Abscisic acid and blue light signaling pathways in chloroplast movements in Arabidopsis mesophyll

  • Aleksandra Eckstein Jagiellonian University, Faculty of Biophysics, Biochemistry and Biotechnology, Department of Plant Biotechnology, Gronostajowa 7, 30-387 Kraków
  • Weronika Krzeszowiec Jagiellonian University, Faculty of Biophysics, Biochemistry and Biotechnology, Department of Plant Biotechnology, Gronostajowa 7, 30-387 Kraków
  • Agnieszka Katarzyna Banaś Jagiellonian University, Faculty of Biophysics, Biochemistry and Biotechnology, Department of Plant Biotechnology, Gronostajowa 7, 30-387 Kraków
  • Franciszek Janowiak The Franciszek Górski Institute of Plant Physiology of Polish Academy of Sciences, ul. Niezapominajek 21, 30-239 Kraków
  • Halina Gabryś Jagiellonian University, Faculty of Biophysics, Biochemistry and Biotechnology, Department of Plant Biotechnology, Gronostajowa 7, 30-387 Kraków
Keywords: abscisic acid, abscisic acid mutants, Arabidopsis thaliana, blue light, chloroplast movement, phototropins


Abscisic acid (ABA) and phototropins act antagonistically to control stomatal movements. Here, we investigated the role of ABA in phototropin-directed chloroplast movements in mesophyll cells of Arabidopsis thaliana. We analyzed the expression of phototropins at mRNA and protein  level under the influence of ABA. PHOT1 mRNA level was decreased  by ABA in the dark while it was insensitive to ABA in light. PHOT2 mRNA level was independent of the hormone treatment. The levels of phototropin proteins were down-regulated by ABA, both in darkness and light. No impact of exogenous ABA on amplitudes and kinetics of chloroplast movements was detected. Chloroplast responses in wild type Arabidopsis and three mutants, abi4, abi2 (abscisic acid insensitive4, 2) and aba1 (abscisic acid1), were measured to account for endogenous ABA signaling. The chloroplast responses were slightly reduced in abi2 and aba1 mutants in strong light. To further investigate the effect, abi2 and aba1 mutants were supplemented with exogenous ABA. In the aba1 mutant, the reaction was rescued but in abi2 it was unaffected. Our results show that ABA is not directly involved in phototropin-controlled chloroplast responses in mature leaves of Arabidopsis. However, the disturbance of ABA biosynthesis and signaling in mutants affects some elements of the chloroplast movement mechanism. In line with its role as a stress hormone, ABA appears to enhance plant sensitivity to light and promote the chloroplast avoidance response.


Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol, 69: 451-462. https://doi.org/10.1007/s11103-008-9427-0

Aggarwal C, Łabuz J, Gabryś H (2013) Phosphoinositides play differential roles in regulating phototropin1-and phototropin2-mediated chloroplast movements in Arabidopsis. PLoS One 8: e55393. https://doi.org/journal.pone.0055393

Anielska-Mazur A, Bernaś T, Gabryś H (2009) In vivo reorganization of the actin cytoskeleton in leaves of Nicotiana tabacum L. transformed with plastin-GFP: Correlation with light-activated chloroplast responses. BMC- Plant Biol 64: 1–14. https://doi.org/10.1186/1471-2229-9-64

Assmann SM, Schwartz A (1992) Synergistic Effect of Light and Fusicoccin on Stomatal Opening. Plant Physiol 98: 1349-1355. https://doi.org/10.1104/pp.98.4.1349

Assmann SM, Snyder JA, Lee Y-RJ (2000) ABA-deficient (aba1) and ABA-insensitive (abi1-1, abi2-1) mutants of Arabidopsis have a wild-type stomatal response to humidity. Plant Cell Environ 23: 387–395. https://doi.org/10.1046/j.1365-3040.2000.00551.x

Augustynowicz J, Krzeszowiec W, Gabrys H (2009) Acquisition of plastid movement responsiveness to light during mesophyll cell differentiation. Int J Dev Biol 53: 121–127. https://doi.org/10.1387/ijdb.062140ja

Banaś AK, Aggarwal C, Łabuz J, Sztatelman O, Gabryś H (2012) Blue light signalling in chloroplast movements. J Exp Bot 63: 1559–1574. https://doi.org/10.1093/jxb/err429

Banaś AK, Gabryś H (2007) Influence of sugars on blue light-induced chloroplast relocations. Plant Signal Behav 2: 221–230. https://doi.org/ 10.4161/psb.2.4.4392

Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56: 2071–2083. https://doi.org/ 10.1093/jxb/eri206

