Microevolutionary differentiation of cereal tetraploid species by formation of recombinant genomes

The process of microevolutionary differentiation of cereals by formation of recombinant genomes was studied in dynamics (F6–F17) with tetraploid wheat-rye amphidiploids as examples. Evidence that joint growing of tetra ploid amphidiploids having a common (pivotal) genome in their composition and differing in secondary (differential) genomes leads to their hybridization with high probability has been found. The forms developed are characterized by a very wide range of variability caused by different combinations of chromosomes and chromosome segments in dif­ferential genomes yet maintain the same structure of the pivotal genome. Intergenomic recombinations at the level of intact chromosomes were characteristic of homeologous groups with a high rate of stabili zation of the chromosomal composition, and recombinations at the level of chromosomal segments, of groups with a low stabilization rate, where heterologous chromosome pairs remained preserved for a long time. Dominance of regulatory genetic systems of the pivotal genome provides a high pairing level of homeologues from heterologous pairs in meiosis followed by intergenomic recombinations at the level of chromosome segments. Experimen tal data suggest that newly developed tetraploid forms interbreed easily forming a single hybrid zone, where permanent redistribution of genetic material of differential genomes and further range expansion of genotypic variability available to selection take place during alternation of generations whereby such a zone becomes a poten tial centre of speciation. Subsequent adaptive radiation of hybrid material in an ecologically separated environment occurs by selection of forms with different variants of the recombinant genome in various ecological niches.

polyploid cereals, microevolution, tetraploid amphidiploids, pivotal genome, recombinant genome, intergenomic recombinations, C-banding

1. Abbott R., Albach D., Ansell S., Arntzen J.W., Baird S.J., Bierne N., Boughman J., Brelsford A., Buerkle C.A., Buggs R., Butlin R.K., Dieckmann U., Eroukhmanoff F., Grill A., Cahan S.H., Hermansen J.S., Hewitt G., Hudson A.G., Jiggins C., Jones J., Keller B., Marczewski T., Mallet J., Martinez-Rodriguez P., Möst M., Mullen S., Nichols R., Nolte A.W., Parisod C., Pfennig K., Rice A.M., Ritchie M.G., Seifert B., Smadja C.M., Stelkens R., Szymura J.M., Väinölä R., Wolf J.B., Zinner D. Hybridization and speciation. J. Evol. Biol. 2013;26(2):229-246. DOI 0.1111/j.1420-9101.2012.02599.x

2. Adams K.L., Wendel J.F. Polyploidy and genome evolution in plants: Genome studies and molecular genetics. Curr. Opin. Plant Biol. 2005;8(1):135-141. DOI 10.1016/j.pbi.2005.01.001

3. Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408(6814): 796-815. DOI 10.1038/35048692

4. Badaev N.S., Badaeva E.D., Dubovets N.I. Bolsheva N.L., Bormotov V.E., Zelenin A.V. Formation of a synthetic karyotype of tetraploid triticale. Genome. 1992;35(2):311-317. DOI 10.1139/g92-047

5. Badaeva E.D., Amosova A.V., Samatadze T.E., Zoshchuk S.A., Shostak N.G., Chikida N.N., Zelenin A.V., Raupp W.J., Friebe B., Gill B.S. Genome differentiation in Aegilops. 4. Evolution of the U-genome cluster. Plant Syst. Evol. 2004;246(1-2):45- 76. DOI 10.1007/s00606-003-0072-4

6. Badaeva E.D., Badaev N.S., Gill D.S., Filatenko A.A. Intraspecific karyotype divergence in Triticum araraticum (Poaceae). Plant Syst. Evol. 1994;192(1):117-145. DOI 10.1007/BF00985912.

7. Blanc G., Wolfe K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell. 2004;16(7):1667-1678. DOI 10.1105/tpc.021345

8. Bormotov V.E., Shcherbakova A.M., Dubovets N.I. Alloplasmic rye in tetraploid triticale breeding. Selskokhozyaystvennaya Biologiya = Agricultural Biology. 1988;6:31-35.

9. Ceoloni C., Forte P., Ciaffi M., Nenno M., Bitti A., De Vita P., D’Egidio M.G. Chromosomally engineered durum wheat: The potential of alien gene introgressions affecting disease resistance and quality. Proc. Seminar on durum wheat improvement in the mediterranean region: new challenges, Spain, Zaragoza, 12-14 April, 2000;363- 371.

