The novel expression of clonality following whole-genome multiplication compensates for reduced fertility in natural autopolyploids
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37357859
PubMed Central
PMC10291721
DOI
10.1098/rspb.2023.0389
Knihovny.cz E-zdroje
- Klíčová slova
- aneuploidy, apospory, clonality, mixed-ploidy, root-sprouting, unreduced gametes,
- MeSH
- diploidie MeSH
- fertilita * MeSH
- ploidie * MeSH
- polyploidie MeSH
- rozmnožování MeSH
- semena rostlinná MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Exploring the fitness consequences of whole-genome multiplication (WGM) is essential for understanding the establishment of autopolyploids in diploid parental populations, but suitable model systems are rare. We examined the impact of WGM on reproductive traits in three major cytotypes (2x, 3x, 4x) of Pilosella rhodopea, a species with recurrent formation of neo-autopolyploids in mixed-ploidy populations. We found that diploids had normal female sporogenesis and gametogenesis, high fertility, and produced predominantly euploid seed progeny. By contrast, autopolyploids had highly disturbed developmental programs that resulted in significantly lower seed set and a high frequency of aneuploid progeny. All cytotypes, but particularly triploids, produced gametes of varying ploidy, including unreduced ones, that participated in frequent intercytotype mating. Noteworthy, the reduced investment in sexual reproduction in autopolyploids was compensated by increased production of axillary rosettes and the novel expression of two clonal traits: adventitious rosettes on roots (root-sprouting), and aposporous initial cells in ovules which, however, do not result in functional apomixis. The combination of increased vegetative clonal growth in autopolyploids and frequent intercytotype mating are key mechanisms involved in the formation and maintenance of the largest diploid-autopolyploid primary contact zone ever recorded in angiosperms.
Department of Biology University of Fribourg Fribourg Switzerland
Herbarium Collections and Department of Botany Charles University Prague Czechia
Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Germany
Plant Science and Biodiversity Centre Slovak Academy of Sciences Bratislava Slovakia
Zobrazit více v PubMed
Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Molec. Plant 11, 414-428. (10.1016/j.molp.2018.01.002) PubMed DOI
Comai L. 2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846. (10.1038/nrg1711) PubMed DOI
Parisod C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5-17. (10.1111/j.1469-8137.2009.03142.x) PubMed DOI
Ramsey J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl Acad. Sci. USA 108, 7096-7101. (10.1073/pnas.1016631108) PubMed DOI PMC
Barker MS, Husband BC, Pires JC. 2016. Spreading winge and flying high: the evolutionary importance of polyploidy after a century of study. Amer. J. Bot. 103, 1139-1145. (10.3732/ajb.1600272) PubMed DOI
Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424. (10.1038/nrg.2017.26) PubMed DOI
Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Proc. R. Soc. B 369, 20130352. (10.1098/rstb.2013.0352) PubMed DOI PMC
Spoelhof JP, Soltis PS, Soltis DE. 2017. Pure polyploidy: closing the gaps in autopolyploid research. J. Syst. Evol. 55, 340-352. (10.1111/jse.12253) DOI
Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS. 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56, 13-30. (10.2307/25065732) DOI
Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Evol. Syst. 29, 467-501. (10.1146/annurev.ecolsys.29.1.467) DOI
Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Evol. Syst. 33, 589-639. (10.1146/annurev.ecolsys.33.010802.150437) DOI
Cifuentes M, Grandont L, Moore G, Chèvre AM, Jenczewski E. 2010. Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol. 186, 29-36. (10.1111/j.1469-8137.2009.03084.x) PubMed DOI
Levin D. 1975. Minority cytotype exclusion in local plant populations. Taxon 24, 35-43. (10.2307/1218997) DOI
Husband BC. 2000. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proc. R. Soc. Lond. B 267, 217-223. (10.1098/rspb.2000.0990) PubMed DOI PMC
Köhler C, Mittelsten Scheid O, Erilova A. 2010. The impact of the triploid block on the origin and evolution of polyploid plants. Trends Genet. 26, 142-148. (10.1016/j.tig.2009.12.006) PubMed DOI
Eliášová A, Trávníček P, Mandák B, Münzbergová Z. 2014. Autotetraploids of Vicia cracca show a higher allelic richness in natural populations and a higher seed set after artificial selfing than diploids. Ann. Bot. 113, 159-170. (10.1093/aob/mct252) PubMed DOI PMC
Van Drunen WE, Friedman J. 2022. Autopolyploid establishment depends on life history strategy and the mating outcomes of clonal architecture. Evolution 76, 1953-1976. (10.1111/evo.14582) PubMed DOI
Koltunow M. 1993. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5, 1425-1437. (10.1105/tpc.5.10.1425) PubMed DOI PMC
Klimeš L, Klimešová J, Hendriks R, van Groenendael J. 1997. Clonal plant architectures: a comparative analysis of form and function. In The ecology and evolution of clonal plants (eds de Kroon H., van Groenendael J), pp. 1-29. Leiden, The Netherlands: Backhuys Publishers.
