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Length of the dark period affects flower opening and the expression of circadian-clock associated genes as well as xyloglucan endotransglucosylase/hydrolase genes in petals of morning glory (Ipomoea nil)

Plant Cell Reports volume 33, pages 1121–1131 (2014)Cite this article

Abstract

Key message

We isolated differentially expressed and dark-responsive genes during flower development and opening in petals of morning glory.

Abstract

Flower opening usually depends on petal expansion and is regulated by both genetic and environmental factors. Flower opening in morning glory (Ipomoea nil) is controlled by the dark/light regime just prior to opening. Opening was normal after 8- or 12-h dark periods but progressed very slowly after a 4-h dark period or in continuous light. Four genes (InXTH1–InXTH4) encoding xyloglucan endotransglucosylase/hydrolases (XTHs) and three genes (InEXPA1–InEXPA3) encoding alpha-expansins (EXPAs) were isolated. The expression patterns of InXTH2, InXTH3, and InXTH4 in petals were closely correlated with the rate of flower opening controlled by the length of the dark period prior to opening, but those of the EXPA genes were not. The expression pattern of InXTH1 gene was closely correlated with petal elongation. Suppression subtractive hybridization was used to isolate dark-responsive genes accompanying flower opening. The expressions of ten isolated genes were associated with the length of the dark period prior to flower opening. One gene was highly homologous to Arabidopsis PSEUDO-RESPONSE REGULATOR7, which is associated with the circadian clock and phytochrome signaling; another to Arabidopsis REVEILLE1, which affects the output of the circadian clock. Other genes were related to light responses, plant hormone effects and signal transduction. The possible roles of these genes in regulation of flower opening are discussed.

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Abbreviations

BTB:

Bric-a-Brac/Tramtrack/Broad complex

CCA1:

CIRCADIAN CLOCK ASSOCIATED 1

CDS:

Coding sequence

EXPA:

α-Expansin

GPAT6:

GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE 6

HGO:

Homogentisate 1,2-dioxygenase

LHY:

LATE ELONGATED HYPOCOTYL

LRB:

LIGHT-RESPONSE BTB

PIF:

PHYTOCHROME INTERACTING FACTOR

PRR:

PSEUDO-RESPONSE REGULATOR

RVE1:

REVEILLE 1

SDIR1:

SALT-AND DROUGHT-INDUCED RING FINGER 1

SSH:

Suppression subtractive hybridization

XTH:

Xyloglucan endotransglucosylase/hydrolase

References

  • Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250

    Article  CAS  PubMed  Google Scholar 

  • Breeze E, Wagstaff C, Harrison E, Bramke I, Rogers H, Stead A et al (2004) Gene expression patterns to define stages of post-harvest senescence in Alstroemeria petals. Plant Biotechnol J 2:155–168

    Article  CAS  PubMed  Google Scholar 

  • Christians MJ, Gingerich DJ, Hua Z, Lauer TD, Vierstra RD (2012) The light-response BTB1 and BTB2 proteins assemble nuclear ubiquitin ligases that modify phytochrome B and D signaling in Arabidopsis. Plant Physiol 160:118–134

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S et al (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484

    Article  PubMed  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B et al (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dixon DP, Edwards R (2006) Enzymes of tyrosine catabolism in Arabidopsis thaliana. Plant Sci 171:360–366

    Article  CAS  PubMed  Google Scholar 

  • Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujimori T, Yamashino T, Kato T, Mizuno T (2004) Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in A. thaliana. Plant Cell Physiol 45:1078–1086

    Article  CAS  PubMed  Google Scholar 

  • Gookin TE, Hunter DA, Reid MS (2003) Temporal analysis of α and β-expansin expression during floral opening and senescence. Plant Sci 164:769–781

