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Effect of light and auxin transport inhibitors on endoreduplication in hypocotyl and cotyledon

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Abstract

Key message

Enhancement of endoreduplication in dark-grown hypocotyl is a common feature in dicotyledonous polysomatic plants, and TIBA-mediated inhibition of the endoreduplication is partially due to abnormal actin organization.

Abstract

Many higher plant species use endoreduplication during cell differentiation. However, the mechanisms underlying this process have remained elusive. In this study, we examined endoreduplication in hypocotyls and cotyledons in response to light in some dicotyledonous plant species. Enhancement of endoreduplication was found in the dark-grown hypocotyls of all the polysomatic species analyzed across five different families, indicating that this process is a common feature in dicotyledonous plants having polysomatic tissues. Conversely, endoreduplication was enhanced in the light-grown cotyledons in four of the five species analyzed. We also analyzed the effect of a polar auxin transport inhibitor, 2,3,5-triiodobenzoic acid (TIBA) on endoreduplication in hypocotyl and cotyledon tissues of radish (Raphanus sativus L. var. longipinnatus Bailey). TIBA was found to inhibit and promote endoreduplication in hypocotyls and cotyledons, respectively, suggesting that the endoreduplication mechanism differs in these organs. To gain insight into the effect of TIBA, radish and spinach (Spinacia oleracea L.) seedlings were treated with a vesicle-trafficking inhibitor, brefeldin A, and an actin polymerization inhibitor, cytochalasin D. Both of the inhibitors partially inhibited endoreduplication of the dark-grown hypocotyl tissues, suggesting that the prominent inhibition of endoreduplication by TIBA might be attributed to its multifaceted role.

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Abbreviations

BFA:

Brefeldin A

CytD:

Cytochalasin D

DAG:

Days after germination

DAPI:

4′,6-diamidino-2-phenylindole

FCM:

Flow cytometry

HFCA:

9-hydroxyfluorene-9-carboxylic acid

NPA:

N-1-Naphthylphthalamic acid

PCIB:

2-(p-chlorophenoxy)-2-methylpropionic acid

TIBA:

2,3,5-Triiodobenzoic acid

References

  • Amijima M, Iwata Y, Koizumi N, Mishiba KI (2014) The polar auxin transport inhibitor TIBA inhibits endoreduplication in dark grown spinach hypocotyls. Plant Sci 225:45–51

    Article  CAS  PubMed  Google Scholar 

  • Barow M (2006) Endopolyploidy in seed plants. BioEssays 28:271–281

    Article  CAS  PubMed  Google Scholar 

  • Barow M, Jovtchev G (2007) Endopolyploidy in plants and its analysis by flow cytometry. In: Doležel J, Greilhuber J, Suda J (eds) Flow cytometry with plant cells. Wiley-VCH, Weinheim, pp 349–372

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Blum DE, Neff MM, van Volkenburgh E (1994) Light-stimulated cotyledon expansion in the blu3 and hy4 mutants of Arabidopsis thaliana. Plant Physiol 105:1433–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro S, Loureiro J, Rodriguez E, Silveira P, Navarro L, Santos C (2007) Evaluation of polysomaty and estimation of genome size in Polygala vayredae and P. calcarea using flow cytometry. Plant Sci 172:1131–1137

    Article  CAS  Google Scholar 

  • Colijn-Hooymans CM, Hakkert JC, Jansen J, Custers JBM (1994) Competence for regeneration of cucumber cotyledons is restricted to specific developmental stages. Plant Cell Tissue Organ Cult 39:211–217

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hašek J, Paciorek T, Petrášek J, Seifertová D, Tejos R, Meisel LA, Zažímalová E, Gadella TWJ, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Nat Acad Sci USA 105:4489–4494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:221–230

    Article  CAS  PubMed  Google Scholar 

  • Giles KW, Myers A (1964) The role of nucleic acids in the growth of the hypocotyl of Lupinus albus under varying light and dark regimes. Biochim Biophys Acta 87:460–477

