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The distribution pattern of endopolyploidy in maize

  • Silu Li
  • Linsan Liu
  • Ting Li
  • Tianru Lan
  • Yahui Wang
  • Zhengquan Zhang
  • Jianchao Liu
  • Shutu Xu
  • Xinghua Zhang
  • Jianchu Zhu
  • Jiquan Xue
  • Dongwei GuoEmail author
Original Article
  • 38 Downloads

Abstract

Key message

We discovered that endopolyploidization is common in various organs and tissues of maize at different development stages. Endopolyploidy is not specific in maize germplasm populations.

Abstract

Endopolyploidy is caused by DNA endoreplication, a special type of mitosis with normal DNA synthesis and a lack of cell division; it is a common phenomenon and plays an important role in plant development. To systematically study the distribution pattern of endopolyploidy in maize, flow cytometry was used to determine the ploidy by measuring the cycle (C) value in various organs at different developmental stages, in embryos and endosperm during grain development, in roots under stress conditions, and in the roots of 119 inbred lines from two heterotic groups, Shaan A and Shaan B. Endopolyploidy was observed in most organs at various developmental stages except in expanded leaves and filaments. The endosperm showed the highest C value among all organs. During tissue development, the ploidy increased in all organs except the leaves. In addition, the endopolyploidization of the roots was significantly affected by drought stress. Multiple comparisons of the C values of seven subgroups revealed that the distribution of endopolyploidization was not correlated with the population structure. A correlation analysis at the seedling stage showed a positive relationship between the C value and both the length of the whole plant and the length of main root. A genome-wide association study (GWAS) identified a total of 9 significant SNPs associated with endopolyploidy (C value) in maize, and 8 candidate genes that participate in cell cycle regulation and DNA replication were uncovered in 119 maize inbred lines.

Notes

Acknowledgements

This work was supported by the Shaanxi Province Comprehensive Project (Grant Number: 2015KTZDNY01-01-01) and the Yangling District Technical Plan Project (Grant Number: 2014NY-01).

Authors’ contribution statement

DWG conceived this research. SLL measured the endopolyploidy data, performed the data analyses and interpretation and drafted the manuscript. LSL edited the manuscript and assisted in the data interpretation. TL and STX performed the DNA extractions and SNP sequencing. TRL and JCL conducted the genotypic assays. YHW measured the agronomic traits in the field. JQX provided all of the plant germplasms. ZQZ, XHZ and JCZ performed the cultivation of the greenhouse and field materials. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standards

We state that all experiments in the study comply with the ethical standards in China.

Supplementary material

122_2019_3294_MOESM1_ESM.tif (5.3 mb)
Fig. S1 The flow cytometry histograms of the tested organs of maize inbred line B73 at seedling stage (V2–V5 stage) (TIFF 5401 kb)
122_2019_3294_MOESM2_ESM.tif (11.4 mb)
Fig. S2 The flow cytometry histograms of the tested organs of maize inbred line B73 from elongation stage to trumpet stage (V6–V12 stage) (TIFF 11641 kb)
122_2019_3294_MOESM3_ESM.tif (17.8 mb)
Fig. S3 The flow cytometry histograms of the tested organs of maize inbred line B73 during reproductive stage (VT stage-7 DAP) (TIFF 18238 kb)
122_2019_3294_MOESM4_ESM.tif (8 mb)
Fig. S4 The flow cytometry histograms of the B73 grain during pollination (TIFF 8212 kb)
122_2019_3294_MOESM5_ESM.tif (1.4 mb)
Fig. S5 Hierarchical clustering of the cycle value. Group I: low-level cycle value (L); Group II: medium-level cycle value (M); Group III: high-level cycle value (H) (TIFF 1480 kb)
122_2019_3294_MOESM6_ESM.docx (82 kb)
Supplementary material 6 (DOCX 81 kb)

