (1999) Isolation and characterization of a gene expressed during early embryo sac development in apomictic Guinea grass (Panicum maximum). J Plant Physiol 154:55–62
Cheng ZK, Presting GG, Buell CR, Wing RA, Jiang J (2001) High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics 157:1749–1757
Crane C (2001) Classification of apomictic mechanisms. In: Savidan Y, Carman JG, Dresselhaus T (eds) The flowering of apomixis: from mechanisms to genetic engineering. CIMMYT, IRD, European Commission DG VI (FAIR), Mexico
Dmitri P, Junakovic N (1999) Reviving the selfish DNA hypothesis: new evidence on accumulation of transposable elements in heterochromatin Trends Genet 15:123–124
Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603
Doust A, Kellogg EA (2002) Inflorescence diversification in the Panicoid "bristle grass" clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology. Am J Bot 89:1203–1222
Dujardin M, Hanna WW (1983) Apomictic and sexual pearl millet x Pennisetum squamulatum hybrids. J Hered 74:277–279
Dujardin M, Hanna W (1984a) Microsporogenesis, reproductive behavior, and fertility in five Pennisetum species [wild relatives of cultivated pearl millet]. Theor Appl Genet 67:197–201
Dujardin M, Hanna W (1984b) Cytogenetics of double cross hybrids between Pennisetum americanum-P. purpureum amphiploids and P. americanum × Pennisetum squamulatum interspecific hybrids. Theor Appl Genet 69:97–100
Dujardin M, Hanna W (1985) Cytology and reproduction of reciprocal backcrosses between pearl millet and sexual and apomictic hybrids of pearl millet × Pennisetum squamulatum. Crop Sci 25:59–62
Dujardin M, Hanna WW (1989a) Crossability of pearl millet with wild Pennisetum species. Crop Sci 29:77–80
Dujardin M, Hanna WW (1989b) Developing apomictic pearl millet—characterization of a BC3 plant. J Genet Breed 43:145–151
Duvall MR, Noll JD, Minn AH (2001) Phylogenetics of Paniceae (Poaceae). Am J Bot 88:1988–1992
Eckardt NA (2001) A sense of self: the role of DNA sequence elimination in allopolyploidization. Plant Cell 13:1699–1703
Eddy SR (2001) Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2:919–929
Fisher WD, Bashaw EC, Holt EC (1954) Evidence for apomixis in Pennisetum ciliare and Cenchrus setigerus. Agron J 46:401–404
Gale MD, Devos KM (1998) Plant comparative genetics after 10 years. Science 282:656–659
Giussani LM, Cota-Sanchez JH, Zuloaga FO, Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C-4 photosynthesis. Am J Bot 88:1993–2012
Goel S, Chen ZB, Conner JA, Akiyama Y, Hanna WW, Ozias-Akins P (2003) Delineation by FISH of a single hemizygous chromosomal region responsible for aposporous embryo sac formation in Pennisetum squamulatum and Cenchrus ciliaris. Genetics 163:1069–1082
Grimanelli D, Leblanc O, Espinosa E, Perotti E, Gonzalez de Leon D, Savidan Y (1998) Mapping diplosporous apomixis in tetraploid Tripsacum: one gene or several genes? Heredity 80:33–39
Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17:597–604
Grossniklaus U, Nogler G, van Dijk PJ (2001) How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell 13:1491–1497
Gustine DL, Sherwood RT, Gounaris Y, Huff D (1996) Isozyme, protein, and RAPD markers within a half-sib family of buffelgrass segregating for apospory. Crop Sci 36:723–72
Gustine DL, Sherwood RT, Huff DR (1997) Apospory-linked molecular markers in buffelgrass. Crop Sci 37:947–951
Hanna WW (1987) Utilization of wild relatives of pearl millet. Proceedings of the international pearl millet workshop, 7–11 April 1986. ICRISAT, pp 33–42
Hanna WW (1995) Use of apomixis in cultivar development. Adv Agron 54:333–350