    CAS  PubMed  Google Scholar 

  • Harashima H, Schnittger (2010) The integration of cell division, growth and differentiation. Curr Opin Plant Biol 13:66–74

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kudo N, Mii M (2001) Flow cytometric evidence for endopolyploidy in seedlings of some Brassica species. Theor Appl Genet 102:104–110

    Article  CAS  Google Scholar 

  • Kudo N, Mii M (2004) Endoreduplication cycles during hypocotyl growth of cabbage (Brassica oleracea L.) under light and dark conditions. Plant Biotechnol 21:295–298

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemontey C, Mousset-Déclas C, Munier-Jolain N, Boutin JP (2000) Maternal genotype influences pea seed size by controlling both mitotic activity during early embryogenesis and final endoreduplication level/cotyledon cell size in mature seed. J Exp Bot 51:167–175

    Article  CAS  PubMed  Google Scholar 

  • Mishiba KI, Tawada KI, Mii M (2006) Ploidy distribution in the explant tissue and the calluses induced during the initial stage of internode segment culture of Asparagus officinalis L. In Vitro Cell Dev Biol Plant 42:83–88

    Article  Google Scholar 

  • Moon DO, Kim MO, Kang SH, Lee KJ, Heo MS, Choi KS, Choi YH, Kim GY (2008) Induction of G2/M arrest, endoreduplication, and apoptosis by actin depolymerization agent pextenotoxin-2 in human leukemia cells, involving activation of ERK and JNK. Biochem Pharmacol 76:312–321

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Neff MM, van Volkenburgh E (1994) Light-stimulated cotyledon expansion in Arabidopsis seedlings: the role of phytochrome B. Plant Physiol 104:1027–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rewers M, Sliwinska E (2012) Endoreduplication intensity as a marker of seed developmental stage in the Fabaceae. Cytometry A 81A:1067–1075

    Article  CAS  Google Scholar 

  • Scharpé A, van Parijs R (1973) The formation of polyploid cells in ripening cotyledons of Pisum sativum L. in relation to ribosome and protein synthesis. J Exp Bot 24:216–222

    Article  Google Scholar 

  • Sliwinska E, Lukaszewska E (2005) Polysomaty in growing in vitro sugar-beet (Beta vulgaris L.) seedlings of different ploidy level. Plant Sci 168:1067–1074

    Article  CAS  Google Scholar 

  • Sliwinska E, Bassel GW, Bewley D (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. J Exp Bot 60:3587–3594

    Article  CAS  PubMed  Google Scholar 

  • Smulders MJM, Rus-Kortekaas W, Gilissen LJW (1994) Development of polysomaty during differentiation in diploid and tetraploid tomato (Lycopersicon esculentum) plants. Plant Sci 97:53–60

    Article  Google Scholar 

  • van Oostveldt P, van Parijs R (1975) Effect of light on nucleic-acid synthesis and polyploidy level in elongating epicotyl cells of Pisum sativum. Planta 124:287–295

    Article  PubMed  Google Scholar 

  • Vandenbussche F, Verbelen JP, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27:275–284

    Article  CAS  PubMed  Google Scholar 

  • von Arnim A, Deng XW (1996) Light control of seedling development. Ann Rev Plant Physiol Plant Mol Biol 47:215–243

    Article  Google Scholar 

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Acknowledgments

We would like to thank Mr. Junich Iijima (Cytotechs) and Dr. Kyoko Kano (Sysmex) for help with the flow cytometry. We also thank Editage (http://www.editage.jp) and Dr. Megumi Mishiba for English language editing.

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Correspondence to Kei-ichiro Mishiba.

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Communicated by K. K. Kamo.

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Tanaka, R., Amijima, M., Iwata, Y. et al. Effect of light and auxin transport inhibitors on endoreduplication in hypocotyl and cotyledon. Plant Cell Rep 35, 2539–2547 (2016). https://doi.org/10.1007/s00299-016-2054-3

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