References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchishinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78Google Scholar
  2. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664Google Scholar
  3. Anisimov AP (2005) Endopolyploidy as a morphogenetic factor of development. Cell Biol Int 29:993–1004Google Scholar
  4. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488Google Scholar
  5. Barow M (2006) Endopolyploidy in seed plants. BioEssays 28:271Google Scholar
  6. Barow M, Meister A (2010) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant, Cell Environ 26:571–584Google Scholar
  7. Bhosale R, Boudolf V, Cuevas F, Lu R, Eekhout T, Hu Z, van Isterdael G, Lambert G, Xu F, Nowack MK, Smith RS, Vercauteren I, De Rycke RM, Storme V, Beeckman T, Larkin JC, Kremer A, Höfte H, Galbraith DW, Kumpf RP, Maere S, De Veylder L (2018) A spatiotemporal DNA endoploidy map of the Arabidopsis root reveals roles for the endocycle in root development and stress adaptation. Plant Cell 30:2330–2351Google Scholar
  8. Bourdon M, Pirrello J, Cheniclet C, Coriton O, Bourge M, Brown S, Moïse A, Peypelut M, Rouyère V, Renaudin JP (2012) Evidence for karyoplasmic homeostasis during endoreduplication and a ploidy-dependent increase in gene transcription during tomato fruit growth. Development 139:3817–3826Google Scholar
  9. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635Google Scholar
  10. Bradley MV, Crane JC (1955) The effect of 2,4,5-trichlorophenoxyacetic acid on cell and nuclear size and endopolyploidy in parenchyma of apricot fruits. Am J Bot 42:273–281Google Scholar
  11. Bringezu TGG, Sharbel TF, Weber WE (2011) Grain development and endoreduplication in maize and the impact of heat stress. Euphytica 182:363–376Google Scholar
  12. Callebaut A, Van OP, Van PR (1982) Endomitosis and the effect of gibberellic acid in different Pisum sativum L. cultivars. Planta 156:553Google Scholar
  13. Chong JP, Thömmes P, Blow JJ (1996) The role of MCM/P1 proteins in the licensing of DNA replication. Trends Biochem Sci 21:102Google Scholar
  14. Coleman LC (2011) Nuclear conditions in normal stem tissue of VICIA FABA. Can J Res 28:382–391Google Scholar
  15. Dan H, Imaseki H, Wasteneys GO, Kazama H (2003) Ethylene stimulates endoreduplication but inhibits cytokinesis in cucumber hypocotyl epidermis. Plant Physiol 133:1726–1731Google Scholar
  16. Dante RA, Sabelli PA, Sun Y, Dilkes BP, Gordon-Kamm WJ, Larkins BA (2005) Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiol 138:2323–2336Google Scholar
  17. Dante RA, Larkins BA, Sabelli PA (2014a) Cell cycle control and seed development. Front Plant Sci 5:493Google Scholar
  18. Dante RA, Sabelli PA, Hong NN, Leivaneto JT, Tao Y, Lowe KS, Hoerster GJ, Gordonkamm WJ, Jung R, Larkins BA (2014b) Cyclin-dependent kinase complexes in developing maize endosperm: evidence for differential expression and functional specialization. Planta 239:493–509Google Scholar
  19. Dolfini SF, Landoni M, Tonelli C, Bernard L, Viotti A (2010) Spatial regulation in the expression of structural and regulatory storage-protein genes in Zea mays endosperm. Genesis 13:264–276Google Scholar
  20. Doyle J (1991) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  21. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581Google Scholar
  22. Edgar BA, Zielke N, Gutierrez C (2014) Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol 15:197Google Scholar
  23. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379Google Scholar
  24. Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96:985–989Google Scholar
  25. Gendreau E, Höfte H, Grandjean O, Brown S, Traas J (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J Cell Mol Biol 13:221Google Scholar
  26. Gendreau E, Orbovic V, Höfte H, Traas J (1999) Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 209:513–516Google Scholar
  27. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9:e90346Google Scholar
  28. Grafi G, Larkins BA (1995) Endoreduplication in maize endosperm: involvement of M phase—promoting factor inhibition and induction of S phase—related kinases. Science 269:1262Google Scholar
  29. Guo DW, Fei LI, Liu-Yin MA, Lian-Cheng LI, You-Zhi MA, Ri-Fei Sun (2008) Endopolyploidization phenomenon of Chinese cabbage (Brassica rapa ssp. pekinensis). Acta Agronomica Sinica 34:1386–1392Google Scholar