Vallejo-Marín M, Dorken ME, Barrett SCH. 2010. The ecological and evolutionary consequences of clonality for plant mating. Annu. Rev. Ecol. Evol. Syst. 41, 193-213. (10.1146/annurev.ecolsys.110308.120258) DOI
Chrtek J, Herben T, Rosenbaumová R, Münzbergová Z, Dočkalová Z, Zahradníček J, Krejčíková J, Trávníček P. 2017. Cytotype coexistence in the field cannot be explained by inter-cytotype hybridization alone: linking experiments and computer simulations in the sexual species Pilosella echioides (Asteraceae). BMC Evol. Biol. 17, 87. (10.1186/s12862-017-0934-y) PubMed DOI PMC
Ortiz JP, et al. 2013. Harnessing apomictic reproduction in grasses: what we have learned from Paspalum. Ann. Bot. 112, 767-787. (10.1093/aob/mct152) PubMed DOI PMC
Karunarathne P, Hojsgaard D. 2021. Single independent autopolyploidization events from distinct diploid gene pools and residual sexuality support range expansion of locally adapted tetraploid genotypes in a South American grass. Front. Genet. 12, 736088. (10.3389/fgene.2021.736088) PubMed DOI PMC
Beck BB, Windham MD, Pryer KM. 2011. Do asexual polyploid lineages lead short evolutionary lives? A case study from the fern genus Astrolepis. Evolution 65, 3217-3229. (10.1111/j.1558-5646.2011.01362.x) PubMed DOI
Chrtek J, et al. 2020. Evolutionary history and genetic diversity of apomictic allopolyploids in Hieracium s.str. morphological versus genomic features. Amer. J. Bot. 107, 66-90. (10.1002/ajb2.1413) PubMed DOI
Müntzing A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21, 363-378. (10.1111/j.1601-5223.1936.tb03204.x) DOI
Gustafsson A. 1948. Polyploidy, life-form and vegetative reproduction. Hereditas 34, 1-22. (10.1111/j.1601-5223.1948.tb02824.x) DOI
Obeso JR. 2002. The costs of reproduction in plants. New Phytol. 155, 321-348. (10.1046/j.1469-8137.2002.00477.x) PubMed DOI
Herben T, Suda J, Klimešová J. 2017. Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. Ann. Bot. 120, 341-349. (10.1093/aob/mcx009) PubMed DOI PMC
Van Drunen WE, Husband BC. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytol. 224, 1266-1277. (10.1111/nph.15999) PubMed DOI
Eckert CG, Lui K, Bronson K, Corradini P, Bruneau A. 2003. Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Molec. Ecol. 12, 331-344. (10.1046/j.1365-294X.2003.01737.x) PubMed DOI
Fialová M, Jandová M, Ohryzek J, Duchoslav M. 2014. Biology of the polyploid geophyte Allium oleraceum (Amaryllidaceae): variation in size, sexual and asexual reproduction and germination within and between tetra-, penta- and hexaploid cytotypes. Flora 209, 312-324. (10.1016/j.flora.2014.04.001) DOI
Baldwin SJ, Husband BC. 2013. The association between polyploidy and clonal reproduction in diploid and tetraploid Chamerion angustifolium. Molec. Ecol. 22, 1806-1819. (10.1111/mec.12217) PubMed DOI
Martínková J, Klimešová J, Doležal J, Kolář F. 2015. Root sprouting in Knautia arvensis (Dipsacaceae): effects of polyploidy, soil origin and nutrient availability. Plant Ecol. 216, 901-911. (10.1007/s11258-015-0477-5) DOI
Weiss-Schneeweiss H, Emadzade K, Jang TS, Schneeweiss GM. 2013. Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenet. Genome Res. 140, 137-150. (10.1159/000351727) PubMed DOI PMC
Van Drunen WE, Husband BC. 2018. Immediate vs. evolutionary consequences of polyploidy on clonal reproduction in an autopolyploid plant. Ann. Bot. 122, 195-205. (10.1093/aob/mcy071) PubMed DOI PMC
