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.
Similar content being viewed by others
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
Barow M (2006) Endopolyploidy in seed plants. BioEssays 28:271–281
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
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
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
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
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
De Veylder L, Larkin JC, Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16:624–634
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
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
Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96:985–989
Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428
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
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
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
Harashima H, Schnittger (2010) The integration of cell division, growth and differentiation. Curr Opin Plant Biol 13:66–74
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
Kudo N, Mii M (2001) Flow cytometric evidence for endopolyploidy in seedlings of some Brassica species. Theor Appl Genet 102:104–110
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
Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: polyploidy with purpose. Genes Dev 23:2461–2477
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
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
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
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Neff MM, van Volkenburgh E (1994) Light-stimulated cotyledon expansion in Arabidopsis seedlings: the role of phytochrome B. Plant Physiol 104:1027–1032
Rewers M, Sliwinska E (2012) Endoreduplication intensity as a marker of seed developmental stage in the Fabaceae. Cytometry A 81A:1067–1075
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
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
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
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
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
Vandenbussche F, Verbelen JP, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27:275–284
von Arnim A, Deng XW (1996) Light control of seedling development. Ann Rev Plant Physiol Plant Mol Biol 47:215–243
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by K. K. Kamo.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-016-2054-3