Skip to main content
SpringerLink
Log in

Light, genotype, and abscisic acid affect chloroplast positioning in guard cells of Arabidopsis thaliana leaves in distinct ways

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The goal of this study was to investigate the effects of light intensity, genotype, and various chemical treatments on chloroplast movement in guard cells of Arabidopsis thaliana leaves. After treatment at various light intensities (dark, low, and high light), leaf discs were fixed with glutaraldehyde, and imaged using confocal laser microscopy. Each chloroplast was assigned a horizontal (close to pore, center, or epidermal side) and vertical (outer, middle, inner) position. White light had a distinct effect on chloroplast positioning, most notably under high light (HL) when chloroplasts on the upper leaf surface of wild-type (WT) moved from epidermal and center positions toward the pore. This was not the case for phot1-5/phot2-1 or phot2-1 plants, thus phototropins are essential for chloroplast positioning in guard cells. In npq1-2 mutants, fewer chloroplasts moved to the pore position under HL than in WT plants, indicating that white light can affect chloroplast positioning also in a zeaxanthin-dependent way. Cytochalasin B inhibited the movement of chloroplasts to the pore under HL, while oryzalin did not, supporting the idea that actin plays a role in the movement. The movement along actin cables is dependent on CHUP1 since chloroplast positioning in chup1 was significantly altered. Abscisic acid (ABA) caused most chloroplasts in WT and phot1-5/phot2-1 to be localized in the center, middle part of the guard cells irrespective of light treatment. This indicates that not only light but also water stress influences chloroplast positioning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Assmann SM, Shimazaki K-I (1999) The multisensory guard cell. Stomatal responses to blue light and abscisic acid. Plant Physiol 119:809–815

    Article  CAS  PubMed  Google Scholar 

  • Berg R, Königer M, Schjeide B-M, Dikmak G, Kohler S, Harris GC (2006) A simple low cost microcontroller-based photometric instrument for monitoring chloroplast movement. Photosynth Res 87(3):303–311

    Article  CAS  PubMed  Google Scholar 

  • Celaya RB, Liscum E (2005) Phototropins and associated signaling: providing the power of movement in higher plants. Photochem Photobiol 81:73–80

    Article  CAS  PubMed  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  CAS  PubMed  Google Scholar 

  • DeBlasio SL, Mullen JL, Luesse DR, Hangarter RP (2003) Phytochrome modulation of blue-light-induced chloroplast movement in Arabidopsis. Plant Physiol 133:1471–1479

    Article  CAS  PubMed  Google Scholar 

  • DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  PubMed  Google Scholar 

  • Dong X-J, Nagai R, Takagi S (1998) Microfilamants anchor chloroplasts along the outer periclinal wall in Vallisneria epidermal cells through cooperation of PFR and photosynthesis. Plant Cell Physiol 39:1299–1306

    CAS  Google Scholar 

  • Eun S-O, Bae S-H, Lee Y (2001) Cortical actin filaments in guard cells respond differently to abscisic acid in wild-type and abi-1 mutant Arabidopsis. Planta 212:466–469

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Galatis B, Apostolakos P (2004) The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol 161:613–639

    Article  Google Scholar 

  • Haupt W (1959) Chloroplastenbewegung. In: Ruhland W (ed) Encyclopedia of plant physiology, vol 17. Springer, Berlin, pp 278–317

    Google Scholar 

  • Havaux M, Bonfils J-P, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. Plant Physiol 124:273–284

    Article  CAS  PubMed  Google Scholar 

  • Hwang J-U, Lee Y (2001) Abscisic acid-induced actin reorganization in guard cells of dayflower is mediated by cytosolic calcium levels and by protein kinase and protein phosphatase activities. Plant Physiol 125:2120–2128

    Article  CAS  PubMed  Google Scholar 

  • Hwang J-U, Suh S, Yi H, Kim J, Lee Y (1997) Actin filaments modulate both stomatal opening and inward K+-channel activities in guard cells of Vicia faba L. Plant Physiol 115:335–342

    CAS  PubMed  Google Scholar 

  • Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954

    Article  CAS  PubMed  Google Scholar 

  • Kagawa T (2003) The phototropin family as photoreceptors for blue light-induced chloroplast relocation. J Plant Res 116:77–82

    CAS  PubMed  Google Scholar 

  • Kagawa T, Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41:84–93

    CAS  PubMed  Google Scholar 

  • Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  CAS  PubMed  Google Scholar 

  • Kandasamy MK, Meagher RB (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskelet 44:110–118

    Article  CAS  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Shimazaki KI (1999) Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18(20):5548–5558

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K-I (2001) phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Emi T, Tominaga M, Sakamoto K, Shigenaga A, Doi M, Shimazaki K-I (2003) Blue-light- and phosphorylation-dependent binding of a 14–3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiol 133:1453–1463

    Article  CAS  PubMed  Google Scholar 

  • Kong S-G, Suzuki T, Tamura K, Mochizuki N, Hara-Nishimura I, Nagatani A (2006) Blue light-induced association of phototropin 2 with the Golgi apparatus. Plant J 45:994–1005

    Article  CAS  PubMed  Google Scholar 

  • Königer M, Delamaide JA, Marlow ED, Harris GC (2008) Arabidopsis thaliana leaves with altered chloroplast numbers and chloroplast movement exhibit impaired adjustments to both low and high light. J Exp Bot 59(9):2285–2297

    Article  PubMed  Google Scholar 

  • Kumatani T, Sakurai-Ozato N, Miyawaki N, Yokota E, Shimmen T, Terashima I, Takagi S (2006) Possible association of actin filaments with chloroplasts of spinach mesophyll cells in vivo and in vitro. Protoplasma 229:45–52