Husband BC, Ozimec B, Martin SL, Pollock L. 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. Int. J. Plant Sci. 169, 195-206. (10.1086/523367) DOI
Van Drunen WE, Husband BC. 2018. Whole genome duplication decreases clonal stolon production and genet size in the wild strawberry Fragaria vesca. Amer. J. Bot. 105, 1712-1724. (10.1002/ajb2.1159) PubMed DOI
Blakeslee A, Avery A. 1937. Methods of inducing doubling of chromosomes in plants by treatment with colchicine. J. Hered. 28, 393-411. (10.1093/oxfordjournals.jhered.a104294) DOI
Münzbergová Z. 2017. Colchicine application significantly affects plant performance in the second generation of synthetic polyploids and its effects vary between populations. Ann. Bot. 120, 329-339. (10.1093/aob/mcx070) PubMed DOI PMC
Jaskani MJ, Kwon SW, Kim DH. 2005. Comparative study on vegetative, reproductive and qualitative traits of seven diploid and tetraploid watermelon lines. Euphytica 145, 259-268. (10.1007/S10681-005-1644-X) DOI
Cohen H, Fait A, Tel-Zur N. 2013. Morphological, cytological and metabolic consequences of autopolyploidization in Hylocereus (Cactaceae) species. BMC Plant Biol. 13, 173. (10.1186/1471-2229-13-173) PubMed DOI PMC
Bretagnolle F, Thompson JD. 1995. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129, 1-22. (10.1111/j.1469-8137.1995.tb03005.x) PubMed DOI
Yamauchi A, Hosokawa A, Nagata H, Shimoda M. 2004. Triploid bridge and role of parthenogenesis in the evolution of autopolyploidy. Amer. Nat. 164, 101-112. (10.1086/421356) PubMed DOI
Mason AS, Pires JC. 2015. Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet. 31, 5-10. (10.1016/j.tig.2014.09.011) PubMed DOI
Šingliarová B, Hodálová I, Mráz P. 2011. Biosystematic study of the diploid-polyploid Pilosella alpicola complex with variation in breeding system: patterns and processes. Taxon 60, 450-470. (10.1002/TAX.602014) DOI
Šingliarová B, Zozomová-Lihová J, Mráz P. 2019. Polytopic origin and scale-dependent spatial segregation of cytotypes in primary diploid–autopolyploid contact zones of Pilosella rhodopea (Asteraceae). Biol. J. Linn. Soc. 127, 173. (10.1093/biolinnean/blz035) DOI
Šingliarová B, Mráz P, Chrtek J, Plačková I. 2011. Allozyme variation in diploid, polyploid and ploidy-mixed populations of the Pilosella alpicola group (Asteraceae): relation to morphology, origin of polyploids and breeding system. Folia Geobot. 46, 387-410. (10.1007/s12224-011-9102-0) DOI
Krahulcová A, Krahulec F, Chapman HM. 2000. Variation in Hieracium subgen. Pilosella (Asteraceae): What do we know about its sources? Folia Geobot. 35, 319-338. (10.1007/BF02803122) DOI
Šingliarová B, Šuvada R, Mráz P. 2013. Allopatric distribution, ecology and conservation status of the Pilosella alpicola species group (Asteraceae). Nord. J. Bot. 31, 122-128. (10.1111/j.1756-1051.2012.01603.x) DOI
Otto F. 1990. DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In Methods in cell biology (eds Crissman H, Darzynkiewicz Z), pp. 105-110. New York, NY: Academic Press. PubMed
Doležel J, Göhde W. 1995. Sex determination in dioecious plants Melandrium album and M. rubrum using high resolution flow cytometry. Cytometry 19, 103-106. (10.1002/cyto.990190203) PubMed DOI
Schönswetter P, Suda J, Popp M, Weiss-Schneeweiss H, Brochmann C. 2007. Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Molec. Phylogen. Evol. 42, 92-103. (10.1016/j.ympev.2006.06.016) PubMed DOI
Loureiro J, Rodriguez E, Doležel J, Santos C. 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann. Bot. 100, 875-888. (10.1093/aob/mcm152) PubMed DOI PMC