  30. Hunter T (1987) A thousand and one protein kinases. Cell 50:823Google Scholar
  31. Inzé D, Veylder LD (2006) Cell cycle regulation in plant development 1. Annu Rev Genet 40:77Google Scholar
  32. Jonathan B, Katja W, Christina W, Farshad R, Remmy K, Larkin JC, Martin H, Arp S (2010) Endoreplication controls cell fate maintenance. PLoS Genet 6:e1000996Google Scholar
  33. Joubès J, Chevalier C (2000) Endoreduplication in higher plants. Plant Mol Biol 43:735–745Google Scholar
  34. Katagiri Y, Hasegawa J, Fujikura U, Hoshino R, Matsunaga S, Tsukaya H (2016) The coordination of ploidy and cell size differs between cell layers in leaves. Development 143:1120–1125Google Scholar
  35. Kearsey SE, Labib K (1998) MCM proteins: evolution, properties, and role in DNA replication. Biochimica et Biophysica Acta (BBA)-Gene Struct Express 1398:113–136Google Scholar
  36. Kearsey SE, Maiorano D, Holmes EC, Todorov IT (1996) The role of MCM proteins in the cell cycle control of genome duplication. BioEssays 18:183–190Google Scholar
  37. Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? Curr Opin Plant Biol 3:488–492Google Scholar
  38. Kowles RV, Yerk GL, Haas KM, Phillips RL (1997) Maternal effects influencing DNA endoreduplication in developing endosperm of Zea mays. Genome 40:798Google Scholar
  39. Kudo N, Kimura Y (2001) Flow cytometric evidence for endopolyploidy in seedlings of some Brassica species. Theor Appl Genet 102:104–110Google Scholar
  40. Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo YM, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Bot 52:183Google Scholar
  41. Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: polyploidy with purpose. Genes Dev 23:2461Google Scholar
  42. Leiva-Neto JT, Grafi G, Sabelli PA, Dante RA, Woo YM, Maddock S, Gordon-Kamm WJ, Larkins BA (2004) A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm. Plant Cell 16:1854–1869Google Scholar
  43. Li T, Qu J, Wang Y, Chang L, He K, Guo D, Zhang X, Xu S, Xue J (2018) Genetic characterization of inbred lines from Shaan A and B groups for identifying loci associated with maize grain yield. BMC Genet 19:63Google Scholar
  44. Lur HS, Setter TL (1993) Role of auxin in maize endosperm development (timing of nuclear DNA endoreduplication, zein expression, and cytokinin). Plant Physiol 103(1):273–280Google Scholar
  45. Lynch JP, Chimungu JG, Brown KM (2014) Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J Exp Bot 65:6155Google Scholar
  46. Matsui K, Umemura Y, Ohmetakagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant Journal 55:954–967Google Scholar
  47. Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668Google Scholar
  48. Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L (2007) An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477Google Scholar
  49. Mishiba KI, Okamoto T, Mii M (2001) Increasing ploidy level in cell suspension cultures of Doritaenopsis by exogenous application of 2,4-dichlorophenoxyacetic acid. Physiol Plant 112:142–148Google Scholar
  50. Mohamed Y, Bopp M (1980) Distribution of polyploidy in elongating and non-elongating shoot axis of Pisum sativum. Zeitschrift Für Pflanzenphysiologie 98:25–33Google Scholar
  51. Nguyen HN, Sabelli PA, Larkins BA (2007) Endoreduplication and programmed cell death in the cereal endosperm. Springer, BerlinGoogle Scholar
  52. Niu Y (2001) Adapting the specialization of cell wall in the plant tissue to the functions. J Hengshui Normal Coll 3:49–51Google Scholar
  53. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113Google Scholar
  54. Pesch M, Hülskamp M (2009) One, two, three…models for trichome patterning in Arabidopsis? Curr Opin Plant Biol 12:587–592Google Scholar
  55. Roeder AH, Chickarmane V, Cunha A, Obara B, Manjunath BS, Meyerowitz EM (2010) Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol 8(5):e1000367Google Scholar
  56. Sabelli PA (2012) Replicate and die for your own good: endoreduplication and cell death in the cereal endosperm. J Cereal Sci 56:9–20Google Scholar
  57. Sabelli PA (2014) Cell cycle regulation and plant development: a crop production perspective. In: Pessarakli M (ed) Handbook of Plant and Crop Physiology. CRC Press, Boca Raton, FL, pp 32–61Google Scholar
