Photosynthesis Research

, Volume 129, Issue 2, pp 217–225 | Cite as

Chloroplast avoidance movement as a sensitive indicator of relative water content during leaf desiccation in the dark

Technical Communication

Abstract

In the context of global climate change, drought is one of the major stress factors with negative effect on photosynthesis and plant productivity. Currently, chlorophyll fluorescence parameters are widely used as indicators of plant stress, mainly owing to the rapid, non-destructive and simple measurements this technique allows. However, these parameters have been shown to have limited sensitivity for the monitoring of water deficit as leaf desiccation has relatively small effect on photosystem II photochemistry. In this study, we found that blue light-induced increase in leaf transmittance reflecting chloroplast avoidance movement was much more sensitive to a decrease in relative water content (RWC) than chlorophyll fluorescence parameters in dark-desiccating leaves of tobacco (Nicotiana tabacum L.) and barley (Hordeum vulgare L.). Whereas the inhibition of chloroplast avoidance movement was detectable in leaves even with a small RWC decrease, the chlorophyll fluorescence parameters (FV/FM, VJ, ФPSII, NPQ) changed markedly only when RWC dropped below 70 %. For this reason, we propose light-induced chloroplast avoidance movement as a sensitive indicator of the decrease in leaf RWC. As our measurement of chloroplast movement using collimated transmittance is simple and non-destructive, it may be more suitable in some cases for the detection of plant stresses including water deficit than the conventionally used chlorophyll fluorescence methods.

Keywords

Chlorophyll fluorescence Chloroplast avoidance movement Desiccation Relative water content Transmittance 

Abbreviations

Chl

Chlorophyll

FV/FM

Maximum quantum yield of photosystem II photochemistry

NPQ

Non-photochemical chlorophyll fluorescence quenching

PAR

Photosynthetically active radiation

PSII

Photosystem II

RWC

Relative water content

RI

Relative increase of collimated transmittance reflecting chloroplast avoidance movement induced by blue light

