Abstract
The prothalli of the fern Ceratopteris richardii exhibit negative gravitropism when grown in darkness. However, no sedimentable organelles or substances have been detected in the prothallial cells, suggesting that a non-sedimentable gravisensor exists. We investigated whether chloroplasts are involved in the gravisensing system of C. richardii prothalli. We used a clumped-chloroplast mutant, clumped chloroplast 1 (cp1), in which the chloroplasts are detached from the plasma membrane and clustered around the nucleus likely because of a partial deletion in the KINESIN-LIKE PROTEIN FOR ACTIN-BASED CHLOROPLAST MOVEMENT 1 gene. The cp1 mutation resulted in prothalli that had a significantly diminished gravitropic response, while the phototropic response occurred normally. These results suggest that plasma membrane-anchored chloroplasts in prothallial cells function as one of the gravisensors in C. richardii prothalli.
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References
Bai H, Wolverton C (2011) Gravitropism in lateral roots of Arabidopsis pgm-1 mutants is indistinguishable from that of wild-type. Plant Signal Behav 6:1423–1424. doi:10.4161/psb.6.10.16963
Banaś AK, Aggarwal C, Labuz J, Sztatelman O, Gabryś H (2012) Blue light signalling in chloroplast movements. J Exp Bot 63:1559–1574. doi:10.1093/jxb/err429
Banbury GH (1962) Geotropism of lower plants. In: Aletsee et al. (eds) Physiology of movements/Physiologie der bewwgungen. Springer, Heidelberg, p 344–377. doi:10.1007/978-3-642-94852-7_8
Banks JA (1994) Sex-determining genes in the homosporous fern Ceratopteris. Development 120:1949–1958
Barlow PW (1995) Gravity perception in plants: a multiplicity of systems derived by evolution? Plant Cell Environ 18:951–962
Caspar T, Pickard BG (1989) Gravitropism in a starchless mutant of Arabidopsis: implications for the starch-statolith theory of gravity sensing. Planta 177:185–197. doi:10.1007/BF00392807
Chen R, Rosen E, Mass PH (1999) Gravitropism in higher plants. Plant Physiol 120:343–350. doi:10.1104/pp.120.2.343
Edwards ES, Roux SJ (1994) Limited period of graviresponsiveness in germinating spores of Ceratopteris richardii. Planta 195:150–152
Edwards ES, Roux SJ (1998) Influence of gravity and light on the developmental polarity of Ceratopteris richardii fern spores. Planta 205:553–560
Guyomarc’h S, Leran S, Auzon-Cape M, Perrine-Walker F, Lucas M, Laplaze L (2012) Early development and gravitropic response of lateral roots in Arabidopsis thaliana. Philos Trans R Soc Lond B Bio Sci 367:1509–1516. doi:10.1098/rstb.2011.0231
Haberlandt G (1900) Ueber die perception des geotropischen reizes. Ber Deutsch Bot Ges 18:261–272
Hashiguchi Y, Tasaka M, Morita MT (2013) Mechanism of higher plant gravity sensing. Am J Bot 100:91–100. doi:10.3732/ajb.1200315
Kagawa T, Wada M (1993) Light-dependent nuclear positioning in prohtallial cells of Adiantum capillus-veneris. Protoplasma 177:82–85
Kamachi H, Noguchi M (2012) Negative gravitropism in dark-grown gametophytes of the fern Ceratopteris richardii. Am Fern J 102:147–153. doi:10.1640/0002-8444-102.2.147
Kamachi H, Matsunaga E, Noguchi M, Inoue H (2004) Novel mutant phenotypes of a dark-germinating mutant dkg1 in the fern Ceratopteris richardii. J Plant Res 117:163–170. doi:10.1007/s10265-004-0143-9
Kamachi H, Iwasawa O, Hickok LG, Nakayama M, Noguchi M, Inoue H (2007) The effects of light on sex determination in gametophytes of the fern Ceratopteris richardii. J Plant Res 120:629–634. doi:10.1007/s10265-007-0106-z
Kiss JZ, Wright JB, Caspar T (1996) Gravitropism in roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97:237–244. doi:10.1034/j.1399-3054.1996.970205.x
Kiss JZ, Miller KM, Ogden LA, Roth KK (2002) Phototropism and gravitropism in lateral roots of Arabidopsis. Plant Cell Physiol 43:35–43. doi:10.1093/pcp/pcf017
