Abstract
Key message
Non-tip-focused Ca 2+ gradient indicated by genetically expressing a FRET-based calcium sensor YC3.60 was established in spherical expanding cotton fibers, which is vital for cotton fiber initiation.
Abstract
Cotton fiber is a single cell elongated from ovule epidermis. It is not only the most important natural fiber used in the textile industry but also an ideal model for studying cell differentiation and elongation. Before linear cell growth, cotton fibers undergo spherical expansion at the beginning of initiation. Ca2+, as an important secondary messenger, plays a central role in polarized cell growth including cotton fiber elongation. However, the role of Ca2+ in fiber initiation is far from well understood. In this paper, through ovule culture we demonstrate that Ca2+ is crucial for fiber initiation. Using transgenic cotton expressing the fluorescent Ca2+ indicator YC3.60, we show cellular and intracellular distribution of Ca2+ in cotton ovule epidermis and fiber cells. In the initiating fiber cell, Ca2+ accumulated mainly at the base of the cell, while in the fast elongating cell, the Ca2+ was enriched in the tip region. This cellular distribution of Ca2+ reported by YC3.60 was confirmed by the staining with a Ca2+-sensitive dye fluo-3/AM. Compared to the fluorescent dye staining, the YC3.60 system can reveal more detailed information on the intracellular distribution without photobleaching. Taken together, our data suggest that Ca2+ plays an important role in spherical expansion of cotton fiber initials.
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References
Basra AS, Malik CP (1984) Development of the cotton fiber. In: Bourne GH, Danielli JF, Jeon KW (eds) International review of cytology. Academic Press, London, pp 65–113
Beasley CA, Ting IP (1973) The effects of plant growth substances on in vitro fiber development from fertilized cotton ovules. Am J Bot 60:130–139
Behera S, Wang N, Zhang C, Schmitz-Thom I, Strohkamp S, Schültke S, Hashimoto K, Xiong L, Kudla J (2015) Analyses of Ca2+ dynamics using a ubiquitin-10 promoter-driven Yellow Cameleon 3.6 indicator reveal reliable transgene expression and differences in cytoplasmic Ca2+ responses in Arabidopsis and rice (Oryza sativa) roots. New Phytol 206:751–760
Bibikova NT, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505
Cleland RE, Rayle DL (1977) Reevaluation of the effect of calcium ions on auxin-induced elongation. Plant Physiol 60:709–712
Gao P, Zhao P-M, Wang J, Wang H-Y, Wu X-M, Xia G-X (2007) Identification of genes preferentially expressed in cotton fibers: a possible role of calcium signaling in cotton fiber elongation. Plant Sci 173:61–69
Graves DA, Stewart JM (1988) Chronology of the differentiation of cotton (Gossypium hirsutum L.) fiber cells. Planta 175:254–258
He P, Shan L, Sheen J (2007) The use of protoplasts to study innate immune responses. In: Ronald PC (ed) Plant–pathogen interactions: methods and protocols. Humana Press, Totowa, NJ, pp 1–9
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155
Hepler PK, Kunkel JG, Rounds CM, Winship LJ (2012) Calcium entry into pollen tubes. Trends Plant Sci 17:32–38
Himschoot E, Beeckman T, Friml J, Vanneste S (2015) Calcium is an organizer of cell polarity in plants. Biochimica et Biophysica Acta (BBA) Molecular Cell Res 1853:2168–2172
Huang Q-S, Wang H-Y, Gao P, Wang G-Y, Xia G-X (2008) Cloning and characterization of a calcium dependent protein kinase gene associated with cotton fiber development. Plant Cell Rep 27:1869–1875
Iwano M, Shiba H, Miwa T, Che F-S, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136:3562–3571
Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A, Takayama S (2009) Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 150:1322–1334
Kim HJ, Triplett BA (2001) Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol 127:1361–1366
Krebs M, Held K, Binder A, Hashimoto K, Den Herder G, Parniske M, Kudla J, Schumacher K (2012) FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics. Plant J 69:181–192
Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PLoS One 6:e18549
Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401
Luo M, Xiao Y, Li X, Lu X, Deng W, Li D, Hou L, Hu M, Li Y, Pei Y (2007) GhDET2, a steroid 5α-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant J 51:419–430
Mei W, Qin Y, Song W, Li J, Zhu Y (2009) Cotton GhPOX1 encoding plant class III peroxidase may be responsible for the high level of reactive oxygen species production that is related to cotton fiber elongation. J Genet Genom 36:141–150
Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887
Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci 101:10554–10559
Padmalatha KV, Patil DP, Kumar K, Dhandapani G, Kanakachari M, Phanindra ML, Kumar S, Mohan TC, Jain N, Prakash AH, Vamadevaiah H, Katageri IS, Leelavathi S, Reddy MK, Kumar PA, Reddy VS (2012) Functional genomics of fuzzless-lintless mutant of Gossypium hirsutum L. cv. MCU5 reveal key genes and pathways involved in cotton fibre initiation and elongation. BMC Genom 13:1–15
Pang M, Sanford N, Wilkins T (2013) ROS accumulation in cotton ovule epidermal cells is necessary for fiber initiation. bioRxiv. doi:10.1101/000745
Perochon A, Aldon D, Galaud JP, Ranty B (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93:2048–2053
Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–173
Qin Y, Dong J (2015) Focusing on the focus: What else beyond the master switches for polar cell growth? Mol Plant 8:582–594
Qin Y, Zhu Y (2011) How cotton fibers elongate: a tale of linear cell-growth mode. Curr Opin Plant Biol 14:106–111
Ryser U (1999) Cotton fiber initiation and histodifferentiation. In: Basra AS (ed) Cotton fibers: developmental biology, quality improvement, and textile processing. The Haworth Press, New York, pp 1–34
Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta 187:455–459
Singh B, Avci U, Eichler Inwood SE, Grimson MJ, Landgraf J, Mohnen D, Sørensen I, Wilkerson CG, Willats WGT, Haigler CH (2009) A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol 150:684–699
Swanson SJ, Choi W-G, Chanoca A, Gilroy S (2011) In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Annu Rev Plant Biol 62:273–297
Taliercio E, Boykin D (2007) Analysis of gene expression in cotton fiber initials. BMC Plant Biol 7:22
Tang W, He Y, Tu L, Wang M, Li Y, Ruan Y-L, Zhang X (2014a) Down-regulating annexin gene GhAnn2 inhibits cotton fiber elongation and decreases Ca2+ influx at the cell apex. Plant Mol Biol 85:613–625
Tang W, Tu L, Yang X, Tan J, Deng F, Hao J, Guo K, Lindsey K, Zhang X (2014b) The calcium sensor GhCaM7 promotes cotton fiber elongation by modulating reactive oxygen species (ROS) production. New Phytol 202:509–520
Thomas D, Tovey SC, Collins TJ, Bootman MD, Berridge MJ, Lipp P (2000) A comparison of fluorescent Ca2+ indicator properties and their use in measuring elementary and global Ca2+ signals. Cell Calcium 28:213–223
Tiwari SC, Wilkins TA (1995) Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Can J Bot 73:746–757
Verrillo F, Occhipinti A, Kanchiswamy CN, Maffei ME (2014) Quantitative analysis of herbivore-induced cytosolic calcium by using a Cameleon (YC 3.6) calcium sensor in Arabidopsis thaliana. J Plant Physiol 171:136–139
Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439
Yang SS, Cheung F, Lee JJ, Ha M, Wei NE, Sze S-H, Stelly DM, Thaxton P, Triplett B, Town CD, Chen ZJ (2006) Accumulation of genome-specific transcripts, transcription factors and phytohormonal regulators during early stages of fiber cell development in allotetraploid cotton. Plant J 47:761–775
Zhang M, Zheng X, Song S, Zeng Q, Hou L, Li D, Zhao J, Wei Y, Li X, Luo M, Xiao Y, Luo X, Zhang J, Xiang C, Pei Y (2011) Spatiotemporal manipulation of auxin biosynthesis in cotton ovule epidermal cells enhances fiber yield and quality. Nat Biotechnol 29:453–458
Zhu Y, Xu K, Luo B, Wang J, Chen X (2003) An ATP-binding cassette transporter GhWBC1 from elongating cotton fibers. Plant Physiol 133:580–588
Acknowledgements
We would like to thank Dr. Megumi Iwano (Nara Institute of Science and Technology) and Dr. Atsushi Miyawaki (RIKEN Brain Science Institute) for kindly providing the plasmid pSLJAct1-YC3.60. This study was funded by the National Natural Science Foundation of China (31130039 to Y.P.), the Foundation for the Author of National Excellent Doctoral Dissertation of PR China (201466 to M.Z.), the Program for New Century Excellent Talents in University (to M.Z.) and the Natural Science Foundation of Chongqing, China (cstc2012jjjq80001 to M.Z.).
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Communicated by Kang Chong.
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Zhang, M., Cao, Hz., Hou, L. et al. In vivo imaging of Ca2+ accumulation during cotton fiber initiation using fluorescent indicator YC3.60. Plant Cell Rep 36, 911–918 (2017). https://doi.org/10.1007/s00299-017-2122-3
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DOI: https://doi.org/10.1007/s00299-017-2122-3