Mráz P, Šingliarová B, Urfus T, Krahulec F. 2008. Cytogeography of Pilosella officinarum (Compositae): altitudinal and longitudinal differences in ploidy level distribution in the Czech Republic and Slovakia and the general pattern in Europe. Ann. Bot. 101, 59-71. (10.1093/aob/mcm282) PubMed DOI PMC
Hand ML, Vít P, Krahulcová A, Johnson SD, Oelkers K, Siddons H, Chrtek J, Fehrer J, Koltunow AM. 2015. Evolution of apomixis loci in Pilosella and Hieracium (Asteraceae) inferred from the conservation of apomixis-linked markers in natural and experimental populations. Heredity 114, 17-26. (10.1038/hdy.2014.61) PubMed DOI PMC
Matzk F, Meister A, Schubert I. 2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J. 21, 97-108. (10.1046/j.1365-313x.2000.00647.x) PubMed DOI
R Core Team. 2023. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. (http://www.r-project.org).
Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R. 2017. Nlme: linear and nonlinear mixed effects models. R package version 3.1-131. Vienna, Austria: R Foundation for Statistical Computing.
Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48. (10.18637/jss.v067.i01) DOI
Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biom. J. 50, 346-363. (10.1002/bimj.200810425) PubMed DOI
Stoffel MA, Nakagawa S, Schielzeth H. 2020. partR2: Partitioning R2 in generalized linear mixed models. bioRxiv. (10.1101/2020.07.26.221168) DOI
Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, Kubešová M, Suda J. 2009. Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Ann. Bot. 103, 963-974. (10.1093/aob/mcp016) PubMed DOI PMC
Castro S, Münzbergová Z, Raabová J, Loureiro J. 2011. Breeding barriers at a diploid–hexaploid contact zone in Aster amellus. Evol. Ecol. 25, 795-814. (10.1007/s10682-010-9439-5) DOI
Mráz P, Španiel S, Keller A, Bowmann G, Farkas A, Šingliarová B, Rohr RP, Broennimann O, Müller-Schärer H. 2012. Anthropogenic disturbance as a driver of microspatial and microhabitat segregation of cytotypes of Centaurea stoebe and cytotypes interactions in secondary contact zones. Ann. Bot. 110, 615-627. (10.1093/aob/mcs120) PubMed DOI PMC
Hardy OJ, De Loose M, Vekemans X, Meerts P. 2001. Allozyme segregation and inter-cytotype reproductive barriers in the polyploid complex Centaurea jacea. Heredity 87, 136-145. (10.1046/j.1365-2540.2001.00862.x) PubMed DOI
Koutecký P, Baďurová T, Štech M, Košnar J, Karásek J. 2011. Hybridization between diploid Centaurea pseudophrygia and tetraploid C. jacea (Asteraceae): the role of mixed pollination, unreduced gametes, and mentor effects. Biol. J. Linn. Soc. 104, 93-106. (10.1111/j.1095-8312.2011.01707.x) DOI
Morgan EJ, Čertner M, Lučanová M, Deniz U, Kubíková K, Venon A, Kovářík O, Lafon Placette C, Kolář F. 2021. Disentangling the components of triploid block and its fitness consequences in natural diploid–tetraploid contact zones of Arabidopsis arenosa. New Phytol. 232, 1449-1462. (10.1111/nph.17357) PubMed DOI
Lafon-Placette C, et al. 2017. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc. Natl Acad. Sci. USA 114, E1027-E1035. (10.1073/pnas.1615123114) PubMed DOI PMC
Santner A, Calderon-Villalobos LI, Estelle M. 2009. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301-307. (10.1038/nchembio.165) PubMed DOI
Hojsgaard D, Pullaiah T. 2022. Apomixis in angiosperms: mechanisms, occurrences and biotechnology. Boca Raton, FL: CRC Press.
