Varietal variation and chromosome behaviour during meiosis in Solanum tuberosum.


Journal

Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007

Informations de publication

Date de publication:
10 2020
Historique:
received: 16 12 2019
accepted: 02 06 2020
revised: 02 06 2020
pubmed: 12 6 2020
medline: 27 8 2021
entrez: 12 6 2020
Statut: ppublish

Résumé

Naturally occurring autopolyploid species, such as the autotetraploid potato Solanum tuberosum, face a variety of challenges during meiosis. These include proper pairing, recombination and correct segregation of multiple homologous chromosomes, which can form complex multivalent configurations at metaphase I, and in turn alter allelic segregation ratios through double reduction. Here, we present a reference map of meiotic stages in diploid and tetraploid S. tuberosum using fluorescence in situ hybridisation (FISH) to differentiate individual meiotic chromosomes 1 and 2. A diploid-like behaviour at metaphase I involving bivalent configurations was predominant in all three tetraploid varieties. The crossover frequency per bivalent was significantly reduced in the tetraploids compared with a diploid variety, which likely indicates meiotic adaptation to the autotetraploid state. Nevertheless, bivalents were accompanied by a substantial frequency of multivalents, which varied by variety and by chromosome (7-48%). We identified possible sites of synaptic partner switching, leading to multivalent formation, and found potential defects in the polymerisation and/or maintenance of the synaptonemal complex in tetraploids. These findings demonstrate the rise of S. tuberosum as a model for autotetraploid meiotic recombination research and highlight constraints on meiotic chromosome configurations and chiasma frequencies as an important feature of an evolved autotetraploid meiosis.

Identifiants

pubmed: 32523055
doi: 10.1038/s41437-020-0328-6
pii: 10.1038/s41437-020-0328-6
pmc: PMC7490355
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

