Endopolyploidy in Plants

Abstract

Endopolyploidy is a general term describing the multiplication of nuclear DNA within the cell. In plants, this takes place via several mechanisms but mainly through the process of endoreduplication. Endoreduplication involves the replication of chromosomal deoxyribonucleic acid (DNA) without intervening mitoses and no obvious chromatin condensation/decondensation, with chromatids staying united either at the centromere or rarely, along their entire length. The occurrence of this form of endopolyploidy is uneven across plants; thus far, it has not been detected in some lineages (e.g. liverworts), whereas it is common in angiosperms (flowering plants), where very high levels (up to 24 567C) of endopolyploidy have been reported in some tissues. Internal and external factors contribute to the mechanisms underlying endopolyploidy, which can be seen as a key part of the developmental flexibility of plants. Recent work has shown that endopolyploidy may also play an important role in the response of plants to environmental stress.

Key Concepts

  • The frequency of endopolyploidy varies across different lineages of land plants.
  • Three types of endopolyploidy have been reported in plants – endocycles, endomitosis and progressive partial endoreduplication, of which the endocycle is the most common.
  • Endopolyploidy can reach very high levels in some plant cells (up to 24 567C).
  • Endopolyploidy can lead to an increase in cell size, especially when the number of endocycles is high.
  • The switch from the mitotic cell cycle to the endocycle involves changes in the regulation and abundance of a variety of cyclin‐dependent kinases (CDKs), cyclins (CYC) and regulatory proteins/transcription factors.
  • Endopolyploidy is common in reproductive tissues of plants, for example the nutritive tissue of the endosperm in seeds.
  • The onset of endopolyploidy is induced in some cell tissues in response to stress.

Keywords: endopolyploidy; endoreduplication; endocycle; endomitosis; ploidy; cell size; cell differentiation; cell cycle; stress; DNA damage response

Figure 1. Endopolyploidy in plants. The canonical mitotic cell cycle is shown on the left, which includes different phases: synthesis (S phase) where DNA is replicated and mitosis (M phase) where chromosomes segregate and cells divide to produce two daughter cells, with each precededd by a gap phase (G1 or G2) preceding each. In the endocycle, mitosis (M phase) is absent, resulting in one G phase and S phase and a doubling of DNA (4C) per endocycle but not chromosome number (2n). In endomitosis, cells enter mitosis and chromosomes segregate but exit before cell division (i.e. partial M phase), resulting in a doubling of chromosome number as well as DNA (4C, 4n). Finally, in partial endocycles (also known as partial progressive endoreduplication – PPE), cells skip M phase, but during S phase, they only replicate specific parts of the chromosomal DNA, resulting in cells with partial increases in DNA content (2C + P where P is the part of the 2C genome that has been replicated). Figure based on Breuer et al. 2014 © Elsevier.
Figure 2. Cell size is closely correlated with ploidy in the leaf epidermis of Arabidopsis thaliana. Nuclei are stained with 4′6‐diamidino‐2‐phenylindole (DAPI). Scale Bar, 100 µm in a large panel and 10 µm in the insets.
Figure 3. Endopolyploidy in Feulgen‐stained antipodal cell nuclei of grasses. (a) Nuclei of hexaploid Triticum aestivum (2n = 6x = 42) comparing the large endopolyploid antipodal cell nucleus containing a 256C DNA content with two somatic nuclei with 4C DNA contents. (b) Four 256‐stranded chromosomes (arrowed) from an antipodal cell of Secale cereale compared with ovular nuclei with 2C or 4C DNA contents. Scale bar = 10 µm. Reproduced with permission from Bennett 2004 © John Wiley and Sons.
Figure 4. Distribution of endopolyploidy across land plants superimposed on a summary phylogenetic tree showing broadscale relationships between land plant groups (according to a current consensus of molecular phylogenetic results). Presence (+), absence (−), rare occurrence (∼) or lack of available data (?) are indicated for the major lineages of vascular and nonvascular land plants. ANA grade, Amborella, Nymphaeales and Austrobaileyales.
Figure 5. Molecular mechanisms underpinning the endocycle in plants, showing the interaction of cyclin‐dependent kinases (CDKs) and cyclins (CYCs) in the cell cycle (a) and endocycle (b). CDKA and CDKB determine the transition from one phase of the cell cycle to the next, with CDKA present constantly and CDKB thought to be specific for the G2/M transition. The anaphase‐promoting complex/cyclosome (APC/C) participates in the degradation of CYCs, therefore preventing cells from entering mitosis prematurely. The switch to the endocycle is governed by a decrease in CYC‐CDKB1 activity and inactivation of CYCA2;3. Only CYCA and CYCD have been shown to be active during the endocycle, where constant activity of APC/C ensures that cells do not enter mitosis.
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References

Adachi S, Minamisawa K, Okushima Y, et al. (2011) Programmed induction of endoreduplication by DNA double‐strand breaks in Arabidopsis. Proceedings of the National Academy of Sciences 108: 10004–10009.