    Article  CAS  Google Scholar 

  • Harada T, Torii Y, Morita S, Masumura T, Satoh S (2010) Differential expression of genes identified by suppression subtractive hybridization in petals of opening carnation flowers. J Exp Bot 61:2345–2354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harada T, Torii Y, Morita S, Onodera R, Hara Y, Yokoyama R, Nishitani K, Satoh S (2011) Cloning, characterization, and expression of xyloglucan endotransglucosylase/hydrolase and expansin genes associated with petal growth and development during carnation flower opening. J Exp Bot 62:815–823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377

    Article  CAS  PubMed  Google Scholar 

  • Ho L, Nichols R (1977) Translocation of 14C-sucrose in relation to changes in carbohydrate content in rose corollas cut at different stages of development. Ann Bot 41:227–242

    Google Scholar 

  • Hoeberichts FA, van Doorn WG, Vorst O, Hall RD, van Wordragen MF (2007) Sucrose prevents up-regulation of senescence-associated genes in carnation petals. J Exp Bot 58:2873–2885

    Article  CAS  PubMed  Google Scholar 

  • Kaczorowski KA, Quail PH (2003) Intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. Plant Cell 15:2654–2665

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaihara S, Takimoto A (1979) Environmental factors controlling the time of flower-opening in Pharbitis nil. Plant Cell Physiol 20:1659–1666

    Google Scholar 

  • Kaihara S, Takimoto A (1980) Studies on the light controlling the time of flower-opening in P. nil. Plant Cell Physiol 21:21–26

    Google Scholar 

  • Kaihara S, Takimoto A (1981a) Effects of light and temperature on flower-opening of P. nil. Plant Cell Physiol 22:215–221

    Google Scholar 

  • Kaihara S, Takimoto A (1981b) Physical basis of flower-opening in P. nil. Plant Cell Physiol 22:307–310

    Google Scholar 

  • Kaihara S, Takimoto A (1983) Effect of plant growth regulators on flower-opening of P. nil. Plant Cell Physiol 24:309–316

    CAS  Google Scholar 

  • Kim BH, von Arnim AG (2006) The early dark-response in A. thaliana revealed by cDNA microarray analysis. Plant Mol Biol 60:321–342

    Article  CAS  PubMed  Google Scholar 

  • Koning R (1986) The role of ethylene in corolla unfolding in Ipomoea nil (Convolvulaceae). Amer J Bot 73:152–155

    Article  Google Scholar 

  • Laitinen RAE, Pöllänen E, Teeri TH, Elomaa P, Kotilainen M (2007) Transcriptional analysis of petal organogenesis in Gerbera hybrida. Planta 226:347–360

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li J, Jia D, Chen X (2001) HUA1, a regulator of stamen and carpel identities in Arabidopsis, codes for a nuclear RNA binding protein. Plant Cell 13:2269–2281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li-Beisson Y, Pollard M, Sauveplane V, Pinot F, Ohlrogge J, Beisson F (2009) Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci USA 106:22008–22013

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu YB, Lu SM, Zhang JF, Liu S, Lu YT (2007) A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 226:1547–1560

    Article  CAS  PubMed  Google Scholar 

  • Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T et al (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50:447–462

    Article  CAS  PubMed  Google Scholar 

  • Ok SH, Park HM, Kim JY, Bahn SC, Bae JM, Suh MC et al (2003) Identification of differentially expressed genes during flower development in carnation (Dianthus caryophyllus). Plant Sci 165:291–297

    Article  CAS  Google Scholar 

  • Osato Y, Yokoyama R, Nishitani K (2006) A principal role for AtXTH18 in A. thaliana root growth: a functional analysis using RNAi plants. J Plant Res 119:153–162

    Article  CAS  PubMed  Google Scholar 

  • Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X et al (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7:e40120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pomeranz M, Finer J, Jang JC (2011) Putative molecular mechanisms underlying tandem CCCH zinc finger protein mediated plant growth, stress, and gene expression responses. Plant Signal Behav 6:647–651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rawat R, Schwartz J, Jones M (2009) REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 106:16883–16888