Hanna WW, Powell JB (1973) Stubby head, an induced facultative apomict in pearl millet. Crop Sci 13:726–728
Hanna WW, Powell JB (1974) Radiation-induced female-sterile mutant in pearl millet. J Hered 65:247–249
Harlan JR, DeWet JMJ (1971) Toward a rational classification of cultivated plants. Taxonomy 20:509–517
Hitchcock AS (1951) Manual of the grasses of the United States. USDA Misc Publ 200:1-1051
Jauhar PP (1981) Cytogenetics and breeding of pearl millet and related species. Liss, New York
Jessup RW, Burson BL, Burow GB, Wang Y-W, Chang C, Li Z, Paterson AH, Hussey MA (2002) Disomic inheritance, suppressed recombination, and allelic interactions govern apospory in buffelgrass as revealed by genome mapping. Crop Sci 42:1688–1694
Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genet 33:102–106
Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1-24
Kim JS, Childs KL, Islam-Faridi MN, Menz MA, Klein RR, Klein PE, Price HJ, Mullet JE, Stelly DM (2002) Integrated karyotyping of sorghum by in situ hybridization of landed BACs. Genome 45:402–412
Koltunow AM (1993) Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437
Koltunow AM, Soltys K, Nito N, McClure S (1995a) Anther, ovule, seed, and nuclear embryo development in Citrus sinensis cv. Valencia. Can J Bot 73:1567–1582
Koltunow A, Bicknell RA, Chaudhury AM (1995b) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiol 108:1345–1352
Kuroda-Kawaguchi T, Skaletsky H, Brown LG, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Silber S, Oates R, Rozen S, Page DC (2001) The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nature Genet 29:279–286
Labombarda P, Busti A, Caceres ME, Pupilli F, Arcioni S (2002) An AFLP marker tightly linked to apomixis reveals hemizygosity in a portion of the apomixis-controlling locus in Paspalum simplex. Genome 45:513–519
Langdon T, Seago C, Jones RN, Ougham H, Thomas H, Forster JW, Jenkins G (2000) De novo evolution of satellite DNA on the rye B chromosome. Genetics 154:869–884
Leblanc O, Grimanelli D, Gonzalez-de-Leon D, Savidan Y (1995) Detection of the apomictic mode of reproduction in maize-Tripsacum hybrids using maize RFLP markers. Theor Appl Genet 90:1198–1203
Leblanc O, Armstead I, Pessino S, Ortiz JP, Evans C, Dovalle C, Hayward MD (1997) Nonradioactive messenger-RNA fingerprinting to visualize gene-expression in mature ovaries of Brachiaria hybrids derived from B. brizantha, an apomictic tropical forage. Plant Sci 126:49–58
Lin XY, Kaul SS, Rounsley S, Shea TP, Benito MI, Town CD, Fujii CY, Mason T, Bowman CL, Barnstead M, Feldblyum TV, Buell CR, Ketchum KA, Lee J, Ronning CM, Koo HL, Moffat KS, Cronin LA, Shen M, Pai G, VanAken S, Umayam L, Tallon LJ, Gill JE, Adams MD, Carrera AJ, Creasy TH, Goodman HM, Somerville CR, Copenhaver GP, Preuss D, Mierman WC, White O, Eisen JA, Salzberg SL, Fraser CM, Venter JC (1999) Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402:761–768
Llave C, Kassachau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619
Lubbers EL, Arthur L, Hanna WW, Ozias-Akins P (1994) Molecular markers shared by diverse apomictic Pennisetum species. Theor Appl Genet 89:636–642
Marchais L, Tostain S (1997) Analysis of reproductive isolation between pearl millet (Pennisetum glaucum (L.) R.Br.) and P. ramosum, P. schweinfurthii, P. squamulatum, Cenchrus ciliaris. Euphytica 93:97–105
McDonald JF (1995) Transposable elements: possible catalysts of organismic evolution. Trends Ecol Environ 10:123–126
McDonald JF (1998) Transposable elements, gene silencing and macroevolution. Trends Ecol Environ 13:94–95
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 USA 88:9828–9832