Bainard J, Henry T, Bainard L and Newmaster S (2011a) DNA content variation in monilophytes and lycophytes: large genomes that are not endopolyploid. Chromosome Research 19: 763–775.

Bainard JD, Bainard LD, Henry TA, Fazekas AJ and Newmaster SG (2012) A multivariate analysis of variation in genome size and endoreduplication in angiosperms reveals strong phylogenetic signal and association with phenotypic traits. New Phytologist 196: 1240–1250.

Bainard JD and Newmaster SG (2010) Endopolyploidy in Bryophytes: widespread in mosses and absent in liverworts. Journal of Botany 2010: 7Article ID 316356.

Bainard JD and Villarreal JC (2013) Genome size increases in recently diverged hornwort clades. Genome 56: 431–435.

Bainard LD, Bainard JD, Newmaster SG and Klironomos JN (2011b) Mycorrhizal symbiosis stimulates endoreduplication in angiosperms. Plant, Cell & Environment 34: 1577–1585.

Barow M and Meister A (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant, Cell & Environment 26: 571–584.

Bennett MD (2004) Perspectives on polyploidy in plants ‐ ancient and neo. Biological Journal of the Linnean Society 82: 411–423.

Bory S, Catrice O, Brown SC, et al. (2008) Natural polyploidy in Vanilla planifolia (Orchidaceae). Genome 51: 816–826.

Brady T (1973) Feulgen cytophotometric determination of the DNA content of the embryo proper and suspensor cells of Phaseolus coccineus. Cell Differentiation 2: 65–75.

Ceccarelli M, Santantonio E, Marmottini F, Amzallag GN and Cionini PG (2006) Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolor. Protoplasma 227 (2): 113–118.

Chen P and Umeda M (2015) DNA double‐strand breaks induce the expression of flavin‐containing monooxygenase and reduce root meristem size in Arabidopsis thaliana. Genes to Cells 20: 636–646.

Ciccia A and Elledge SJ (2010) The DNA damage response: making it safe to play with knives. Molecular Cell 40: 179–204.

Cookson SJ, Radziejwoski A and Granier C (2006) Cell and leaf size plasticity in Arabidopsis: what is the role of endoreduplication? Plant, Cell & Environment 29 (7): 1273–1283.

de Almeida Engler J and Gheysen G (2012) Nematode‐induced endoreduplication in plant host cells: why and how? Molecular Plant‐Microbe Interactions 26: 17–24.

De Veylder L, Larkin JC and Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends in Plant Science 16: 624–634.

Dodsworth S, Chase MW, Leitch AR. (2016) Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Botanical Journal of the Linnean Society 180: 1–5.

El Maataoui M and Pichot C (1999) Nuclear and cell fusion cause polyploidy in the megagametophyte of common cypress, Cupressus sempervirens L. Planta 208: 345–351.

Erbrich P (1965) Über Endopolyploidie und Kernstrukturen in Endospermhaustorien. Österreichische botanische Zeitschrift 112: 197–262.

Frisch B and Nagl W (1979) Patterns of endopolyploidy and 2C nuclear DNA content (Feulgen) in Scilla (Liliaceae). Plant Systematics and Evolution 131: 261–276.

Galbraith DW, Harkins KR and Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiology 96: 985–989.

Garreta AG, Siguan MAR, Soler NS, Lluch JR and Kapraun DF (2010) Fucales (Phaeophyceae) from Spain characterized by large‐scale discontinuous nuclear DNA contents consistent with ancestral cryptopolyploidy. Phycologia 49: 64–72.

Gegas VC, Wargent JJ, Pesquet E, et al. (2014) Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV‐B. Journal of Experimental Botany 65: 2757–2766.

Goff LJ and Coleman AW (1990) DNA microspectrofluorometric studies. In: Cole KM and Sheath RG (eds) Biology of Red Algae, pp. 43–72. Cambridge: Cambridge University Press.

Hu Z, Cools T and De Veylder L (2016) Mechanisms used by plants to cope with DNA damage. Annual Review of Plant Biology 67: 439–462.

Husband BC, Baldwin SJ and Suda J (2013) The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Leitch IJ, Greilhuber J, Doležel J and Wendel JF (eds) Plant Genome Diversity, vol 2, Physical Structure, Behaviour and Evolution of Plant Genomes, pp. 255–276. Wien: Springer‐Verlag.

Ishida T, Adachi S, Yoshimura M, et al. (2010) Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 137: 63–71.

Kinoshita I, Sanbe A and Yokomura E‐I (2008) Difference in light‐induced increase in ploidy level and cell size between adaxial and abaxial epidermal pavement cells of Phaseolus vulgaris primary leaves. Journal of Experimental Botany 59 (6): 1419–1430.

Kondorosi E and Kondorosi A (2004) Endoreduplication and activation of the anaphase‐promoting complex during symbiotic cell development. FEBS Letters 567: 152–157.