Kong SG, Wada M (2016) Molecular basis of chloroplast photorelocation movement. J Plant Res 129:159–166. doi:10.1007/s10265-016-0788-1
Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720. doi:10.1146/annurev.arplant.043008.092042
Morita MT, Nakamura M (2012) Dynamic behavior of plastids related to environmental response. Curr Opin Plant Biol 15:722–728. doi:10.1016/j.pbi.2012.08.003
Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, Kurisu G, Fujita Y (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465:110–114. doi:10.1038/nature08950
Murata T, Sugai M (2000) Photoregulation of asymmetric cell division followed by rhizoid development in the fern Ceratopteris prothalli. Plant Cell Physiol 41:1313–1320. doi:10.1093/pcp/pcd063
Němec B (1900) Über die art der wahrnehmung des schwerkraftreizes bei den pflanzen. Ber Deutsch Bot Ges 18:241–245
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. doi:10.1105/tpc.016428
Oikawa K, Yamasato A, Kong SG, 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 Physiology 148:829–842. doi:10.1104/pp.108.123075
Raghavan V (1989) Developmental biology of fern gametophytes. Cambridge University Press, Cambridge
Ridge RW, Sack FD (1992) Cortical and cap sedimentation in gravitropic Equisetum roots. Am J Bot 79:328–334
Sack FD (1997) Plastids and gravitropic sensing. Planta 203:S63–S68
Salmi ML, ul Haque A, Bushart TJ, Stout SC, Roux SJ, Porterfield DM (2011) Changes in gravity rapidly alter the magnitude and direction of a cellular calcium current. Planta 233:911–920. doi:10.1007/s00425-010-1343-2
Scott RJ, Hickok LG (1991) Inheritance and characterization of a dark-germinating, light-inhibited mutant in the fern Ceratopteris richardii. Can J Bot 69:2616–2619. doi:10.1139/b91-326
Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:8860–8865. doi:10.1073/pnas.0912773107
Suetsugu N, Sato Y, Tsuboi H, Kasahara M, Imaizumi T, Kagawa T, Hiwatashi Y, Hasebe M, Wada M (2012) The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol 53:1854–1865. doi:10.1093/pcp/pcs133
Toyota M, Ikeda N, Sawai-Toyota S, Kato T, Gilroy S, Tasaka M, Morita MT (2013) Amyloplast displacement is necessary for gravisensing in Arabidopsis shoots as revealed by a centrifuge microscope. Plant J 76:648–660. doi:10.1111/tpj.12324
Tsuboi H, Wada M (2012) Chloroplasts move towards the nearest anticlinal walls under dark condition. J Plant Res 125:301–310. doi:10.1007/s10265-011-0433-y
Vaughn KC, Hickok LG, Warne TR, Farrow AC (1990) Structural analysis and inheritance of a clumped-chloroplast mutant in the fern Ceratopteris. J Hered 81:146–151
Weise SE, Kuznetsov OA, Hasenstein KH, Kiss JZ (2000) Curvature in Arabidopsis inflorescence stems is limited to the region of amyloplast displacement. Plant Cell Physiol 41:702–709. doi:10.1093/pcp/41.6.702
Wilkins MB (1966) Geotropism. Annu Rev Plant Physiol 17:379–408
Wolverton C, Ishikawa H, Evans ML (2002a) The kinetics of root gravitropism: dual motors and sensors. J Plant Growth Regul 21:102–112. doi:10.1007/s003440010053
Wolverton C, Mullen JL, Ishikawa H, Evans ML (2002b) Root gravitropism in response to a signal originating outside of the cap. Planta 215:153–157. doi:10.1007/s00425-001-0726-9
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This work was supported by JSPS KAKENHI Grant Number JP15K11914.
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Kamachi, H., Tamaoki, D. & Karahara, I. Plasma membrane-anchored chloroplasts are necessary for the gravisensing system of Ceratopteris richardii prothalli. J Plant Res 130, 397–405 (2017). https://doi.org/10.1007/s10265-016-0889-x
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DOI: https://doi.org/10.1007/s10265-016-0889-x