Böcher T. 1951. Cytological and embryological studies in the amphi-apomictic Arabis holboellii complex. Biol. Skr. 6, 1-58.
Janas AB, Szeląg Z, Musiał K. 2021. In search of female sterility causes in the tetraploid and pentaploid cytotype of Pilosella brzovecensis (Asteraceae). J. Plant Res. 134, 803-810. (10.1007/s10265-021-01290-8) PubMed DOI PMC
Hojsgaard D. 2018. Transient activation of apomixis in sexual neotriploids may retain genomically altered states and enhance polyploid establishment. Front. Plant Sci. 9, 230. (10.3389/fpls.2018.00230) PubMed DOI PMC
Rosenberg O. 1906. Über die Embryobildung in der Gattung Hieracium. Ber. Deutsch. Bot. Ges. 24, 157-161. (10.1111/j.1438-8677.1906.tb06494.x) DOI
Rosenberg O. 1907. Cytological studies on the apogamy in Hieracium. Bot. Tiddskr. 28, 143-170.
Koltunow AMG, Johnson SD, Okada T. 2011. Apomixis in hawkweed: Mendel's experimental nemesis. J. Exp. Bot. 62, 1699-1170. (10.1093/jxb/err011) PubMed DOI
Catanach AS, Erasmuson SK, Podivinsky E, Jordan BR, Bicknell R. 2006. Deletion mapping of genetic regions associated with apomixis in Hieracium. Proc. Natl Acad. Sci. USA 103, 18 650-18 655. (10.1073/pnas.0605588103) PubMed DOI PMC
Hojsgaard D, Hörandl E. 2019. The rise of apomixis in natural plant populations. Front. Plant Sci. 10, 358. (10.3389/fpls.2019.00358) PubMed DOI PMC
Zahn KH. 1930. Hieracium L. In Synopsis der mitteleuropäischen Flora XXII/1 (eds Graebner P, Graebner P). Liepzig, Germany: Borntraeger.
Peterson RL, Thomas AG. 1971. Buds on the roots of Hieracium florentinum (hawkweed). Botany 49, 53-54.
Bomblies K. 2020. When everything changes at once: finding a new normal after genome duplication. Proc. R. Soc. B. 287, 2020215420202154. (10.1098/rspb.2020.2154) PubMed DOI PMC
Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D. 2009. Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J. 57, 626-644. (10.1111/j.1365-313X.2008.03715.x) PubMed DOI
Rosspopoff O, et al. 2017. Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development 144, 1187-1200. (10.1242/dev.142570) PubMed DOI
Martínková J, et al. 2023. What determines root-sprouting ability: injury or phytohormones? Am. J. Bot. 110, e16102. (10.1002/ajb2.16102) PubMed DOI
Martínková J, et al. 2023. Why is root-sprouting not more common among plants? Phytohormonal clues and ecological correlates. Environ. Exp. Bot. 205, 105147. (10.1016/j.envexpbot.2022.105147) DOI
Šingliarová B, Hojsgaard D, Müller-Schärer H, Mráz P. 2023. The novel expression of clonality following whole-genome multiplication compensates for reduced fertility in natural autopolyploids. Figshare. (10.6084/m9.figshare.c.6700004) PubMed DOI PMC
figshare
10.6084/m9.figshare.c.6700004