10. Cuadrado M.C., Romero C. Different genetic systems in rye affecting homoeologous pairing in wheat-rye combinations. Genome. 1988; 30(5):793-796. DOI 10.1139/g88-127

11. Cui L., Wall P.K., Leebens-Mack J.H., Lindsay B.G., Soltis D.E., Doyle J.J., Soltis P.S., Carlson J.E., Arumuganathan K., Barakat A., Albert V.A., Ma H., dePamphilis C.W. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006; 16(6):738-749. DOI 10.1101/gr.4825606

12. Dubovets N. I. Tetraploid triticales as a model of cereals hybrid genome formation. Proc. 11th EWAC Conference, Novosibirsk, 24–28 July 2000 / Ins. Cytol. & Genet. SB RAS, Novosibirsk, Russia, Cer. Res. Dep., John Innes Centre, Norwich, UK. Eds T.A. Pshenichnikova, A.J. Worland. EWAC NEWSLETTER. 2001;21-24.

13. Dubovets N.I., Sycheva E.A., Solovey L.A., Shtyk T.I., Bondarevich E.B. Recombinant genome of cereals: The pattern of formation and the role in evolution of polyploid species. Genetika = Genetics (Moscow). 2008;44(1):54-61.

14. Dubovets N. I., Sycheva E.A., Solovey L. A., Shtyk T.I., Bondarevich E.B. Recombinant genome of cereals: The pattern of formation and the role in evolution of polyploid species. Russ. J. Genet. 2008;44(1):44-50. DOI 10.1134/S1022795408010067

15. Ehrendorfer F.L. Polyploidy and distribution. Polyploidy-Biological Relevance. N.Y.: Plenum Press, 1980;45-60.

16. Feldman M., Levy A.A. Allopolyploidy – a shaping force in the evolution of wheat genomes. Cytogenet. Genome Res. 2005;109(1-3): 250-258. DOI 10.1159/000082407

17. Goff S.A., Ricke D., Lan T.H., Presting G., Wang R., Dunn M., Glazebrook J., Sessions A., Oeller P., Varma H., Hadley D., Hutchison D., Martin C., Katagiri F., Lange B.M., Moughamer T., Xia Y., Budworth P., Zhong J., Miguel T., Paszkowski U., Zhang S., Colbert M., Sun W.L., Chen L., Cooper B., Park S., Wood T.C., Mao L., Quail P., Wing R., Dean R., Yu Y., Zharkikh A., Shen R., Sahasrabudhe S., Thomas A., Cannings R., Gutin A., Pruss D., Reid J., Tavtigian S., Mitchell J., Eldredge G., Scholl T., Miller R.M., Bhatnagar S., Adey N., Rubano T., Tusneem N., Robinson R., Feldhaus J., Macalma T., Oliphant A., Briggs S. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002;296(5565):92-100. DOI 10.1126/science.1068275

18. Goh W.L., Chandran S., Franclin D.C., Isagi Y., Koshy K.C., Sungkaew S., Yang H.Q., Xia N.H., Wong K.M. Multi-gene region phylogenetic analyses suggest reticulate evolution and a clade of Australian origin among paleotropical woody bamboos (Poaceae: Bambusoideae: Bambuseae). Plant Syst. Evol. 2013;299(1):239- 257. DOI 10.1007/s00606-012-0718-1

19. Greer E., Martin A., Pendle A., Colas I., Jones A.M., Moore G., Shaw P. The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell. 2012;24(1):152-162. DOI 10.1105/tpc.111.094771

20. Grimanelli D., Leblanc O., Perotti E., Grossniklaus U. Developmental genetics of gametophytic apomixes. Trends Genet. 2001;17(10):597-604. DOI 10.1016/S0168-9525(01)02454-4

21. Hunt H.V., Badakshi F., Romanova O., Howe C.J., Jones M.K., Heslop- Harrison J.S. Reticulate evolution in Panicum (Poaceae): the origin of tetraploid broomcorn millet, P. miliaceum. J. Exp. Bot. 2014; 65(12):3165-3175. DOI 10.1093/jxb/eru161

22. Koltunov A.M., Grossniklaus U. Apomixis: a developmental perspective. Ann. Rev. Plant Biol. 2003;54:547-574. DOI 10.1146/annurev.arplant.54.110901.160842

23. Lakin G.F. Biometriya [Biometrics]. Moscow, Vysshaya shkola, 1990.

24. Lapinsky B., Schwarzacher T. Wheat-rye chromosome translocations in improved lines of 4x-triticale. Plant cytogenetics: Proc. Spring Symp. Cieszyn, 19-22 May 1997. Katowice: Wydawnictwo Uniwersytetu Slaskiego. 1998;210-215.