212-226

Subventions

Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/N008952/1

Références

Abraham K, Nemorin A, Lebot V, Arnau G (2013) Meiosis and sexual fertility of autotetraploid clones of greater yam Dioscorea alata L. Genet Resour Crop Evol 60:819–823
Akhunov ED, Goodyear AW, Geng S, Qi L-L, Echalier B, Gill BS et al. (2012) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763
Anderson L, Lohmiller LD, Tang X, Hammond DB, Javernick L, Shearer L et al. (2014) Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. Proc Natl Acad Sci USA 111(37):13415–13420
pubmed: 25197066
Armstrong SJ, Sanchez-Moran E, Franklin FCH (2009) Cytological Analysis of Arabidopsis thaliana Meiotic Chromosomes. Methods Molecular Biology. In: Keeney S Ed Methods in Molecular Biology. Humana Press, Totowa, NJ, p. 131–145
Barton DW (1951) Localized chiasmata in the differentiated chromosomes of the tomato. Genetics 36:372–381
Bauer E, Falque M, Walter H, Bauland C, Camisan C, Campo L et al. (2013) Intraspecific variation of recombination rate in maize. Genome Biol 14:R103
pubmed: 24050704 pmcid: 4053771
Blary A, Jenczewski E (2019) Manipulation of crossover frequency and distribution for plant breeding. Theor Appl Genet 132:575–592
pubmed: 30483818
Boden SA, Langridge P, Spangenberg G, Able JA (2009) TaASY1 promotes homologous chromosome interactions and is affected by deletion of Ph1. Plant J 57:487–497
pubmed: 18826431
Bomblies K, Higgins JD, Yant L (2015) Meiosis evolves: adaptation to external and internal environments. N. Phytol 208:306–323
Bomblies K, Jones G, Franklin C, Zickler D, Kleckner N (2016) The challenge of evolving stable polyploidy: could an increase in “crossover interference distance” play a central role? Chromosoma 125:287–300
pubmed: 26753761 pmcid: 4830878
Bourke P, Voorrips R, Visser RG, Maliepaard C (2015) The double-reduction landscape in tetraploid potato as revealed by a high-density linkage map. Genetics 201:853–863
pubmed: 26377683 pmcid: 4649655
Bourke PM, Arens P, Voorrips RE, Esselink GD, Koning-Boucoiran CF, Van’t Westende WP et al. (2017) Partial preferential chromosome pairing is genotype dependent in tetraploid rose. Plant J 90:330–343
pubmed: 28142191
Braz GT, He L, Zhao H, Zhang T, Semrau K, Rouillard JM et al. (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523
pubmed: 29242292
Brown SW (1949) The structure and meiotic behavior of the differentiated chromosomes of tomato. Genetics 34:437–461
pubmed: 17247326 pmcid: 1209457
Chen J, Leach L, Yang J, Zhang F, Tao Q, Dang Z, et al. (2020) A tetrasomic inheritance model and likelihood-based method for mapping quantitative trait loci in autotetraploid species. N. Phytol https://doi.org/10.1111/nph.16413
Chen J, Zhang F, Wang L, Leach L, Luo Z (2018) Orthogonal contrast based models for quantitative genetic analysis in autotetraploid species. N. Phytol 220:332–346
Copenhaver GP, Housworth EA, Stahl FW (2002) Crossover interference in Arabidopsis. Genetics 160:1631–1639
pubmed: 11973316 pmcid: 1462055
Davies A, Jenkins G, Rees H (1990) Diploidization of Lotus corniculatus L. (Fabacaea) by elimination of multivalents. Chromosoma 99:289–295
Dawson C (1941) Tetrasomic inheritance in Lotus corniculatus L. J Genet 42:49–73
De Carvalho CE, Colaiácovo MP (2006) SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev 20:1986–1992
pubmed: 16882975
Deniz B, Dogru U (2006) Meiotic behaviour in natural diploid, tetraploid, and commercial diploid crested wheatgrass. NZ J Agric Res 49:405–409
Dong F, Song J, Naess SK, Helgeson JP, Gebhardt C, Jiang J (2000) Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor Appl Genet 101:1001–1007
Dumont BL, Broman KW, Payseur BA (2009) Variation in genomic recombination rates among heterogeneous stock mice. Genetics 182:1345–1349
pubmed: 19535547 pmcid: 2728871
Esch E, Szymaniak JM, Yates H, Pawlowski W, Buckler ES (2007) Using crossover breakpoints in recombinant inbred lines to identify quantitative trait loci controlling the global recombination frequency. Genetics 177:1851–1858
pubmed: 17947409 pmcid: 2147985
Fjellstrom RG, Beuselinck PR, Steiner JJ (2001) RFLP marker analysis supports tetrasomic inheritance in Lotus corniculatus L. Theor Appl Genet 102:718–725
Gavrilenko T (2007) Potato cytogenetics. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives. Elsevier, p. 203–216. https://www.sciencedirect.com/book/9780444510181/potato-biology-and-biotechnology?via=ihub=#book-info
Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J (2015) Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics 220:771–779
He L, Braz GT, Torres GA, Jiang J (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513
pubmed: 30242479