Blackman PG, Davies WJ (1983) The effects of cytokinins and ABA on stomatal behaviour of maize and Commelina. J Exp Bot 34: 1619-1626. https://doi.org/10.1093/jxb/34.12.1619

Brady SM, McCourt P (2003) Hormone cross-talk in seed dormancy. J Plant Growth Regul 22: 25-31. https://doi.org/10.1007/s00344-003-0018-7

Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant–pathogen interactions. Journal Plant Res, 124: 489-499. https://doi.org/10.1007/s10265-011-0409-y

Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, Liscum E, Briggs WR (1998). Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282: 1698-1701. https://doi.org/ 10.1126/science.282.5394.1698

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. https://doi.org/10.1104/pp.105.063743

DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139: 101-114. https://doi.org/10.1104/pp.105.061887

Desikan R, Last K, Harrett‐Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill, SJ (2006) Ethylene‐induced stomatal closure in Arabidopsis occurs via AtrbohF‐mediated hydrogen peroxide synthesis. The Plant Journal, 47(6), 907-916. https://doi.org/10.1111/j.1365-313X.2006.02842.x

Dubas E, Janowiak F, Krzewska M, Hura T, Żur I (2013) Endogenous ABA concentration and cytoplasmic membrane fluidity in microspores of oilseed rape (Brassica napus L.) genotypes differing in responsiveness to androgenesis induction. Plant Cell Rep 32: 1465–1475. https://doi.org/10.1007/s00299-013-1458-6

Eckstein A, Krzeszowiec W, Waligórski P, Gabryś H (2016) Auxin and chloroplast movements. Physiol Plantarum 156: 351-366. https://doi.org/10.1111/ppl.12396

Eckstein A, Zięba P, Gabryś H (2012) Sugar and light effects on the condition of the photosynthetic apparatus of Arabidopsis thaliana cultured in vitro. J Plant Growth Regul 31: 90-101 https://doi.org/10.1007/s00344-011-9222-z

Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5, 765-771. https://doi.org/10.1046/j.1365-313X.1994.5060765.x

Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell 10: 1043–1054. https://doi.org/10.1105/tpc.10.6.1043

Gabryś H (2004) Blue light-induced orientation movements of chloroplasts in higher plants: Recent progress in the study of their mechanisms. Acta Physiol Plant 26: 473–478. https://doi.org/10.1007/s11738-004-0038-3

Gabryś H (2012) Blue-Light-Activated Chloroplast Movements: Progress in the Last Decade. In Progress in Botany 73. Lüttge U, Beyschlag W, Büdel B, Francis D eds, pp 189–205. Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-22746-2_7

Gabryś H, Krzeszowiec W (2012) Chloroplast movements induced by light: diversity of mechanisms in various taxa. In Biological diversity. Łaska G ed, pp 9–24. Bialystok: Polish Botanical Society.

Grabalska M, Malec P (2004) Blue Light-induced Chloroplast Reorientations in Lemna trisulca L.(Duckweed) are Controlled by Two Separable Cellular Mechanisms as Suggested by Different Sensitivity to Wortmannin. Photochem Photobiol 79: 343–348. https://doi.org/10.1111/j.1751-1097.2004.tb00019.x

Haubrick LL, Torsethaugen G, Assmann SM (2006) Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts. Physiol Plantarum 128: 134-143. https://doi.org/10.1111/j.1399-3054.2006.00708.x

Haupt W (1999) Chloroplast movement: from phenomenology to molecular biology. In Progress in Botany. Esser K, Kadereit JW, Runge M eds, pp 3–36. Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-59940-8_1

Haupt W, Scheuerlein R (1990) Chloroplast movement. Plant Cell Environ 13: 595–614. https://doi.org/10.1111/j.1365-3040.1990.tb01078.x

Hubbard KE, Nishimur N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24: 1695–1708. https://doi.org/10.1101/gad.1953910

Inoue SI, Kinoshita T, Takemiya A, Doi M, Shimazaki KI (2008) Leaf positioning of Arabidopsis in response to blue light. Mol Plant 1: 15–26. https://doi.org/10.1093/mp/ssm001

Iwabuchi K, Sakai T, Takagi S (2007) Blue light-dependent nuclear positioning in Arabidopsis thaliana leaf cells. Plant Cell Physiol 48: 1291–1298. https://doi.org/10.1093/pcp/pcm095

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. https://doi.org/10.1038/35073622

Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakanod A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106: 13106–13111. https://doi.org/10.1073/pnas.0906250106

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. https://doi.org/10.1126/science.291.5511.2138

Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420: 829–832. https://doi.org/10.1038/nature01213

