Abstract
The suppression of sprout growth is critical for the long-term storage of potato tubers. 1,4-Dimethylenapthlene (DMN) is a new class of sprout control agent but the metabolic mode of action for this compound has yet to be elucidated. Changes in transcriptional profiles of meristems isolated from potato tubers treated with the DMN were investigated using an Agilent 44 K 60-mer-oligo microarray. RNA was isolated from nondormant Russet Burbank meristems isolated from tubers treated with DMN for 3 days or activated charcoal as a control. RNA was used to develop probes that were hybridized against a microarray developed by the Potato Oligo Chip Initiative. Analysis of the array data was conducted in two stages: total array data was examined using a linear model and the software Limma and pathway analysis was conducted by linking the potato sequences to the Arabidopsis thaliana. DMN elicited a change in a number of transcripts associated with cold responses, water regulation, salt stress, and osmotic adjustment. DMN also resulted in a repression of cyclin or cyclin-like transcripts. DMN also resulted in a 50% decrease in thymidine incorporation suggesting a repression of the S phase of the cell cycle. Quantitative real-time polymerase chain reaction analysis demonstrated that DMN increased transcripts for the cell cycle inhibitors KRP1 and KRP2. We conclude the DMN results in alteration of genes associated with the maintenance of a G1/S phase block possibly through the induction of the cell cycle inhibitors KRP1 and KRP2.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215:403–410
Beveridge J, Dalziel J, Duncan HJ (1981) Dimethylnaphthalene as a sprout suppressent for seed and ware potatoes. Potato Res 24:77–88
Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043
Brewster JL, Valoir TD, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259(5102):1760–1763
Campbell MA, Suttle J, Sell TW (1996) Changes in cell cycle status and expression of p34cdc2 kinase during potato tuber meristem dormancy. Physiol Plant 98:743–752
Campbell MA, Segear E, Beers L, Knauber D, Suttle J (2008) Dormancy in potato tuber meristems: chemically induced cessation in dormancy matches the natural process based on transcript profiles. Funct Integr Genom 8:317–328
Campbell MA, Gleichsner A, Alsbury R, Horvath D, Suttle J (2010) The sprout inhibitors chlorpropham and 1,4-dimethylnaphthalene elicit different trasncriptional profiles and do not supress growth through a prolongation of the dormant state. Plant Mol Biol 73:181–189
Clotet J, Posas F (2007) Control of cell cycle in response to osmostress: lessons from yeast. Methods Enzymol 428:63–76
De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. The Plant Cell Online 13(7):1653–1668
De Veylder L, Joubes J, Inzé D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6:536–543
Destefano-Beltran L, Knauber D, Huckle L, Suttle JC (2006) Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 61(4–5):687–697
Doonan J, Kitsios G (2009) Functional evolution of cyclin-dependent kinases. Mol Biotechnol 42(1):14–29
Escote X, Zapater M, Clotet J, Posas F (2004) Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6(10):997–1002
Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62(4):1264–1300
Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155(2):776–796
Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197(1):1–32
Horvath D (2010) Bud dormancy and growth. Plant Dev Biol-Biotechnol Perspect 2:53–70
Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, dePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. PNAS 108(26):10756–10761
Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. The Plant Cell Online 13(4):889–906
Keim D, Hailat N, Melhem R, Zhu XX, Lascu I, Veron M, Strahler J, Hanash SM (1992) Proliferation-related expression of p19/nm23 nucleoside diphosphate kinase. J Clin Investig 89(3):919–924
Kloosterman B, De Koeyer D, Griffiths R, Flinn B, Steuernagel B, Scholz U, Sonnewald S, Sonnewald U, Bryan GJ, Prat S, Bánfalvi Z, Hammond JP, Geigenberger P, Nielsen KL, Visser RG, Bachem CW (2008) Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Funct Integr Genom 8(4):329–340
Lakso M, Steeq P, Westphal H (1992) Embryonic expression of nm23 during mouse organogenesis. Cell Growth Differ 3(12):873–879
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endodormancy, paradormancy, and ecodormancy—physiological terminology and classification for dormancy research. HortSci 22(3):371–377
Menges M, de Jager S, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566
Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci 100(1):358–363
Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y, Shinozaki K, Nambara E, Seki M (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62(1):39–51
O’Rourke SM, Herskowitz I (2004) Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15(2):532–542
Pinhero RG, Coffin R, Yada RY (2009) Post-harvest storage of potatoes. In: Singh J, Kaur L (eds) Advances in potato chemistry and technology. Academic, New York, pp 339–370
Senning M, Sonnewald U, Sonnewald S (2010) Deoxyuridine triphosphatase expression defines the transition from dormant to sprouting potato tuber buds. Mol Breed 26(3):525–531
Simko I, McMurray S, Yang HM, Manschot A, Davies PJ, Ewing EE (1997) Evidence from polygene mapping for a causal relationship between potato tuber dormancy and abscisic acid content. Plant Physiol 115:1453–1459
Smyth G (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3. doi:10.2202/1544-6115.1027
Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, pp 397–420
Suttle JC (2007) Dormancy and sprouting. In: Vreugdenhill D, Bradshaw J, Gebhart C et al. (eds) Potato biology and biotechnology: advances and perspectives. Amsterdam, Elsevier
Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y, De Bodt S, Maere S, Laukens K, Pharazyn A, Ferreira PC, Eloy N, Renne C, Meyer C, Faure JD, Steinbrenner J, Beynon J, Larkin JC, Van de Peer Y, Hilson P, Kuiper M, De Veylder L, Van Onckelen H, Inzé D, Witters E, De Jaeger G (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 6. doi:10.1038/msb.2010.53
Vaughn K, Lehnen G (1991) Mitotic disrupter herbicides. Weed Sci 39:450–457
Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139:1099–1106
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A portion of this work was supported through a grant from the 1,4-Group to MAC.
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Campbell, M.A., Gleichsner, A., Hilldorfer, L. et al. The sprout inhibitor 1,4-dimethylnaphthalene induces the expression of the cell cycle inhibitors KRP1 and KRP2 in potatoes. Funct Integr Genomics 12, 533–541 (2012). https://doi.org/10.1007/s10142-011-0257-9
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DOI: https://doi.org/10.1007/s10142-011-0257-9