Kwiatkowska M, Wojtczak A and Poptoriska K (1998) Effect of GA3 treatment on the number of spermatozoids and endopolyploidy levels of non‐generative cells in antheridia of Chara vulgaris L. Plant and Cell Physiology 39: 1388–1390.

Larkins BA, Dilkes BP, Dante RA, et al. (2001) Investigating the hows and whys of DNA endoreduplication. Journal of Experimental Botany 52: 183–192.

Lee HO, Davidson JM and Duronio RJ (2009) Endoreplication: polyploidy with purpose. Genes & Development 23: 2461–2477.

Leitch AR and Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytologist 194: 629–646.

Magyar Z, Ito M, Binarová P, Mohamed B and Bogre L (2013) Cell cycle modules in plants for entry into proliferation and for mitosis. In: Leitch IJ, Greilhuber J, Doležel J and Wendel JF (eds) Plant Genome Diversity, vol 2, Physical Structure, Behaviour and Evolution of Plant Genomes, pp. 77–97. Wien: Springer‐Verlag.

Maluszynska J, Kolano B and Sas‐Nowosielska H (2013) Endopolyploidy in plants. In: Leitch IJ, Greilhuber J, Doležel J and Wendel JF (eds) Plant Genome Diversity, vol 2, Physical Structure, Behaviour and Evolution of Plant Genomes, pp. 99–119. Wien: Springer‐Verlag.

Mendell JE, Clements KD, Choat JH and Angert ER (2008) Extreme polyploidy in a large bacterium. Proceedings of the National Academy of Sciences 105: 6730–6734.

Nagl W (1976) DNA endoreduplication and polyteny understood as evolutionary strategies. Nature 261: 614–615.

Nagl W (1978) Endopolyploidy and Polyteny in Differentiation and Evolution. Amsterdam: Elsevier.

Noir S, Bömer M, Takahashi N, et al. (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand‐by mode. Plant Physiology 161: 1930–1951.

Radziejwoski A, Vlieghe K, Lammens T, et al. (2011) Atypical E2F activity coordinates PHR1 photolyase gene transcription with endoreduplication onset. The EMBO Journal 30 (2): 355–363.

Ramirez‐Parra E and Gutierrez C (2007) E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiology 144: 105–120.

Repetto O, Massa N, Gianinazzi‐Pearson V, Dumas‐Gaudot E and Berta G (2007) Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 17 (2): 111–120.

Scholes DR and Paige KN (2011) Chromosomal plasticity: mitigating the impacts of herbivory. Ecology 92 (8): 1691–1698.

Scholes DR and Paige KN (2014) Plasticity in ploidy underlies plant fitness compensation to herbivore damage. Molecular Ecology 23: 4862–4870.

Scholes DR and Paige KN (2015) Plasticity in ploidy: a generalized response to stress. Trends in Plant Science 20: 165–175.

Soltis PS, Marchant DB, Van de Peer Y and Soltis DE (2015) Polyploidy and genome evolution in plants. Current Opinion in Genetics & Development 35: 119–125.

Takatsuka H and Umeda M (2015) Epigenetic control of cell division and cell differentiation in the root apex. Frontiers in Plant Science 6: 1178Article 1178..

Trávníček P, Ponert J, Urfus T, et al. (2015) Challenges of flow‐cytometric estimation of nuclear genome size in orchids, a plant group with both whole‐genome and progressively partial endoreplication. Cytometry Part A 87: 958–966.

Tschermak‐Woess E (1956) Karyologische Pflanzenanatomie. Protoplasma 46: 798–834.

Yamasaki S, Shimada E, Kuwano T, Kawano T and Noguchi N (2010) Continuous UV‐B irradiation induces endoreduplication and peroxidase activity in epidermal cells surrounding trichomes on cucumber cotyledons. Journal of Radiation Research 51 (2): 187–196.

Yoo CY, Pence HE, Jin JB, et al. (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. The Plant Cell 22 (12): 4128–4141.

Further Reading

Breuer C, Braidwood L and Sugimoto K (2014) Endocycling in the path of plant development. Current Opinion in Plant Biology 17: 78–85.

Okello RCO, de Visser PHB, Heuvelink E, Marcelis LFM and Struik PC (2016) Light mediated regulation of cell division, endoreduplication and cell expansion. Environmental and Experimental Botany 121: 39–47.

Orr‐Weaver TL (2015) When bigger is better: the role of polyploidy in organogenesis. Trends in Genetics 31: 307–315.

Yokoyama R, Hirakawa T, Hayashi S, Sakamoto T and Matsunaga S (2016) Dynamics of plant DNA replication based on PCNA visualization. Scientific Reports 6: Article number: 29657.

Yoshiyama KO (2015) SOG1: a master regulator of the DNA damage response in plants. Genes & Genetic Systems 90: 209–216.

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Leitch, Ilia J, and Dodsworth, Steven(Apr 2017) Endopolyploidy in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020097.pub2]