Kinoshita T, Shimazaki KI (2001) Analysis of the phosphorylation level in guard-cell plasma membrane H+-ATPase in response to fusicoccin. Plant Cell Physiol 42: 424-432. https://doi.org/10.1093/pcp/pce055

Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki KI (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414: 656–660. https://doi.org/10.1038/414656a

Kodama Y, Suetsugu N, Kong SG, Wada M (2010). Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc Natl Acad Sci USA 107: 19591-19596. https://doi.org/10.1073/pnas.1007836107

Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana . Physiol Plant 61: 377-383. https://doi.org/10.1111/j.1399-3054.1984.tb06343.x

Königer M, Jessen B, Yang R, Sittler D, Harris GC (2010) Light, genotype, and abscisic acid affect chloroplast positioning in guard cells of Arabidopsis thaliana leaves in distinct ways. Photosynth Res 105: 213–27. https://doi.org/10.1007/s11120-010-9580-6

Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316: 715–719. https://doi.org/10.1126/science. 1140516

Krzeszowiec W, Rajwa B, Dobrucki J, Gabryś H (2007) Actin cytoskeleton in Arabidopsis thaliana under blue and red light. Biol Cell 99: 251–260. https://doi.org/10.1042/BC20060077

Krzeszowiec W, Gabrys H (2007) Phototropin mediated relocation of myosins in Arabidopsis thaliana. Plant Signal Behav 2: 333–336. https://doi.org/10.4161/psb.2.5.4509

León P, Sheen J (2003) Sugar and hormone connections. TrendsPlant Sci 8: 110-116. https://doi.org/10.1016/S1360-1385(03)00011-6

León P, Gregorio J, Cordoba E (2013) ABI4 and its role in chloroplast retrograde communication. Front Plant Sci 3: 304. https://doi.org/10.3389/fpls.2012.00304

Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264: 1448-1451. https://doi.org/10.1126/science.7910981

Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759–771. https://doi.org/10.1105/tpc.9.5.759

Lohse G, Hedrich R (1992) Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Planta 188: 206-214. https://doi.org/10.1007/BF00216815

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. https://doi.org/10.1104/pp.106.080333

Łabuz J, Sztatelman O, Banaś AK, Gabryś H (2012) The expression of phototropins in Arabidopsis leaves: developmental and light regulation. J Exp Bot 63: 763–771. https://doi.org/10.1093/jxb/ers061

Łabuz J, Hermanowicz P, Gabryś H (2015) The impact of temperature on blue light induced chloroplast movements in Arabidopsis thaliana. Plant Science 239: 238–249. https://doi.org/10.1016/j.plantsci.2015.07.013

Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064–1068. https://doi.org/10.1126/science.1172408

Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll, A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15: 2331.

Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25: 295–303. https://doi.org/10.1046/j.1365-313x.2001.00965.x

Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452-1455. https://doi.org/10.1126/science.8197457

Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42: 1383-1388.

Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165-185. https://doi.org/ 10.1146/annurev.arplant.56.032604.144046

Nauš J, Rolencová M, Hlaváčkova V (2008) Is chloroplast movement in tobacco plants influenced systemically after local illumination or burning stress? Journal Integr Plant Biol 50: 1292–1299. https://doi.org/10.1111/j.1744-7909.2008.00743.x

Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15: 2805–2815. https://doi.org/10.1105/tpc.016428

Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068–1071. https://doi.org/10.1126/science.1173041

Pilot G, Lacombe B, Gaymard F, Cherel I, Boucherez J, Thibaud J-B, Sentenac H (2001) Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J Biol Chem 276: 3215–3221. https://doi.org/10.1074/jbc.M007303200

Rock CD, Zeevaart JA (1991) The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA 88: 7496–7499. https://doi.org/10.1073/pnas.88.17.7496

Rodriguez PL, Benning G, Grill E (1998) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett, 421: 185-190. https://doi.org/ 10.1016/S0014-5793(97)01558-5

Rojas-Pierce M, Whippo CW, Davis PA, Hangarter RP, and Springer PS (2014) PLASTID MOVEMENT IMPAIRED1 mediates ABA sensitivity during germination and implicates ABA in light-mediated chloroplast movements. Plant Physiol Biochem 83: 185–193. https://doi.org/10.1016/j.plaphy.2014.07.014

Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29: 426-434. https://doi.org/10.1111/j.1365-3040.2005.01477.x

Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, 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. https://doi.org/10.1073/pnas.101137598

Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14: 1723-1735. https://doi.org/10.1105/tpc.003293

Senn G (1908) Die Gestalts- und Lageveranderung der Pflanzenchromatophoren. Leipzig Stuttgart: W. Engelmann

Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Gen 9:e1003577. https://doi.org/10.1371/journal.pgen.1003577

Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J Exp Bot 60: 1439–1463. https://doi.org/10.1093/jxb/ern340

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. https://doi.org/10.1104/pp.105.067371

Suhita D, Kolla VA, Vavasseur A, Raghavendra AS (2003) Different signaling pathways involved during the suppression of stomatal opening by methyl jasmonate or abscisic acid. Plant Sci 164: 481-488. https://doi.org/10.1016/S0168-9452(02)00432-6

Sztatelman O, Waloszek A, Banaś AK, Gabryś H (2010) Photoprotective function of chloroplast avoidance movement: In vivo chlorophyll fluorescence study. J Plant Physiol 167: 709–716. https://doi.org/10.1016/j.jplph.2009.12.015

Sztatelman O, Łabuz J, Hermanowicz P, Banaś AK, Bażant A, Zgłobicki P, Aggarwal C, Nadzieja M, Krzeszowiec W, Strzałka W, Gabryś H (2016) The interplay of phototropins in signaling to chloroplast movements. J Exp Bot, in press.

Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206: 1963–1969. https://doi.org/ 10.1242/jeb.00215

Takemiya A, Shimazaki K (2010) Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase. Plant Physiol 153: 1555-1562. https://doi.org/ 10.1104/pp.110.155689

Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki, K. I. (2013). Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nature communications 4: 2094. https://doi.org/ 10.1038/ncomms3094

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138: 2337-2343. https://doi.org/10.1104/pp.105.063503

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57: 2259-2266. https://doi.org/10.1093/jxb/erj193

Tlałka M, Runquist M, Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna trisulca L. Plant J 20: 447-459. https://doi.org/10.1046/j.1365-313x.1999.00614.x

Trojan A, Gabryś H (1996) Chloroplast distribution in Arabidopsis thaliana (L.) depends on light conditions during growth. Plant Physiol 111: 419–425. https://doi.org/10.1104/pp.111.2.419

Tseng TS, Craig Whippo C, Hangarter RP, Briggsa WR (2012) The Role of a 14-3-3 Protein in Stomatal Opening Mediated by PHOT2 in Arabidopsis. Plant Cell 24: 1114–1126. https://doi.org/10.1105/tpc.111.092130

Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106: 17588-17593. https://doi.org/10.1073/pnas.0907095106

Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51: 1821-1839. https://doi.org/10.1093/pcp/pcq156

Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57: 201–212. https://doi.org/10.1093/jxb/erj026

Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54: 455–468. https://doi.org/10.1146/annurev.arplant.54.031902.135023

Wada M, Suetsugu N (2004) Plant organelle positioning. Curr Opin Plant Biol 7: 626–631. https://doi.org/10.1016/j.pbi.2004.09.005

Walczak T, Gabryś H (1980) New type of photometer for measurements of transmission changes corresponding to chloroplast movements in leaves. Photosynth 14: 65–72.

Walker-Simmons MK, Abrams SR (1991) Use of ABA immunoassays. In Abscisic acid physiology and biochemistry. Davies WJ, Jones HG eds, pp 53–63. Oxford: Bios Scientific Publishers.

Wang XL, Gao XQ, Wang XC (2011) Stochastic dynamics of actin filaments in guard cells regulating chloroplast localization during stomatal movement. Plant Cell Environ 34: 1248–1257. https://doi.org/10.1111/j.1365-3040.2011.02325.x

Wind JJ, Peviani A, Snel B, Hanson J, Smeekens SC (2013) ABI4: versatile activator and repressor. Trends Plant Sci 18: 125–132. https://doi.org/10.1016/j.tplants.2012.10.004

Yamburenko MV, Zubo YO, Börner T (2015) Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C‐dependent activation of nuclear genes: repression by guanosine‐3′‐5′‐bisdiphosphate and activation by sigma factor 5. Plant J 82: 1030-1041. https://doi.org/10.1111/tpj.12876

Zhang Z, Feng L-Y, Cheng J, Tang H, Xu F, Zhu F, Zhao ZY, Yuan M, Chen Y-E, Wang J-H, Yuan S, Lin H-H (2013) The roles of two transcription factors, ABI4 and CBFA, in ABA and plastid signalling and stress response. Plant Mol Biol 83: 445–458. https://doi.org/10.1007/s11103-013-0102-8

Zhang X, Wang H, Takemiya A, Song C, Kinoshita T, Shimazaki K (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiology 136: 4150-4158. https://doi.org/10.1104/pp.104.046573

Zurzycki J (1955) Chloroplast arrangement as a factor in photosynthesis. Acta Soc Bot Pol 24: 27–63.