  58. Sabelli PA, Larkins BA (2008) The endoreduplication cell cycle: regulation and function. Springer, BerlinGoogle Scholar
  59. Sabelli PA, Dante RA, Leivaneto JT, Jung R, Gordonkamm WJ, Larkins BA (2005) RBR3, a member of the retinoblastoma-related family from maize, is regulated by the RBR1/E2F pathway. Proc Natl Acad Sci USA 102:13005–13012Google Scholar
  60. Sabelli PA, Hoerster G, Lizarraga LE, Brown SW, Gordonkamm WJ, Larkins BA (2009) Positive regulation of minichromosome maintenance gene expression, DNA replication, and cell transformation by a plant retinoblastoma gene. Proc Natl Acad Sci USA 106:4042–4047Google Scholar
  61. Sabelli PA, Yan L, Dante RA, Lizarraga LE, Hong NN, Brown SW, Klingler JP, Yu J, Labrant E, Layton TM (2013) Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm. PNAS 110:E1827Google Scholar
  62. Schenk PW, Snaarjagalska BE (1999) Signal perception and transduction: the role of protein kinases. Biochem Biophys Acta 1449:1Google Scholar
  63. Schnittger A, Jurgens G, Hulskamp M (1998) Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. Development 125:2283–2289Google Scholar
  64. Schnittger A, Weinl C, Bouyer D, Schöbinger U, Hülskamp M (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled arabidopsis trichomes reduces Endoreduplication and cell size and induces cell death. Plant Cell 15:303–315Google Scholar
  65. Scholes DR, Paige KN (2015) Plasticity in ploidy: a generalized response to stress. Trends Plant Sci 20:165–175Google Scholar
  66. Shi H, Wang LL, Sun LT, Dong LL, Liu B, Chen LP (2015) Cell division and endoreduplication play important roles in stem swelling of tuber mustard (Brassica juncea Coss. var. tumida Tsen et Lee). Plant Biology 14:956–963Google Scholar
  67. Shu Z, Row S, Deng W (2018) Endoreplication: the good, the bad, and the ugly. Trends Cell Biol 28(6):465–474Google Scholar
  68. Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108:451Google Scholar
  69. Sun Y, Flannigan BA, Setter TL (1999) Regulation of endoreduplication in maize (Zea mays L.) endosperm. Isolation of a novel B1-type cyclin and its quantitative analysis. Plant Mol Biol 41:245–258Google Scholar
  70. Tong SY, Song FB (2012) Physiological characteristic changes of leaf and leaf sheath at different stem nodes of Maize in the late growth stage. Heilongjiang Agric SciGoogle Scholar
  71. Valente P, Tao W, Verbelen JP (1998) Auxins and cytokinins control DNA endoreduplication and deduplication in single cells of tobacco. Plant Sci 134:207–215Google Scholar
  72. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A (2003) Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula Nodules. Plant Cell 15:2093–2105Google Scholar
  73. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15:501–510Google Scholar
  74. Yamagata T, Kato H, Kuroda S, Abe S, Davies E (2003) Uncleaved legumin in developing maize endosperm: identification, accumulation and putative subcellular localization. J Exp Bot 54:913–922Google Scholar
  75. Young TE, Gallie DR (2000a) Programmed cell death during endosperm development. Plant Mol Biol 44:283Google Scholar
  76. Young TE, Gallie DR (2000b) Regulation of programmed cell death in maize endosperm by abscisic acid. Plant Mol Biol 42:397–414Google Scholar
  77. Zhang JJ, Hu YF, Zhou H, Huang YB (2007) Starch accumulation and activities of key enzymes involved in starch synthesis in the grains of maize inbred lines with different starch contents. J Plant Physiol Mol Biol 33:123Google Scholar
  78. Zhu J (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Silu Li
    • 1
    • 2
  • Linsan Liu
    • 1
    • 2
  • Ting Li
    • 1
    • 2
  • Tianru Lan
    • 1
    • 2
  • Yahui Wang
    • 1
    • 2
  • Zhengquan Zhang
    • 1
    • 2
  • Jianchao Liu
    • 1
    • 2
  • Shutu Xu
    • 1
    • 2
  • Xinghua Zhang
    • 1
    • 2
  • Jianchu Zhu
    • 1
    • 2
  • Jiquan Xue
    • 1
    • 2
  • Dongwei Guo
    • 1
    • 2
    Email author
  1. 1.The Key Laboratory of Biology and Genetics Improvement of Maize in Arid Area of Northwest Region, Ministry of Agriculture, College of AgronomyNorthwest A&F UniversityYanglingChina
  2. 2.Maize Engineering Technology Research Centre of Shaanxi ProvinceYanglingChina

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