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rose J, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki Y, Tanabata T, Ogiwara I, Yamada T, Kanekatsu M (2011) Application of digital image analysis system for fine evaluation of varietal differences and the role of ethylene in visible petal senescence of morning glory. J Plant Growth Regul 30:229–234

    Article  CAS  Google Scholar 

  • Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q et al (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Doorn WG, van Meeteren U (2003) Flower opening and closure: a review. J Exp Bot 54:1801–1812

    Article  PubMed  Google Scholar 

  • van Doorn WG, Balk P, van Houwelingen M, Hoeberichts F, Hall RD, Vorst O et al (2003) Gene expression during anthesis and senescence in Iris flowers. Plant Mol Biol 53:845–863

    Article  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genom 9:44

    Article  Google Scholar 

  • Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M et al (2003) BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316–321

    Article  CAS  PubMed  Google Scholar 

  • Yamada T, Takatsu Y, Kasumi M, Ichimura K, van Doorn WG (2006) Nuclear fragmentation and DNA degradation during programmed cell death in petals of morning glory (I. nil). Planta 224:1279–1290

    Article  CAS  PubMed  Google Scholar 

  • Yamada T, Ichimura K, Kanekatsu M, van Doorn WG (2007) Gene expression in opening and senescing petals of morning glory (I. nil) flowers. Plant Cell Rep 26:823–835

    Article  CAS  PubMed  Google Scholar 

  • Yamada K, Norikoshi R, Suzuki K, Imanishi H, Ichimura K (2009a) Determination of subcellular concentrations of soluble carbohydrates in rose petals during opening by nonaqueous fractionation method combined with infiltration–centrifugation method. Planta 230:1115–1127

    Article  CAS  PubMed  Google Scholar 

  • Yamada K, Takahashi R, Fujitani C, Mishima K, Yoshida M, Joyce DC et al (2009b) Cell wall extensibility and effect of cell-wall-loosening proteins during rose flower opening. J Jpn Soc Hort Sci 78:242–251

    Article  Google Scholar 

  • Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y et al (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell 42:451–461

    Article  CAS  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q et al (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. T. Ookawa and H. Fugo for their help. We thank all members of the Plant Breeding Laboratory, Tokyo University of Agriculture and Technology, Fuchu, Japan, for useful discussions throughout the work. This work was supported by a Sasakawa Scientific Research Grant from The Japan Science Society (Grant Number 23-418 to Y. S.).

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Authors and Affiliations

  1. Department of Plant Production, United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Yoshihito Shinozaki, Ryusuke Tanaka, Hanako Ono, Isao Ogiwara, Motoki Kanekatsu & Tetsuya Yamada

  2. Mann Laboratory, Department of Plant Sciences, University of California, Davis, CA, 95616, USA

    Wouter G. van Doorn

  3. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Yoshihito Shinozaki

Authors
  1. Yoshihito Shinozaki
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  2. Ryusuke Tanaka
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  3. Hanako Ono
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  4. Isao Ogiwara
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  5. Motoki Kanekatsu
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  6. Wouter G. van Doorn
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  7. Tetsuya Yamada
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Corresponding author

Correspondence to Tetsuya Yamada.

Additional information

Communicated by Z. -Y. Wang.

Y. Shinozaki and R. Tanaka have contributed equally to this work.

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Shinozaki, Y., Tanaka, R., Ono, H. et al. Length of the dark period affects flower opening and the expression of circadian-clock associated genes as well as xyloglucan endotransglucosylase/hydrolase genes in petals of morning glory (Ipomoea nil). Plant Cell Rep 33, 1121–1131 (2014). https://doi.org/10.1007/s00299-014-1601-z

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  • DOI: https://doi.org/10.1007/s00299-014-1601-z

Keywords

  • Cell growth
  • Dark-responsive expression
  • Expansin
  • Japanese morning glory
  • Petal unfolding
  • Xyloglucan endotransglucosylase/hydrolase (XTH)