Henderson KA, Keeney S (2004) Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc Natl Acad Sci USA 101:4519–4524
pubmed: 15070750
Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500
pubmed: 16230536 pmcid: 1257403
Higgins JD, Wright KM, Bomblies K, Franklin FC (2014) Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Front Plant Sci 4:546
pubmed: 24427164 pmcid: 3879461
Hollister JD, Arnold BJ, Svedin E, Xue KS, Dilkes BP, Bomblies K (2012) Genetic adaptation associated with genome doubling in autotetraploid Arabidopsis arenosa. PLoS Genet 8:e1003093
pubmed: 23284289 pmcid: 3527224
Hussain T (2016) Potatoes: ensuring food for the future. Adv Plants Agric Res 3(6):178–182
Iovene M, Zhang T, Qunfeng L, Buell CR, Jiang J (2013) Copy number variation in potato—an asexually propagated autotetraploid species. Plant J 75:80–89
pubmed: 23573982
Jones GH, Khazanehdari KA, Ford-Lloyd BV (1996) Meiosis in the leek (Allium porrum L.) revisited. II. Metaphase I Observations Heredity 76:186–191
Kamiri M, Stift M, Costantino G, Dambier D, Kabbage T, Ollitrault P, Froelicher Y (2018) Preferential homologous chromosome pairing in a tetraploid intergeneric somatic hybrid (Citrus reticulate + Poncirus trifoliata) revealed by molecular marker inheritance. Front Plant Sci 9:1557
pubmed: 30450106 pmcid: 6224360
Khawaja HIT, Sybenga J, Ellis JR (1997) Chromosome pairing and chiasma formation in autopolyploids of different Lathyrus species. Genome 40(6):937–944
pubmed: 18464879
Khazanehdari KA, Jones GH, Ford-Lloyd BV (1995) Meiosis in the leek (Allium porrum L.) revisited I. Prophase I pairing. Chromosome Res 3:443–439
Koul KK, Nagpal R, Sharma A (1999) Peculiarities of chromosomal behaviour in the natural autotetraploid Pennisetum orientale L.C. Rich. Caryologia 52:185–195
Kunzel G, Waugh R (2002) Integration of microsatellite markers into the translocation-based physical RFLP map of barley chromosome 3H. Theor Appl Genet 105:660–665
pubmed: 12582478
Lloyd A, Bomblies K (2016) Meiosis in autopolyploid and allopolyploid Arabidopsis. Curr Opin Plant Biol 30:116–122
pubmed: 26950252
López E, Pradillo E, Oliver C, Romero C, Cunado N, Santos JL (2012) Looking for natural variation in chiasma frequency in Arabidopsis thaliana. J Exp Bot 63:887–894
pubmed: 22048037
Luo ZW, Zhang Z, Leach L, Zhang RM, Bradshaw JE, Kearsey MJ (2006) Constructing genetic linkage maps under a tetrasomic model. Genetics 172:2634–2645
Magoon ML, Ramanujam S, Cooper DC (1962) Cytogenetical studies in relation to the origin and differentiation of species in the genus Solanum L. Caryologia 15:151–252
Marand AP, Jansky SH, Zhao H, Leisner CP, Zhu X, Zeng Z, Crisovan E, Newton L, Hamernik AJ, Veilleux RE, Buell R, Jiang J (2017) Meiotic crossovers are associated with open chromatin and enriched with Stowaway transposons in potato. Genome Biol 18:203
pubmed: 29084572 pmcid: 5663088
McCollum CD (1958) Comparative studies of chromosome pairing in natural and induced tetraploid Dactylis. Chromosoma 9:571–605
pubmed: 13619012
Morgan C, Zhang H, Henry CE, Franklin FCH, Bomblies K (2020) Derived alleles of two axis proteins affect meiotic traits in autotetraploid Arabidopsis arenosa. Proc Natl Acad Sci USA 117:8980–8988
pubmed: 32273390
Morgan CH, Zhang H, Bomblies K (2017) Are the effects of elevated temperature on meiotic recombination and thermotolerance linked via the axis and synaptonemal complex? Philos Trans R Soc B 372:20160470
Mulligan A (1967) Diploid and tetraploid Physaria vitulifera (Cruciferae). Can J Bot 45:183–188
Osman K, Yang J, Roitinger E, Lambing C, Heckmann S, Howell E et al. (2018) Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J 93:7–33
Park T-H, Kim J-B, Hutten RCB, van Eck HJ, Jacobsen E, Visser RGF (2007) Genetic positioning of centromeres using helf-tetrad analysis in a 4x-2x cross population of potato. Genetics 176:85–94
pubmed: 17339217 pmcid: 1893073
Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. N. Phytol 186:5–17
Parra-Nunez P, Pradillo M, Santos JL (2019) Competition for chiasma formation between identical and homologous (but not identical) chromosomes in synthetic autotetraploids of Arabidopsis thaliana. Front Plant Sci 9:1924
pubmed: 30687342 pmcid: 6333688
Qu L, Hancock JF, Whallon JH (1998) Evolution in an autopolyploid group displaying predominantly bivalent pairing at meiosis: Genomic similarity of diploid Vaccinium darrowi and autotetraploid V. corymbosum (Ericaceae). Am J Bot 85:698–703
pubmed: 21684952
Qu M, Li K, Han Y, Chen L, Li Z, Han Y (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164
pubmed: 29262412
Quiros CF (1982) Tetrasomic segregation for multiple alleles in alfalfa. Genetics 101(1):117–127
pubmed: 17246077 pmcid: 1201845
Sanchez-Moran E, Armstrong SJ, Santos JL, Franklin FCH, Jones GH (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res 9:121–128