25. Lukaszewski A.J., B. Apolinarska B., Gustafson J.P., Krolow K.D. Chromosome constitution of tetraplod triticale. Z. Pflanzenzuchtg. 1984;93(3):222-236.

26. Molnár I., Šimkova H., Leverington-Waite M., Goram R., Cseh A., Vrána J., Farkas A., Doležel J., Molnár-Láng M., Griffiths S. Syntenic relationships between the U and M genomes of Aegilops, wheat and the model species Brachypodium and rice as revealed by COS markers. PLoS One. 2013;8(8):e70844. DOI 10.1371/journal.pone.0070844

27. Paterson A.H., Bowers J.E., Chapman B.A. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. USA. 2004;101(26):9903-9908. DOI 10.1073/pnas.0307901101

28. Perrino P. Collection and use of genetic resources of Triticum. Evolution und Taxonomie von pflanzengenetischen Ressourcen. Festschrift fur Peter Hanelt. Gatersleben, Germany, 5-6 Dezember, 1995; 179-202.

29. Probatova N.S. Khromosomnye chisla v semeystve Poaseae i ikh znachenie dlya sistematiki, filogenii i fitogeografii (na primere zlakov Dalnego Vostoka Rossii) [Chromosome numbers in the family Poaceae and their implications for taxonomy, phylogeny and phytogeography (by the example of Russian Far East cereals)]. Komarovskie chteniya [Komarov Readings]. Vladivostok, Dalnauka, 2007;55:9-103.

30. Rieseberg L.H. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 1997;28(1):359-389. DOI 10.1146/annurev.ecolsys.28.1.359

31. Sears E.R. Genetic control of chromosome pairing in wheat. Annu. Rev. Genet. 1976;10(Part 4):31-51.

32. Soltis P.S., Soltis D.E. The role of genetic and genomic attributes in the success of polyploids. Proc. Natl Acad. Sci. USA. 2000;97(13): 7051-7057. DOI 10.1073/pnas.97.13.7051

33. Soltis P.S., Soltis D.E. The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 2009;60(1):561-588. DOI 10.1146/annurev.arplant.043008.092039

34. Stebbins G.L. Chromosomal Evolution in Higher Plants. London: Arnold, 1971.

35. Sycheva E. A., Dubovets N.I. Tetraploid triticale as an object for cytogenetic investigations. I. Studies of the role of individual wheat chromosomes in the regulation of meiotic pairing. Vestsi NAN Belarusi. Ser. biyal. navuk = Proceedings of the National Academy of Sciences of Belarus. Biological series. 2003;2:52-55.

36. Tzvelev N.N. Sistema zlakov (Poaceae) i ikh evolyutsiya [The system of grasses (Poaceae) and their evolution]. Leningrad, Nauka, 1987.

37. Wang J.-B., Wang C., Shi S.H., Zhong Y. Evolution of parental ITS regions of nuclear rDNA in allopolyploid Aegilops (Poaceae) species. Hereditas. 2000;133(1):1-7. DOI 10.1111/j.1601-5223.2000.t01-1-00001.x

38. Wendel J.F. Genome evolution in polyploids. Plant Mol. Biol. 2000; 42(1):225-249. DOI 10.1023/A:1006392424384

39. Wolfe K.H. Yesterday’s polyploids and the mystery of diploidization. Nat. Rev. Genet. 2001;2(5):333-341. DOI 10.1038/35072009

40. Wong S., Butler G., Wolfe K.H. Gene order evolution and paleopoliploidy in hemiascomycete yeasts. Proc. Natl. Acad. Sci USA. 2002; 99(16):9272-9277. DOI 10.1073/pnas.142101099

41. Yan С., Sun G., Sun D. Distinct origin of the Y and St genome in Elymus species: Evidence from the analysis of a large sample of St genome species using Two Nuclear Genes. PLoS One. 2011;6(10):e26853. DOI 10.1371/journal.pone.0026853

42. Zohary D., Feldman M. Hybridization between amphidiploids and the evolution of polyploids in the wheat (Aegilops – Triticum) group. Evolution. 1962;16(1):44-61.