Morgan RN, Alvernaz J, Arthur L, Hanna WW, Ozias-Akins P (1997) Genetic characterization and floral development of female sterile and stubby head, two aposporous mutants of pearl millet. Sex Plant Reprod 10:127–135
Morgan RN, Ozias-Akins P, Hanna WW (1998) Seed set in an apomictic BC3 pearl millet. Int J Plant Sci 159:89–97
Nogler GA (1982) How to obtain diploid apomictic Ranunculus auricomus plants not found in the wild state. Bot Helv 92:13–22
Nogler GA (1984a) Gametophytic apomixis. In: Johri BM (ed) Embryology of angisoperms. Springer, Berlin Heidelberg New York
Nogler GA (1984b) Genetics of apospory in apomictic Ranunculus auricomus. V. Conclusion. Bot Helv 92:411–423
Noyes RD, Rieseberg LH (2000) Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics 155:379–390
Nybom H (1996) DNA fingerprinting—a useful tool in the taxonomy of apomictic plant groups. Folia Geobot Phytotax 31:295–304
Okada S, Sone T, Fujisawa M, Nakayama S, Takenaka M, Ishizaki K, Kono K, Shimizu-Ueda Y, Hanajiri T, Yamato KT, Fukuzawa H, Brennicke A, Ohyama K (2001) The Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene. Proc Natl Acad Sci USA 98:9454–9459
Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607
Ozias-Akins P, Lubbers EL, Hanna WW, McNay JW (1993) Transmission of the apomictic mode of reproduction in Pennisetum: co-inheritance of the trait and molecular markers. Theor Appl Genet 85:632–638
Ozias-Akins P, Roche D, Hanna WW (1998) Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus which may have no allelic form in sexual genotypes. Proc Natl Acad Sci USA 95:5127–5132
Paran I, Michelmore RW (1993) Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor Appl Genet 85:985–993
Peacock WJ (1992) Genetic engineering and mutagenesis for apomixis in rice. Apomixis Newsl 4:3-7
Peel MD, Carman JG, Leblanc O (1997) Megasporocyte callose in apomictic buffelgrass, Kentucky bluegrass, Pennisetum squamulatum Fresen, Tripsacum L., and weeping lovegrass. Crop Sci 37:724–732
Pessino SC, Ortiz JPA, Leblanc O, do Valle CB, Evans C, Hayward MD (1997) Identification of a maize linkage group related to apomixis in Brachiaria. Theor Appl Genet 94:439–444
Pessino SC, Evans C, Ortiz JPA, Armstead I, do Valle CB, Hayward MD (1998) A genetic map of the apospory-region in Brachiaria hybrids: identification of two markers closely associated with the trait. Hereditas 128:153–158
Pessino SC, Espinoza F, Martinez EJ, Ortiz JPA, Valle EM, Quarin CL (2001) Isolation of cDNA clones differentially expressed in flowers of apomictic and sexual Paspalum notatum. Hereditas 134:35–42
Plasterk RHA (2002) RNA silencing: the genome's immune system. Science 296:1263–1265
Pupilli F, Labombarda P, Caceres ME, Quarin CL, Arcioni S (2001) The chromosome segment related to apomixis in Paspalum simplex is homoeologous to the telomeric region of the long arm of rice chromosome 12. Mol Breed 8:53–61
Roche D, Cong P, Chen ZB, Hanna WW, Gustine DL, Sherwood RT, Ozias-Akins P (1999) An apospory-specific genomic region is conserved between buffelgrass (Cenchrus ciliaris L.) and Pennisetum squamulatum Fresen. Plant J 19:203–208
Roche D, Hanna W, Ozias-Akins P (2001a) Is supernumerary chromatin involved in gametophytic apomixis of polyploid plants? Sex Plant Reprod 13:343–349
Roche D, Chen Z, Hanna W, Ozias-Akins P (2001b) Non-Mendelian transmission of an apospory-specific genomic region in a reciprocal cross between sexual pearl millet (Pennisetum glaucum) and an apomictic F1 (P. glaucum x P. squamulatum). Sex Plant Reprod 13:217–223
Roche D, Conner JA, Budiman MA, Frisch D, Wing R, Hanna WW, Ozias-Akins P (2002) Construction of BAC libraries from two apomictic grasses to study the microcolinearity of their apospory-specific genomic regions. Theor Appl Genet 104:804–812