RIn

The RI values normalized to the values of fresh control leaves

S

Maximal slope of the linear part of the normalized TC(t) curve

Sn

The S values normalized to the values of fresh control leaves

TC

Collimated transmittance

VJ

Relative height of the J-step in O-J-I-P transient

ФPSII

Effective quantum yield of photosystem II photochemistry

References

  1. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621CrossRefPubMedGoogle Scholar
  2. 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 87:303–311CrossRefPubMedGoogle Scholar
  3. Bertolli SC, Rapchan GL, Souza GM (2012) Photosynthetic limitations caused by different rates of water-deficit induction in Glycine max and Vigna unguiculata. Photosynthetica 50:329–336CrossRefGoogle Scholar
  4. Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185CrossRefPubMedGoogle Scholar
  5. Brugnoli E, Björkman O (1992) Chloroplast movements in leaves: influence of chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth Res 32:23–35CrossRefPubMedGoogle Scholar
  6. Carter GA, McCain DC (1993) Relationship of leaf spectral reflectance to chloroplast water content determined using NMR microscopy. Remote Sens Environ 46:305–310CrossRefGoogle Scholar
  7. Cazzaniga S, Dall´Osto L, Kong S-G, Wada M, Bassi R (2013) Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. Plant J 76:568–579CrossRefPubMedGoogle Scholar
  8. Davis PA, Hangarter RP (2012) Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves. Photosynth Res 112:153–161CrossRefPubMedGoogle Scholar
  9. Erismann ND, Machado EC, Tucci MLS (2008) Photosynthetic limitation by CO2 diffusion in drought stressed orange leaves on three rootstocks. Photosynth Res 96:163–172CrossRefGoogle Scholar
  10. Frolec J, Řebíček J, Lazár D, Nauš J (2010) Impact of two different types of heat stress on chloroplast movement and fluorescence signal of tobacco leaves. Plant Cell Rep 29:705–714CrossRefPubMedGoogle Scholar
  11. Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  12. Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji HM, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drough-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498CrossRefPubMedGoogle Scholar
  13. Guissé B, Srivastava A, Strasser RJ (1995) The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat-stressed leaves. Archs Sci Genéve 48:147–160Google Scholar
  14. Guo Y, Tan J (2015) Recent advances in the application of chlorophyll a fluorescence from photosystem II. Photochem Photobiol 91:1–14CrossRefPubMedGoogle Scholar
  15. Havaux M (1992) Stress tolerance of photosystem II in vivo. Plant Physiol 100:424–432CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106:13106–13111CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kaiser WM (1987) Effects of water deficit on photosynthetic capacity. Physiol Plant 71:142–149CrossRefGoogle Scholar
  18. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832CrossRefPubMedGoogle Scholar
  19. Kondo A, Kaikawa J, Funaguma T, Ueno O (2004) Clumping and dispersal of chloroplasts in succulent plants. Planta 219:500–506CrossRefPubMedGoogle Scholar
  20. Kong S-G, Wada M (2011) New insights into dynamic actin-based chloroplast photorelocation movement. Mol Plant 4:771–781CrossRefPubMedGoogle Scholar
  21. Kong S-G, Wada M (2014) Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement. Biochim Biophys Acta 1837:522–530CrossRefPubMedGoogle Scholar
  22. Königer M, Bollinger N (2012) Chloroplast movement behaviour varies widely among species and does not correlate with high light stress tolerance. Planta 236:411–426CrossRefPubMedGoogle Scholar
  23. Lazár D, Nauš J, Matoušková M, Flašarová M (1997) Mathematical modeling of changes in chlorophyll fluorescence induction caused by herbicides. Pestic Biochem Physiol 57:207–210CrossRefGoogle Scholar
  24. Lazár D, Pospíšil P, Nauš J (1999) Decrease of fluorescence intensity after the K step in chlorophyll a fluorescence induction is suppressed by electron acceptors and donors to photosystem 2. Photosynthetica 37:255–265CrossRefGoogle Scholar
  25. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662CrossRefGoogle Scholar
  26. Maai E, Shimada S, Yamada M, Sugiyama T, Miyake H, Taniguchi M (2011) The avoidance and aggregative movements of mesophyll chloroplasts in C4 monocots in response to blue light and abscisic acid. J Exp Bot 62:3213–3221CrossRefPubMedGoogle Scholar
  27. Matoušková M, Bartošková H, Nauš J, Novotný R (1999) Reaction of photosynthetic apparatus to dark desiccation sensitively detected by the induction of chlorophyll fluorescence quenching. J Plant Physiol 155:399–406CrossRefGoogle Scholar
  28. McCain DC, Croxdale J, Markley JL (1988) Water is allocated differently to chloroplasts in sun and shade leaves. Plant Physiol 86:16–18CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mishra KB, Iannacone R, Petrozza A, Mishra A, Armentano N, La Vecchia G, Trtílek M, Cellini F, Nedbal L (2012) Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Sci 182:79–86CrossRefPubMedGoogle Scholar
  30. Nauš J, Rolencová M, Hlaváčková V (2008) Is chloroplast movement in tobacco plants influenced systematically after local illumination or burning stress? J Integr Plant Biol 50:1292–1299CrossRefPubMedGoogle Scholar
  31. Nauš J, Prokopová J, Řebíček J, Špundová M (2010) SPAD chlorophyll meter reading can be pronouncedly affected by chloroplast movement. Photosynth Res 105:265–271CrossRefPubMedGoogle Scholar
  32. Ning L, Lu Z, Daley LS, Callis JB (1994) In vivo imaging of the interior of Tradescantia zebrinas leaves by optical cross correlation interferometry. Biochem Biophys Res Commun 205:638–644CrossRefPubMedGoogle Scholar
  33. Park YI, Chow WS, Anderson JM (1996) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867–875PubMedPubMedCentralGoogle Scholar
  34. Passioura J (2007) The drought environment: physical, biological and agricultural perspectives. J Exp Bot 58:113–117CrossRefPubMedGoogle Scholar
  35. Proctor MCF, Ligrone R, Duckett JG (2007) Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann Bot 99:75–93CrossRefGoogle Scholar
  36. Rojas-Pierce M, Whippo CW, Davis PA, Hangarter RP, Springer PS (2014) PLASTID MOVEMENT IMPAIRED1 mediates ABA sensitivity during germination and implicates ABA in light-mediated chloroplast movements. Plant Physiol Biochem 83:185–193CrossRefPubMedGoogle Scholar
  37. Samardakiewicz S, Krzeszowiec-Jelen W, Bednarski W, Jankowski A, Suski S, Gabrys H, Wozny A (2015) Pb-induced avoidance-like chloroplast movements in fronds of Lemna trisulca L. PLoS One 10:e0116757CrossRefPubMedPubMedCentralGoogle Scholar
  38. Skotnica J, Matoušková M, Nauš J, Lazár D, Dvořák L (2000) Thermoluminescence and fluorescence study of changes in Photosystem II photochemistry in desiccating barley leaves. Photosynth Res 65:29–40CrossRefPubMedGoogle Scholar
  39. Sniegowska-Swierk K, Dubas E, Rapacz M (2015) Drough-induced changes in the actin cytoskeleton of barley (Hordeum vulgare L.) leaves. Acta Physiol Plant 37:73CrossRefGoogle Scholar
  40. Strasser RJ, Govindjee (1992) On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. In: Murata N (ed) Research in Photosynthesis, vol II. Kluwer, Dordrecht, pp 29–32Google Scholar
  41. Sztatelman O, Waloszek A, Banas AK, Gabrys H (2010) Photoprotective function of chloroplast avoidance movement: in vivo chlorophyll fluorescence study. J Plant Physiol 167:709–716CrossRefPubMedGoogle Scholar
  42. Wada M (2013) Chloroplast movement. Plant Sci 210:177–182CrossRefPubMedGoogle Scholar
  43. Walczak T, Gabrys H (1980) New type of photometer for measurements of transmission changes corresponding to chloroplast movements in leaves. Photosynthetica 14:65–72Google Scholar
  44. Williams WE, Gorton HL, Witiak SM (2003) Chloroplast movement in the field. Plant Cell Environ 26:2005–2014CrossRefGoogle Scholar
  45. Yamada M, Kawasaki M, Sugiyama T, Miyake H, Taniguchi M (2009) Differential positioning of C4 mesophyll and bundle sheath chloroplasts: aggregative movement of C4 mesophyll chloroplasts in response to environmental stresses. Plant Cell Physiol 50:1736–1749CrossRefPubMedGoogle Scholar
  46. Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Jan Nauš
    • 1
  • Slavomír Šmecko
    • 1
  • Martina Špundová
    • 1
  1. 1.Department of Biophysics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of SciencePalacký UniversityOlomoucCzech Republic

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