    Article  CAS  PubMed  Google Scholar 

  • Lemichez E, Wu Y, Sanchez J-P, Mettouchi A, Mathur J, Chua N-H (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15:1808–1816

    Article  CAS  PubMed  Google Scholar 

  • Luesse DR, DeBlasio SL, Hangarter RP (2006) Plastid movement impaired 2, a new gene involved in normal blue-light-induced chloroplast movements in Arabidopsis. Plant Physiol 141:1328–1337

    Article  CAS  PubMed  Google Scholar 

  • MacRobbie EAC (1998) Signal transduction and ion channels in guard cells. Phil Trans R Soc Lond B 353:1475–1488

    Article  CAS  Google Scholar 

  • Malec P, Rinaldi RA, Gabrys H (1996) Light-induced chloroplast movements in Lemna triscula. Identification of the motile system. Plant Sci 120:127–137

    Article  CAS  Google Scholar 

  • Mayer F (1964) Lichtorientierte Chloroplastenverlagerung bei Selaginella martensii. Zeitschr f Botanik 52:346–381

    Google Scholar 

  • Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning 1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815

    Article  CAS  PubMed  Google Scholar 

  • Oikawa K, Yamasato A, Kong S-G, Kasahara M, Nakai M, Takahashi F, Ogura Y, Kagawa T, Wada M (2008) Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol 148:829–842

    Article  CAS  PubMed  Google Scholar 

  • Outlaw WH Jr, Manchester J (1979) Guard cell starch concentration quantitatively related to stomatal aperture. Plant Physiol 64(1):79–82

    Article  CAS  PubMed  Google Scholar 

  • Park Y-I, Chow WS, Anderson JM (1996) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867–875

    CAS  PubMed  Google Scholar 

  • Paves H, Truve E (2007) Myosin inhibitors block accumulation movement of chloroplasts in Arabidopsis thaliana leaf cells. Protoplasma 230:165–169

    Article  CAS  PubMed  Google Scholar 

  • Pfannenschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  Google Scholar 

  • Reisen D, Hanson MR (2007) Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol 7:6

    Article  PubMed  Google Scholar 

  • Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the watergate’. New Phytol 167(3):665–691

    Article  CAS  PubMed  Google Scholar 

  • Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735

    Article  CAS  PubMed  Google Scholar 

  • Schmidt von Braun S, Schleiff E (2008) The chloroplast outer membrane protein CHUP1 interacts with actin and profilin. Planta 227:1151–1159

    Article  CAS  PubMed  Google Scholar 

  • Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzenchromatophoren. Engelmann W, Leipzig

    Google Scholar 

  • Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136:3968–3978

    Article  CAS  PubMed  Google Scholar 

  • Shimazaki K-I, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu N, Kagawa T, Wada M (2005) An auxilin-like J-domain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiol 139:151–162

    Article  CAS  PubMed  Google Scholar 

  • Takagi S (2003) Actin-based photo-orientation of chloroplast in plant cells. J Exp Biol 206:1963–1969

    Article  CAS  PubMed  Google Scholar 

  • Talbott LD, Zeiger E (1996) Central roles for potassium and sucrose in guard-cell osmoregulation. Plant Physiol 111(4):1051–1057

    CAS  PubMed  Google Scholar 

  • Tlalka M, Runquist M, Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna triscula L. Plant J 20(4):447–459

    Article  CAS  PubMed  Google Scholar 

  • Tominaga M, Kinoshita T, Shimazaki K-I (2001) Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol 42(8):795–802

    Article  CAS  PubMed  Google Scholar 

  • Trojan A, Gabrys H (1996) Chloroplast distribution in Arabidopsis thaliana (L) depends on light conditions during growth. Plant Physiol 111:419–425

    CAS  PubMed  Google Scholar 

  • Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165(3):665–682

    Article  CAS  PubMed  Google Scholar 

  • Vogelmann TC, Nishio JN, Smith WK (1996) Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Sci 1:65–70

    Article  Google Scholar 

  • Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Pesacreta TC (2004) A subclass of myosin XI is associated with mitochondria, plastids and the molecular chaperone subunit TCP-1a in maize. Cell Motil Cytoskelet 57:218–232

    Article  CAS  Google Scholar 

  • Wang P, Song C-P (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718

    Article  CAS  PubMed  Google Scholar 

  • Wang Y-S, Yoo C-M, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytol 177:525–536

    CAS  PubMed  Google Scholar 

  • Weber F (1925) Lageveränderung der Chloroplasten in Schliesszellen. Planta 1:374–378

    Article  Google Scholar 

  • Wen F, Xing D, Zhang L (2008) Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis. J Exp Bot 59:2891–2901

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  CAS  PubMed  Google Scholar 

  • Zurzycki J (1980) Blue light-induced intracellular movements. In: Senger H (ed) Blue light syndrome. Springer, New York, pp 50–68

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr Winslow Briggs for the gift of phot2-1 and phot1-5/phot2-1 mutant seeds, Dr Nick Rodenhouse for help with the statistical analysis of the data and two reviewers for their constructive criticism of an earlier version of the manuscript. Financial support was provided by a Brachman-Hoffman grant to MK.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Wellesley College, Wellesley, MA, 02481, USA

    Martina Königer, Brita Jessen, Rui Yang, Dorothea Sittler & Gary C. Harris

Authors
  1. Martina Königer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brita Jessen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorothea Sittler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gary C. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martina Königer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Königer, M., Jessen, B., Yang, R. et al. Light, genotype, and abscisic acid affect chloroplast positioning in guard cells of Arabidopsis thaliana leaves in distinct ways. Photosynth Res 105, 213–227 (2010). https://doi.org/10.1007/s11120-010-9580-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-010-9580-6

Keywords

Search

Navigation