Savidan Y (2000) Apomixis: genetics and breeding. Plant Breed Rev 18:13–85
Schmelzer GH (1997) Review of Pennisetum section Brevivalvula (Poaceae). Euphytica 97:1–20
Sherwood RT (1995) Nuclear DNA amount during sporogenesis and gametogenesis in sexual and aposporous buffelgrass. Sex Plant Reprod 8:85–90
Sherwood RT, Berg CC, Young BA (1994) Inheritance of apospory in buffelgrass. Crop Sci 34:1490–1494
Shiu PKT, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107:905–916
Simpson CE, Bashaw EC (1969) Cytology and reproductive characteristics in Pennisetum setaceum. Am J Bot 56:31–36
Snyder LA, Hernandez AR, Warmke HE (1955) The mechanism of apomixis in Pennisetum ciliare. Bot Gaz 116:209–221
Spillane C, Steimer A, Grossniklaus U (2001) Apomixis in agriculture: the quest for clonal seeds. Sex Plant Reprod 14:179–187
Steinemann M, Steinemann S (1997) The enigma of Y chromosome degeneration: TRAM, a novel retrotransposon is preferentially located on the neo-Y chromosome of Drosophila miranda. Genetics 145:261–266
Stitou S, Diaz de la Guardia R, Jimenez R, Burgos M (2000) Inactive ribosomal cistrons are spread throughout the B chromosomes of Rattus rattus (Rodentia, Muridae). Implications for their origin and evolution. Chromosome Res 8:305–311
Storz G (2002) An expanding universe of noncoding RNAs. Science 296:1260–1263
Taliaferro CM, Bashaw EC (1966) Inheritance and control of obligate apomixis in breeding buffelgrass, Pennisetum ciliare. Crop Sci 6:473–476
van Dijk PJ, Tas ICQ, Falque M, Bakx-Schotman JMT (1999) Crosses between sexual and apomictic dandelions (Taraxacum). II. The breakdown of apomixis. Heredity 83:715–721
van Dijk P, van Damme J (2000) Apomixis technology and the paradox of sex. Trends Plant Sci 5:81–84
Vance V, Vaucheret H (2001) RNA silencing in plants—defense and counterdefense. Science 292:2277–2280
Vielle JP, Burson BL, Bashaw EC, Hussey MA (1995) Early fertilization events in the sexual and aposporous egg apparatus of Pennisetum ciliare (L.) link. Plant J 8(2):309–316
Vielle-Calzada JP, Nuccio ML, Budiman MA, Thomas TL, Burson BL, Hussey MA, Wing RA (1996) Comparative gene expression in sexual and apomictic ovaries of Pennisetum ciliare (L.) Link. Plant Mol Biol 32:1085–1092
Voinnet O (2002) RNA silencing: small RNAs as ubiquitous regulators of gene expression. Curr Opin Plant Biol 5:444–451
Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18(24):7213–7218
Wen XS, Ye XL, Li YQ, Chen ZL, Xu SX (1998) Embryological studies on apomixis in Pennisetum squamulatum. Acta Bot Sin 40:598–604
Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acid Res 18:6531–6535
Wu KK, Burnquist W, Sorrells ME, Tew TL, Moore PH, Tanksley SD (1992) The detection and estimation of linkage in polyploids using single-dose restriction fragments. Theor Appl Genet 83:294–300
Zeyl C, Bell G (1996) Symbiotic DNA in eukaryotic genomes. Trends Environ Ecol 11:10–15
Acknowlegements
This work has been funded by the Rockefeller Foundation, Pioneer Hi-Bred International, Limagrain SA, USDANRI (award nos. 93-37304-9363 and 99-35300-7691), and NSF (award no. 0115911). We thank Linsey Forlow for developing the illustrations in Figs. 1 and 2, and Joann Conner, Geraldine Fleming, Shailendra Goel, John McDonald, and Dominique Roche for their comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ozias-Akins, P., Akiyama, Y. & Hanna, W.W. Molecular characterization of the genomic region linked with apomixis in Pennisetum/Cenchrus . Funct Integr Genomics 3, 94–104 (2003). https://doi.org/10.1007/s10142-003-0084-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-003-0084-8