pubmed: 11321367
Sanchez-Moran E, Armstrong SJ, Santos JL, Franklin FCH, Jones GH (2002) Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162:1415–1422
pubmed: 12454084 pmcid: 1462347
Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220–2233
pubmed: 17785529 pmcid: 1950860
Sangowawa BG (1989) Meiotic studies in a wild tetraploid potato (Solanum hjertingii Hawkes). Cytologia 54:617–626
Santos JL, Alfaro D, Sanchez-Moran E, Armstrong SJ, Franklin FCH, Jones GH (2003) Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165:1533–1540
pubmed: 14668400 pmcid: 1462840
Searchinger T, Waite R, Hanson C, Ranganathan J, Dumas D (2018) World Resources Report Creating a sustainable food future: synthesis report https://wrr-food.wri.org/authors-and-contributors-acknowledgments
Sharma SK, Bolser D, de Boer J, Sonderkaer M, Amoros W, Carboni MF et al. (2013) Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. G3 3:2031–2047
pubmed: 24062527
Sharma SK, MacKenzie K, McLean K, Dale F, Daniels S, Bryan GJ (2018) Linkage disequilbrium and evaluation of genome-wide association mapping models in tetraploid potato. G3 8:3185–3202
pubmed: 30082329
Shaver DL (1962) A study of meiosis in perennial Teosinte, in tetraploid maize and in their tetraploid hybrid. Caryologia 15:43–57
Sherman JD, Stack SM (1995) Two-dimensional spreads of synaptonemal complexes from Solanaceous plants VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141:683–708
pubmed: 8647403 pmcid: 1206766
Soltis DE, Soltis PS, Rieseberg LH (1993) Molecular data and the dynamic nature of polyploidy. Crit Rev Plant Sci 12:243–247
Stift M, Berenos C, Kuperus P, Van Tienderen P (2008) Segregation models for disomic, tetrasomic and intermediate inheritance in tetraploids: a general procedure applied to Rorippa (yellow cress) microsatellite data. Genetics 179:2113–2123
pubmed: 18689891 pmcid: 2516083
Stift M, Reeve R, van Tienderen PH (2010) Inheritance in tetraploid yeast revisited: segregation patterns and statistical power under different inheritance models. J Evol Biol 23:1570–1578
pubmed: 20524952
Stronghill PE, Azimi W, Hasenkampf CA (2014) A novel method to follow meiotic progression in Arabidopsis using confocal microscopy and 5-ethynyl-2′-deoxyuridine labeling. Plant Methods 10:33
pubmed: 25337148 pmcid: 4203904
Sturtevant AH (1915) The behavior of chromosome as studied through linkage. Z indukt Abstamm-u VererbLehre 13:234–287
Swaminathan MS (1954) Microsporogenesis in some commercial potato varieties. J Heredity 45:265–272
Sybenga J (1975) The Analysis of Chromosome Pairing, in Meiotic Configurations: A Source of Information for Estimating Genetic Parameters. Springer, Berlin, Heidelberg, p. 134–199
Sym M, Roeder GS (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. Cell Biol 128:455–466
Tang X, de Boer J, van Eck H, Bachem C, Visser RG, de Jong H (2009) Assignment of genetic linkage maps to diploid Solanum tuberosum pachytene chromosomes by BAC-FISH technology. Chromosome Res 17:899–915
pubmed: 19774472 pmcid: 2776164
The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 585:635–641
Vincent JE, Jones GH (1993) Meiosis in autotetraploid Crepis capillaris I. Triploids and trisomics; implications for models of chromosome pairing. Chromosoma 102:195–206
Wolf PG, Soltis PM, Soltis DE (1989) Tetrasomic inheritance and chromosome pairing behaviour in the naturally occurring autotetraploid Heuchera grossulariifolia (Saxifragaceae). Genome 32:655–659
Wu JH, Datson PM, Manako KI, Murray BG (2014) Meiotic chromosome pairing behaviour of natural tetraploids and induced autotetraploids of Actinidia chinensis. Theor Appl Genet 127:549–557
pubmed: 24306317
Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P et al. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195
pubmed: 21743474
Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, Bomblies K (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol 23:2151–2156
pubmed: 24139735

Auteurs

Anushree Choudhary (A)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.

Liam Wright (L)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.

Olga Ponce (O)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.

Jing Chen (J)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.

Ankush Prashar (A)

School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK.

Eugenio Sanchez-Moran (E)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.

Zewei Luo (Z)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK.
Institute of Biostatistics, Fudan University, Shanghai, 200433, China.

Lindsey Compton (L)

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK. l.j.compton@bham.ac.uk.

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